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ON THE ORIGINS OF HUMAN COGNITION

Alfredo Ardila
Department of Communication Sciences and Disorders Florida International University Miami, Florida, USA

2012

CONTENT

1. Introduction
Statement of the Problem References

7 7 15 23 23 24 25 29 30 36 37 41 41 43 45 46 46 47

2. Origins of Language
Introduction There are only two fundamental aphasia syndromes
The selection disorder The sequencing disorder

Other aphasia syndromes Three stages in language development


Initial communication systems The function of noises (grunts) in human communication Second stage: Lexical/semantic Third stage: Grammar

Brain representation of nouns and verbs Memory systems for nouns and verbs Using verbs and using grammar is a single ability Understanding Brocas area

Origins of the lexical/semantic system Origins of the grammatical system Grammar at the origin of the executive functions Conclusions References

52 54 56 60 60 81 81 83 83 84 85 86 89 92 93

3. Origins of Spatial Abilities


Introduction How we get oriented in the space?
Perceptual Constancy Reference Systems Cultural Differences in Visuoperceptual Abilities

Acquired spatial cognition disorders Neuroimaging studies Conclusions References

4. Origins of Writing
Introduction How did writing appear? How many people can write? Agraphia as a neuropsychological syndrome
Dysexecutive agraphia

100 100 101 106 107 108 108

Is any area in the brain specialized for writing?

Brain activation during writing Writing in different systems From agraphia to dystypia Conclusions References

109 110 113 117 118

5. Origins of Calculation Abilities


Introduction Numerical concepts in animals Development of calculation abilities in children
Numerical abilities in pre-school children

124 124 125 126 127 131 132 142 147 150 151

Development of numerical abilities at school Calculation abilities in pre-historic man Further developments of arithmetical abilities The neuroscience of calculation abilities Conclusion References

6. Origins of Executive Functions


Introduction What does executive functions mean? Is there any fundamental core ability accounting for executive functions?

161 161 162

167

Two proposed fundamental executive functions Metacognitive executive functions as an internalization of action Is there anything special in the prefrontal cortex? Executive functions in pre-historical man Metacognitive executive functions as a cultural product Tentative conclusions References

169

173 178 181 183 184 186 202 202 203 208 210 212 217 218 230 230 231 233 235 235

7. How we recognize other people?


Introduction Own-species members recognition Gender recognition Emotional expression and emotional recognition Individuals' recognition Conclusions References

8. Culture and Cognitive Testing


Introduction What is culture? Why culture affects cognitive test performance?
Patterns of abilities Cultural values

Familiarity Language Education

238 239 240 246 249 254

Culture minorities groups Norms in different national and cultural groups References

1. Introduction
Nothing in biology makes sense except in the light of evolution
(Theodosius Dobzhansky, 1973)

Understanding the historical evolution of cognition represents a crucial question for our interpretations of the human specie. This is a question that has been approached since long ago by different classical authors, including Wundt (1863/1864), James (1890), Vygotsky (1931), Luria (1974, 1976), Leontiev (1981), and many others, and still remains an unsettled question. As a matter of fact, during the last decades, a myriad of books and journal papers has been published (e.g., Ardila, 1993; Cummins & Allen, 1998; Heyes & Huber, 2000; Parker & McKinney, 1999; Tomasello, 2001; Travis, 2007; Walsh, 2001; Woods, 1996; Zimmer, 2005) approaching this question and attempting to shed light on the origins of complex psychological processes, such as language, complex perception, and executive functions. This is a question that in no way is easy to answer but is most important for understanding the idiosyncrasies of our own specie. It is a question that can be approached from different perspectives, including a neuropsychological one. This book includes a collection of papers around the general question: How - from a neuropsychological perspective -, did cognition emerge in human history?

Statement of the Problem

Anthropology has striven to understand how man's living conditions were 10,000, 100,000 or 1,000,000 years ago. The Stone Age (usually divided in the Old Stone Age or Paleolithic, and New Stone Age or Neolithic) extended until some 3,000-6,000 years ago (Hours, 1982; Toth & Schick, 2007). Agriculture appeared some 10,000 years ago; first cities some 6,000 years ago; first civilizations about 5,000 years ago; writing has only five or six thousand years history; and arithmetical abilities, about 6,000 years (Childe, 1936; No author, 1993; Sampson, 1985; Toth & Schick, 2007). But most important to bear in mind, when considering that agriculture appeared some 10,000 years ago and writing has five or six thousand years history, it does not mean that the whole human species began to live in cities 10,000 years ago and to use written language five or six thousand years ago. It only means that some few people began to live a sedentary life and to use written language. The diffusion of the changes that occurred during the last 10,000 years has been a particularly slow process. Nowadays, for instance, there are human groups that are still nomads (regardless that the first cities were created some 10,000 years ago), and about 20% of the world population is illiterate (UNESCO, portal.unesco.org) (regardless that writing was invented some five-six thousand years ago). Contemporary man (Homo sapiens sapiens) has lived on the earth probably since about 200,000 years ago (Wells, 2003; Wood, 1996; Zimmer, 2005). We can state, with certain level of confidence, that during this time, his brain structural changes have been minimal (Barkow, Cosmides & Tooby, 1992; Harris, 1983; Streidter, 2005). It is easy to conclude that human brain adaptation was accomplished to survive more exactly in Stone-Age life conditions (during about 99% of human technological history) than in those existing nowadays. Only when departing from the analysis of these original living conditions can we understand the specific characteristics and idiosyncrasies of his brain adaptation. It would seem reasonable for any neuroscientist to raise the question: What type of information processing abilities did the human brain become adapted for? Consequently, which are man's basic or universal cognitive abilities? The search for universals has guided an important proportion of the anthropological

and linguistic activity during the last decades. Anthropology and linguistics have departed from three different approaches, attempting to reconstruct the way of life and the languages spoken by the prehistorical man: 1. Archeological findings are used as elements to reconstruct prehistoric ways of life. 2. By comparing existing human groups, it is possible to find some common social, behavioral, and linguistic characteristics. Those common characteristics that eventually are disclosed most likely already existed in prehistorical times, and probably are the result of man's specific biological adaptation. Several thousands of different cultures have been described (Bernatzik, 1957; Harris, 1983), and contemporary man speaks close to 7,000 different languages (www.ethnologue.com). By comparing all these cultures and all these languages, some universals can be discovered (Greenberg, 1978; Haviland, 2007; Swadesh, 1971). 3. By taking existing cultures and/or living languages into consideration, similar in a specific parameter to prehistorical cultures and/or languages, it is possible to propose how prehistorical living forms and language characteristics could have been with regard to that particular parameter. These three approaches (to use archeological findings, to find common characteristics when comparing different human groups, and to use an existing human group, similar in a certain parameters to the prehistorical groups) are potentially useful, and, as a matter of fact, have been used in neuropsychological research, although in a restricted way. 1. We can attempt to reconstruct how some neuropsychological characteristics may have been several thousand years ago, departing from some archeological findings. For instance, we can study handedness in Neolithic man departing from

On the Origins of Human Cognition 10

pictorial rests (Spennemann, 1984). 2. We can search for commonality among existing groups. For example, we can study aphasic language disturbances throughout different world languages, looking for common characteristics and consequently, basic brain language organization (Menn & Obler, 1990; Paradis, 2001). And finally, 3. We can study some neuropsychological variables in living human groups, similar in a specific parameters to the prehistorical man. For instance, we can analyze illiteracy in order to attempt to figure out how linguistic or praxic abilities were in pre-writing societies (e.g., Ardila et al., 1989; Rosselli et al., 1990; Ardila et al., 2010; Lecours et al., 1987, 1988); or we can analyze constructional abilities among Stone Age-like Amazonian Indians (Pontius, 1989). Undoubtedly, neuropsychology has tremendously advanced in some specific areas; for instance, in the assessment of the sequelae of brain pathology; or in the establishment of clinical/anatomical correlations. Our fundamental and basic knowledge about the brain organization of cognitive activity under normal and pathological conditions has significantly advanced during the last decades thanks very specially to the use of contemporary neuroimaging techniques (e.g., Cabeza & Nyberg, 2000; Brodmanns interactive atlas, www.fmriconsulting.com/ brodmann/). Nevertheless, we do not have enough understanding about what can be understood and what can be considered as "basic cognitive abilities". Thus, for instance, classification of spatial cognition disturbances is still very confusing and partially contradictory (e.g., De Renzi, 1982; Rizzolatti, Berti & Gallese, 2000; Robertson, 2003). We barely have dealt with individual differences in neuropsychological performance (e.g., Hartlage & Telzrow, 1985). And our understanding of cultural differences is, to be optimistic, very insufficient (Ardila, 1995; Fletcher-Janzen, Strickland & Reynolds, 2000; Helm, 1992; Uzzell, Pontn & Ardila, 2007; Pedraza & Mungas, 2008). Some significant interest toward cultural and historical issues, however, has recently been observed in neuropsychology. However, this interest in obtaining a better

On the Origins of Human Cognition 11

understanding of cultural and historical issues in the neuropsychology sphere is not new. Some precursor attempts are found in literature. For instance, A.R. Luria is well-known in neuropsychology for his contributions to the analysis of the brain organization of language; or, his research on the prefrontal syndrome. However, his cultural approach to neuropsychology is less recognized. Nonetheless, Luria departed from the analysis of cultural issues (Luria, 1934, 1976; see Footnote 1) and only moved further toward neuropsychology. Unfortunately, most of his cross-cultural research proposals in neuropsychology (for example, the analysis of hemi-neglect syndrome in different cultural groups; the cross-linguistic analysis of aphasias; the comparison of alexias in different writing systems, etc.) never turned into concrete research programs. But his great interest and emphasis on cultural and historical variables in neuropsychology was always reflected in his writings. During the last decades a significant number of papers devoted directly or indirectly to the analysis of cultural variables on neuropsychological performance have been recorded in literature. It could be mentioned: the bilingualism research (e.g., Albert & Obler, 1978; Dupont et al., 1992; Paradis, 1987, 2004; Vaid, 1986); the studies on illiteracy (e.g., Ardila et al., 1989, 2010; Lecours et al., 1987, 1988; Matute, 2000; Ostrosky et al., 1998; Reis & Castro-Caldas,1998; Rosselli et al., 1990 ); the cross-linguistic analysis of aphasia (e.g., Bates et al., 1987a, 1987b, 1988; Menn & Obler, 1990; Paradis, 2001); the research about the influence of socioeducational factors in neuropsychological performance (e.g., Ardila et al., 2000; Ostrosky et al., 1985; Rosselli & Ardila, 1990); and the studies on cultural variables on handedness (e.g., Ardila et al., 1989a; Bryden, 1987; Bryden et al., 1993; Harris, 1990). This collection of papers attempts to direct the attention of behavioral neurosciences, toward some potentially relevant historical and cultural variables in neuropsychological performance. The purpose of this book is, in consequence, multiple:
1 The book "Cognitive Development" was initially written in the 1930', but it was published in Russian only in 1974 with the name "About the Historical Development of Cognitive Processes". In 1976 it was translated to English with the name "Cognitive Development: Its Cultural and Social Foundations"

On the Origins of Human Cognition 12

1. To integrate some information regarding cross-cultural differences in neuropsychological performance. 2. To review some evidence about the historical origins of cognitive activity. 3. To analyze how the inclusion of a historical and cultural perspective in behavioral neurosciences can contribute to obtain a better understanding about the brain organization of cognition. And, finally, 4. To propose some general guidelines for future research in the area. Different problems are analyzed. In the chapter Origins of Language it is emphasized that there are two fundamental forms of aphasia which are linked to defects in the lexical/semantic and grammatical systems of language (Wernicke-type aphasia and Broca-type aphasia, respectively). Grammar correlates with the ability to represent actions (verbs) and depends on what is known as Brocas area and its related brain circuits, but it is also related to the ability to quickly carry out the sequencing of the articulatory movements required for speaking (speech praxis). Language as a grammatical system seemingly appeared relatively recently and seems to be exclusive to Homo sapiens. The paper Origins of Spatial Abilities analyzes the development and cross-cultural differences of spatial cognition. It is proposed that: (1) Spatial abilities are found to be significantly associated with the complexity of geographical conditions and survival demands; (2) spatial cognition has evolved in a parallel way with cultural evolution and ecological demands; and (3) contemporary city-man may be using those spatial abilities in some new, non-existing in pre-historical times, conceptual tasks (such as mathematics, reading, writing, mechanics, music, etc.).

On the Origins of Human Cognition 13

In the chapter Origins of Writing it is argued that there is no brain area specialized for writing, but rather that writing relies on some basic abilities that existed long before writing was invented. Pre-writing was initially a visuoconstructive and ideomotor ability, and only later did it become the language-related ability of writing. It is also emphasized that most of the neuropsychological syndromes, including agraphia, were described during the late 19th and early 20th century, but living conditions have changed dramatically during the last 100 years. Writing no longer means only using pencil and paper, but also includes using computer word processing programs. Writing using paper and pencil does not require the same cognitive, motor, and spatial tasks as those required when using a computer keyboard. Although the conceptual knowledge of written language can be the same, the motor activity and the spatial abilities that are used are rather different. It can be anticipated that new neuropsychological syndromes resulting from these new living conditions will be described in the future. In the chapter Origins of Calculation Abilities it is pointed out that counting, departing from finger sequencing, is observed in different ancient and contemporary cultures, whereas number representation and arithmetic abilities are found only during the last five-six thousand years. The paper analyzes the rationale of selecting a base of ten in most numerical systems, and the clinical association between acalculia and finger agnosia. Finger agnosia, right-left discrimination disturbances, semantic aphasia, and acalculia is proposed to conform a single neuropsychological syndrome associated with left angular gyrus damage. It is hypothesized that acalculia, finger agnosia, and disorders in right-left discrimination (as in general, in the use of spatial concepts) result from the disruption of common cognitive mechanisms. In the paper Origins of Executive Functions it is proposed that the prefrontal lobe participates in two closely related but different executive function abilities: (1) metacognitive executive functions: problem solving, planning, concept formation, strategy development and implementation, controlling attention, working memory, and the like; that is, executive functions as they are usually understood in contemporary neuroscience; and

On the Origins of Human Cognition 14

(2)

emotional/motivational

executive

functions:

coordinating

cognition

and

emotion/motivation (that is, fulfilling biological needs according to some existing conditions). The first one depends on the dorsolateral prefrontal areas, whereas the second one is associated with orbitofrontal and medial frontal areas. Current tests of executive functions basically tap the first ability (metacognitive). Solving everyday problems (functional application of executive functions), however, mostly requires the second ability (emotional/motivational); therefore, these tests have limited ecological validity. Contrary to the traditional points of view, recent evidence suggests that the human prefrontal lobe is similar to other primates and hominids. Other primates and hominids may possess the second (emotional executive functions) prefrontal ability, but not the first (metacognitive executive functions) one. It is argued that metacognitive executive functions are significantly dependent on culture and cultural instruments. They probably are the result of the development and evolution of some conceptualization instruments; language (and written language as an extension of oral language) may represent the most important one. The second executive function ability (emotional/motivational) probably is the result of a biological evolution shared by other primates. The question of recognizing other individuals is further analyzed ("How we recognize other people? "). It is emphasized that not only visual, but also auditory and even olfactory information may be involved in people recognition. Visual information is proposed to include not only the perception of faces, but also the perception of whole-body and gait, clothes, emotional expressions, and individual marks. Departing from clinical observation, a model for people recognition is presented. It is hypothesized that different "subsystems" or "modules" may be involved in individuals' recognition: "living" versus "nonliving", "own-species" versus "other-species", "familiar" versus "nonfamiliar", "males" versus "females", and "individual identification" versus "emotional identification". The chapter Culture and Cognitive Testing attempts to summarize the major cultural variables affecting neuropsychological test performance. Initially, culture is defined as the specific way of living of a human group, and further, the question why culture affects

On the Origins of Human Cognition 15

cognitive test performance? is approached. Different cultural aspects potentially affecting neuropsychological test performance are reviewed. The issues of familiarity, language and education are also discussed. Cognitive testing of so-called minority groups is analyzed in a special section. Finally, it is concluded that understanding the variables that can affect cognitive test performance seems to be as important as obtaining a large number of norms in different linguistic and cultural groups. Finally, my sincere gratitude goes out to all the colleagues and friends who encouraged me to write this book. I want to thank Florida International University for the opportunity to write this book during my sabbatical year. My gratitude to Natasha Aiguesvives for her editorial support. I sincerely hope that this collection of papers will further the interest in the analysis of historical and cultural variables in cognition, and will contribute to the development and strengthening of cross-cultural neuropsychology. No doubt, cross-cultural neuropsychology represents a critical new direction of research, and will challenge neuropsychologists during the coming years.

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M.H., Matute, E., Nitrini, R., Ostrosky-Solis, F., & Rosselli, M. (2010). Cognition without reading: Neuropsychology of illiteracy. Archives of Clinical Neuropsychology, 25(8):689712. Ardila, A., Rosselli, M., & Rosas, P. (1989) Neuropsychological assessment in illiterates: Visuospatial and memory abilities. Brain and Cognition, 11, 147-166. Ardila, A., Ostrosky-Solis, F., Rosselli, M. & Gomez, C. (2000). Age related cognitive decline during normal aging: The complex effect of education. Archives of Clinical Neuropsychology, 15, 495-514. Barkow, J.H., Cosmides, L. & Tooby, J. (eds) (1992). The Adapted Mind: Evolutionary Psychology and the Generation of Culture. New York, NY: Oxford University Press. Bates, E., Friederici, A. & Wulfeck, B. (1987a). Grammatical morphology in aphasia: Evidence form three languages. Cortex, 23, 545-574. Bates, E., Friederici, A. & Wulfeck, B. (1987b). Comprehension in aphasia: A cross-linguistic study. Brain and Language, 32.19-67. Bates, E., Friederici, A., Wulfeck, B. &Juarez, L.A. (1988). On the preservation of

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Castro-Caldas, A., Petersson, K.M., Reis, A., Stone-Elander, S. & Ingvar, M. (1998) The illiterate brain: Learning to read and write during childhood influences the functional organization of the adult brain. Brain, 121, 1053-63. Childe, V.G. (1936). Man Makes Himself. London: Pitman Publishing. Cummins, D.D. & Allen, C. (1998). The evolution of mind. New York: Oxford University Press. De Renzi, E. (1982). Disorders of space exploration and cognition. New York: John Wiley. Dobzhansky , T. (1973). Nothing in biology makes sense except in the light of evolution. The American Biology Teacher, 35, 125-129. Dupont, S., Ardila, A. & Rosselli, M. (1992) Neuropsychological assessment in bilinguals. In: A.E. Puente, & R.J. McCaffrey (eds), Handbook of Neuropsychological Assessment: A Biopsychosocial Perspective (pp. 193-210). New York: Plenum Press. Fletcher-Janzen, E., Strickland, T.L. & Reynolds, C.R. (Eds) (2000). The Handbook of Cross-Cultural Neuropsychology. New York: Plenum Press.

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Greenberg, J.H. (1978). Universals of Human Language, vols 1-4. Stanford, CA: Stanford University Press. Harris, M. (1983). Culture, people, nature: An introduction to general anthropology. New York: Harper & Row, 3rd ed. Harris, J.L. (1990). Cultural influences on handedness: Historical and contemporary theory and evidence. In: S. Coren (ed), Left-Handedness: Behavioral Implications and Anomalies (pp. 195-258). Amsterdam: North-Holland. Hartlage, L.C. & Telzrow, C.F. (1985). The Neuropsychology of Individual Differences. New York: Plenum Press. Haviland , W.A., Prins, H.E., Walrath, D. & McBride, B. (2007). Cultural Anthropology: The Human Challenge. Belmont, CA: Wadsworth Publishing Company. 13 ed. Heyes, C.M. & Huber, L. (Eds.), (2000). Evolution of cognition. Cambridge, MA: MIT Press. Hours, F. (1982). Les civilisations du Pale ' olithique. Paris : Presses Universitaires de la France. James, W. (1890). The Principles of Psychology. Dover Publications. Lecours, R.L., Mehler, J., Parente, M.A., Caldeira, A. et al. (1987). Illiteracy and brain damage 1: aphasia testing in culturally contrasted populations (control subjects). Neuropsychologia, 25, 231-245 Lecours, A.R., Mehler, J., Parente, M.A., et al. (1988). Illiteracy and brain damage III: A

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contribution to the study of speech and language disorders in illiterates with unilateral brain damage (initial testing). Neuropsychologia, 26, 575-589. Leontiev, A.N., (1981). [Questions about psychological development]. Moscow: Ed. Progress. Luria, A.R. (1934). The second psychological expedition to Central Asia. Journal of Genetic Psychology, 41, 255-259. Luria, A.R. (1974). [About the historical development of cognitive processes]. Moscow: Moscow State University, Luria, A.R. (1976). Cognitive Development. Cambridge, MA: Harvard University Press. Matute, E., Leal, F., Zarabozo, D., Robles, A. & Cedillo, C. (2000) Does literacy have an effect on stick construction tasks? Journal of the International Neuropsychological Society 6, 668-672. Menn, L. & Obler, L.K. (1990). Agrammatic Aphasia: A Cross-Language Narrative Sourcebook. Amsterdam: John Benjamin Publishing Company. No author (1993) La naissance de l'criture. Lhistoire du Monde N2. Larousse. Ostrosky, F., Canseco, E., Quintanar, L., Navarro, E. & Ardila, A. (1985) Sociocultural effects in neuropsychological assessment. International Journal of Neuroscience, 27, 53-66. Ostrosky, F., Ardila, A., Rosselli, M. Lpez-Arango, G., & Uriel-Mendoza, V. (1998). Neuropsychological test performance in illiterates. Archives of Clinical Neuropsychology,

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13, 645- 660. Paradis, M. (1987). The Assessment of Bilingual Aphasia. Hillsdale, NJ: Lawrence Erlbaum Associates. Paradis, M. (ed) (2001). Manifestations of Aphasia Symptoms in Different Languages. New York: Pergamon Press Paradis, M. (2004). A neurolinguistic theory of bilingualism. Amsterdam: John Benjamins. Parker, S.T. & McKinney, M.L. (1999). Origins of Intelligence: The Evolution of Cognitive Development in Monkeys, Apes, and Humans. Baltimore: Johns Hopkins University Press. Pedraza, O. & Mungas, D. (2008). Measurement in cross-cultural neuropsychology. Neuropsychology Review, 18(3),184-93. Pontius, A.A. (1989). Color and spatial error in block design in stone-age Auca Indians: Ecological underuse of occipital- parietal system in men and of frontal lobes in women. Brain and Cognition, 10, 54-75. Rizzolatti, G., Berti, A., & Gallese, V. (2000). Spatial neglect: neuropsychological bases, cortical circuits and theories. In: Boller F & Grafman J. (eds) Handbook of Neuropsychology, vol 1 (pp. 503537). Amsterdam: Elsevier, 2nd ed. Robertson, L.C. (2003). Binding, spatial attention and perceptual awareness. Nature reviews. Neuroscience, 4, 93-102 Rosselli, M., Ardila, A. & Rosas, P. (1990). Neuropsychological assessment in illiterates II:

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2. Origins of Language

Introduction
For many years, the origin of human language has been a controversial topic and different explanatory proposals have been presented (e.g., Atkinson, 2011; Bickerton, 2009; Christiansen & Kirby, 2003; Nowak & Komarova, 2001). At a certain point in history, the debate became so complex and hot, that in 1866 the Linguistic Society of Paris banned discussion of the origin of language, arguing that it is to be an unanswerable problem. Contemporary research on linguistics, archeology, comparative psychology and genetics has significantly advanced in understanding the origins of human language (e.g., Bickerton, 1990; Corballis, 2002; Enard et al., 2002; Mallory, 1989; Nowak & Krakauer, 1999; Ruhlen, 1994; Scott-Phillips, 2010; Swadesh, 1967; Tallerman, 2005). Different disciplines have contributed from their own perspective to make the human communication system more comprehensible. The purpose of this chapter is not to further review and discuss the historical origins of language, but to relate what is known (or supposed) on the origins of language, with contemporary neurology and neuropsychology data, particularly in the area of aphasia. Aphasia knowledge can potentially make a significant contribution to the understanding about the origin and evolution of human language. Initially, some basic neuropsychological data about language impairments in the case of brain pathology will be presented. It will be emphasized that there are two basic

On the Origins of Human Cognition 24

linguistic operations (selecting and sequencing; i.e., language as a paradigm and language as a syntagm) (Jacobson & Halle, 1956; Jacobson, 1971). There are also two basic types of aphasia syndromes named in different ways (e.g., motor/sensory; anterior/ posterior; nonfluent/ fluent; Broca-type/ Wernicke-type; encoding /decoding disorder; expressive/ receptive disorder, etc.), each one related with the disturbance of one of these two basic language elements (lexical/semantic and grammatical) (for a review, see Ardila, 2010). Hence, in considering language evolution these two different dimensions of language have to be recognized. Each one may have emerged at a different historical moment. Analyzing this basic distinction and including it in an interpretation about language evolution can potentially further language evolution understanding.

There are only two fundamental aphasia syndromes


Since the XIX it is well known that there are two major aphasic syndromes (see Table 2.1), named in different ways, but roughly corresponding to Wernicke-type aphasia and Brocatype aphasia (e.g., Albert et al., 1981; Bastian, 1898; Benson & Ardila, 1996; Freud, 1891/1973; Goldstein, 1948; Head, 1926; Hcaen, 1972; Kertesz, 1979; Lichtheim, 1885; Luria, 1976; Pick, 1931; Schuell et al., 1964; Taylor-Sarno, 1998; Wilson, 1926). These two major aphasic syndromes have been related to the two basic linguistic operations: selecting (language as paradigm) and sequencing (language as syntagm) (Jacobson & Halle, 1956; Jacobson, 1971; Luria, 1972/1983). Jacobson (1964) proposed that aphasia tends to involve one of two types of linguistic deficiency. A patient may lose the ability to use language in two rather different ways: the language impairment can be situated on the paradigmatic axis (selection or similarity disorder; Wernicke-type aphasia) or the syntagmatic axis (contiguity or sequencing disorder; Broca-type aphasia). It is important to emphasize that when Dejerine (1914) first proposed the concept of language zone or language area in the brain, he referred indeed to three areas: Brocas

On the Origins of Human Cognition 25

area, Wernickes areas, and the angular gyrus (involved in written language) (Figure 2.1.). Thence, he recognized two brain areas related with spoken language and one cortical area participating in written language. But the point is that for Dejerine it was clear that there are two different spoken language areas in the brain: Brocas area and Wernickes area, and consequently, there are two fundamental types of acquired language disorders. ________________________________________________ expressive motor anterior no fluent paradigmatic impairment coding impairment Wernicke-type receptive sensorial posterior fluent syntagmatic impairment decoding impairment Broca-type

________________________________________________

Table 2.1. Different names used to refer to the two basic aphasic syndromes.

The selection disorder The selection (similarity) disorder restricts the patients ability to select words from the paradigmatic axis. These patients (Wernicke-type aphasia) cannot find words that exist as parts of the system (vocabulary). These aphasics have severely limited access to this language repertoire system. Specific nouns tend to be inaccessible and more general ones (cat becomes animal) take their place. These patients cannot select among alternative names (dog, cat, fox, etc). These patients may instead fill out their discourse with

On the Origins of Human Cognition 26

circumlocutions (the clock is referred as to know the time"). Words no longer have a generic (paradigmatic) meaning for these patients, so verbal expressions tend to be strongly contextualized, and speech becomes empty. A dog can be referred as animal, it barks, fox, etc.

Figure 2.1. The language zone in the brain (Dejerine, 1914.)

Luria (1972/1983) emphasized that the selection disorder can be observed at different levels of the language, corresponding to different aphasia subtypes: phoneme selection (aphasia acoustic agnosic), word selection (aphasia acoustic amnesic), and

On the Origins of Human Cognition 27

meaning selection (amnesic aphasia). By the same token, the contiguity disorder can be observed at different levels: sequencing words (kinetic motor aphasia Broca aphasia) or sequencing sentences (dynamic aphasia transcortical motor aphasia). Noteworthy, different subtypes of Wernicke aphasia are frequently distinguished (e.g., Ardila, 2006). Lurias acoustic agnosic, acoustic amnesic, and amnesic aphasia are indeed subtypes of the language impairment syndrome referred to as a whole as Wernicke aphasia. In Wernicke aphasia, the lexical repertoire tends to decrease and language understanding difficulties are evident. Wernicke aphasia patients do not fully discriminate the acoustic information contained in speech. Lexical (words) and semantic (meanings) association become deficient. Patients have problems in recalling the words (memory of the words) and also in associating the words with specific meanings. Consequently, it is evident that at least three different deficits underlie Wernicke-type aphasia: (1) phoneme discrimination defects, (2) verbal memory defects, and finally (3) lexical/semantic association deficits. Figure 2.2 presents the model proposed by Ardila (1993) to account for the language recognition defects observed in cases of Wernicke-type of aphasia. In Wernicke-type aphasia obviously the language defect is situated at the level of the meaningful words (nouns). Phoneme and word selection are deficient, but language syntax (contiguity: sequencing elements) is well preserved and even overused (paragrammatism in Wernicke aphasia). Nouns seem to depend on an organized pattern of brain activity. Contemporary clinical and neuroimaging studies have corroborated that different semantic categories are differentially impaired in cases of brain pathology. For instance, in anomia it has been traditionally recognized that naming body-parts, external objects and colors depend (and are altered) upon the activity of different brain areas (Hcaen & Albert, 1978). It has also been found that finer distinctions can be made with regard to naming defects, which can be limited to a rather specific semantic category (e.g., peoples names, living things, tools, geographical names, etc) (e.g., Harris & Kay, 1995; Goodglass et al., 1986; Lyons et al., 2002; Warrington & Shallice, 1984) and even as specific as medical terms (Crosson et al., 1997). A brain mapping of the memory organization of different semantic categories could

On the Origins of Human Cognition 28

be supposed.

D Long -term memory for features

F Short -term memory for features

G Long -term memory for phonemes

B Primary auditory analysis

C Frequency intensity recognition

H Categorical perception language recognition level I

ear

Features recognition

Phoneme recognition

I Short -term memory for phonemes J Verbal -acoustic long memory term

K Verbal -acoustic recognition (lexical) L Verbal acoustic short memory M Associations (visual, tactile, etc) -term Categorical perception language recognition level II

N Semantic Recognition Categorical perception language recognition level III

Figure 2.2. Diagram model for language recognition proposed by Ardila (1993).Three levels of language recognition potentially impaired in Wernicke-type aphasia can be distinguished: phonemic (categorical perception level I), lexical (categorical

perception level II), and semantic (categorical perception level III). Three different sub-syndromes can be found: phonemic discrimination defects (acoustic-agnosic or Wernicke aphasia type I), verbal-acoustic memory defects (acoustic-amnesic or Wernicke aphasia type II), and semantic association defects (amnesic, nominal or Extrasylvian sensory aphasia).

On the Origins of Human Cognition 29

The sequencing disorder Broca-type of aphasia represents the clinical syndrome characterized by impairments in the sequencing process (syntagmatic axis defect). It is usually recognized that Broca aphasia has two different distinguishing characteristics: (a) a motor component (lack of fluency, disintegration of the speech kinetic melodies, verbal-articulatory defects, etc., that is usually referred as apraxia of speech); and (b) agrammatism (e.g., Benson & Ardila, 1996; Luria, 1976; Goodglass, 1993; Kertesz, 1985). If both defects are simultaneously observed (i.e., they are very highly correlated), it simply means they both are just two different manifestations of a single underlying defect. It is not easy to understand which one could be the single factor responsible for these two clinical manifestations; but it may be kind of an "inability to sequence expressive elements" (Figure 2.3).

Broca aphasia

Apraxia of speech

Agrammatism

ability to sequence expressive elements ?

Factor

On the Origins of Human Cognition 30

Figure 2.3. A single factor (probably the ability to sequence expressive elements) can underlie the two disturbances observed in Broca aphasia (Ardila & Bernal, 2007). A single common factor underlying both defects should be assumed. Broca's area, most likely, is not specialized in producing language, but in certain neural activity that can support not only skilled movements required for speech, but also morphosyntax. It is interesting to note that deaf-mute subjects (who, in consequence have never produced verbal articulatory movements) present a virtually total impossibility to learn, understand, and use language grammar (Poizner et., 1987). Probably, the lack of verbal articulatory normal development is necessarily associated with a lack of normal grammatical development.

Other aphasia syndromes


Some aphasic syndromes can eventually be considered as variants of the Broca and Wernicke aphasia. For instance, amnesic or anomic or nominal aphasia (usually due to damage in the vicinity of Brodmanns area 37) (Hcaen & Albert, 1978; Head, 1926; Luria, 1976) can be interpreted as a subtype of Wernicke aphasia in which the semantic associations of the words are significantly impaired (see Figure 2.4). Luria himself during a long time was unsure if amnesic aphasia should be regarded an independent aphasia syndrome; or rather, it should be considered simply as a subtype of the sensory aphasia (in addition to the acoustic-agnostic and acoustic-amnesic subtypes). During a long time, Luria referred to six different types of aphasia (e.g., Luria, 1966, 1970) and suggested a seventh one. Only in his later writings (e.g., Luria, 1976) he overtly referred to seven different types of aphasia.

On the Origins of Human Cognition 31

Figure 2.4. Amnesic or nominal or extrasylvian sensory aphasia can be interpreted as a paradigmatic disturbance situated at the level of semantic recognition.

Some other aphasic syndromes can be interpreted as language disturbances due to a more general underlying disorder. For instance, extrasylvian (transcortical) motor aphasia associated with left convexital prefrontal damage could be interpreted as an executive function defect specifically affecting the language use. The ability to actively and appropriately using the language (pragmatics) appears impaired while the phonology, lexicon, semantics, and grammar are preserved. Simply speaking, the question is: should the ability to correctly use language be regarded as a linguistic ability (i.e., cognitive ability) as executive function ability?(i.e., metacognitive ability). It does not seem difficult to argue that the ability to correctly use the language can be interpreted as an executive function and as a metacognitive ability rather than a purely linguistic ability. Some rationales to support this interpretation are: (1) It could be argued that in extrasylvian (transcortical)

On the Origins of Human Cognition 32

motor aphasia there is a defect in verbal initiative rather than in language knowledge (Kleist, 1934). (2) Some authors (Luria, 1976, 1980) have emphasized that this type of aphasia shares the general characteristics of the prefrontal (i.e., dysexecutive) syndrome but specifically with regard to the verbal processes. That means it is the prefrontal (dysexecutive) syndrome affecting the verbal processes. (3) Further, the language defect in extrasylvian (transcortical) motor aphasia does not affect the language understanding, and the fundamental linguistic processes are preserved (Berthier, 1999). And finally, (4) it could be argued that the prefrontal cortex does not participate in basic cognition but in metacognition (e.g., Ardila & Surloff, 2010). Extrasylvian (transcortical) motor aphasia could indeed be referred as dysexecutive aphasia. Some authors have interpreted extrasylvian motor aphasia in a similar way (e.g., Luria, 1976, 1980). Alexander (2006) suggested that transcortical motor aphasia could be more accurately defined as an executive function disorder than as an aphasia. He proposed that the progression of clinical disorders from aphasia to discourse impairments can be interpreted as a sequence of procedural impairments from basic morpho-syntax to elaborated grammar to narrative language, correlated with a progression of the focus of the damage from posterior frontal to polar and/or lateral frontal to medial frontal. Conduction aphasia, on the other hand, usually has been interpreted as a disconnection syndrome (e.g., Damasio & Damasio, 1980; Geschwind, 1965; Wernicke, 1874) usually due to an impairment in the arcuate fasciculus and sporadically in an indirect pathway passing through inferior parietal cortex (Catani et al., 2005) (Figure 2.5). Alternatively, conduction aphasia has also been interpreted as a segmentary ideomotor apraxia (e.g., Ardila & Rosselli, 1990; Brown, 1972, 1975; Luria, 1976, 1980). Usually it is recognized that conduction aphasia has three fundamental and five secondary characteristics; so-called secondary characteristics are frequently but not necessarily found in conduction aphasia (Benson et al., 1973; Benson & Ardila, 1996). The three basic characteristics are: (1) fluent conversational language; (2) almost normal comprehension; (3) significant impairments in repetition. Secondary characteristics include, (1) defects in naming; (2) reading defects; (3) variable writing difficulties (apraxic agraphia);

On the Origins of Human Cognition 33

(4) ideomotor apraxia; (5) neurological abnormalities.

Figure 2.5. Conduction aphasia frequently is interpreted as a disconnection between the Wernickes and Brocas areas, due to an interruption of the arcuate fasciculus.

This description of conduction aphasia clearly recognizes that spontaneous language production and language understanding are significantly preserved. In consequence, some mechanism required for the correct language repetition is abnormal, but the knowledge of the language itself (phonology, lexicon, semantics, and grammar) is not impaired. Should conduction aphasia be interpreted as a primary aphasic syndrome? Obviously, if some animals can repeat, that means that language repetition cannot be considered as a primary

On the Origins of Human Cognition 34

linguistic ability. Bernal and Ardila (2009) pointed out that as a matter of fact the arcuate fasciculus does not connect Wernickes area with Brocas area (BA44), but more exactly with the premotor area (BA6); hence, there is not a direct connection between Wernickes and Brocas area, as illustrated in Figure 2.6.

Figure 2.6. Recent findings suggest that there is not a direct connection between Wernickes and Brocas areas, but there is a relay station located in the precentral gyrus, represented here by the circle labeled BA6, an area with premotor functions (Taken from Bernal & Ardila, 2009).

Conduction aphasia is not really a primary form of aphasia but rather a secondary (or peripheral) defect in language affecting a specific language ability (i.e., the ability to

On the Origins of Human Cognition 35

repeat). The language itself is not impaired, but rather the ability to reproduce the auditory information that is heard aloud is impaired. Of course, this is a most important ability used not only to develop but also to correctly use language (moreover, the correct visualperceptual recognition of the written information is a most important ability required not only for learning to read but also for correctly accessing the written information). Jakobson (1964) suggested a similar distinction when proposed that in aphasia, language could be either disintegrated or just limited (disintegration vs. limitation in aphasia). Obviously, in conduction aphasia language is limited, not really disintegrated. Tabla 2.2. presents the aphasia classification proposed by Ardila (2010). A major distinction in aphasia can be established between primary language disturbances (central aphasias), and secondary language disturbances resulting from peripheral impairments (secondary or peripheral aphasias). Sometimes language is not impaired, but the patient cannot use it appropriately because of executive control impairments (dysexecutive aphasia).

____________________________________________________________________________

Type

Impairment

____________________________________________________________________________

Primary (central) aphasias Wernicke-type aphasia (fluent aphasia)

Language system impaired Phonological level Lexical level Semantic level

Broca-type aphasia (non-fluent aphasia)

Sequencing expressive elements at syntactic and phonetic level

___________________________________________________________________________

On the Origins of Human Cognition 36

Secondary (peripheral) aphasias Conduction aphasia

Mechanisms of production impaired Disconnection (or segmentary ideomotora verbal apraxia)

SMA aphasia

To initiate and maintain voluntary speech production

___________________________________________________________________________

Dysexecutive aphasia

Language executive control impaired

Extra-Sylvian (transcortical) motor aphasia Executive control of language ___________________________________________________________________________

Tabla 2.2. Only two primary aphasic syndromes are recognized: Wernicke-type aphasia (fluent aphasia) and Broca-type aphasia (non-fluent aphasia). Two secondary aphasia syndromes are included (conduction aphasia and aphasia of the supplementary motor area); finally, a dysexecutive (extrasylvian or transcortical motor) aphasia is also included (Ardila, 2010).

Three stages in language development


The question When language began? could be rephrased as the question How language began? Different steps in language development can be proposed, at least: (1) Initial communication systems using sounds and other types of information such

On the Origins of Human Cognition 37

as gestures, etc, similar to the communication systems observed in other animals, including nonhuman primates. (2) Primitive language systems using combined sounds (words) but without a grammar (language as lexical/semantic system). This type of language could be similar to the holophrasic period in language development, observed in children around the age 1 to 1.5 years of age (Hoff, 2003). (3) Communication systems using grammar (language as grammatical system). During childs language development, it is observed that the use of grammar is found after the holophrasic period. It simply means that it is a more advanced and complex stage. By the end of the second year, children begin to combine words into simple sentences. Initially, sentences represent a telegraphic speech (around 24-30 months of age), including twoword utterances in which connecting elements are omitted (e.g., other dog", child eat) (Hoff, 2003). It means, language initially emerges as a system of words (language as a paradigm: lexical/semantic system), and only later as a system of relations among the words (language as a syntagm: grammatical system).

Initial communication systems It is easy to assume that at the beginning of the human language, communication systems were similar to the communication systems found in nonhuman primates. It is known that chimpanzees and other nonhuman primates in natural environments can use some communication strategies. Chimpanzees employ a variety of gestures and facial expressions to communicate and keep in touch with each other. They possess a simple repertoire of noises and postures (body language) that can be used in different contexts with specific

On the Origins of Human Cognition 38

communication purposes. Observations have been collected in different environments, including natural environments and captive groups in human-controlled environments (McCrone, 1991). Chimpanzees make use of simple gestures, make facial expressions and produce a limited amount of vocalizations. Compared to humans, chimps only produce about twelve different vocalizations. In captive conditions and under human training, chimpanzees can learn some artificial languages and close to about 200 words (symbols). Different attempts have been made to teach non human primates to use a more complex communication system. Initially, Hayes and Hayes (1952) trained the chimp Vicki. She became able to produce only four different sounds in six years! (mom," "pa," "cup," and "up"). Other chimps and gorillas have also participated in communication training programs: Nim and Koko used signs; Sara used plastic chips; Lana, Sherman, and Austion manipulated combinations of buttons to communicate (Gardner & Garner, 1979; Limber 1982; Patterson & Linden, 1981). Regardless of the relatively large amount of meaningful elements that chimpanzees can learn, they fail in developing sequencing of elements (grammar). Kanzi learned to use around 200 symbols on a portable electronic symbol board. While chimpanzees can learn to order their symbols to get what they want, it is not clear that they have mastered syntax (Mitani, 1995; Savage-Rumbaugh & Lewin, 1994). The reason is that when they initiate communication, they often abandon the order of phrases they have learned and the order is rather random. There have been occasional reports of chimpanzees signing new combinations of words in response to new situations. Washoe, for example, once was in a boat on a pond when she encountered her first duck. She signed 'water bird' (Terrace, 1979). This could be a new compound noun or it could be two separate responses to the water and a bird. But between two nouns, there is not a grammatical relationship and hence no grammar is involved in 'water bird'. In conclusion, there is not convincing evidence that chimpanzees and other nonhuman primates can learn language syntax (language as syntagm) even after intensive and controlled training.

On the Origins of Human Cognition 39

The question becomes how can this type of simple communication system found in subhuman primates in natural conditions (i.e., to use some few vocalizations, gestures and facial expressions) be further developed into contemporary human language? Certain mechanisms potentially could be used; e.g., words can be created departing from onomatomepias, emotional expressions, etc. Indeed, a diversity of mechanisms has been proposed throughout history to account how human words emerged. It means that different strategies could potentially be useful to create words. This is an ability that is not found in nonhuman primates. Using these strategies certainly requires a brain notoriously more advanced than the chimpanzees brain. During the 19th century different hypotheses were presented in an attempt to explain the origin of language from the lexical point of view. Jespersen (1922) referred to such hypotheses using some unusual names as a way of deriding the hypotheses as simplistic speculation. However, these names became popular and they have been used even in contemporary literature. Some hypotheses are (Yule, 1996): 1. Language began as imitations of natural sounds. It means that words are created departing from onomatopoeias (bow-wow hypothesis). 2. Language began with interjections, emotive cries, and emotional expressions (Pooh-pooh hypothesis). 3. Gestures are at the origin of language, and body movement preceded language. Oral language represents the use of oral gestures that began in imitation of hand gestures that were already in use for communication (ta-ta hypothesis). Recently, Corballis (2002) has argued that gestures represent the most important element in creating human language. 4. Language arose in rhythmic chants and vocalisms uttered by people engaged in

On the Origins of Human Cognition 40

communal labor. Language began as rhythmic chants, perhaps ultimately from the grunts of heavy work or related with assistance or cooperation accompanied by appropriate gestures (Yo-he-ho hypothesis). 5. Language began with the easiest syllables attached to the most significant objects (mama hypothesis). 6. It has been pointed out that there is a certain correspondence between sounds and meanings. Small, sharp, high things tend to have words with high front vowels in many languages, while big, round, low things tend to have round back vowels. This is often referred to as phonetic symbolism (ding-dong hypothesis). 7. It has been also suggested that language comes out of play, laughter, cooing, courtship, emotional mutterings and the like (The sing-song hypothesis) 8. Considering that there is a need for interpersonal contact, language may have began as sounds to signal both identity (here I am!) and belonging (Im with you!) (contact theory) (hey you hypothesis). All these hypotheses may be partially true, and all these factors may have contributed to the creation of new words. As a matter of fact, these hypotheses attempt to explain how the initial communication systems (observed in nonhuman primates) evolved to the second stage in language evolution: the development of a lexical system, which potentially can be transmitted to offspring. But they do not account for the development of grammar. These mechanisms for creating new words continue being useful in the contemporary world. For instance, onomatopeias continue representing a mechanism in the creation of new words (e.g., the ping-pong game). The phonetic symbolism is particularly useful in the creation of adjectives (qualities of the objects).

On the Origins of Human Cognition 41

The function of noises (grunts) in human communication No mention about the function of noises (grunts) in human everyday communication is readily available. As noted above, noises represent a basic communication strategy in chimpanzees, and noises have continued playing a communication function throughout human history. It is evident that people in everyday life use a diversity of noises to say yes, no, to express different emotions, to communicate with animals (e.g., come here, go away), etc. These noises are close to interjections, and sometimes become real interjections (e.g., ooph!). Even though there is not a dictionary of noises, the author of this paper has been able to identify over 30 different noises commonly used in contemporary Spanish language. Some of these noises seem understandable by speakers of other languages, but others seem idiosyncratic of Spanish-speaking people.

Second stage: Lexical/semantic Bickerton (1990) developed the idea that a protolanguage must have preceded the fullfledged syntax of todays discourse. Echoes of this protolanguage can be seen, he argued, (1) in pidgin languages, (2) in the first words of infants, (3) in the symbols used by trained chimpanzees, and (4) in the syntax free utterances of children who do not learn to speak at the normal age. Bickerton (2009) considers that such a protolanguage existed already in the earliest Homo (about 2.3 to 2.4 million years), and was developed due to the pressure of the behavioral adaptations faced by Homo habilis (2.3 to 1.4 million years ago). What made up these original words? Again, the analogy with the childs initial vocabulary can be taken. (1) They were articulatory easiest to produce, most likely using those phonemes regarded as universal (e.g., /p/, /a/). (2) They contained a simple syllable

On the Origins of Human Cognition 42

structure (consonant-vowel) that may have been repeated (e.g., papapa). In this regard, they were similar to the infantile words. (3) They were mostly nouns (real objects) even though they obviously did not have a grammatical category. To move from grunts, onomatopoeias, and emotional expression to words requires the progressive development of a series of oppositions. According to Jacobson (1968) the most basic one is the opposition between vowels and consonants. The second most important one is between oral and nasal articulations. But the production of these oppositions requires some anatomical adaptations. Human articulatory ability has been related to the specific position and configuration of the larynx. The human larynx descends during infancy and the early juvenile periods, and this greatly contributes to the morphological foundations of speech development. This developmental phenomenon is frequently believed to be unique to humans. However, Nishimura (2003; Nishimura et al., 2005) demonstrated that chimpanzees larynges also descend during infancy, as in human infants. This descent was completed primarily through the rapid descent of the laryngeal skeleton relative to the hyoid, but it was not accompanied by the descent of the hyoid itself. The descent is possibly associated with developmental changes of the swallowing mechanism. Moreover, it contributes physically to an increased independence between the processes of phonation and articulation for vocalization. Thus, the descent of the larynx and the morphological foundations for speech production must have evolved in part during hominoid evolution and not in a single shift during human evolution. Several authors have attempted to find universal language characteristics, and even to reconstruct extinct languages (e.g., Greenberg, 1978; Hagge, 1982 ; Van den Berghe 1979) such as the Indo-European (Anderson, 1973; Lehmann, 1974; Martinet, 1975; Shevoroshkin, 1990), whose last speaker passed away over 10,000 years ago. Furthermore, examples of which ones could have been the initial words in human language have been proposed. Swadesh (1971) refers to the communality existing in some words across the world. Although we cannot be sure which were the initial words used by humans, there are clues about the initial meaning sounds and approximately, how the initial

On the Origins of Human Cognition 43

words may have been formed.

Third stage: Grammar What was the crucial leap for the development of grammar? (i.e., syntagmatic dimension of the language). Obviously grammar was initially simple, and sentences contained only two words. How to link two words to create new higher level unit (syntagm)? Further, how to mark the relationship between the two words? The mechanism has to be the simplest one, and it is not unlikely that it may be similar to the mechanism observed in children during language development. Suppose that we have two lexical units: -animal - fruit Different relations between these two words can exist; but the relationship requires an action (verb); it means that there is an interaction between both elements: animal eats fruit; animal has fruit, animal receives fruit; animal likes fruit, etc. In consequence, before creating a syntagmatic relationship between the words, different word categories have to be separated (e.g., objects and actions). According to the Swadesh word list (1952, 1967), the following categories are found across different languages, and may represent the initial word categories: (1) Grammatical words (e.g., I/me), (2) Quantifiers (e.g., All), (3) Adjectives (e.g., Big), (4) Human distinctions (e.g., person), (5) Animals (e.g., fish), (6) High frequency elements (e.g., tree), (7) Body parts (e.g., hair), (8) Actions (e.g., drink), (9) Natural phenomena (e.g., sun), and (10) Colors (e.g., red). For creating a phrase, only two types of elements are really required: nouns (nominal phrase) and verbs (verbal phrase). When putting together two words corresponding to two different classes (e.g., animal sleep), there is already a syntagm and grammar that has appeared. In childhood language it is observed that words corresponding

On the Origins of Human Cognition 44

to two different classes are combined such as, big dog, food good, dad gone. They contain a grammar because the words belong to two different classes. In the first two examples, there is an existence verb (to be) that is omitted (as currently observed in some contemporary languages, such as Russian). Mom dad is not a phrase, but mom big is a primitive sentence. Brown (1973) found that the majority of the utterances at the beginning of the childs grammar could be described by a small set of functional relationships between words:

1. 2. 3. 4. 5. 6. 7. 8.

'agent + action' baby kiss 'action + object' pull car 'agent + object' daddy ball 'action + location' sit chair 'object + location' cup table 'possessor + possession' mommy sock 'object + attribute' car red 'demonstrative + object' there car

So, the crucial point in emerging grammar is not the extension of the vocabulary. What really is crucial is to have words corresponding to different classes that can be combined to form a higher level unit (syntagm). One of the words has to be a noun; the other usually is a verb. Hence, the problem becomes how do verbs appear? Creating nouns does not seem so complicated using the hypothesis mentioned above (e.g., nouns can be created departing from onomatopoeias, etc). Verbs, on the other hand, can be created departing

On the Origins of Human Cognition 45

from the nouns, but with the meaning of an action (e.g., baby kiss). Action usually means moving, doing, executing, not simply perceiving and associating with some visual (or auditory or tactile) information. Kiss can be associated with some sensory information, and obviously the temporal, parietal and occipital brain areas have to participate (kiss as a noun). Kiss can also be associated with an action, and obviously the frontal areas have to be involved in this second type of association (kiss as a verb).

Brain representation of nouns and verbs


It has been observed that choosing verbs and nouns clearly depends on different brain area activity, and naming objects and actions are disrupted in cases of different type of brain pathology. While speaking or thinking in nouns increased activity is observed in the temporal lobe, while speaking or thinking verbs activates the Broca frontal area (Raichle, 1994). By the same token, impairments in finding nouns are associated with temporal lobe pathology, whereas impairments in finding verbs is associated with left frontal damage and Broca aphasia (Ardila & Rosselli, 1994; Damasio & Tranel, 1993) Naming actions activates the left frontal operculum roughly corresponding to the Brocas area (Damasio et al., 2001). The neural correlates of naming concrete entities such as tools (with nouns) and naming actions (with verbs) are partially distinct: the former are linked to the left inferotemporal region, whereas the latter are linked to the left frontal opercular and left posterior middle temporal regions (Tranel et al., 2005). Furthermore, the pattern of brain activation when processing verbs seems similar across languages, at least in Spanish/English bilinguals (Willms et al., 2011). However, understanding action verbs does not rely on early modality-specific visual or motor circuits. Instead, word comprehension relies on a network of amodal brain regions in the left frontal, temporal, and parietal cortices that represent conceptual and grammatical properties of words (Bedny & Caramazza, 2011). Supposedly, interactions between word meanings and sensory-motor

On the Origins of Human Cognition 46

experiences occur in higher-order polymodal brain regions.

Memory systems for nouns and verbs


Two major memory systems are frequently distinguished in contemporary memory literature: declarative memory (divided into semantic and episodic or experiential) and procedural memory (Tulving et al., 2004). It has been suggested that the lexical/semantic and grammar aspects of the language are subserved by different neuroanatomic brain circuitries and depend upon these two different memory systems (Fabbro, 1999, 2001; Paradis, 2004; Ullman, 2001; 2004). Whereas lexical/semantic aspects of the language depend on a declarative semantic memory (knowledge about the meaning of the words), grammar depends on a procedural memory. The lexical/semantic aspect of the language is explicitly learned and represents a type of knowledge we are aware of (declarative memory). It depends on retro-rolandic cortical structures and the hippocampus. Grammar (language sequences, contiguity) is acquired incidentally. Procedural memory for grammar supposes implicit language knowledge. Procedural grammatical learning is related to the execution of sequences of elements (skilled articulatory acts and grammar) used for speaking but also for syntax. Procedural memory is related with frontal/subcortical circuitries (Tulving et al., 2004).

Using verbs and using grammar is a single ability


Brocas area damage results in a defect in grammar and also in an inability to find verbs. In consequence, brain representation of actions and brain representation of grammar is coincidental. Using verbs and using grammar depends upon the very same type of brain activity and both are simultaneously disrupted in cases of Broca aphasia. It can be conjectured that verbs and grammar appeared almost simultaneously in human language;

On the Origins of Human Cognition 47

or rather, they are the two sides of the same medal. Furthermore, grammar is associated with oral praxis skills (i.e., agrammatism and apraxia of speech appear simultaneously in Broca aphasia), and hence, all three have to appear simultaneously in the evolution of human language: using verbs, using grammar, and rapidly sequencing movements with the articulatory organs. However, there is a departing condition for using verbs, namely, the ability to internally represent actions. That is, to interiorize the actions. The obvious question is: can Broca aphasia patients internally represent actions? Although specific research on this question is not readily available, the answer seems to be no. Some observations point to a deficit in internally representing actions in Broca aphasia. For example, Ardila and Rossellis (1994) patient had to make the concrete action to retrieve the corresponding verb. Thence, the internal representation of actions and understanding/using verbs seems to be closely related abilities.

Understanding Brocas area


In the last decade there has been a significant interest in re-analyzing the function of Brocas area (e.g., Grodzinsky & Amunts, 2006; Hagoort, 2005; Thompson-Schill, 2005). So-called Brocas area includes the pars opercularis (Brodmanns area- BA- 44) and probably the pars triangularis (BA45) of the inferior frontal gyrus (Foundas, 1998) (see Figure 2.7). BA45 probably is more cognitive than BA44, which seems to be more motor, more phonetic. From the traditional point of view, Brocas area corresponds to BA44, but several contemporary authors also include BA45. In the traditional aphasia literature it was assumed that damage in the Brocas area was responsible for the clinical manifestations observed in Brocas aphasia. Only with the introduction of the CT scan did it become evident that the damage restricted to the Brocas area was not enough to produce the classical Brocas aphasia; extension to the insula, lower motor cortex, and subjacent

On the Origins of Human Cognition 48

subcortical and periventricular white matter is also required (Alexander et al., 1990). Brocas area aphasia (minor Brocas aphasia) is characterized by mildly non-fluent speech, relatively short sentences and mild agrammatism; phonetic deviations and a few phonological paraphasias can be observed (Mohr, et al., 1978); some foreign accent can also be noticed (Ardila et., 1988). Interestingly, electrical stimulation of Broca's area enhances implicit learning of an artificial grammar (de Vries et al., 2010) and can also modulate naming skills (Fecteau et al., 2011) and is active during speech perception (Vaden et al., 2011).

Figure 2.7. Map illustrating the Brodmanns areas (BA).

Simultaneously including both BA44 and BA45 in Brocas area is problematic. BA 44 is a premotor dysgranular area, whereas BA45 has a granular layer IV and belongs to the heteromodal prefrontal lobe (granular cortex) (Mesulam, 2002). So, from a cytoarchitectonic point of view, BA 44 and BA 45 are quite different. BA 44 is a premotor

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area whereas BA 45 corresponds to the prefrontal cortex. From the aphasia perspective, some authors have referred to different clinical manifestations associated with damage in BA 44 (Broca-type aphasia) and BA 45 (transcortical motor/dynamic aphasia) (e.g., Luria, 1976). Brocas area is, more than likely, involved in different language and language related functions (Fink et al., 2006). Some authors have pointed out that indeed Brocas area is a collective term that can be fractionated in different sub-areas (Lindenberg et al., 2007). Hagoort (2005, 2006) refers to the Brocas complex, including BA44 (premotor), and also BA45 and BA47 (prefrontal cortex). He argues that Brocas complex is not a languagespecific area, and it becomes active during some nonlanguage activities, such as mental imagery of grasping movements (Decety et al., 2004). Functional defined sub-regions could be distinguished in the Brocas complex: BA47 and BA45 are involved in semantic processing, BA44, BA45, and BA46 participate in syntactic processing, and BA44 is involved in phonological processing (Heim et al., 2008; Sahin et al., 2009). Hagoort (2005) proposes that the common denominator of the Brocas complex is its role in selection and unification operations by which individual pieces of lexical information are bound together into representational structures spanning multiword utterances (p. 166). Its core function is, consequently, binding the elements of the language. Thompson-Schill (2005) analyzed the different deficits observed in cases of damage in the Brocas area: articulation, syntax, selection, and verbal working memory, suggesting that there may be more than a single function of Brocas area. Thompson-Schill (2005) analyzed the different deficits observed in cases of damage in the Brocas area: articulation, syntax, selection, and verbal working memory, suggesting that there may be more than a single function of Brocas area. The author proposes a framework for describing the deficits observed in different patients. The proposed framework suggests that Brocas area may be involved in selecting information among competing sources. Fadiga et al. (2006) speculates that the original role played by Brocas area relates to generating/extracting action meanings; that is, organizing/ interpreting the sequence of individual meaningless movements. Ardila and Bernal (2007) conjectured that

On the Origins of Human Cognition 50

the central role of Brocas area was related to sequencing motor/expressive elements. Novick et al. (2005) consider that the role of Brocas area is related with a general cognitive control mechanism for the syntactic processing of sentences. Grodzinsky (2000, 2006) has presented an extensive analysis of the role of Brocas area. He proposed that most syntax is not located in Brocas area and its vicinity (operculum, insula, and subjacent white matter). This brain area does have a role in syntactic processing, but a highly specific one: it is the neural home to receptive mechanisms involved in the computation of the relation between transformationally moved phrasal constituents and their extraction sites (syntactic movement). He further assumes that Brocas area is also involved in the construction of higher parts of the syntactic tree in speech production. Interestingly, blood flow in Brocas area increases when participants process complex syntax (Caplan et al., 2000). Santi and Grodzinsky (2007) also recognize its role in working memory related with a specific syntactic role in processing fillergaps dependency relations. Syntax is indeed neurologically segregated, and its components are housed in several distinct cerebral locations, far beyond the traditional ones (Brocas and Wernickes regions). A new brain map for syntax would also include portions of the right cerebral hemisphere (Grodzinsky & Friederici, 2006). Haverkort (2005) emphasizes that a clear distinction should be established between linguistic knowledge and linguistic use. Patients with Brocas aphasia have a limitation in the use of grammar, but their grammatical knowledge is available. Brocas aphasia patients present a simplified syntax and phrases are usually short. They select simpler syntactic structures that are less complex because they impose a lesser burden on working memory. In consequence, one major factor in Brocas aphasia relates to impairment in verbal working memory. In summary, regardless that expressive language disturbances have been associated for over a century with damage in the left inferior frontal gyrus (later known as Brocas area), currently there is incomplete agreement about its limits and its specific

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functions in language. Different proposals have been presented to explain language disturbances in so-called Brocas aphasia, as summarized in Table 2.3.

_______________________________________________________________________________

Function

Reference

_______________________________________________________________________________ Binding the elements of the language Selecting information among competing sources Generating/extracting action meanings Sequencing motor/expressive elements Cognitive control mechanism for syntactic processing sentences Construction higher parts syntactic tree in speech production Verbal working memory Haverkort, 2005 Thompson-Schill, 2005 Fadiga et al., 2006 Ardila & Bernal, 2007 Novick et al., 2005 Grodzinsky, 2000, 2006 Haverkort, 2005

_______________________________________________________________________________

Table 2.3. Different proposals about the role of Brocas area.

As emphasized above, language activity depends on two discrete brain areas (socalled Wernickes and Brocas areas). Damage in these two brain regions results in disturbances in language as a paradigm (similarity: selection; lexical/semantic system) and syntagm (contiguity: combination; grammatical system). At what moment in human history did the first and the second aspect of language emerge? There is not a simple answer, but obviously language as a lexical/semantic system appeared before language as a grammatical system. Pre-human communication systems continue playing a role in contemporary human communication. Onomatopoeias continue representing a source for the creation of new words. Noises and gestures are actively used nowadays in everyday communication.

On the Origins of Human Cognition 52

Origins of the lexical/semantic system


Paleoneurology (study and analysis of fossil endocasts) can also significantly contribute to the understanding of the origins of the language. How did the brain areas participating in human lexical/semantic knowledge (i.e., temporal lobes) evolve? In monkeys, the temporal lobes are involved in recognizing the sounds and calls of their own species (Rauschecker et al., 1995; Taglialatela et al., 2009; Wang et al., 1995; Wollberg & Newman, 1972), and obviously the temporal lobe was a crucial area in developing a complex lexical/semantic system. Gannon et al (1998) observed that the anatomic pattern and left hemisphere size predominance of the planum temporale, a language area of the human brain, are also present in chimpanzees. They found that the left planum temporale was significantly larger in 94 percent of chimpanzee brains examined. Hence, the crucial lexical/semantic difference between humans and chimpanzees cannot be related to the planum temporale. By the same token, it has been observed that anatomical temporal lobe asymmetries favoring the left hemisphere are found in several Old and New world monkey species (Heilbroner & Halloway, 1988). Development of a human lexical/semantic communication system cannot be related with the temporal lobe asymmetry, because this asymmetry was observed long before the beginning of the human language. Hopkins and Nir (2010) examined whether chimpanzees show asymmetries in the planum temporale for grey matter volume and surface area in a sample of 103 chimpanzees from magnetic resonance images. The results indicated that, overall, the chimpanzees showed population-level leftward asymmetries for both surface area and grey matter volumes. Furthermore, chimpanzees that prefer to gesture with their right-hand had significantly greater leftward grey matter asymmetries compared to ambiguously- and lefthanded apes. Development of a human lexical/semantic communication system in

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consequence cannot be related to the temporal lobe asymmetry, because this asymmetry is observed long before the beginning of the human language. This asymmetry seems to be related with a left temporal lobe specialization for intra-specific communication system. Spocter et al. (2010) affirm that leftward asymmetry of Wernicke's area originated prior to the appearance of modern human language and before our divergence from the last common ancestor. Nonetheless, differences can be related with the temporal lobe volume. Rilling et al. (2002) analyzed the volume of the temporal lobe in different primates. Whole brain, T1weighted MRI scans were collected from 44 living anthropoid primates spanning 11 species. The surface areas of both the entire temporal lobe and the superior temporal gyrus were also measured, as was temporal cortical gyrification. Allometric regressions of temporal lobe structures on brain volume consistently showed apes and monkeys to scale along different trajectories, with the monkeys typically lying at a higher elevation than the apes. Within the temporal lobe, overall volume, surface area, and white matter volume were significantly larger in humans than predicted by the ape regression lines. The largest departure from allometry in humans was for the temporal lobe white matter volume which, in addition to being significantly larger than predicted for brain size, was also significantly larger than predicted for temporal lobe volume. Among the nonhuman primate sample, Cebus have small temporal lobes for their brain size, and Macaca and Papio have large superior temporal gyri for their brain size. The observed departures from allometry might reflect neurobiological adaptations supporting species-specific communication in both humans and old world monkeys. The authors concluded that the entire human temporal lobe and some of its component structures are significantly larger than predicted for a primate brain of human size. The most dramatic allometric departure is in the volume of the human temporal lobe white matter, which, in addition to being large relative to brain size, is also large relative to temporal lobe size. These allometric departures in humans could reflect a reorganization of the temporal lobes driven by expansion of the language cortex and its associated connections. In primates it is interesting to note that the superior temporal gyrus contains neurons tuned to species specific calls, and the magnitude of

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different species residuals might relate to the repertoire of vocal communicative signals as reflections of the complexity of their respective social environments. It has been calculated that this enlargement of the temporal lobe occurred some 200-300 thousand years ago (Kochetkova, 1973). Consequently, it can be conjectured that hominids existing before the contemporary Cro-Magnon Homo sapiens could have developed a certain complex lexical/semantic communication system. For instance, it could be speculated that Nearthental man could have had a language relatively complex as a lexical/semantic system. Brain organization of the lexicon seems to be related with the type of association between words and perceptions. When the word is associated with own-body information, brain representation of the lexicon seems associated with a parietal extension (e.g., bodyparts names); when the word has just a visual association, an occipital extension is found (Roux et al., 2006)

Origins of the grammatical system


Departing from the above observations, it can be speculated that grammar, speech praxis movements, and using verbs appeared roughly simultaneously in human history. In other words, they are strongly interrelated and depend upon a common neural activity. Recently, a milestone observation was made that significantly enlightened our understanding about the origin of language in general and grammar in particular. In England a family, usually referred as the KE family, was found. In over three generations of this family, about half the family members had presented a significant disturbance in language development. Speech was largely unintelligible, and they were taught sign language as a supplement to speech as children. Affected members presented severe disturbances in articulation and other linguistic skills along with broader intellectual and physical problems. From the genetic point of view the disorder was associated with a

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mutation in a single autosomal-dominant gene, FOXP2, located in the chromosome 7 (Vargha-Khadem et al., 1995). The disorder was not restricted to speech and also included the following characteristics: defects in processing words according to grammatical rules; understanding of more complex sentence structure such as sentences with embedded relative clauses; inability to form intelligible speech; defects in the ability to move the mouth and face not associated with speaking (relative immobility of the lower face and mouth, particularly the upper lip); and significantly reduced IQ in the affected compared with the unaffected in both the verbal and the non-verbal domain. Further, affected family members presented a pronounced developmental verbal dyspraxia. The authors refer to the core deficit as one involving sequential articulation and orofacial praxis (Takahashi & Liu, 2009; Vernes et al., 2006; Vargha-Khadem et al., 1998). PET studies revealed functional abnormalities in both cortical and subcortical motor-related areas of the frontal lobe, while quantitative analyses of MRIs revealed structural abnormalities in several of these same areas, particularly the caudate nucleus, which was found to be abnormally small bilaterally. An abnormal gene (SPCH1) in the chromosomal band 7q31 was localized. The genetic mutation or deletion in this region was proposed to result in marked disruption of speech and expressive language, including grammar (Fisher et al., 1998). Enard et al. (2002) analyzed the evolution of the chromosome FOXP2. They noted the extremely conservative nature of FOXP2. The mouse FOXP2 differs in just one amino acid from chimpanzee, gorilla and rhesus monkey. However, human FOXP2 differs from gorilla, chimp and rhesus macaque in two further amino acids (and thus differs from mouse in three amino acids out of 715). So, in 75 million years since the divergence of mouse and chimpanzee lineages only one change occurred in FOXP2, whilst in the six million years since the divergence of man and chimpanzee lineages two changes have occurred in the human lineage. The authors estimated that the last two mutations occurred between 10,000 and 100,000 years ago and speculated that the mutations have been critical for the development of contemporary human speech. This genetic approach to the origins of language seems particularly important in

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understanding the appearance and evolution of language in humans (Scharff & Petri, 2011; Tanabe et al., 2011). It has been pointed out that FOXP2 could have contributed to the evolution of human speech and language by adapting cortico-basal ganglia circuits (Enard, 2011). Although Foxp2 is expressed in many brain regions and has multiple roles during mammalian development, the evolutionary changes that occurred in the protein in human ancestors specifically affect brain regions that are connected via cortico-basal ganglia circuits (Reimers-Kipping et al., 2011).

Grammar at the origin of the executive functions


So-called executive functions represent one of the most intensively studied neuroscience questions during the last decade (e.g., Garcia-Molina et al., 2010; Koechlin et al., 2003; Miller & Cohen, 2001; Stuss & Knight, 2002; Stuss & Levine, 2002). Disagreement persists, however, around the potential unitary factor in executive functions (Mikaye et al., 2000; Stuss & Alexander, 2007). Ardila (2008) emphasized that action representation (i.e., internally representing movements or actions) may constitute at least one basic executive function factor. It could be speculated that action representation and also time perception (potentially derived from action representation) may depend upon one single core ability (sequencing?). Two departing observations are important to support the involvement of prefrontal cortex in motor representation: (a) Anatomical observation. Prefrontal cortex represents an extension and further evolution of the frontal motor areas (Miller &. Cummings, 2007; Risberg, 2006). It may be conjectured that the prefrontal lobe should participate in complex and elaborated motor (executive) activities.

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(b) Clinical observation. A diversity of motor control disturbances are observed in prefrontal pathology, such as perseveration, utilization behavior, paratonia, primitive reflexes, etc. (e.g., Ardila & Rosselli, 2007; Victor & Ropper, 2001). Throughout recent history several authors have argued that thought, reasoning, and other forms of complex cognition (metacognition) depend on an internalization of actions. Vygotsky (1929, 1934/1962, 1934/1978) for instance, proposed that thought (and in general, complex cognitive processes) is associated with some inner speech. Vygotsky represents the most classical author suggesting this interpretation for complex cognition. More recently, Lieberman (2002a,b) suggested that language in particular and cognition in general arise from complex sequences of motor activities. The central point in Vygotskys (1934/1962) idea is that higher forms of cognition (cognitive executive functions) depend on certain mediation (language, writing or any other); the instruments used for mediating these complex cognitive processes are culturally developed. According to Vygotsky (1934/1962) the invention (or discovery) of these instruments will result in a new type of evolution (cultural evolution), not requiring any further biological changes. Thinking is interpreted as a covert motor activity (inner speech). Vocalization becomes unnecessary because the child thinks the words instead of pronouncing them. Inner speech is for oneself, while external social speech is for others. In brief, Vygotsky (1934/1978) argued that complex psychological processes (metacognitive executive functions) derives from language internalization. Thinking relies in the development of an instrument (language or any other) that represents a cultural product. Lieberman (2002a,b) refers specifically to the origins of language. He postulates that neural circuits linking activity in anatomically segregated populations of neurons in subcortical structures and the neocortex throughout the human brain regulate complex behaviors such as walking, talking, and comprehending the meaning of sentences. The neural substrate that regulates motor control (basal ganglia, cerebellum, and frontal cortex) in the common ancestor of apes and humans most likely was modified to enhance cognitive

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and linguistic ability. The cerebellum and prefrontal cortex are also involved in learning motor acts (e.g., Matsumura et al., 2004; Hernandez-Mueller et al., 2005). Lieberman (2002a,b) proposes that the frontal regions of the cortex are implicated in virtually all cognitive acts and the acquisition of cognitive criteria; posterior cortical regions are clearly active elements of the brains dictionary. Real-word knowledge appears to reflect stored conceptual knowledge in regions of the brain traditionally associated with visual perception and motor control. Some aspects of human linguistic ability, such as the basic conceptual structure of words and simple syntax, are phylogenetically primitive and most likely were present in the earliest hominids. Lieberman (2002a,b) further suggests that speech production, complex syntax, and a large vocabulary developed in the course of hominid evolution, and Homo erectus most likely talked, had large vocabularies, and commanded fairly complex syntax. These two authors (Vygotsky and Lieberman), although using rather different approaches, have both postulated that the development of language and complex cognition are related with some motor programs, sequencing, internalizing actions, and the like. Many other authors have presented a similar point of view (e.g., (Hommel et al., 2001; Jeannerod, 1997; Luria, 1969; Morsella et al., 2009; Prinz, 1999). Some contemporary research seems to support this interpretation; for instance, Clerget et al. (2009) using transcranial magnetic stimulation to interfere transiently with the function of left BA44 in healthy individuals found that a virtual lesion of left BA44 impairs individual performance only for biological actions, and more specifically for object-oriented syntactic actions. The authors concluded that these finding provide evidence that Broca's area plays a crucial role in encoding complex human movements, a process which may be crucial for understanding and/or programming actions. The recent discovery of mirror neurons (Di Pellegrino et al., 1992; Rizzolatti & Arbib, 1998; Rizzolatti et al., 1996) could significantly contribute to the understanding of the brain organization for verbs. A mirror neuron is a neuron which fires both when an animal performs an action and also when the animal observes the same action performed by another animal. Mirror neurons were initially observed in monkeys (Di Pellegrino et al.,

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1992), but in humans, brain activity consistent with mirror neurons has been found in the premotor cortex and the inferior parietal cortex (Rizzolatti et al., 1996; Rizzolatti & Craighero, 2004). These neurons (mirror neurons) appear to represent a system that matches observed events to similar, internally generated actions. Transcranial magnetic stimulation and positron emission tomography (PET) experiments suggest that a mirror system for gesture recognition indeed exists in humans and includes Brocas area (Rizzolatti & Arbib, 1998). The discovery of mirror neurons in Brocas area might have important consequences for understanding brain language organization and language evolution (Arbib, 2006; Craighero et al., 2007). An obvious implication of mirror neurons is that they can participate in the internal representation of actions, and the internal representation of actions may represent the origin of grammar. Neuroimaging data have shown that interactions involving Brocas area and other cortical areas are weakest when listening to spoken language accompanied by meaningful speechassociated gestures (hence, reducing semantic ambiguity), and strongest when spoken language is accompanied by self-grooming hand movements or by no hand movements at all, suggesting that Brocas area may be involved in action recognition (Skipper et al., 2007). PET studies have associated the neural correlates of inner speech with activity of Brocas area (McGuire et al., 1996). De Zubicaray et al. (2010) emphasize the importance of Brocas area to covert verbalization. Clerget et al. (2009) using transcranial magnetic stimulation to interfere transiently with the function of left BA44 in healthy individuals found that a virtual lesion of left BA44 impairs individual performance only for biological actions, and more specifically for object-oriented syntactic actions. The authors concluded that these finding provide evidence that Broca's area plays a crucial role in encoding complex human movements, a process which may be crucial for understanding and/or programming actions. Conversely, left BA 44 plays a role in motor sequence learning (Clerget et al., 2011). In brief, there is some converging evidence that something like action representation may constitute the departing point for both grammar and executive functions.

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Conclusions
Aphasia can contribute to the understanding of human language evolution. According to contemporary aphasia knowledge, in cases of brain pathology, language can be disturbed in two rather different ways: as a lexical/semantic system (Wernicke-type aphasia) and as a grammatical system (Broca-type aphasia). Both language systems not only depend upon different brain areas (temporal and frontal), but also upon different types of learning (declarative and procedural) supported by different neuroanatomical circuitries. Observations with childrens language development and experiments with nonhuman primates demonstrate that language initially appears as a lexical/semantic system. Grammar is correlated with the ability to represent and use actions. This is an ability that depends on the so-called Brocas area and related brain circuits. But this ability also depends, is correlated, and likely appeared simultaneously in human history with the ability to rapidly sequence articulatory movements (speech praxis). While the lexical/semantic language system may have appeared during human evolution long before the contemporary man, the grammatical language system probably represents a relatively recent acquisition. Language grammar may be the departing ability for the development of the metacognitive executive functions and is probably based in the ability to internally represent actions.

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3. Origins of Spatial Abilities

Introduction
Contemporary city life, in which direct orientation in space has been replaced by the logical application of mathematical coordinates, represents not just a recent cultural acquisition, but also, it is found only in some contemporary human groups. For a very long time, education consisted of learning how to get oriented in the space, how to recognize the relevant signals to follow prey, and how to move in the surrounding environment. This, of course, is still valid for contemporary people living in the Amazonian jungle, for Eskimos, for desert inhabitants, and many other world inhabitants. For thousands (and even millions) of years, mans survival depended on the correct interpretation of spatial signals, memory of places, calculation of distances, and so forth, and his brain must have become adapted precisely to handle this type of spatial information (Ardila & Ostrosky, 1984). Paleolithic (prehistorical era characterized by the development of the first stone tools) extended since about 2,500,000 years (first hominids using stone tools) until some 10,000 years ago (Childe, 1936; Hours, 1982; Toth & Schick, 2007). About this time, agriculture appeared, and man began to domesticate and raise some animals. This produced a tremendous change in his way of life (the Neolithic Revolution). Paleolithic represents in consequence about 99% of human technology history. That means, for about 99% of history, humans were nomads, and the correct spatial orientation represented the most crucial ability for surviving. It could be conjectured that biological adaptation was accomplished to survive under those conditions existing during the Paleolithic time. Recent mans evolution corresponds in

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a significant extent to a cultural type of evolution, not necessarily requiring further overt biological changes. Agriculture replaced fruit collection; domestication of animals replaced hunting; written language extended oral language; arithmetic extended finger counting; and the use of maps and logical spatial coordinates replaced the direct orientation in space (Vygotsky, 1962). There is evidence that Australopitecus africanus (probably the direct ancestor of Homo) lived on open savannas. Although his ancestors lived in forests, he moved to live in open fields (Lee & DeVore, 1968; Wilson, 1975). He strongly depended on animal food, especially small preys (tortoises, lizards, snakes, rabbits) and fruit collecting. Homo sapiens appeared in Europe about 50,000 years ago (middle Paleolithic), and it is supposed that he hunted, usually small but also big prey, used rudimentary stone tools (knives, axes), and lived in caverns or rudimentary shelters built with tree branches. He was a nomad and he had to be moving from one place to another all the time while looking for prey, fruits, and shelter. He created some hunting weapons like the arrow and the spear, and used fire (Washburn, 1978; Hours, 1982; Boyd & Silk, 2003). It could be supposed that spatial abilities were even more crucial for survival in prehistorical than in contemporary man. Survival in current urban living conditions somehow requires different cognitive abilities. We go around in our cities using logical-mathematical coordinates, reading a printed-on-a-paper map, without taking into consideration the sun position in the sky, or avoiding potential predators. Adaptation to contemporary world conditions requires more verbally-based abilities. If the question "What moon-phase is today?" (instead of "What date is today?") was included in a mental state examination, it is very likely the majority of city people would probably fail. By the same token, city people usually ignore the exact sunrise and sunset points (they usually respond "East and West"), but sunrise and sunset points change a little every day, and it could have been an important piece of information for prehistorical man's survival, as it is for contemporary man to know that "Today is May 6th, 2011." Furthermore, our current educational system strongly emphasizes verbal, logical, and mathematical abilities, not spatial orientation abilities. Of course, those are currently the most useful abilities to live in

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our contemporary world. Generally speaking, city people have limited opportunities to develop and use spatial orientation abilities.

How we get oriented in the space?


Cross-cultural differences in spatial orientation strategies under normal and pathological conditions could be illustrative to understand how pre-historical man could have used spatial information. Furthermore, it could shed some light about the potential spatial abilities that contemporary man possesses. Brain organization of spatial abilities under pathological conditions has been extensively studied in contemporary schooled Western (particularly European and North American) people. To my best knowledge, however, no clinical observations about disturbances in spatial abilities associated with brain pathology in other (non-Western) culture have ever been reported. Characteristics of spatial abilities in different cultures can be illustrative. Perceptual constancy (stability of perception despite changes in the actual characteristics of the stimuli) represents the most fundamental ability in the interpretation of the surrounding spatial environment (Ardila, 1980; Walsh & Kulikowski, 1998).

Perceptual Constancy In general, cross-cultural comparisons have demonstrated that perceptual constancy (size and shape constancy) is more accurate in low-schooled and non-Western societys people than in literate and westernized subjects (Pick & Pick, 1978). Beveridge (1940) demonstrated a greater constancy of shape and size among West African adults than among British adults. Myambo (1972) observed almost perfect shape constancy in uneducated Malawi adults, whereas the educated Africans and Europeans did not perform so accurately. Perceptual constancy may be expected to have been high (and crucial for survival) not only in pre-historical man, but also to be high in people currently requiring a

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complex interpretation of the surrounding spatial environment.

Reference Systems People living in different environments develop different systems of spatial reference (rivers, mountains, sun position, streets, buildings, etc). Geographic features affect the terms of local reference systems, and differences in reference systems may, in turn, be related to differences in perception of spatial orientation (Pick & Pick, 1978). The analysis of different reference systems can be illustrative. Gladwin (1970) analyzed the system used by Puluwat sailors to navigate among clusters of islands in the Western Pacific. He disclosed that many different features of the sea and sky comprise the information of which the system is based. Knowledge of the habits of local sea birds provides cues for one's location. The sailors learn to defect the coral reefs formation changes, which of course, differ depending on the conditions of the weather, sea and sky. Ability to detect change in the "feel" of the boat moving through the waves on a particular course is a skill used to maintain a course. There is a complex reference system based on the position and patterns of stars in the night sky, and the rules for navigating between specific islands are described in terms of the star patterns and islands. Parallax information is also explicitly included in the system as descriptions of the way in which the islands "move" as the boat passes on one or the other side of them (Pick & Pick, 1978). Amazonian Indians simultaneously use a variety of different types of information to move around in the jungle. They use small rivers, orientation and color of trees, soil characteristics, sun position, animal routes, olfactory cues, and many other signals to move in the jungle. Vegetation is mildly different when closer to rivers, moss grows different in trees according to the sun direction, and directions of river-flows are different. Additionally, when moving in the jungle, they permanently break small bush branches, to recognize later they have already crossed (and approximately how long time ago) that particular point. All

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these environmental signals are simultaneously interpreted for getting oriented and moving around the jungle. Evidently, members of different cultures dwelling in different spatial environments operate in terms of complex spatial reference systems, depending on their particular demands and geographic environments. Demands and geographic environment were quite different in Paleolithic times than they currently are for contemporary city-man. Evidently, spatial orientation and reference systems used by pre-historical man were closer to Puluwat sailors' or Amazonian Indians' reference systems than to our contemporary orientation system in cities.

Cultural Differences in Visuoperceptual Abilities Cross-cultural differences in perceptual abilities have been extensively studied and can be particularly illustrative to understand perceptual skills in pre-historical man (Brislin, 1983; Laboratory of Comparative Human Cognition, 1983; Segall, 1986). Hudson (1960, 1962) studied depth perception using pictures that contained figures of an elephant, an antelope, and a man with a spear; the basic question referred to what the man was doing with the spear. There were four pictures differing with respect to the cues available for the interpretation of the picture. This set of pictures was used with different groups of people from Africa and Europe. It was observed that European children around 7-8 years have a great difficulty perceiving the picture as three-dimensional. However, around 12 years, virtually all children perceived the picture as three-dimensional. Not so with Bantu or Guinean children. Nonliterated Bantu and European laborers responded to the picture as flat, not three-dimensional. They cannot interpret represented-on-a-paper three-dimensional figures; this also holds true in general for illiterate people (Ardila et al., 1989). However, as mentioned above, illiterate African people do better than Western literate subjects in perceptual constancy tasks with real objects. But they do worse when the external space is represented on a paper.

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Berry (1971, 1979) proposes that hunting people with specific ecological demands usually present good visual discrimination and excellent spatial skills. For instance, the embedded figures tests are better performed by cultural groups for whom hunting is important for survival. Berry emphasizes that ecological demands and cultural practices are significantly related to the development of perceptual and cognitive skills. A good example of a specific culture-dependent cognitive skill was that reported by Gay and Cole (1967); when Kpelle farmers are contrasted with American working class, the former were considerably more accurate in estimating the amount of rice on several bowls of different sizes containing different amounts of rice. By the same token, any cattle farmer is able to accurately calculate the weight of a cow; or any dactylographist can easily and quickly distinguish two different fingerprints; or any neurologist can distinguish a Parkinsonian patient at one glance. Demands and training history are strongly associated with visuoperceptual abilities. Spatial abilities differ among cultures and depend on the specific ecological demands. In neuropsychology, the perceptual ability disturbances of a very limited subsample of the human species -contemporary Western, and most often, urban and literate brain-damaged individuals have been relatively well analyzed. Nevertheless, our understanding of the brain organization of spatial abilities, and their disturbances in cases of brain pathology, are necessarily not only partial but, doubtless, biased. Norms for perceptual performance in a sufficiently broad array of neuropsychological tests and an extended analysis of perceptual disturbances in different cultural and ecological contexts are required.

Acquired spatial cognition disorders


Visuospatial impairments resulting from brain damage have been extensively analyzed in neuropsychology (e.g., De Renzi, 1982, 1985; Hcaen, 1962; Morrow & Ratcliff, 1988;

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Newcombe & Ratcliff, 1989; Rosselli, 1986; Stiles, Stiles-Davis, Kritchevsky & Bellugi, 1988; Beis et al., 2003; Hodgson & Kennard, 2003; Vallar, 2007). Different brain syndromes have been distinguished. Spatial agnosia represents an impairment in the perception and use of spatial-dependent information resulting from brain pathology. It refers to an acquired inability to recognize and integrate spatial information, regardless that there is not a primary sensory defect capable to explain it (Ardila & Rosselli, 1992). Spatial agnosia includes impairments in the recognition of line orientation, defects in depth perception, impairments in handling spatial information, and deficits in spatial memory (De Renzi, 1983; Hcaen & Albert, 1978). Different types of spatial agnosia have been distinguished. Holmes (1918) separates different categories of spatial agnosia: defects in objects localization, topographic amnesia, inability to count objects, inability to perceive movement, loss of stereoscopic vision, and deficits in eye movements. Critchley (1968) includes the following groups: (1) disorders in spatial perception with regard to the three-dimensional perception, (2) disorders in spatial concepts, and (3) disorders in spatial manipulation, which includes disorders in topographical memory, defects in orientation, and unilateral spatial agnosia. Hcaen (1962) proposed to separate: (1) disorders in spatial perception, (2) defects in spatial manipulation, including, the loss of topographical concepts, and unilateral spatial agnosia, (3) loss of topographical memory, and (4) Balint's syndrome. De Renzi (1982, 1985) presents some modifications to Hcaen's classification. Balint's syndrome is included within visual exploration disorders, and instead of disorders in manipulation of spatial information, introduces the group of disorders in spatial thought. Table 3.1 presents the classification of spatial agnosias proposed by Ardila and Rosselli (2007). It is interesting to emphasize that all these disorders appear (mainly or exclusively) in cases of right hemisphere pathology. That means the right hemisphere seems to be specialized in spatial cognition. Language and ideomotor praxic abilities developed in left brain areas that in the right brain are involved in spatial cognition (LeDoux, 1984). Supposedly, similar spatial cognition disturbances are to be found in a similar way in

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every individual, regardless of the cultural background and the ecological demands. However, not only commonality but also differences would be expected to be found. If the degree (not the direction) of brain lateralization of language depends on literacy, and in general, on the verbal training history (Lecours et al., 1987, 1988; Matute, 1988), it would seem reasonable to suppose that the degree of lateralization of spatial cognition would also depend on the spatial abilities training history. At least some spatial disturbances (e.g., hemi-spatial neglect) have been reported to be more frequently observed associated with left-hemisphere pathology in individuals with a history of low verbal trainings (i.e., low educational level), but normal, and eventually even superior trainings in spatial abilities (Rosselli et al., 1985).
________________________________________________________________ TYPE OF DISORDER LOCATION OF DAMAGE _______________________________________________________________ DISORDERS IN SPATIAL EXPLORATION Balint's syndrome DISORDERS IN SPATIAL PERCEPTION Inability to locate stimuli Impairments in depth perception Distortion in line orientations Inability to estimate the number of stimuli DISORDERS IN SPATIAL MANIPULATION Unilateral spatial agnosia Loss of topographical concepts Right occipital-parietal and frontal Parietal-temporal-occipital specially right Right parietal Bilateral parietal-occipital Right parietal-occipital and frontal Right hemisphere especially parietal Bilateral parietal-occipital

DISORDERS IN ORIENTATION AND SPATIAL MEMORY Topographic agnosia Biteral temporal-occipital

Topographic amnesia Right (or bilateral) parietal-occipital ________________________________________________________________

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Table 3.1. Classification of spatial agnosias (according to Ardila & Rosselli, 2007). If, despite the existence of some basic characteristics in its brain organization, language disturbances (oral and written) are associated with language idiosyncrasies (i.e., aphasia is not completely equivalent in Chinese and Spanish; alexia can be different in English and Japanese, etc; Sasanuma & Fujimura, 1971; Yamadori, 1975; Yu-Huan et al, 1990), spatial cognition disturbances may also depend on spatial ability training histories. This, of course, has to be demonstrated. And, it can be demonstrated only if spatial disturbances are analyzed in individuals with different cultural backgrounds and different spatial demands. Nevertheless, contemporary city man's spatial abilities are not necessarily inferior to pre-historical man's or Amazonian Indians' spatial abilities. Spatial abilities may have evolved with the new living and cultural conditions (in a similar way as spoken language evolved and extended with the development of new cultural conditions, e.g., through written language). Spatial abilities can be required in many contemporary, conceptual, and historically recent skills. The author of this paper had the opportunity to study a university chemistry professor who suffered a small right-parietal infarction. Although she had no evidence of spatial difficulty in her everyday activities, and no significant spatial disturbances were disclosed in formal testing, she could not continue teaching chemistry, because she was "unable to have a spatial representation of molecules and all the time got confused". Mathematics (Ardila &Rosselli, 1990; Luria, 1977), painting, playing chess (Chabris & Hamilton, 1992), reading and writing (Ardila & Rosselli, 1993; Benson & Ardila, 1996), mechanics (Benton, 1989), and even music (Henson, 1985), represent (at least partially) spatially-based skills. Mathematics, painting, playing chess, reading and writing, mechanics, and music abilities can be impaired in cases of right hemisphere damage of those same areas that in a Eskimo or Amazonian Indian could imply an impossibility to move around the snow or the jungle.

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Neuroimaging studies

Some few studies have analyzed brain activity in different spatial recognition and orientation tasks. Thus, by using functional Magnetic Resonance Imaging (fMRI) techniques, it has been demonstrated that the right posterior part of the parahippocampal gyrus is critical for the acquisition of novel information about the environment (buildings and landscapes), and that the same region plus the anterior half of the lingual gyrus and the adjacent fusiform gyrus play an important role in the identification of familiar buildings and landscapes (Takahashi & Kawamura, 2002). Ino et al (2008) described two patients who presented with transient directional disorientation as a manifestation of cerebral ischemia. The patients suddenly lost sense of direction in a familiar environment despite preserved ability to recognize landmarks. Brain MRI revealed an ischemic lesion in the right medial occipital lobe and the corpus callosum in case 1 and in the right parieto-occipital sulcus in case 2. Using a larger sample, Gil-Nciga et al. (2002) studied 10 patients with transient topographical disorientation; they found that the episodes of transient topographical disorientation could be separated into two types: the patients either reported difficulties in spatial orientation with preserved abilities to recognize landmarks and objects (spatial agnosia), or the difficulties appeared with the recognition of landmarks (topographical agnosia). Tests exploring spatial orientation, as well as higher visuoperceptive capacities, were altered in most of the patients, and brain SPECT showed hypoperfusion of the right hemisphere in all patients, which could also be demonstrated two years later in some cases. The crucial role of the right parieto-occipital area in spatial orientation and topographical recognition has been confirmed by diverse authors. Thus, van der Ham et al (2010) reported two cases with navigation problems resulting from parieto-occipital right hemisphere damage. Rusconi et al (2008) described the case of a young woman with longlasting topographical disorientation following a hemorrhagic lesion of the right temporo-

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occipital region involving the hippocampus. She was unable to orient herself in novel environments and to perform learning spatial tasks both in real-world settings and laboratory conditions. Her ability to recall and navigate through known routes as well as to recognize familiar landmarks was preserved. A similar neuropsychological pattern was observed 8 years later when she showed a persistent topographical disorientation and a slight worsening of verbal and visuo-spatial long-term memory disorders. Turriziani et al (2003) described a patient who, following cerebral hypoxia, developed severe difficulty in orienting himself in new environments in the context of a mild global amnesic syndrome. Some episodes he related suggested that his main difficulty was remembering the spatial/directional value of landmarks he recognized. A neuroradiological examination documented severe bilateral atrophy of the hippocampi associated with atrophic changes in the cerebral hemispheres, mostly marked in the dorsal regions. Several notable features emerge from consideration of the case reports of relatively pure topographical disorientation in the presence of a retrosplenial lesion (Maguire, 2001). The majority of cases follow damage to the right retrosplenial cortex, with Brodmann's area 30 (association cortical area in the transitional region between the posterior cingulate gyrus and the medial temporal lobe) apparently compromised in most cases. All patients displayed impaired learning of new routes, and defective navigation in familiar environments complaining they could not use preserved landmark recognition to aid orientation. The deficit generally improved during the following weeks. The majority of functional neuroimaging studies involving navigation or orientation in large-scale space also activate the retrosplenial cortex, usually bilaterally, with good concordance in the locations of the voxel of peak activation across studies, again with Brodmann's area 30 featuring prominently. Currently, there is strong evidence for right medial temporal lobe involvement in spatial orientation; it also seems that the inputs the hippocampus and related structures receive from and convey to right retrosplenial cortex have a similar spatial preference, while the left medial temporal and left retrosplenial cortices seem primarily concerned with more general aspects of episodic memory.

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Conclusions
Some tentative conclusions regarding the evolution of spatial abilities can be proposed:

1. Homo sapiens presented a nomad way of life during the majority of his history. Sedentary way of life appears only with domestication of animals and development of agriculture, that if, some ten thousand years ago. Nomad way of life is strongly associated with high spatial ability demands. 2. Disorders in spatial cognition represent a particularly complex and insufficiently understood array of impairments. Spatial knowledge has been strongly associated with right hemisphere activity. Virtually all the defects in spatial perception and orientation are found exclusively or predominantly in cases of right hemisphere damage. 3. It can be supposed that right hemisphere specialization for spatial abilities is correlated with language acquisition and evolution. Furthermore, it has been suggested that right hemisphere specialization on spatial skills, as well as left hemisphere specialization in verbal and praxic abilities, is found to be correlated with literacy, that is, with language complexization. Spoken language evolved with appearance of new cultural conditions, and it may be supposed that spatial abilities also evolved with the appearance of new cultural and ecological conditions. 4. It has been conjectured that earlyhominids and pre-historical man presented a more bilateral representation of spatial abilities. Visuospatial disorders might have been expected in cases of right and left hemisphere pathology. Not only language development and complexization, but also the development of new spatially-based abilities may have

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increased the right hemisphere specialization for handling information with a spatial content, as well as the left specialization for linguistic abilities (LeDoux, 1984).

References
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Luria, A.R. (1977). Higher Cortical Functions in Man. New York: Basic Books. Maguire, E.A. (2001. The retrosplenial contribution to human navigation: a review of lesion and neuroimaging findings. Scandinavian Journal of Psychology, 42(3), 225-38. Matute, E. (1988). El aprendizaje de la lectoescritura y la especializacin hemisfrica para el lenguaje. In: A. Ardila & F. Ostrosky-Solis (eds), Lenguaje Oral y Escrito (pp. 310-338). Mxico: Editorial Trillas. Morrow, L. & Ratcliff, G. (1988). The neuropsychology of spatial cognition. In: J. Stiles-Davis, M. Kritchevsky, & U. Bellugi (eds), Spatial Cognition: Brain Bases and Development (pp. 5-32). Hillsdale: Lawrence Erlbaum Associates. Myambo, K. (1972). Shape constancy as influenced by culture, Western education, and age. Journal of Cross-Cultural Psychology, 3, 221-232. Newcombe, F. & Ratcliff, G. (1989). Disorders of visuospatial analysis. In: H. Goodglass & A.R. Damasio (eds), Handbook of Clinical Neuropsychology, vol 2 (pp. 333-356). Amsterdam: Elsevier. Pick, A.D. & Pick, H.L. (1978). Culture and perception. In: Carterette & M.P. Friedman (eds), Handbook of Perception, vol 10: Perceptual Ecology (pp.19-39.). New York: Academic Press. Rosselli, M. (1986). Conocimiento espacial y sus alteraciones. Acta Neurolgica Colombiana, 2, 5-10. Rosselli, M., Rosselli, A., Vergara, I. & Ardila, A. (1985). The topography of the

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hemi-inattention syndrome. International Journal of Neuroscience, 20, 153-160. Rusconi, M.L., Morganti, F. & Paladino, A. (2008). Long-lasting topographical disorientation in new environments. Journal of Neurological Sciences, 273, 57-66. Sasanuma, S. & Fujimura, O. (1971). Kanji versus Kana processing in alexia with transient agraphia. Cortex, 7, 1-18. Segall, M.H. (1986). Culture and behavior: Psychology in global perspective. Annual Review of Psychology, 37, 523-564. Stiles, J., Stiles-Davis, J., Kritchevsky, M. & Bellugi, U. (1988). Spatial cognition: brain bases and development. New York: Lawrence Erlbaum Associates Takahashi, N. & Kawamura, M. (2002). Pure topographical disorientation--the anatomical basis of landmark agnosia. Cortex, 38(5),717-25. Toth, N & Schick, K. (2007). Handbook of Paleoanthropology. Springer Berlin Heidelberg. Turriziani, P., Carlesimo, G.A., Perri, R., Tomaiuolo, F., & Caltagirone, C. (2003). Loss of spatial learning in a patient with topographical disorientation in new environments. Journal of Neurology, Neurosurgery and Psychiatry, 74(1), 61-9. Vallar, G. (2007). Spatial neglect, Balint-Homes' and Gerstmann's syndrome, and other spatial disorders. CNS Spectrumsm,12(7), 527-36 van der Ham, I.J., van Zandvoort, M.J., Meilinger, T., Bosch, S.E., Kant, N., & Postma, A. (2010). Spatial and temporal aspects of navigation in two neurological patients. Neuroreport, 14, 21(10), 685-9.

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Vygotsky, L.S. (1962). Thought and Language. Cambridge, MA: Massachusetts Institute of Technology Press, Walsh, V. & Kulikowski, J. (Ed.) (1998). Perceptual Constancy: Why Things Look as They Do. Cambridge: Cambridge University Press, Washburn, S.L. (1978). The evolution of man. Scientific American, 239(3), 194-207 Wilson, A.O. (1975). Sociobiology. Cambridge, MA: The Belknap Press of the Harvard University Press. Yamadori, A. (1975). Ideogram reading in alexia. Brain, 98, 231-298. Yu-Huan, H., Ying-Guan, Q., & Gui-Qing, Z .(1990) Crossed aphasia in Chinese: A clinical survey. Brain and Language, 39, 347-356.

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4. Origins of Writing

Introduction
Writing represents a relatively recent acquisition in human history. Its development was particularly slow, advancing through different steps of complexity. Writing began several millennia ago, but still nowadays, significant changes in writing strategies are observed very specially associated with the progressively more extended use of computer word processors. The need for a clear understanding of the origins of current cognitive abilities is evident. The example of reading and writing may be illustrative of the need for a historical/anthropological analysis of neuropsychological syndromes. Varney (2002) points out that reading is a cultural, not an evolutionary, development. He emphasizes that our capacity of reading did not evolve biologically; it evolved through cultural developments that were only acquired as typical human abilities within the last 200 years in Europe and America, and only after World War II in the rest of the World (p. 3). The origins of reading can be found in certain abilities that existed long before reading was developed. Reading and writing were far from universal even at the beginning of the 21st century. According to the United Nations, a person who is literate can, with understanding, both read and write a short simple statement on his or her everyday life. A person is functionally literate who can engage in all of those activities in which literacy is required for effective function of his or her group and community and also for enabling him or her to continue to use reading, writing, and calculation for his or her own and the communitys development (UNESCO, 2003). Surveys throughout the world have been conducted to

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observe populations speaking various languages and their inability to read or write a simple message. In the first survey (1950), at least 44% of the worlds population was found to be illiterate. A 1978 study showed the rate to have dropped to 32.5%. In 1990 illiteracy worldwide dropped to about 27%, and by 1998 to 16%. However, a study by the United Nations Childrens Fund (UNICEF) published in 1998 predicted that the world illiteracy rate would increase in the 21st century because only a quarter of the worlds children were in school by the end of the 20th century. The highest illiteracy rates were found in the less developed nations of Africa, Asia, and South America. The lowest illiteracy rates were found in Australia, Japan, North Korea, and the more technologically advanced nations of Europe and North America. Currently, there are an estimated 862 million illiterate adults in the world, of whom about two thirds are women (UNESCO, 2011). The mean educational level of contemporary man is only about 34 years of school! Varney (2002) analyzed the origins of reading ability. He suggested that the ancient skills of gesture comprehension and animal tracking were the underpinnings of brain organization that permitted reading to occur. He demonstrated that alexia is significantly associated with impaired pantomime and animal footprint recognition. Thus, these abilities, existing since early human history, were prerequisites that led the way to the cultural development of reading. Gesture recognition may have existed for several millions of years, but reading developed just a few millennia ago.

How did writing appear?


Wall paintings appeared during the Paleolithic era, some 3035,000 years ago (Childe, 1936). Across Europe, particularly in France and Spain, cave paintings dating from the Paleolithic age have been found. Mainly animals, but also people, instruments, and environmental conditions, are represented in these paintings. Further evolution in pre-

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writing is represented by paintings becoming standardized for representing specific elements (i.e., a standard bird means bird). Lecours, Pea-Casanova, and Ardila (1998) pointed out that writing began with concrete pictograms that reflect realities accessible to the senses, particularly to vision. These pictograms further evolved and became abstract, progressively separating from the concrete representation (Figure 4.1). This situation was observed in Sumer (contemporary Iraq) about 53 centuries ago, and it is usually regarded as the beginning of writing in human history. Symbols (graphemes) referred to the meaning of the words, so these original writing systems are regarded as logographic. Graphemes representing sounds (syllables) appeared later, about 4000 years ago in Phoenicia (Sampson, 1985), and graphemes representing phonemes appeared even later in Greece. The sequence of the evolution of writing in consequence was:

Drawings -> pictograms -> logograms -> syllabic graphemes -> phonemic graphemes

Writing systems can be divided in different ways; a major distinction between logographic (representing meanings) and sonographic (representing sounds) systems can be established (OMNIGLOT; Sampson, 1985). The fundamental difference between logographic writing systems and other scripts is that each logographic symbol means something. As a result, logographic writing systems generally contain a large number of symbols: anything from several hundred to tens of thousands. In fact there is no theoretical upper limit to the number of symbols in some logographic scripts, such as Chinese.

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Figure 4.1. Evolution from pictograms to cuneiform logograms

Logographic scripts may include the following types of symbols: 1. Logogramssymbols that represent parts of words or whole words. Some logograms resemble the things they represent and are sometimes known as pictograms or pictographs (Figure 4.2).

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2. Ideogramssymbols that graphically represent abstract ideas. 3. Semantic-phonetic compoundssymbols that include a semantic element, which represents or hints at the meaning of the symbol, and a phonetic element, which denotes or hints at the pronunciation. 4. Sometimes symbols are used for their phonetic value alone, without regard for their meaning. In sonographic writing systems, syllables (syllabic alphabets) or phonemes (phonemic alphabets) can be used. Alphabetic writing systems come in two varieties. 1. Abjads (consonant alphabets) represent consonants only, or consonants plus some vowels. Even though not common, full vowel indication (vocalization) can be added, usually by means of diacritics. 2. Alphabets (phonemic alphabets) represent consonants and vowels. Thus, initial writing (or rather, pre-writing) was a visuoconstructive ability (i.e., representing external elements visually), and only later did it become an ideomotor praxis ability (i.e., making certain learned and fixed sequences of movements with the hand to create a pictograma standardized representation of external elements). Still later, after writing became an ideomotor praxis ability, it became a linguistic ability (i.e., associating the pictogram with a word, and further analyzing the word in its constituting sounds). It is not surprising that three major disorders in writing can be observed as a result of brain pathology: visuoconstructive (spatial or visuospatial agraphia), ideomotor (apraxic agraphia), and linguistic (aphasic agraphia). In addition, of course, writing requires visual and motor integrity.

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Figure 4.2. Example of a logographic writing system. Japanese Kanji uses Chinese characters that were imported from China which is use for to write nouns, adjectives, adverbs and verbs.

It can be proposed that writing is based in three different abilities: visuoconstructive, praxic and linguistic. Consistent with this notion, three major disorders in writing can be observed as a result of brain injury or pathology: visuoconstructive (spatial or visuospatial agraphia), ideomotor (apraxic agraphia), and linguistic (aphasic agraphia) (Table 4.1). Perhaps not coincidentally, anthropological origins of writing appear to mirror these three different abilities. In prehistory, writing developed first using a visuospatial modality to create three-dimensional clay tokens to represent objects, which later progressed into

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drawings. It is not surprising that three major disorders in writing can be observed as a result of brain pathology: visuoconstructive (spatial or visuospatial agraphia), ideomotor (apraxic agraphia), and linguistic (aphasic agraphia). In addition, of course, writing requires visual and motor integrity.

--------------------------------------------------------------------------Spatial or visuospatial agraphia Apraxic agraphia Aphasic or linguistic or central agraphia --------------------------------------------------------------------------Table 4.1. There are three fundamental forms of agraphia (Ardila, 2004).

How many people can write?


Even though writing began several millennia ago up to as recently as the 1950s, about half of the worlds population was illiterate. The percentage of illiteracy dramatically increases as we go back in time, and up to only a couple of centuries ago, the overwhelming majority were illiterate. Until the 15th century, when the printing press was invented, writing may well have been limited to a few intellectual people and monks. Even though there are no statistics available, it may be conjectured that 99% or more of the population was illiterate. Furthermore, it has to be kept in mind that the mean level of education of contemporary man is about 3 years of school, which may not be enough to develop automatic reading and writing. It is evident that writing represents an unusual ability in humans. The overwhelming majority of members of our species who have lived could not read or write. Reading and writing is obviously far from being a primary or biologically based cognitive ability. Clearly, writing represents a cognitive ability that depends on the human cultural evolution

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(Vygotsky, 1962).

Agraphia as a neuropsychological syndrome


Agraphia can be defined as the partial or total loss of the ability to produce written language and is associated with brain pathology. The ability to write can be impaired as a result of linguistic defects (aphasia), but other elements not related to language (e.g., motor and spatial) also participate in the writing ability. It supposes knowledge of the language codes (phonemes, words), an ability to convert language sounds in graphemes, knowledge of the graphemic system (alphabet), an ability to perform fine movements, and an appropriate use of the space for distributing, joining, and separating letters. It is evident that diverse types of writing disturbances can be found in clinical practice. Different attempts to classify writing disturbances are found in the history of neuropsychology. Goldstein (1948) distinguished two major types of agraphia: apractoamnesic and aphasic-amnesic. Luria (1976, 1980) referred to five different types of agraphia, three of them associated with aphasia (sensory agraphia, afferent motor agraphia, and kinetic agraphia) and two associated with visuospatial defects. Hecaen and Albert (1978) distinguished four types of agraphia: pure, apraxic, spatial, and aphasic. Regardless of the diversity of classifications of agraphia, a basic distinction can be established between (1) agraphias due to a language impairment (linguistic or aphasic agraphias), (2) agraphias due to other types of impairments (most often, motor or spatial) disturbing the normal ability to write (Benson & Ardila, 1996), or simply (3) central and peripheral agraphias (Ellis, 1988). In the first case, agraphia is just a secondary manifestation of the aphasic syndrome. In the second, it can be interpreted as a result of a broader visuoconstructive/visuospatial impairment (Ardila & Rosselli, 1993), or motorapraxic disturbance (Hecaen & Albert, 1978). Consequently, writing can be interpreted as a particular type of cross-modal learning. Certain visuoconstructive and ideomotor abilities become associated with language.

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It can be proposed that writing is based in three different abilities: visuoconstructive, praxic and linguistic. Consistent with this notion, three major disorders in writing can be observed as a result of brain injury or pathology: visuoconstructive (spatial or visuospatial agraphia), ideomotor (apraxic agraphia), and linguistic (aphasic agraphia). Perhaps not coincidentally, anthropological origins of writing appear to mirror these three different abilities. In prehistory, writing developed first using a visuospatial modality to create threedimensional clay tokens to represent objects, which later progressed into drawings.

Dysexecutive agraphia Regardless that many types of writing disorders associated with brain pathology have been described throughout the history, limited mention to the writing disturbances associated with prefrontal pathology, however, is found. Clinical observations of patients not only with focal prefrontal pathology but also with other conditions affecting the frontal lobe system (e.g., traumatic head injury, dementia) confirm the assumption that these patients present an overt decrease in the ability to express ideas in writing. It can be argued that complex aspects of writing, such as planning, narrative coherence, and maintained attention, are significantly disturbed in cases of impairments of executive functions (dysexecutive syndrome). Frontal lobe patients not only have difficulties in keeping the effort required for writing, but also to organize the ideas in the written texts. The term dysexecutive agraphia (Ardila & Surloff, 2006) has been proposed to refer to this writing disorder.

Is any area in the brain specialized for writing?


Writing is a functional system (Luria, 1976) that requires, and is based on, some more fundamental abilities: praxis abilities (i.e., learning sequences of movements required to write the letters), spatial abilities (distributing letters and words in the space, and

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understanding the value of space in writing), constructional abilities (reproducing a model using certain movements), and obviously, the knowledge of the language and the association between verbal auditory elements and visual symbols. Varney (2002) refers to the anthropological concept of pre-adaptation, which states that the evolution of a structure for one purpose can enable that structure to perform another purpose. This must be true for writing (as for any other abilities depending on cultural evolution). Visuoconstructive and ideomotor abilities represent prerequisites for writing; they are probably related to the ability to make tools and weapons and generally to use the hands in a skilled way.

Brain activation during writing


The use of contemporary neuroimagening techniques has significantly advanced the understanding of the brain organization of writing (see www.fmriconsulting.com/ brodmann/). It has been observed that writing is associated with an extended pattern of brain activity, usually including a diversity of anterior and posterior, right and left areas. Indeed, writing is a complex act, requiring not only linguistic but also motor and spatial abilities. Functional studies have demonstrated that writing single letters is associated with a significant activity of Brodmanns areas 37 (temporal-occipital area, related with auditoryvisual associations) and 7 (superior parietal lobe) (Rektor et al., 2006). Other parietal areas are also active during writing including the border between the parietal superior and inferior lobuli Brodmanns area (Brodmanns areas 2 and 40), deep in the intraparietal sulcus, with a surprising right-sided dominance. The right parietal activation may reflect the spatial dimension of writing. Comparing the brain activity observed during writing and drawing a relatively similar pattern of activation for both has been reported (Harrington et al., 2007) including bilaterally

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the premotor, inferior frontal, posterior inferior temporal and parietal areas. Significant differences between the two conditions (writing and drawing) are found in areas of the brain known for language processing (perisylvian area); greater activation for writing is observed in the left hemispheres, whereas greater right hemisphere activation for drawing is found in homologous areas, particularly Brodmanns area 46 (part of the prefrontal cortex - anterior middle frontal gyrus) and 37 (temporal-occipital). Sugihara et al. (2006) recorded the brain activation while writing with the right and the left hand using Japanese Kana (phonograms representing syllables). Three areas were found to be activated: (1) the posterior end of the left superior frontal gyrus, which is superior and posterior to the so-called Exner's area (an area just above Broca's area and anterior to the primary motor control area, initially described as the writing center); (2) the anterior part of the left superior parietal lobule; and (3) the lower part of the anterior limb of the left supramarginal gyrus. In the single-subject analysis, whereas the first two of the above three areas were found to be crucial for writing in all individuals, an interindividual inconsistency of involvement with writing was observed in last area: the lower part of the anterior limb of the left supramarginal gyrus (60% involved); the right frontal region (47%); and the right intraparietal sulcus (47%).

Writing in different systems


Few papers have approached the question of the potential similarities and differences in agraphia clinical manifestations across different writing systems. Some studies have approached the comparison of writing disturbances and brain activation patterns in Japanese Kana and Kanji. More recently, studies of agraphia in other languages have become available. Indeed, Japanese represents a unique language using two different writing systems; Kana is a phonographic system and symbols represents syllables; whereas Kanji is a

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logographic system and symbols represent meanings (morphograms). Various types of alexia with or without agraphia in the Japanese language cause specific type of Kanji/Kana dissociation; it has been further proposed that there is a semantic reading pathway via Brodmanns area 37 on the inferior border of the left temporal lobe and a phonological reading pathway via middle portion of the left lateral occipital lobe (Iwata, 2004) Yaguchi et al. (2006) reported a case of pure (apraxic) agraphia observed both in Kana and Kanji writing to dictation and copying. Most errors in Kana and Kanji writing to dictation and copying were no response. The patient, however, was able to write numerals from 1 to 12 precisely. Magnetic resonance imaging showed a cerebral infarction in the left parietal lobe which included a part of superior parietal lobule and supramarginal gyrus. That means the apraxic agraphia was similarly affecting both writing systems Kana and Kanji. Sakurai et al. (2008) analyzed two patients with lesions of the left posterior middle temporal gyrus. Patient 1 first presented with pure alexia more impaired for Kana after an infarction in the left middle and inferior occipital gyri and right basal occipital cortex, and after a second infarction in the left posterior middle temporal gyrus adjoining the first lesion he showed alexia with agraphia for Kanji and worsened alexia for Kana; Kanji alexia recovered over the following six to 10 months. Patient 2 presented with alexia with agraphia for Kanji following a hemorrhage in the left posterior middle and inferior temporal gyri, which resolved to agraphia for Kanji at two months after onset. In both patients, Kanji agraphia was mostly due to impaired character recall. The authors concluded that damage to the left posterior middle temporal gyrus alone can cause agraphia for Kanji. If the adjacent mid fusiform/inferior temporal gyri (Brodmanns area 37) are spared, the Kanji alexia is transient. This report also demonstrates that agraphia for Kana and for Kanji can be at least partially dissociated. Ihori et al. (2006) reported the case of a right-handed patient who exhibited right unilateral jargonagraphia after a traumatic callosal hemorrhage. The lesions involved the entire corpus callosum, except for the lower part of the genu and the splenium. The patient's right unilateral jargonagraphia was characterized by neologisms and perseveration in Kanji and Kana, and was more prominent in Kana than Kanji. The authors propose that

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at least two factors seem to explain that Kana was more defective than Kanji. First, writing in Kana, which is assumed to be processed mainly via a sub-word phoneme to grapheme conversion route, might depend more strongly on lateralized linguistic processing than writing in kanji. Second, kanji, which represent meaning as well as phonology, with much more complicated graphic patterns than kana, are assumed to be processed in both hemispheres. Fukui and Lee (2008) reported three patients with progressive agraphia; initially, these patients complained primarily of difficulties writing Kanji while other language and cognitive impairments were relatively milder. It was proposed that agraphia was generally more prominent, although not exclusive, for Kanji, probably because of later acquisition and larger total number of Kanji symbols leading to lower frequency of use and familiarity per symbol. For comparing purpose, it is worthy to mention the case of progressive agraphia in a Spanish speaking woman reported by Ardila et al., (2003). This patient presented a progressive deterioration of writing abilities, associated with acalculia and anomia. An MRI disclosed a left parietal-temporal atrophy. Using Spanish orthography was the initial writing difficulty noted in this woman. The correct use of orthography (i.e., selecting between two or more homophone alternatives) represents for normal people the most difficult aspect in Spanish writing, and it is not surprising to find it was the most fragile writing ability in this patient. In a further evaluation two years after the initial symptomatology, the patient demonstrated not only orthographic (homophone) errors, but also letter omissions and additions, and even non homophone errors. It is noteworthy that, regardless of her inability to write spontaneously or by dictation, her writing by copy was virtually perfect. It was conjectured that writing by copy does not really represent a linguistic ability but rather visuoperceptual and visuoconstructive ability. Lin et al. (2007) using fMRI examined the neural correlates for Chinese writing, by comparing the writing of logographic characters and that of pinyin, a phonetic notation system for Chinese characters. The temporal profile of the activations indicated that the middle frontal gyrus, superior parietal lobule, and posterior inferior temporal gyrus reflected more central processes for writing. Although pinyin writing elicited greater activity overall

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than character writing, the critical finding was that the two types of symbols recruited essentially the same brain regions. Liu et al. (2007) trained native English speakers with no knowledge of Chinese on 60 Chinese characters. Following the training, fMRI scans taken during passive viewing of Chinese characters showed activation in brain regions that partially overlap the regions found in studies of skilled Chinese readers, but typically not found in alphabetic readers. Areas include bilateral middle frontal (Brodmanns area 9), right occipital (Brodmanns area 18/19), and fusiform (Brodmanns area 37) regions. The results suggest that learners acquired skill in reading Chinese characters using a brain network similar to that used by Chinese native speakers. Meschyan and Hernandez (2006) compared the pattern of brain activation during single word reading in a group of English/Spanish bilinguals. Participants were slower in reading words in their less proficient language (Spanish) than in their more proficient language (English). fMRI revealed that reading words in the less proficient language yielded greater activity in the articulatory motor system, consisting of supplementary motor area/cingulate, insula, and putamen. Orthographic transparency also played a neuromodulatory role. More transparent Spanish words yielded greater activity in superior temporal gyrus (Brodmanns area 22), a region implicated in phonological processing, and orthographically opaque English words yielded greater activity in visual processing and word recoding regions, such as the occipital-parietal border and inferior parietal lobe (Brodmanns area 40).

From agraphia to dystypia


Contemporary literate man is using handwriting less and less, and relying on computers more and more. In an informal survey of 40 people with a college-level education background, they reported using a computer about 90% of the time when writing and handwrote only 10% of the time. Obviously, this sample does not represent all of humankind, and computers are not accessible to a large percentage of the human

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population. But this sample seems to illustrate the way in which writing is evolving: from handwriting to typing on a computer. Handwriting and using computers represent significantly different cognitive and motor abilities. During handwriting, fingers are maintained in a relatively steady position while the hand moves. In typing, the opposite pattern is observed. When typing, the right hand does not move from one side to the other and back as in handwriting, but the hands remain relatively stationary and only the fingers are moved. Letters are not written but selected. Both hands have to be used in a similar way when typing. Because of using both hands, we have to assume that a major interhemispheric integration is required. It is obvious to assume that right-hemisphere lesions located in the frontal and parietal areas should significantly impair the typewriting ability of the left hand. Similarly, the use of the space is different. The normal spatial distribution of the words on the page is automatic on the computer and, hence, writing in this way cannot be spatially disorganized, which may be the case in handwriting. By the same token, letters are neatly written and easily recognizable. When typing, we are not using a space that is directly manipulated with the hands (constructional space), but only a visual space. Furthermore, typing is not a constructional task (we do not have to construct the letters) but rather a motor-spatial task. Many people type using a spatial memory for the position of the letters in the keyboard. This is a type of memory not required in handwriting, and it probably depends on right hippocampal and parietal activity (Moser, Hollup, & Moser, 2002). Other people have to look at the keys to select the letters when typing. In this case, literal reading is a prerequisite for writing. Letters have to be recognized visually before they are written. In handwriting, we use a mental representation of the visual form of the letters. Interestingly, few peopleif any, regardless of how well they can typeare able to reproduce (i.e., describe verbally or by drawing) how the different letters are arranged on the keyboard. Memory for their location seems to be a purely spatial and motor memory of which we are poorly aware. For typing some special symbols (e.g., interrogation marks) and letters (the Spanish

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N ), some relatively sophisticated motor maneuvers are required, sometimes requiring the use of special keys or sequences of movements. In handwriting, however, special symbols are written using the mental forms that we have learned. When typing, if a letter needs to be lower or upper case, a key has to be pushed. No other change to the movement is made. We can also select different writing styles and letter sizes using some special commands and menus, all without changing the sequences of the hand movements. In cases of brain damage, how is typewriting altered? To the best of my knowledge, only one case of agraphia for typewriting has been published (Otsuki, Soma, Arihiro, Watanabe, Moriwaki, & Naritomi, 2002). Nonetheless, it can be assumed that different types of brain pathology may affect the ability for typing on a computer word processor. The following can be conjectured. 1. An anterior callosal lesion would impair the ability to coordinate the movements between the hands. Furthermore, the left hand would be isolated from the linguistic left hemisphere and would be unable to write. Left-hand hemiagraphia in callosal lesions has been observed (Benson & Ardila, 1996). 2. By the same token, it has been observed that damage in the supplementary motor area results in disturbances in the coordinated movements between both hands (Middleton & Strick, 2001). We can anticipate supplementary motor area typing agraphia. 3. Spatial memory disturbances should result in difficulties in recalling the positions of the letters on the keyboard. Typing would be slow and would require a continual search for the letters. Otsuki et al. (2002) reported on a 60-year-old right-handed Japanese man who showed an isolated persistent typing impairment without aphasia, agraphia, apraxia, or any other neuropsychological deficit. They proposed the term dystypia for this peculiar neuropsychological manifestation. The symptom was caused by an infarction in the left

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frontal lobe involving the foot of the second frontal convolution and the frontal operculum. The patients typing impairment was not attributable to a disturbance of the linguistic process, since he had no aphasia or agraphia. Nor was it attributable to an impairment of the motor execution process, since he had no apraxia. Thus, it was deduced that his typing impairment was based on a disturbance of the intermediate process where the linguistic phonological information is converted into the corresponding performance. The authors hypothesized that the foot of the left second frontal convolution and the operculum may play an important role in the manifestation of dystypia. Using a computer is somehow equivalent to a new writing system. Obviously, there is no brain area related to typing on a computer, as there is no brain area related to reading and writing. These are cultural and technological elements recently developed through human evolution. However, there are basic cognitive abilities (pre-adaptative abilities) that are required for the use of these new cultural elements: e.g., certain visuoperceptual abilities and cross-modal associations for reading, phonological awareness and some fine movements for writing, etc. Using computers is notoriously more complex, yet we can assume a functional system participating in their use. It can be conjectured that using computers requires at least the following abilities: 1. A conceptual ability (executive functioning) to understand the principles governing the functioning of a computer. 2. Some visuoperceptual abilities to recognize icons, windows, etc. 3. Some skilled movements to type on the keyboard and manoeuvre the mouse correctly. 4. Some spatial abilities to handle the working space (monitor screen). 5. Some memory abilities to learn programs, to use the spatial position of the keys,

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etc. Obviously, the ability to use computers can potentially be disrupted as a consequence of a failure in any one of these abilities (acumputuria syndrome). In the future, apart from dystypia, more complex disturbances in the ability to use computers will probably be established.

Conclusions
The origins of writing can be traced back to cave paintings. Writing (or pre-writing) was initially a visuoconstructive ability, later involving some stereotyped movements to represent pictograms, and finally involving spoken language. It makes sense, therefore, that the ability to write can be disturbed in three major forms: as a visuospatial/visuoconstructive dexterity, as an ideomotor skill, and as a linguistic ability. Writing has followed a long evolution since cave painting during the Palaeolithic times. Different strategies have been used to represent spoken language visually (ideograms, alphabets, etc). Writing, however, has continued to evolve since its initial invention. The use of punctuation marks and the distinction between upper and lower case in writingto mention just two examplesare relatively recent in history (Sampson, 1985). Evolution has continued with the development of different technical instruments for writing: the feather, the pencil, the typewriter, and the computer. Brain representation of written language has necessarily changed in some way, too. Neuropsychological syndromes associated with brain pathology have evolved over time. We can assume that the consequences of brain pathology in a Palaeolithic man were not the same as for a 19th-century individual (when agraphia was first described), or for contemporary man or woman (some of whom frequently spending most of their working day in front of a computer screen). It can be anticipated that in the future new

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neuropsychological syndromes resulting from new living conditions will be described.

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5. Origins of Calculation Abilities2

Introduction
Calculation ability represents an extremely complex cognitive process. It has been understood to represent a multifactor skill, including verbal, spatial, memory, and executive function abilities (Ardila et al., 1998). Calculation ability is quite frequently impaired in cases of focal brain pathology (Ardila & Rosselli, 2002; Dansilio, 2008; Domahs et al., 2011; Grafman, 1988; Hecaen et al., 1961) and dementia (Deloche et al., 1995; Grafman et al., 1989; Parlatto et al., 1992; Rosselli & Ardila, 1998). The loss of the ability to perform calculation tasks resulting from a cerebral pathology is known as acalculia or acquired dyscalculia. Acalculia has been defined as an acquired disturbance in computational ability (Loring, 1999). The developmental defect in the acquisition of numerical abilities, on the other hand, is usually referred to as developmental dyscalculia or dyscalculia. Calculation abilities have followed a long process from the initial quantification systems up to modern algebra, geometryy, and physics. Some rudimentary numerical concepts are observed in animals, and there is no question that pre-historic man used some quantification. However, the ability to represent quantities, the development of a numerical system, and the use of arithmetical operations are found only in old civilizations. This chapter reviews the evolution of calculation abilities, including numerosity and counting in non-human animals, calculation abilities in primitive and modern humans, and links between language and number concepts throughout human history. In addition, the paper reviews contemporary studies of the neurological substrates of numerical abilities and discusses the implications of technological advances with regard to continued evolution of these abilities.

1. A previous version of this paper was published in: Ardila, A. On the evolution of calculation abilities. Frontier in

Evolutionary Neurosciences, 2, 1-8.

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Numerical concepts in animals


The origin of mathematical concepts can be traced to sub-human species. Throughout recent history different reports have argued that animals (horses, rats, dogs, chimpanzees, dolphins, and even birds) can use numerical concepts and perform arithmetical operations. Some of these reports represent evident charlatanry directed to the general public. Some others, however, are rigorous and highly controlled scientific studies (e.g., Rugani et al., 2009). There is, in general, agreement that some rudimentary numerical concepts are observed in animals. These basic numerical skills can be considered as the real origin of the calculation abilities found in contemporary man. For instance, pigeons can be trained to peck a specific number of times on a board, and rats can be trained to press a lever a certain amount of times to obtain food (Koehler, 1951; Mechner, 1958; Capaldi & Miller, 1988). It could be conjectured that pigeons and rats can count, at least up to a certain quantity; that is, they can recognize how many times a motor act to peck on a board or to press a lever has been repeated. Whether or not this behavior can really be interpreted as counting is nonetheless questionable. However, this behavior can be observed after long and painstaking training. Nonetheless, these animal responses (to peck or to press the lever) are not precise but just approximate. In other words, when the rat is required to press the lever seven times, the rat presses it about seven times (i.e., 5, 6, 7, 8 times). As Dehaene (1997) emphasizes, for an animal, 5 plus 5 does not make 10, but only about 10. According to him, such fuzziness in the internal representation of numbers prevents the emergence of exact numerical arithmetical knowledge in animals. Using highly controlled and sophisticated designs, it has been pointed out that chimpanzees can even use and add simple numerical fractions (e.g., 1/2 + 1/4 = 3/4) (Woodruff & Premack, 1981). These observations support the assumption that some quantity concepts can be found in different animals.

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Counting (or rather, approximately counting) motor responses is a motor act as is walking or running. Counting lever pressings is not very different from estimating the effort (e.g., number of steps or general motor activity) required in going from one point to another. Counting in such a case could be linked to some proprioceptive and kinesthetic information. In the human brain Kansaku et al. (2006) identified a network of areas involved in enumerating small numbers of auditory, visual, and somatosensory stimuli, and in enumerating sequential movements of hands and feet, in the bilateral premotor cortex, presupplementary motor area, posterior temporal cortex, and thalamus. The most significant consistent activation across sensory and motor counting conditions was observed in the lateral premotor cortex. Lateral premotor activation was not dependent on movement preparation, stimulus presentation timing, or number word verbalization. Furthermore, movement counting, but not sensory counting, activated the anterior parietal cortex. Chimpanzees, but also rats and many other animals, can distinguish numerosity (i.e., global quantification); for instance, they prefer a bowl containing a larger number of nutritive elements (such as chocolates or pellets) when selecting between two bowls containing different amounts (Davis & Perusse, 1988). It may be conjectured that global quantification (numerosity perception) and counting (at least the approximate counting of motor responses) represent kinds of basic calculation abilities found at the animal level. Rats prefer a bowl containing 20 pellets to a bowl containing only 10 pellets; however, they do not prefer a bowl containing 20 pellets to a bowl containing 21 pellets. Obviously, numerosity perception is related to the size and shape of the visual image projected to the retina. It can be assumed that 20 pellets in a bowl result in a larger and more complex retinal image than 10 pellets. But the visual image corresponding to 20 pellets is difficult to distinguish from the visual image corresponding to 21 pellets.

Development of calculation abilities in children

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During child development, different stages in the acquisition of numerical knowledge are observed (Klein & Starkey, 1987). They include global quantification, recognition of small quantities, numeration, correspondence construction, counting, and arithmetic (Table 5.1). As mentioned, some fundamental numerical concepts can be observed at the animal level, and it is not surprising to find them in small children. The initial levels of numerical knowledge are found in pre-school children. The development of complex numerical concepts requires long school training. Complex arithmetical concepts depend upon a painstaking learning process, and they are not usually found in illiterate people. The different stages in the acquisition of numerical concepts are associated with the language, perceptual, and general cognitive development. Variability is normally observed, and some children can be faster in the acquisition of numerical abilities. The different stages appear in a sequential way, and the understanding of more complex concepts requires the acquisition of more basic levels. A percentage of otherwise normal children can fail in using numerical concepts normally expected at their age. The term developmental dyscalculia has been used to refer to this group of underperforming children.

Numerical abilities in pre-school children Global quantification or numerosity perception represents the most elementary quantification process. Global quantification supposes the discrimination between collections containing different number of objects (Davis et al., 1985). Global quantification simply means which set of elements is bigger and which one is smaller. Global quantification is observed at the animal level: Many animals can select the larger collection of elements when they have to choose. However, the ability to distinguish which collection is larger depends upon the number of elements in the collections. To distinguish 3 and 4 elements may be easy (4 is 25% larger than 3). To distinguish 10 and 11 elements is obviously harder (11 is only 10% larger than 10). By the same token, to distinguish 10 from 20 elements is easy (the double), but to distinguish 100 from 110 is hard (one tenth). What

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is important is the ratio existing between the two collections of elements (so called psychophysics Weber's fraction).
__________________________________________________________________________________ Global quantification Recognition small quantities Enumeration Correspondence construction Counting one-one principle What collection is bigger and smaller Differentiate one, two and three elements Sequencing the elements in a collection To compare collections. A unique number name is paired with each object Each object in a collection is to be paired with one and only one number name stable order principle cardinal principle Each name is assigned to a permanent ordinal position in the list The final number name used in a counting sequence refers to the cardinal value of the sequence Arithmetic Number permutability (e.g., adding, subtracting).

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Table 5.1. Different levels of numerical knowledge (adapted from Klein and Starkey, 1987)

Global quantification is expressed in the language with words such a "many", "a lot" and similar terms. For small quantities, the words "several", "a few" and similar quantity

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adverbs are included in the language. Quantity adverbs used in everyday speech represent global quantifiers. Quantity adverbs appear early in language history and also in child language development earlier than the numerical system. As mentioned before, all known world languages use global quantification and possess words to refer to many, a lot. All languages oppose small quantities (one, two, a few) to many, a lot. As a matter of fact, many, much and similar global quantifiers represent early words in language development. Global quantification, however, does not represent a truly numerical process because it does not suppose a one-to-one correspondence. Enumeration (sequencing the elements in a collection of elements; this process supposes the individualization of each element) represents the most elementary type of true numerical knowledge (Klein & Starkey, 1987). Enumeration is required to distinguish the individual elements in the collection (this, this, and this, etc). In child language development, the most elementary distinction is between this and other. This and other are also early words in child language development. Correspondence construction constitutes a type of enumeration used to represent the number of objects in a collection and to compare collections. The amount of elements in a collection is matched with the amount of elements in an external aid (fingers, pebbles, knots, strokes, marks, dots, etc.). It implies, in consequence, a one-to-one correspondence: Each one of the elements in the collection corresponds to one finger, or pebble, knot, stroke, mark, or dot, or whatever. An external devise can be used for making the correspondence construction. The most immediate devise are the fingers. During enumeration usually the fingers are used to point the objects. Counting represents a sophisticated form of enumeration: a unique number name is paired with each object in a collection, and the final number name that is used stands for the cardinal value of that collection. The initial object that is pointed to corresponds to one, the following to two and so on. Some times, the very same finger name is used as

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number name (i.e., the very same word is used for one and thumb, two and index finger, etc.). The collection has the amount of objects that corresponds to the last pointed object (cardinal principle). Arithmetic represents an advanced numerical system, which comprises number permutability (e.g., adding, subtracting). Human infants are able to recognize numerosity for small quantities (usually up to three-six items) (Antell & Keating, 1983), but the ability to construct correspondences emerges only during the child's second year (Langer, 1986). During the second year the child also begins to use some number name, and usually develops the ability to correctly count up to three. The child thus acquires the knowledge of two basic principles in counting. (1) One-to-one principle (i.e., each object in a collection is to be paired with one and only one number name). (2) The stable order principle (each name is assigned to a permanent ordinal position in the list; the sequence of numbers is always the very same: one, two, three, etc.). At this point, however, the child does not yet exhibit a cardinal principle; i.e., the final number name used in a counting sequence refers to the cardinal value of the sequence. If a collection is counted one, two, three, it means that in that collection there are three objects) (Klein & Starkey, 1987). Cardinal principle will be observed in three-year-old children (Gelman & Meck, 1983). At this point, the child can count small quantities, usually below 10. During this period the child is also learning how the numerical system works and memorizing the number words. Most often, the numerical system contains three different segments: (1) from one to ten different words are used. (2) From 10 to 20 counting becomes idiosyncratic and quite frequently irregular. In English eleven has not any apparent relationship with one; twelve has an evident relation with two but it is a unique word number; from 13 to 19 the ending teen is used. In Spanish, from 11 (once) to 15 (quince) the ending ce is used. From 15 to 19 the words numbers are formed as ten and six, ten and seven etc. 20 (veinte) has not any apparent relation with 2 (dos). And (3) from 20 on the numerical system becomes regular. Word numbers are formed as twenty and one, twenty and two, etc. Learning of the whole numerical system usually is completed at school.

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Computational strategies (e.g., adding; if a new item is included in a collection, the collection will become larger and the next cardinal number-name will be given to that collection) are found in three-to five-year-old children, initially only for small quantities.

Development of numerical abilities at school


Adding and subtracting numerical quantities and the use of computational principles are observed during in first-and-second grade children, but they only become able to manipulate the principles of multiplying and dividing after a long and painstaking training period, usually during third to fifth grade. Understanding that subtracting is the inverse operation of adding is usually acquired at about five to six years of age. At this age the child begins to use three different procedures for performing additions and subtractions: (1) Counting using the fingers. (2) Counting aloud not using the fingers. And, (3) memorizing additions and subtractions for small quantities (one plus one is two; two plus two is four; two minus one is one, etc.). The last strategy becomes progressively stronger when advancing age and schooling. Nonetheless, children continue using the finger for adding and subtracting larger quantities. From the age of 10 until about 13 years, counting using the fingers progressively disappears, but counting aloud, and performing arithmetical operations aloud, remains. Automatic memory not only for additions and subtractions, but also multiplications (multiplication tables) and divisions, becomes progressively more important. (Siegler, 1987; Grafman, 1988). As a matter of fact, adding and subtracting one digit quantities (e.g., 7 + 5 = 12; 4 + 5 = 9; 8 5 = 3; etc.) represents a type of numerical rote learning, similar to the multiplication tables. Interesting to note, the performance of arithmetical operations aloud may remain during adulthood, even in highly educated people. It should be emphasized that there is a significant variability in the specific strategies used by different children at the same age. Furthermore, the very same child can recur to different strategies when solving different arithmetical problems. In some situations, for

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instance, the child can recur to the fingers, whereas in a different operation, it may not require using the fingers. Or, the child can be able to use some multiplication tables whereas failing with others. At about the age of eight to nine the children usually learn to multiply. This requires the memorization of the multiplication tables. The errors most frequently found when learning the multiplication tables are those answers that could be correct for other number within the same series (e.g., 4 X 5 = 16). These errors may be the result of some interference. They can be observed in children at any age, and even they are some times found in normal adults (Graham, 1987). Development of abstract reasoning and increase in working memory span contribute to the use of mathematical algorithms, i.e., the set of rules used for solving arithmetical problems following a minimal number of steps. The development of algorithms begins when learning the basic arithmetical operations. Progressively, they become more automatic, representing basic strategies for solving arithmetical problems. Development of abstract thinking allows for the use of magnitudes to be applied to different systems (use of the numerical system in measuring time, temperature, etc.) and to the understanding of quantities expressed in a symbolic way

Calculation abilities in pre-historic man


Chimpanzees are capable of various forms of numerical competence, including some correspondence constructions (that is, comparing two collections of elements) for low quantities (Premack, 1976; Davis & Perusse, 1988). Most likely, these numerical abilities also existed in pre-historic man. Homo sapiens antecessors may have been capable of using correspondence constructions in some social activities, such as food sharing. It has been proposed that Homo habilis (ancestor of Homo erectus, living about 2.3 million to 1.4 million years ago) needed to use correspondence constructions when butchering large animal carcasses (Parker & Gibson, 1979). Distributing pieces of a divided whole (e.g.,

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prey) into equal parts required the ability to construct one-to-one correspondences. Paleolithic man was probably able to match the number of objects in different groups and, eventually, the number of objects in a collection with the number of items in some external cue system, e.g., fingers or pebbles (incidentally, calculus means pebbles). The immediate recognition of certain small quantities is found not only in animals, but also in small children. Animals and children can readily distinguish one, two, or three objects (Fuson, 1988; Wynn, 1990, 1992; Cook & Cook, 2009). Antell and Keating (1983) observed that newborn infants were able to discriminate among visual stimulus arrays consisting of a few dots. It was found that infants were able to discriminate between small numbers (2 versus 3) but not for larger sets. This ability for discriminating and also representing and remembering small numbers of items has also been reported by other authors (e.g., Starkey & Cooper, 1980). Interestingly, evoked potentials at three months are already capable of marking changes in the nature and number of a set of objects, and these activation changes relate to the parietal lobe (Dehaene & Dehaene-Lambertz, 2009). Noteworthy, in normally developing children and adults, the increase in arithmetic competence is associated with shift of activation from frontal brain areas to parietal areas. A shift of activation is also observed within the parietal lobe from the intraparietal sulci to the left angular gyrus; experts arithmetic proficiency depends on a more extended activation than the network found in beginners. In expert individuals with solid, extensive mathematical training, specific brain activation changes are also observed (Zamarian et al., 2009). Oneness, twoness, and threeness seemingly are basic perceptual qualities that our brain can distinguish and process without counting. It can be conjectured that when prehistoric humans began to speak, they may have been able to name only the numbers one, two, and three, corresponding to specific perceptions. To name them was probably no more difficult than naming any other sensory attribute (Dehaene, 1997). Of note, all world languages can count up to three, even though three may represent many, several, or a lot (Hurford, 1987). One is obviously the unit, the individual (the speaker may also be one). Two conveys the meaning of another (for example, in English and also in

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Spanish, second is related with the verb to second and the adjective secondary). Three may be a residual form of a lot, beyond the others, or many (for example, troppo, which in Italian means too much, is seemingly related with the word three -tre). In the original Indo-European language, spoken perhaps some 1500020000 years ago, apparently the only numbers were one, one and another (two), and a lot, several, or many (three) (Dehaene, 1997). Interestingly, in some contemporary languages, two different plurals are found: a plural for small quantities (usually two, sometimes three and four) and a second plural for larger quantities; for instance, in Russian, one house is odin dom, two, three, or four houses is dva, tri, cheterye doma but five houses is pyat domov. Of note, in different world languages, the word one does not have any apparent relationship with the word first; and the word two is also not related with the word second. Three may sometimes, but not always, hold some relationship with third. Beyond three, ordinals are clearly associated with cardinal numbers (Table 5.2). The conclusion is obvious: for small quantities (one, two, three), cardinals and ordinals must have a different origin. For larger quantities, ordinal numbers are derived from cardinals. As a matter of fact, one/first and two/second correspond to different conceptual categories. It may be speculated that for pre-historic man the first person and the second person in a line (or the first animal and the second animal during hunting, or other similar concepts) do not seem to be related with the number one and the number two. For small children first has the meaning of initial (e.g., I go first) whereas second is related to later or after (e.g., you go second). These words have a temporal and also spatial meaning, but not an evident numerical meaning. The association between one and first, and two and second seems a relatively advanced process in the development of numerical concepts. That is, the numerical meaning of first and second seems to appear after its temporal and spatial meaning. The association between ordinals and cardinals becomes evident only for larger quantities (more than three) and seems to represent a later acquisition in human evolution and the complexization of numerical concepts. Moreover, in many contemporary languages (e.g., the Huitoto language, spoken by the Huitoto Indians in the Amazonian

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jungle; indian-cultures.com/ Cultures/huitoto.html) there are no ordinal numbers. For first, the Huitoto language uses the beginning; to express second the word another is used.

____________________________________________________________________________________

English Spanish Russian

Greek Persian

Arab

Hindi

Aymara(1)

Ibo (2)

____________________________________________________________________________________ One First Two Second Three Third Four Fourth Five Fifth Six Sixth Uno Primero Dos Odin Pervie Dva Ena Proto Dio Yek Aval Dou Wahid Awal Ek Pahla Maya Nairankiri Phaya Payairi Kimsa Kimsairi Pusi Nbu Onye-nbu Ibua Onye-ibua Ito Nke-ito Ano Nke-ano Ise Nke-ise Isi Nke-isi

Ethnaim Do Thani Dusra

Segundo Vtoroi Tres Tercero Cuatro Cuarto Cinco Quinto Seis Sexto Tri Treti Cheterie Chetviorti Piat Piati Shest Shestoi

Deftero Douvoum Tria Trito Seh Sevoum

Thalatha Tin Thalith Arrbaa Rabiek Khamsa Khamis Sitta Sadis Tisra Char

Tesera Chahaar Tetarto Pente Chaharoum Pang

Chautha Pusiiri Panch Pheschka

Pemto Panjoum Exi Ekto Shash Shashoom

Panchvan Pheskairi Chha Sojjta

Chhatha Sojjtairi

On the Origins of Human Cognition 136 Seven Siete Siem Epta Haft Sabaa Sabieh Sat Pakallko Isaa Nke-isaa Asato Nke-asato Itonu Mke-Itonu Iri Mke-iri

Seventh Septimo Sidmoi Eight Eighth Nine Ninth Ten Tenth Ocho Octavo Nueve Noveno Diez Decimo Vosiem Vosmoi Dievit Diviati Diesit Disiati

Evthomo Haftoom Octo Hasht

Satvan Pakallkoiri Kimsakallko Kimsakallkiri Llatunca

Thamania Ath Thamin Tisaa Tasih Ashra Asher Athvan Nau

Ogdoo Hashtoom Enea Enato Deka Nouh Houhum Dah

Nauvan Llatuncairi Das Tunca

Dekato Dahoom

Dasvan Tuncairi

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(1) Ameridian language spoken in Bolivia; (2) Ibo: Eastern Nigeria

Table 5.2. Cardinal and ordinal numbers in different languages

Arithmetical abilities are clearly related with counting. Counting not simply recording the approximate amount of motor responses required for obtaining reinforcement, but actually saying aloud a series of number words that correspond to a collection of objects is relatively recent in human history. Counting also occurs relatively late in child development. In human history, as well as in child development, counting using number words begins with sequencing the fingers (i.e., using a correspondence construction) (Hitch et al., 1987). The name of the finger and the corresponding number can be represented using the very same word (that means the very same word is used for naming the thumb and the number one; the very same word is used to name the index finger and the number two, etc.). The fingers (and toes; as a matter of fact, many languages such as Spanish use

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a single word (dedo) to name both the fingers and toes) are usually sequenced in a particular order. This strategy represents a basic procedure found in different ancient and contemporary cultures around the world (LevyBruhl, 1910/1947; Cauty, 1984; Klein & Starkey, 1987; Dansilio, 2008). Interestingly, it has been demonstrated that children with low arithmetical skills also present a finger misrepresentation on the Draw-a-Person test (Pontius, 1989). This observation has been confirmed in different cultural groups. By the same token, difficulty in recognizing and naming the fingers represents a reliable predictor of developmental dyscalculia (Kaufmann, 2008). Taking a typical example as an illustration, the Colombian Sikuani or Guahibo Amazonian jungle Indians (indian-cultures.com/Cultures/guahibo.html) count in the following way: the person (an adult when counting or a child when learning to count) places his/her left hand in supination; to point to number one, the right index points to the left little finger, which is then bent (Queixalos, 1989). The order followed in counting is always from the little finger to the index. To point to number five, the hand is turned and the fingers opened; for six, both thumbs are joined, the left fingers are closed, and the right opened; they are opened one after the other for seven, eight, nine and ten. Between 11 and 20, the head points to the feet and the sequence is re-initiated. The lexicon used is: 1: kae (the unit, one) 2: aniha-behe (a pair, both) 3: akueyabi 4: penayanatsi (accompanied; that is, the fingers together) 5: kae-kabe (one hand) Numbers from six to nine, are formed with one hand and (a certain number) of fingers. Ten becomes two hands: 6: kae-kabe kae-kabesito-nua (one hand and one finger) 7: kae-kabe anih-akabesito-behe (one hand and a pair of fingers)

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10: anih-akabe-behe (two hands) Two hands is maintained between 10 and 20. Toes (taxawusito) are added between 11 and 14; and one foot (kaetaxu) is used in 15. Twenty is two hands together with two feet: 11: aniha-kabe-behe kae-taxuwusito (two hands and one toe) 12: aniha-kabe-behe aniha-tuxuwusito-behe (two hands and two toes) 15: aniha-kabe-behe kae-taxu-behe (two hands and one foot) 16: aniha-kae-behe kae-taxu-behe kaetaxuwusito (two hands, one foot, and one toe) 20: aniha-kabe-behe aniha-taxu-behe (two hands and two feet) Fingers are named according to their order in counting (as mentioned above, counting begins always with the little finger of the left hand). The Sikuani language possesses number words only up to three (kae, aniha-behe, akueyabi). Four (penayanatsi = accompanied, together) represents a correspondence construction. Strictly speaking, the Sikuani language counts only up to three. From four to twenty, they use a correspondence construction, not really counting; and for higher quantities, they resort to a global quantification. Sometimes not only the fingers (and toes) but also other body segments may be used in counting: the wrist, the shoulders, the knees, etc. (Levy-Bruhl, 1910/1947; Cauty, 1984; Dansilio, 2008). However, sequencing the fingers (and toes) represents the most universal procedure in counting. Some languages (e.g., some Mayan dialects and Greenland Eskimo) use the same word to denote the number 20 (that is, all the fingers and all the toes) and a person. In different Amerindian languages, for higher than 10 or 20 figures, most often many is used (global quantification principle) (Cauty, 1984; Ifrah, 2000). Or, they can refer to other peoples hands (correspondence construction) (e.g., thirty-five might be something like my two hands, my two feet, my fathers two hands, my fathers one foot). As

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mentioned, twenty sometimes becomes something like one person, a sort of higher order numeral. It is interesting to note that in some contemporary languages (like English and Spanish) one means the unit, but it is also used as a sort of indefinite personal pronoun. In English and Spanish we can also use one as synonymous with myself. Twenty is found to be the base number in the Mayan numerical system (Swadesh, 1967; Cauty, 1984). In many contemporary languages, a 10 and/or 20 base is evident. Digit (from Latin digitus) means both number and finger. The correspondence construction between numbers and fingers is evident. Latin number notation was originally Etruscan (Turner, 1984) and referred (as in other languages) to the fingers. One, two, and three were written simply by making vertical strokes. In four, the Latin system resorts to a simplification. Originally, four was written IIII, but later on it became IV. Five (V) represented the whole hand with the arm bent (that is, all the fingers of the hand), and ten (X) the two arms crossed. From a neuropsychological perspective, a strong relationship between numerical knowledge, finger gnosis, and even lateral (rightleft) knowledge is evident (Ardila and Rosselli, 2002; Kaufmann, 2008). Finger agnosia (and probably rightleft discrimination disturbances) could be interpreted as a restricted form of autotopagnosia (inability to recognize or localize the various body parts) (Ardila et al., 1989, 2000). It is not surprising to find that a decimal (or vigesimal, i.e., with a base of 20) system has been most often developed. Simultaneously or very close in time, decimal systems appeared in different countries (Sumer, Egypt, India, and Crete). Different symbols were used to represent 1, 10, 100, and 1000 (Childe, 1936; Dansilio, 2008) (Figure 5.1.).

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Tabla 5.3. Different numerical systems

There is, however, an interesting and intriguing exception: Sumerian and later Babylonians (about 2,000 BC) developed not only a decimal but also a sexagesimal system: a symbol represented 60 or any 60-multiple and another different symbol represented the number 10 and any 10-multiple. Thus, for example, the number 173 was then represented: 2 60 (the symbol for 60 repeated twice) + 5 10 (the symbol for 10 repeated five times) + 3 (a symbol for units repeated three times). A base of 60 has remained for some contemporary time measures (e.g., minutes and seconds). Twelve is also frequently maintained as a second-order unit (e.g., a dozen). Evidently, 60 results from five times twelve. Five obviously is one hand, and the question becomes, where

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does 12 come from? What are the two additional units? It might be speculated that 12 means the 10 fingers plus the two feet or even the two elbows or the two shoulders or the two knees (individuality of components is easier to appreciate in the hands than in the feet). But this is only speculation, although it is feasible according to our knowledge about counting procedures used in different cultural groups (Levy-Bruhl, 1910/1947; Ifrah, 2000; Dansilio, 2008). Maya Indians developed a similar system, but had 20 as a base (Leon-Portilla, 1986). They used different symbols to represent 20, 400 (20 20), and 8000 (20 20 20) (Cauty, 1984) (Figure 5.1.)

Figure 5.1. Maya vigesimal numerical system.

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Thus, reviewing the history of numerical concepts, it is found that world languages developed a base 10 (10 fingers) or 20 (10 fingers plus 10 toes) or even five (five fingers) to group quantities. In some contemporary languages a residual 20-base can be found (e.g., in French 80 can be four twenties). In many contemporary languages, different words are used between 1 and 10. Between 10 and 20, the numerical systems usually become irregular, unpredictable, and idiosyncratic. From 20 onward, numbers are formed simply with the words twenty plus one, twenty plus two, etc. Some contemporary languages still use a five-base in counting. For instance, in the Amerindian language Tanimuca in South America (www.ethnologue.com), speakers count up to five. Between five and 10, numbers are five one, five two, and so on.

Further developments of arithmetical abilities


Writing numbers appeared earlier in history than writing language. Some cultures (e.g., Incas) developed a number representing system, but not a language representing system (Swadesh, 1967). As mentioned before, calculus means pebble. Pebbles, marks, knots, or any other element were used as a correspondence construction to record the number of elements (people, cows, fishes, houses, etc). In Sumer, the first number writing system has been found (about 3,000 BC) (Childe, 1936; Ifrah, 2000): Instead of using pebbles, fingers, or knots, it was simpler just to make a mark (a stroke or a point) on the floor, on a tree branch, or on a board if one wanted to keep the record. In Egypt, India and later in Crete, a similar system was developed: units were represented by a conventional symbol (usually a stroke) repeated several times to mean a digit between one and nine; a different symbol was used for 10 and 10-multiples. Incas Indians developed a special system to represent numbers with knots in a rope (quipus) (Ascher & Ascher, 1980) (Figure 5.2).

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Positional digit value is clearly evident in Babylonians, and around 1,000 BC, the zero was introduced. Positional value and zero are also evident in Maya Indians (Leon-Portilla, 1986). Egyptians and Babylonians commonly used fractions. Small fractions (1/2, 1/3, and 1/4) are relatively simple numerical concepts, and even chimpanzees can be trained to use small fractions (Woodruff & Premack, 1981). As pointed out, recognition of individual marks or elements up to three is easy: It represents an immediate perception readily recognizable. Beyond three, the number of marks (strokes or dots) usually has to be counted and errors are more likely. Furthermore, it is rather time-consuming and cumbersome to be constantly counting marks. Interestingly, the different digit notational systems always represent one, two and three with strokes (or points, or any specific mark). In other words, the numbers one, two and three are written making one, two or three strokes. But beyond these figures, digit writing may give way to other strategies. In our Arabic digit notation system, one is a vertical line whereas two and three were originally horizontal lines that became tied together by being handwritten (Ifrah, 2000). This observation may be related with the inborn ability to perceptually recognize up to three elements. Beyond three, errors become progressively more likely. Perceptually distinguishing eight and nine strokes is not as easy as distinguishing between two and three strokes. The introduction of a different representation for quantities over three was a useful and practical simplification.

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Figure 5.2. Example of an Inca Indian quipu.

The numerical system, along with measurement units, were developed departing from the body dimensions (fingers, hands, arm, steps, etc.). This tendency to use the human body not only to count but also as measure units is still observed in some contemporary measurement units (e.g., foot). Adding, subtracting, multiplying and dividing were possible in the Egyptian system, but of course, following procedures was quite different from those procedures we currently use. Egyptians based multiplication and division on the duplication and halving method (Childe, 1936). Interestingly, this very same procedure (duplicating and halving quantities) is also observed in illiterate people when performing arithmetical operations. Thus, to multiply 12 18 in the Egyptian system the following procedure was followed:

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1 2 *4 *8 Total

18 36 72 144 _____ 216

(The number 18 is duplicated one or several times, and the amounts corresponding to 12 (4 + 8 in this example) are selected and summed up: 72 + 144 = 216. To divide, the inverse procedure was used. Therefore, the procedure used to divide 19 by 8 would be: 1 *2 2 *4 *8 8 16 4 2 1

That is, 2 + 4 + 8 (2 + 1/4 + 1/8), which is 2.375 In brief, different steps were followed in the development of arithmetical abilities: representing quantities, initially as correspondence constructions (i.e., one mark represents one element), later new marks were added to represent larger quantities (usually 10); providing a positional value to the marks; using fractions; and computing quantities (adding and subtracting; and later multiplying and dividing). As pointed out, recognition of individual marks or elements up to three is easy: It represents an immediate perception readily recognizable. Beyond three, the number of marks (strokes or dots) usually has to be counted and errors are more likely. Furthermore, it is rather time-consuming and cumbersome to be constantly counting marks. Interestingly, the different digit notational

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systems always represent one, two and three with strokes (or points, or any specific mark). In other words, the numbers one, two and three are written making one, two or three strokes. But beyond these figures, digit writing may give way to other strategies. In our Arabic digit notation system, one is a vertical line whereas two and three were originally horizontal lines that became tied together by being handwritten (Ifrah, 2000) (Figure 5.3.) This observation may be related with the inborn ability to perceptually recognize up to three elements. Beyond three, errors become progressively more likely. Perceptually distinguishing eight and nine strokes is not as easy as distinguishing between two and three strokes. The introduction of a different representation for quantities over three was a useful and practical simplification.

Figure 5.3. Origins of the Arabic numbers 1, 2 and 3.

The numerical system, along with measurement units, was developed departing from the body dimensions (fingers, hands, arm, steps, etc.). This tendency to use the human body not only to count but also as measure units is still observed in some contemporary measurement units (e.g., foot).

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The neuroscience of calculation abilities


Since primary acalculia (a basic defect in computational ability) was initially described by Henschen (1925) it has been associated with left posterior parietal damage (e.g., Mazzoni et al., 1990; Ardila et al., 2000; Mayer et al., 2003). Furthermore, it was suggested that different cerebral pathways are responsible for processing rote numerical knowledge (e.g., multiplication tables) and semantic knowledge of numerical quantities. Dehaene and Cohen (1997) have proposed that a left subcortical network contributes to the storage and retrieval of rote verbal arithmetical facts, whereas an inferior parietal network is dedicated to the mental manipulation of numerical quantities. Neuroimaging techniques (e.g., fMRI) have been used to analyze the pattern of brain activity during diverse calculation tasks. It has been demonstrated that different brain areas are active during arithmetical tasks, but the specific pattern of brain activity depends on the particular type of task that is used. At minimum, the following brain areas become activated during calculation: the upper cortical surface and anterior aspect of the left middle frontal gyrus (Burbaud et al., 1995); the supramarginal and angular gyrus (bilaterally) (Rueckert et al., 1996); the left dorsolateral prefrontal and premotor cortices, Brocas area, and the inferior parietal cortex (Burbaud et al., 1999); and the left parietal and inferior occipitotemporal regions (lingual and fusiform gyri) (Rickard et al., 2000). The diversity of brain areas involved in arithmetical processes supports the assumption that calculation ability represents a multifactor skill, including verbal, spatial, memory, body knowledge, and executive function abilities (Ardila & Rosselli, 2002). Dehaene et al. (2004), however, proposed that regardless of the diversity of areas that become active during arithmetical tasks, the human ability for arithmetic is associated with activation of very specific brain areas, in particular, the intraparietal sulcus (Figure 5.4). Neuroimaging studies with humans have demonstrated that the intraparietal sulcus is systematically activated during a diversity

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of number tasks and could be regarded as the most crucial brain region in the understanding and use of quantities (Ashkenazi et al., 2008). These observations have been supported using brain electrostimulation (Roux et al., 2009). Other brain areas, such as the precentral area, the inferior prefrontal cortex, and the inferior parietal cortex are also activated when subjects engage in mental calculations (Kas et al., 2011). Roca (2009) has proposed that there exists a frontoparietosubcortical circuit responsible for complex arithmetic calculations and that procedural knowledge relies on a visuo-spatial sketchpad that contains a representation of each sub-step of the procedure.

Figure 5.4. Left hemisphere intraparietal sulcus.

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Traditionally, calculation defects have been associated with posterior left parietal damage (Henschen, 1925; Boller & Grafman, 1983), and are frequently included in the socalled Gerstmanns (or angular gyrus) syndrome. Symptoms of Gerstmanns syndrome (acalculia with agraphia, disorders in right-left orientation, and finger agnosia) (Gerstmann, 1940) can be found during direct cortical stimulation in the angular gyrus region (Roux et al., 2003). Using fMRI, it has been observed that the left angular gyrus is not only involved in arithmetic tasks requiring simple fact retrieval, but may show significant activations as a result of relatively short training of complex calculation (Delazer et al., 2003). Colvin et al. (2005) investigated numerical abilities in a split-brain patient using experiments that examined the hemispheres abilities to make magnitude comparisons. One experiment examined the ability to enumerate sets of stimuli, and another two experiments required judgments about two concurrently presented stimuli that were either identically coded (i.e., two Arabic numerals, two number words, or two arrays of dots) or differently coded (e.g., an Arabic numeral and a number word). Both hemispheres were equally able to enumerate stimuli and make comparisons between numerical representations regardless of stimuli coding. However, the left hemisphere was more accurate than the right when the task involved number words. Cohen et al. (2000) reported a patient with a lesion in the left perisylvian area who showed a severe impairment in all tasks involving numbers in a verbal format, such as reading aloud, writing to dictation, or responding verbally to questions of numerical knowledge. In contrast, her ability to manipulate non-verbal representation of numbers, i.e., Arabic numerals, was comparatively well preserved. This observation supports the proposal that language and calculation disorders can be dissociated (Basso et al., 2000). Some authors have assumed that language and numerical concepts are organized differently in the brain and follow distinct developmental patterns in children (Gelman & Butterworth, 2005). Other authors have suggested that calculation and language are mediated by partially different and also partially overlapped brain systems (Baldo & Dronkers, 2007).

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Semenza et al. (2006) have emphasized that calculation and language usually share the same hemisphere. In summary, diverse brain areas are activated during the performance of different arithmetical tasks, although contemporary evidence suggests that the intraparietal sulcus seems to play the most crucial role. During the learning of new calculation abilities, additional brain areas become involved and the specific pattern of brain activity depends on the particular type of test that is used. It can be assumed that during human history, the development of new numerical abilities was correlated with the involvement of new brain areas during the performance of progressively more complex numerical tasks.

Conclusion
Arithmetical abilities and number representation have existed for only some 50006000 years. Most likely, during the Stone-Age, only simple counting up to three and, of course, bigger and smaller (magnitude judgment) concepts were present. Global quantification is observed at the pre-human level. Correspondence constructions allowed for increasing the amount of numbers to be used. The most immediate correspondence construction is performed with the fingers. Finger knowledge and counting represent, to a certain extent, the same cognitive ability, as is still evident in some contemporary languages, such as Sikuani. Counting, finger gnosis, and even lateral spatial knowledge may present a common historical origin. Seemingly, calculation abilities were derived from finger sequencing. Number representation and arithmetical operations are observed only since some 5000 6000 years ago. Currently, calculation abilities are rapidly evolving due to the introduction of modern technology and resulting cognitive demands. Right-left discrimination (as well as the use of other spatial concepts) most likely was present in pre-historic man, because requirements of spatial abilities may have been very high, even higher than in

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contemporary man (Hours, 1982; Ardila and Ostrosky, 1984; Ardila, 1993). Right-left discrimination and finger gnosis are strongly interdependent, and they can even be interpreted as components of the autotopagnosia syndrome. It seems, in consequence, that there is a rationale for finding a common brain activity for finger gnosis, calculation, and right-left discrimination (and in general, spatial knowledge mediated by language) (Ardila and Rosselli, 2002). Contemporary neuroimaging techniques, specifically fMRI, have demonstrated that the left parietal lobe, particularly the intraparietal sulcus, is systematically activated during a diversity of number tasks; other areas, particularly the frontal lobe, are also involved in processing numerical information and solving arithmetical problems. Also, it has been suggested there exists a frontoparietosubcortical circuit responsible for complex arithmetic calculations and procedural knowledge. It can be conjectured that numerical abilities continue evolving due to advances in mathematical knowledge and the introduction of new technologies; for instance, instead of writing numbers down on paper and applying certain computational rules, we more often require the ability to use a pocket calculator or a computer program. Doubtless, computation ability is evolving in a new direction. Brain representation of calculation may be taking a new direction, and even the acalculia syndrome may present different clinical manifestations.

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6. Origins of Executive Functions3

Introduction
"Executive functions" is a relatively new term in the neurosciences. Luria (1966, 1973, 1980) is the direct antecessor of the concept of executive functions. He distinguished three functional units in the brain: (1) arousal-motivation (limbic and reticular systems); (2) receiving, processing, and storing information (post-rolandic cortical areas); and (3) programming, controlling, and verifying activity, depending on the activity of the prefrontal cortex (Figure 6.1). Luria mentions that this third unit has an executive role. Lezak (1983) referred to "executive functioning" to discriminate cognitive functions from the "how" or "whether" of human behaviors. Baddeley (1986) grouped these behaviors into cognitive domains that included problems in planning, organizing behaviors, disinhibition, perseveration, reduced fluency, and initiation. Baddeley also coined the term "dysexecutive syndrome."

3 A previous version of this paper was published in: Ardila, A. (2008). On the evolutionary origins of executive
functions. Brain and Cognition, 68, 92-99

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Figure 6.1. Three functional units in the brain (Luria, 1966, 1973, 1980)

What does executive functions mean?


The definition of executive function includes the concept of mental flexibility and also ability to filter, interference, engage in goal-directed behaviors, and anticipate the consequences of one's actions (Ardila & Surloff, 2007; Denckla, 1994, 1996; Goldberg, 2001; Luria 1969, 1980; Stuss & Benson 1986; Stuss & Knight, 2002). The concept of morality, ethical behaviors, self-awareness, and the idea of the frontal lobes as manager and programmer of the human psyche are also included (Anderson et al., 1999; Damasio, 1994; Moll et al., 2005; Luria, 1980). During the late 19th and early 20th centuries, clinical investigations documented diverse behavioral disorders in cases of frontal pathology. "Frontal lobe syndrome" was

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conceptualized by Feuchtwanger (1923). He correlated frontal pathology to behaviors that were not related to overt speech, memory, or sensorimotor deficits. He emphasized the personality changes in motivation, affective dysregulation, and the capacity to regulate and integrate other behaviors. Goldstein (1944) expanded the capacity of frontal lobe behaviors to include "the abstract attitude," initiation, and mental flexibility. Luria (1966, 1969) related prefrontal lobe activity with programming motor behavior, inhibiting immediate responses, abstracting, problem solving, verbal regulation of behavior, and reorienting behavior according to behavioral consequences, temporal integration of behavior, personality integrity, and consciousness. During the 1970s, 1980s, and 1990s several books exclusively devoted to the analysis of the prefrontal cortex were published (e.g., Fuster, 1989; Miller & Cummings, 1998; Levin et al., 1991; Perecman, 1987; Pribram & Luria, 1973; Roberts, 1998; Stuss & Benson, 1986). These works usually assumed that "frontal" ("prefrontal") syndrome was synonymous with executive dysfunction (Figure 6.2). Progressively, it became apparent that prefrontal syndrome and executive dysfunction are not synonymous. The prefrontal cortex plays a key monitoring role in executive functions, but other brain areas are also involved (Elliott, 2003). Intact frontal processes, although not synonymous with intact executive functioning, are an integral part of it. Attempts to localize executive functioning to discrete frontal areas have been inconclusive. The emerging view is that executive function is mediated by dynamic and flexible networks. Neuroimaging results have also implicated posterior, cortical, and subcortical regions in executive functioning (Park et al., 2011; Roberts et al., 2002).

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Figure 6.2. Frontal lobe and its major areas.

Historically, Phineas Gage has become the most classical example for prefrontal lobe pathology and disturbances in executive functions (Harlow 1868) (Figure 6.3). Phineas Gage was a reliable foreman for a railroad company who suffered a tragic accident in which a tampering rod was projected through his frontal lobes. Miraculously he survived, but after this accident, he was described as "profane," "irascible," and "irresponsible." Profound personality changes were reported, and according to Harlow, he began to behave as an animal. The Phineas Gage case is usually cited as a typical example of executive function disturbances. It is obvious however, that Phineas Gages impairments were mostly situated at an emotional/motivational level, not at a purely cognitive (or metacognitive) level. Overt behavioral changes were observed as frequently found in frontal lobe pathology, but purely cognitive impairments were illdocumented, partially due to the lack of appropriate cognitive assessment instruments. Most frequently, executive functions are analyzed in experimental conditions using

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diverse research strategies, such as solving diverse problems, finding similarities between two words, providing an answer that requires inhibiting another, etc. A paradigm is created, and the subject is required to solve it. The brain activity can be simultaneously recorded, using brain electrical activity or recording the regional level of activation (e.g., Osaka, 2004). Alternatively, executive functions are analyzed in brain-damaged populations in order to find the contribution of different brain systems (e.g., Jacobs et al., 2007). This last approach represents the classical neuropsychological method. Executive functions, however, rarely are analyzed in natural ecological conditions. How is it that people solve everyday problems? This is obviously a crucial question in understanding human behavior.

Figure 6.3. Reconstruction of the wound suffered by Phineas Gage (according to Damasio et al., 1994)

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Tests for executive function typically represent external tasks, requiring the correct application of some intellectual abilities to be solved; for example, the Wisconsin Card Sorting Test (Berg, 1948; Heaton, 1981), the Tower of Hanoi (Simon, 1975) (Figure 6.4), and the Stroop test (Stroop, 1935) represent unusual and unfamiliar tasks, requiring the development of new strategies, planning, thought, flexibility, etc. Nonetheless, they are emotionally neutral tasks.

Figure 6.4. Tower of Honoi as an example of an executive functions test.

Although executive functions depend on extended networks including different brain areas, it is assumed that the prefrontal cortex plays a major controlling and monitoring role. Most important, prefrontal cortex does not only participate in those classically recognized executive operations (sequencing, alternating, inhibiting, etc), but also plays a crucial role in coordinating cognition and emotion (Mitchell & Phillips, 2007).

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Most of the disturbances reported in Phineas Gage (and in many other cases of prefrontal syndromes) refer to behavioral/emotional disturbances; or more exactly, disturbances in coordinating cognition and emotion/motivation. The prefrontal lobe has extensive connections to the subcortical and limbic system areas (Barbas, 2006; Damasio & Andersen, 1993) and even its orbital portion could be regarded as an extension of the limbic system. It seems that no laboratory test for executive function taps into the ability to coordinate cognition and emotion, and in that regard, no executive function test has significant ecological validity. By coordinating cognition and emotion, the prefrontal lobe plays a major function: controlling the limbic system impulses; that is, making limbic impulses socially acceptable (e.g., Beer, John, Scabini & Knight, 2006; Blair, 2004; Lezak et al., 2004). The inability to make basic biological needs socially acceptable, as clearly described in Phineas Gages case, frequently represents a major disturbance in prefrontal patients. Of course, we all would like to hit somebody when frustrated, to take possession of anything we want, to stay at home instead of performing fatiguing work, and to approach any potential sexual partner. That is exactly what many patients with prefrontal lobe pathology frequently do.

Is there any fundamental core ability accounting for executive functions?


Some disagreement exists around the question of unity or diversity (non-unitary) of executive functions (e.g., Duncan et al., 1996; de Frias, Dixon & Strauss, 2006; Grafman, 2006; Kimberg, dEsposito & Farah, 1997; Parkin & Java, 1999; Stuss, 2011). It is not clear what the particular unitary factor saturating the different executive function tests is. Behavior inhibition has been considered as a potential candidate for the single factor responsible for successful performance in different executive tests (Barkley, 1997) or in combination with working memory (Pennington & Ozonoff, 1996). Salthouse (1996, 2005)

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suggested that reasoning and perceptual speed represent the underlying factors related to all executive functions. Salthouse (2005) observed that performance on two common tests of executive functioning, the Wisconsin Card Sorting Test (Berg, 1948; Heaton, 1981) and the Controlled Oral Word Association Test (Benton, Hamsher & Sivan, 1994), were strongly correlated with reasoning ability and perceptual speed. Other authors challenge the existence of such a unitary factor. Godefroy et al. (1999) emphasized that certain frontal lobe patients perform well on some tests purported to assess executive abilities but not on others. Correlations among different executive tests are frequently moderate or low, and many times lacking statistical significance (Lehto, 1996; Friedman et al., 2006; Salthouse, Atkinson & Berish, 2003). Miyake et al. (2000) adopted an intermediate position. They studied three oftenpostulated aspects of executive functions (shifting, updating, and inhibition) and concluded that, although they are clearly distinguishable, they do share some underlying commonality. Based on the results of their study, the authors stated that executive functions are separable but moderately correlated constructs thus suggesting both unitary and nonunitary components of the executive system. By the same token, several authors have suggested different subcomponents of executive functions (e.g., Anderson, 2001; Delis, Kaplan & Kramer, 2001; Denckla 1994; Elliot, 2003; Hobson & Leeds, 2001; Lafleche & Albert, 1995; Lezak, 1983; Piguet et al., 2002). Stuss (2011) states that specific frontal regions control discrete functions and those very basic cognitive processes can be systematically manipulated to reveal those functions. According to him, recent studies have demonstrated consistent anatomical/functional relationships: dorsomedial for energization, left dorsolateral for task setting, and right dorsolateral for monitoring, and consequently, there is no central executive. There are, instead, numerous domain general processes discretely distributed across several frontal regions that act in concert to accomplish control. Stuss further supports the point of view that there are two additional "frontal" anatomical/functional relationships: ventral-

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medial/orbital for emotional and behavioral regulation, and frontopolar for integrative-even meta-cognitive-functions.

Two proposed fundamental executive functions


It may be conjectured that there are two different, but closely related types, of prefrontal lobe abilities (e.g., Fuster, 2002; Happaney, Zelazo, & Stuss, 2004; Stuss, 2011): (1) Metacognitive executive functions which include problem solving, abstracting, planning, strategy development and implementation, and working memory (the usual understanding of executive functions, generally measured in neuropsychology executive functions tests); these are abilities mostly related with the dorsolateral area of the prefrontal cortex (e.g., Stuss & Knight, 2002).The dorsolateral prefrontal cortex has been observed to participate in diverse planning, abstracting, problem solving, and working memory tasks. Using fMRI dorsolateral prefrontal activation has been found in tasks such as solving the Tower of Hanoi (Fincham, Carter, van Veen, Stenger & Anderson, 2002), Controlled Word Association Test (letter fluency) (Baldo, Schwartz, Wilkins & Dronkers, 2006), working memory (Yoon, Hoffman & D'Esposito, 2007), and solving the Wisconsin Card Sorting Test (Lie, Specht, Marshall & Fink, 2006). (2) Emotional/motivational executive functions, which is responsible for coordinating cognition and emotion. That means, the ability to fulfill basic impulses following socially acceptable strategies. In the last case, what is most important does not necessarily include what the best conceptual and intellectual result is, but what is in accordance with personal impulses (e.g., Bechara, Damasio & Damasio, 2000). In that regard, the core function of the prefrontal lobe is to find acceptable justifications for limbic impulses. Following socially acceptable strategies actually involves inhibition of selfish or unsociable basic impulses in the first place, but not necessarily arriving at the best

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conceptual solution. The ventromedial areas of the prefrontal cortex are involved in the expression and control of emotional and instinctual behaviors (Fuster, 1997, 2002). This function is related with so-called inhibitory control of behavior (Miller & Wang, 2006). Clinical evidence (e.g., Luria, 1969; Stuss & Knight, 2002) as well as experimental research (e.g., Leung & Cai, 2007; Medalla, Lera, Feinberg & Barbas, 2007) suggest that the neural substrate for this inhibitory function resides mainly in the medial and orbital portions of the prefrontal cortex. Fuster ( 2002) points out that The apparent physiological objective of inhibitory influences from orbitomedial cortex is the suppression of internal and external inputs that can interfere with whatever structure of behavior, speech, or cognition is about to be undertaken or currently underway (page 382). There is no question that if metacognitive executive functions were indeed used in solving external problems without the involvement of limbic impulses, most world-wide problems would have been solved by man, because contemporary man has sufficient resources to solve all the major social problems (such as poverty and war). Human conflicts in general would also be significantly reduced. Direct observation suggests that everyday problems usually have an emotional content: talking with a friend, a boss or a spouse; driving in the street; deciding how to approach somebody; spending money, etc., are not emotionally neutral activities, as are the Wisconsin Card Sorting Test (Berg, 1948; Heaton, 1981) and the Tower of Hanoi (Simon, 1975). When other people are involved, it is not easy to remain emotionally neutral. Social issues, simply speaking, are not emotionally neutral, because power/submission, personal benefits, and diverse biological drives are potentially involved (Smith, Bond & Kagitcibas, 2006). Most likely, throughout evolution of mankind (i.e., during the last 150,000 years) fulfilling these drives has been the major application of the prefrontal functions: to get power, to have a dominant role, to take food and goods for ourselves, to get a sexual partner, etc. That means that emotional/motivational executive functions have played a crucial role in survival and reproduction (e.g., facilitating behaviors such as acquiring dominant roles, obtaining sexual partners, etc). Mitchell and Phillips (2007) have argued that emotion can affect executive function

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ability. They propose that mild manipulations of negative mood appear to have little effect on cognitive control processes, whereas positive mood impairs aspects of updating, planning and switching. This effect of emotion on cognition has been supported for different executive function tasks, such as working memory (Spies, Hesse & Hummitzsch, 1996) and planning (Oaksford, Morris, Grainger & Williams, 1996) and using the Tower of London (Shallice, 1982) as a paradigm. In other words, when emotion is involved, metacognitive executive function ability decreases. Mitchell and Phillips (2007) emphasize that current evidence on the effects of mood on regional brain activity during executive functions demonstrates that the prefrontal cortex represents an area of integration between mood and cognition. These two types of executive functions (metacognitive and emotional/ motivational) depend on relatively different prefrontal areas, and as a matter of fact, two major variants in the prefrontal syndrome are frequently distinguished: one mostly impairing cognition (or rather, cognitive control, that is, metacognition); the other one mostly impairing behavior: (1) Dorsolateral syndrome. Cummings (1993) indicated that the dorsolateral circuit is the most important to executive functioning (Figure 6.5). The most noted deficit is an inability to organize a behavioral response to novel or complex stimuli. Symptoms are on a continuum and reflect capacity to shift cognitive sets, engage existing strategies, and organize information to meet changing environmental demands. Various researchers, including Luria (1969), have noted perseveration, stimulus-bound behavior, echopraxia, and echolalia. Lateralization has been noted in executive dysfunction (Goldberg, 2001). Ventral and dorsal portions of prefrontal cortex are bilieved to interact in the maintenance of rational and nonrisky decision making (Manes et al., 2002). According to Fuster (1997, 2002), the most general executive function of the lateral prefrontal cortex is the temporal organization of goal-directed actions in the domains of behavior, cognition, and language.

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Figure 6.5. Location of the dorsolateral prefrontal cortex.

(2) Orbitofrontal and medial frontal syndrome. Orbitofrontal damage has been associated with desinhibition, inappropriate behaviors, personality changes, irritability, mood liability, tactlessness, distractibility, and disregard of important events (Stuss & Knight, 2002). These patients are unable to respond to social cues. Noteworthy, it was observed by Laiacona and colleagues (1989) that these patients have no difficulty with card-sorting tasks. Eslinger and Damasio (1985) coined the term "acquired sociopathy" to describe dysregulation that couples both a lack of insight and remorse regarding these behaviors. The orbitofrontal cortex appears to be linked predominantly with limbic and basal forebrain sites. Medial frontal lobe damage causes apathy or abulia (a severe form of apathy). Acute bilateral lesions in the medial frontal area can cause akinetic mutism, in which the individual is awake and has self awareness, but does not initiate behaviors (Ross & Stewart, 1981). According to Fuster (1997, 2002) the ventromedial areas of the prefrontal cortex are involved in expression and control of emotional and instinctual behaviors (Figure 6.6). It is evident that the two prefrontal syndromes can have rather different clinical

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expressions (metacognitive and emotional/motivational) depending upon the specific location of the damage.

Figure 6.6. Location of the orbitofrontal cortex.

Metacognitive executive functions as an internalization of actions


As pointed above, disagreement persists around the potential unitary factor in executive functions. I will suggest that action representation (i.e., internally representing movements) may constitute at least one basic metacognitive executive function factor. I will refer to action representation and time perception, derived from it; both ultimately potentially depending upon one single core ability (sequencing?). Two departing observations are important to support the involvement of the prefrontal cortex in motor representation:

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1. Anatomical observation: Prefrontal cortex represents an extension and further evolution of the frontal motor areas. It may be conjectured that the prefrontal lobe should participate in complex and elaborated motor (executive) activities. 2. Clinical observation: A diversity of motor control disturbances are observed in prefrontal pathology, such as perseveration, utilization behavior, paratonia, primitive reflexes, etc. (e.g., Ardila & Rosselli, 2007a; Victor & Ropper, 2001). Several authors have argued that thought, reasoning, and other forms of complex cognition (metacognition) depend on an interiorization of actions. Vygotsky (1929, 1934/1962, 1934/1978), for instance, proposed that thought (and in general, complex cognitive processes) is associated with some inner speech. Vygotsky represents the most classical author suggesting this interpretation for complex cognition. More recently, Lieberman (2002a, 2002b) suggested that language in particular and cognition in general arise from complex sequences of motor activities. Vygotsky (1934/1978) developed the concept of extracortical organization of higher mental functions to account for the interaction of biological and cultural factors in the development of human cognition. Vygotskys (1934/1962, 1934/1978) understanding of higher mental functions is roughly equivalent to metacognitive executive functions. According to Vygotsky, a major factor in systemic organization of higher cognitive processes is the engagement of external instruments (objects, symbols, signs), which have an independent history of development within culture. Vygotsky called this principle of construction of brain functional systems the principle of extracortical organization of complex mental functions, implying that all types of mankinds conscious activities are formed with the support of external auxiliary tools or aids. However, different mediators and means, or significantly different details within them, (e.g., the direction of writing and degree of letter-sound correspondence, orientation by maps or by the behavior of sea-birds, etc.,) may develop, and in fact are developed in different cultures. Therefore, the analysis of

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cognitive processes must necessarily take into account these cross-cultural differences (Kotik-Friedgut & Ardila, 2004). The central point in Vygotskys (1934/1962) idea is that higher forms of cognition (cognitive executive functions) depend on certain mediation (language, writing or any other); the instruments used for mediating these complex cognitive processes are culturally developed. According to Vygotsky (1934/1962), the invention (or discovery) of these instruments will result in a new type of evolution (cultural evolution), not requiring any further biological changes. Thinking is interpreted as a covert motor activity (inner speech). Vygotsky (1929) assumes that thought and speech develop differently and independently having different genetic roots. Before two years of age, the development of thought and speech are separate. They converge and join at about the age of two years, and thought from this point on becomes language mediated (verbal thought). Language in consequence becomes the primary instrument for conceptualization and thinking. According to Vygotsky (1934/1962), speech develops first with external communicative/social speech, then egocentric speech, and finally inner speech. Vocalization becomes unnecessary because the child "thinks" the words instead of pronouncing them. Inner speech is for oneself, while external, social speech is for others. Vygotsky considered that thought development is determined by language. Vygotsky (1987) separated two different types of concepts: spontaneous and scientific. Spontaneous concepts are developed in a parallel way with language, whereas scientific concepts are concepts learned at school. Children progressively develop reflective consciousness through the development of scientific concepts. School is intimately related with learning a new conceptual instrument: reading. Written language is an extension of oral language, and represents the most elaborated form of language. Luria further extended Vygotskys ideas and attempted to find the neurological correlates for different components of complex cognitive processes. He clearly stated that mental functions are social in origin and complex and hierarchical in their structure and they all are based on a complex system of methods and means... (Luria, 1973; p. 30).

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In brief, Vygotsky (1934/1962) argued that complex psychological processes (metacognitive executive functions) derives from language internalization. Thinking relies on the development of an instrument (language or any other) that represents a cultural product. Lieberman (2002a, 2002b) refers specifically to the origins of language. He postulates that neural circuits linking activity in anatomically segregated populations of neurons in subcortical structures and the neocortex throughout the human brain regulate complex behaviors such as walking, talking, and comprehending the meaning of sentences. The neural substrate that regulates motor control (basal ganglia, cerebellum, frontal cortex) in the common ancestor of apes and humans most likely was modified to enhance cognitive and linguistic ability. Lieberman (2002a, 2002b) suggests that motor activity is the departing point for cognition. Speech communication played a central role in this process. The neural bases of mankinds linguistic abilities are complex, involving structures other than Brocas and Wernickes areas. Many other cortical areas and subcortical structures form part of the neural circuits implicated in the lexicon, speech production and perception, and syntax. The subcortical basal ganglia support the cortical-striatal-cortical circuits that regulate speech production, complex syntax, and the acquisition of the motor and cognitive pattern generators that underlie speech production and syntax. They most likely are involved in learning the semantic referents and sound patterns that are instantiated as words in the brains dictionary. The cerebellum and prefrontal cortex are also involved in learning motor acts (e.g., Hernandez-Mueller et al., 2005; Matsumura et al., 2004). Lieberman (2002a, 2002b) proposes that the frontal regions of the cortex are implicated in virtually all cognitive acts and the acquisition of cognitive criteria; posterior cortical regions are clearly active elements of the brains dictionary. The anterior cingulate cortex plays a part in virtually all aspects of language and speech. Real-word knowledge appears to reflect stored conceptual knowledge in regions of the brain traditionally associated with visual perception and motor control. Some aspects of human linguistic ability, such as the basic conceptual structure of words and simple syntax, are phylogenetically primitive and most likely were present in the

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earliest hominids. Lieberman (2002a, 2002b) further suggests that speech production, complex syntax, and a large vocabulary developed in the course of hominid evolution, and Homo erectus most likely talked, had large vocabularies, and commanded fairly complex syntax. Full human speech capability, enhancing the robustness of vocal communication, most likely is a characteristic of anatomically modern humans. These two authors (Vygotsky and Lieberman), although using rather different approaches, have both postulated that the development of language and complex cognition are related with some motor programs, sequencing, internalizing actions, and the like. The recent discovery of so-called mirror neurons represents a new element in understanding inner speech and action representation. A mirror neuron is a neuron which fires both when an animal performs an action and also when the animal observes the same action performed by another animal. In humans, brain activity consistent with mirror neurons has been found in the premotor cortex and the inferior parietal cortex (Rizzolatti et al., 1996; Rizzolatti & Craighero, 2004). In monkeys, the rostral part of ventral premotor cortex (area F5) contains neurons that discharge, both when the monkey grasps or manipulates objects and when it observes the experimenter performing similar actions. These neurons (mirror neurons) appear to represent a system that matches observed events to similar, internally generated actions. Transcranial magnetic stimulation and positron emission tomography (PET) experiments suggest that a mirror system for gesture recognition also exists in humans and includes Broca's area (Rizzolati & Arbib, 1998). The discovery of mirror neurons in the Brocas area might have immense consequences for understanding the organization and evolution of mankind cognition (Arbib, 2006; Craighero, Metta, Sandini & Fadiga, 2007). An obvious implication of mirror neurons is that they can participate in the internal representation of actions. Neuroimaging data have showed that interactions involving Broca's area and other cortical areas are weakest when listening to spoken language accompanied by meaningful speech-associated gestures (hence, reducing semantic ambiguity), and strongest when spoken language is accompanied by self-grooming hand movements or by no hand movements at all suggesting that Brocas area may be involved

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in action recognition (Skipper, Goldin-Meadow, Nusbaum & Small, 2007). PET studies have associated the neural correlates of inner speech with activity of the Brocas area (McGuire, Silbersweig, Murray, David, Frackowiak & Frith, 1996).

Is there anything special in the prefrontal cortex?


For some time it has been assumed that the prefrontal cortex is significantly larger in humans than in other primates (e.g., Blinkov & Glezer, 1968). This difference in volume was assumed to represent a major reason to account for differences in complex forms of cognition (executive functions) observed in humans. Nonetheless, such an assumption turned out to be incorrect. Measures of prefrontal lobe volumes have not found differences between mankind and non-human primates. Semendeferi et al (1997, 2002) measured the volume of the frontal lobe as a whole and of its main sectors (including cortex and immediately underlying white matter) in humans, chimpanzees, gorillas, orangutans, gibbons, and macaques using three-dimensional reconstructions of magnetic resonance (MR) scans of the brain. Although the absolute volume of the brain and the frontal lobe was found to be largest in humans, the relative size of the frontal lobe was similar across hominoids: macaque (28.1%), gibbon (31.1%), orangutan (35.3%), gorilla (32.4%), chimpanzee (35.9%) and human (36.7%). Most significantly, it was found that humans do not have a larger frontal lobe than expected from a primate brain of mankind size (Figure 6.7 and 6.8). Furthermore, the relative size of the sectors of the frontal lobe (dorsal, mesial, and orbital) was similar across the primate species studied. Semendeferi and colleagues suggested that the special cognitive abilities attributed to a frontal advantage may be due to differences in individual cortical areas and to a richer interconnectivity, none of which required an increase in the overall relative size of the frontal lobe during hominid evolution.

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Figure 6.7. Relative size of the prefrontal cortex in different primates (according to Semendeferi et al., 1997, 2002).

Schoenemann, Sheehan, and Glotzer (2005) found that a major difference between humans and other primates was the white matter volume. Using MRI from 11 primate species, the authors measured gray, white, and total volumes for both prefrontal and the entire cerebrum on each specimen. In relative terms, prefrontal white matter was found to have the largest difference between human and nonhuman, whereas gray matter showed no significant difference. Increased brain interconnectivity may represent a major characteristic of the human brain. As a note of caution, it is important to keep in mind that subjects used in this study were contemporary people, living in city environments, with a high level of education, etc., not humans living in those conditions existing 150,000 years

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ago. Stimulation can be rather different not only qualitatively but even probably quantitatively, potentially impacting on brain interconnectivity. It can be tentatively concluded that it is questionable that the size of the prefrontal cortex can account for the human executive functions. Some other factors have to be considered, such as connectivity (increased stimulation?).

Figure 6.8. Volume of the frontal lobe across species. Values include both hemispheres (according to Semendeferi et al., 1997, 2002).

Executive functions in pre-historical man

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Some recent studies have approached the question of the evolution of the prefrontal cortex and executive functions (Roth & Dicke, 2005; Risberg, 2006; Winterer & Goldman, 2003). It is usually accepted that Homo sapiens sapiens appeared about 150,000 years ago, and during this time, his brain evolution has been minimal (Wood, 1992). It means that humans existing since about 150,000 years ago had basically the very same neurological organization of contemporary individuals, including the biological foundations for the socalled executive functions. How were executive functions used by pre-historical man? Of course, we cannot be sure, but some few papers have approached this question (e.g., Bednarik, 1994, 2003; Coolidge & Wynn, 2001, 2005; Sugarman, 2002; Wayne, 2006). Coolidge and Wynn (2001) raised the question of how executive functions (supposedly, one of the key evolutionary acquisitions that led to the development of modern thinking) were demonstrated by prehistoric people. Coolidge and Wynn assumed that it is possible to match many of the features of executive function with activities reconstructed from archaeological evidence. The potential application of several components of executive function (such as sequential memory, task inhibition, and organization and planning) is analyzed by the authors: (1) Sequential memory: it can be speculated in the Palaeolithic Lithic reduction sequences, but even sophisticated procedures like Levallois can be explained without resort to closely-linked sequences of action. The production and use of barbed bone projectile points is another potential marker. The final product depends much more closely on a set sequence of actions. It is a true multi-step technology. (2) Tasks of inhibition, in which immediate gratification and action are delayed, are harder to identify archaeologically. Agriculture requires such inhibition. Facilities such as traps that capture remotely are technologies of inhibition and were probably present in the European Mesolithic. Palaeolithic examples are less convincing. Coolidge and Wynn (2001, 2005) consider that nothing of Middle Palaeolithic foraging, however, would require tasks of inhibition (indeed, they conclude that nothing in the archaeological record of Palaeolithic appears to require executive function). (3) Organization and planning is another basic

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executive function ability that likely was required for activities such as migration and colonization. Coolidge and Wynns (2001) review of the archaeological evidence finds no convincing demonstration for executive functions among the traces left by Neanderthals. The authors conclude that the archaeological records support the hypothesis that executive function was a late and critical acquisition in human cognitive evolution. In a very ingenious study, Stout and Chaminade (2007) using Positron Emission Tomography (PET) recorded the brain activity from six inexperienced subjects learning to make stone tools of the kind found in the earliest archaeological records. The authors found that tool making is associated with the activation of diverse parieto-frontal perceptual-motor systems, but no activation was observed in dorsolateral prefrontal cortex. They concluded that human capacities for sensorimotor adaptation, rather than abstract conceptualization and planning, were central factors in the initial stages of human technological evolution, such as making stone tools. Nonetheless, complex cognitive processes (i.e., metacognitive executive functions) seem to be crucial for further development and survival of Homo sapiens. The key factor for Homo sapiens late evolution seems to be the mental ability to plan and strategize, which allowed them to find innovative solutions to the many changing environmental problems to which they were exposed (Coolidge & Wynn, 2008). This may be one reason to account why Homo sapiens survived while Homo neanderthalensis disappeared. Changing environmental conditions (e.g., global climates changes) may require flexible survival strategies. It has been conjectured that during the past history changing physical environment conditions resulted in a selection that gave human ancestors adaptive versatility to endure increasing environmental instability (Bonnefille, Potts, Chali, Jolly, Peyron, 2004; Potts, 1996, 2004). Mithen (1994, 1996) has proposed the accessibility of mental modules as the impetus for mankind culture at the time of the Middle/Upper Palaeolithic transition, about 60,000 to about 30,000 years ago. He identified these mental modules as general intelligence, social intelligence, natural history intelligence, technical intelligence, and language. Probably, language was the most important one, increasing communication, and

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facilitating the transmission of knowledge, potentially resulting in an increased probability of survival and reproduction. It could be speculated that at the beginning of human history, transmitting knowledge from generation to generation was limited. Although some forms of learning can be transmitted by modeling or imitation (vicarious learning or social learning or modeling) (e.g., Bandura, 1977), language development represented a powerful instrument to accumulate and transmit knowledge about the world. The crucial point in the origins of executive functions becomes the possibility to conceptualize the environment (concepts are represented in words) and to transmit and progressively accumulate this knowledge about the world.

Metacognitive executive functions as a cultural product


There is no convincing evidence that Paleolithic individuals used executive functions (Coolidge & Wynn, 2001), which can be understood as the ability for planningetc. (first interpretation of prefrontal abilities: metacognitive executive functions). For thousands of years, prefrontal abilities were in consequence exclusively used to fulfill basic impulses following socially acceptable strategies (e.g., hierarchy in the group) (second interpretation of prefrontal abilities: emotional/motivational executive functions). Which were the milestones for cultural development and how did metacognitive executive functions appear? It could be speculated that some crucial inventions fueled the development of cultural evolution (Vygotsky, 1934/1962). For instance, a kind of cognitive fluidity has been postulated as a basic requisite for executing complex human activities (Gardner, 1983). The most important candidate for this crucial invention that fueled the development of cultural evolution is language. Language allows for the transmission of knowledge and facilitates survival and reproduction. Without language, children can learn from parents by imitation, but imitation is limited to some elementary activities, such as

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making a simple stone ax. Language represents a major instrument of internal representation of the world and thinking (Vygotsky,1934/1978). Language development obviously was a slow process taking thousands of years, but the most critical element of human language is the use of grammar, likely appearing some 10,000-100,000 years ago (Ardila, 2006). Probably, Homo neanderthalensis did not have a grammatical language and according to archeological evidence, did not use executive functions (Coolidge & Wynn, 2008). Language grammar likely developed from action internalization (Ardila, 2006). Written language represents an extension of oral language. Written language appeared only some 6,000-8,000 years ago and its diffusion has been so slow that even nowadays about 20% of the world population is illiterate (UNESCO, 2000). Performance in psychometric executive function tests has been observed to be very significantly correlated with subjects educational level (e.g., Ardila, Rosselli & Rosas,1989; Ardila et al., 2000; Ardila & Rosselli, 2007b; Ostrosky et al., 1998; Reis & Castro-Caldas, 1997; Rosselli et al., 1990). For instance, Gomez -Perez and Ostrosky-Solis (2006) observed that whereas tests related to memory are sensitive to aging, those related to executive functioning are mostly sensitive to education. It can be argued that illiterates possess basic executive functions (e.g., ability to internally represent actions) but they lack an important instrument to organize executive functions: written language.

Tentative conclusions
The analysis of executive functions represents one of the most intensively studied neuroscience questions during the last decade. The emphasis in reasoning, abstracting skills, behavioral control, anticipating the consequences of behavior, and similar abilities has contributed to the frequently found false idea that human behavior is guided by rationality. Human history blatantly contradicts this idea.

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This misinterpretation of mankind behavior is linked to the assumptions that the human brain is unique and superior to the brain of other species. We refer to our species as the wise man (Homo sapiens). By analyzing executive functions, it may be concluded that two different types of executive functions could be separated: metacognitive and emotional/motivational, depending on different brain systems. It could be argued that only the first one should be referred to as executive functions; usually, however, they are considered together in most definitions of executive functions, assuming a certain unity. Contemporary testing of executive functions has focused on abstracting, problemsolving, and similar metacognitive abilities. These metacognitive abilities seem to be useful in solving external and emotionally neutral problems. When social situations and biological drives are involved, the ability to rationally solve problems seems to decrease in a significant way. In this regard, contemporary testing of executive functions has limited ecological validity. Archeological analysis has discovered only some if any evidence of metacognitive executive functions in prehistorical man. We have to conclude that metacognitive abilities represent a recent acquisition, not obviously dependent on recent biological changes. The development of some cultural instruments, potentially resulting in a new type of evolution has been suggested. Language as an instrument not only to conceptualize the immediate experience, but for its transmission of knowledge, has been proposed as the major cultural instrument for metacognition. Language complexity has historically increased with the development of written language. There is no question that some other cultural instruments have also contributed to the development of metacognitive abilities; for instance, mathematics, drawing, and technology (from the wheel to computers). From the point of view of the brain, metacognitive executive functions are not necessarily correlated with a further brain development; increased neural interconnectivity may potentially support the increased complexization of executive functions found in contemporary Homo sapiens.

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7. How we recognize other people?

Introduction
Recognition of own-species members represents a basic survival ability not only for prehistorical man, but also for every living creature. Lacking this ability, any species would quickly disappear. Recognition of the own species members is based on a wide range of multiple sensory information. For instance, insects rely especially on olfactory information to identify other members of their own species, whereas primates use mainly but not exclusively visual information (de Waal , 2003; Hinde, 1974; Jolly, 1972; Rssler & Zube, 2010). In mankind, the critical and distinguishing signal features used in the recognition of other species members have somehow evolved in a parallel way with cultural evolution, as a result of the use of different clothes, costumes, paintings, hair-styles, make-ups, etc. People also use a diversity of non-verbal behavior strategies to communicate a given intention without pre-established conventions (Noordzij et al., 2009). Paleolithic man most likely lived in small social groups, similar in size to a primate troop, that is, about 10-100 individuals, composed by one or several couples and their offsprings (Ridley, 1986); noteworthy, in modern society, we keep affectively living in a primate-like troop composed by some 10-100 individuals relatives and friendswith whom we maintain a close affective relationship. Some primitive societies that depend on hunting and gathering of patchy distributed resources form casual societies not unlike the primate model (Lee & DeVore, 1968; Wilson, 1975), and the primate model was most likely the first type of social organization (Van den Berghe, 1979). However, the number of individual faces that we are potentially able to recognize -"familiar faces", is notoriously over 100, and probably it can be situated in the order of several thousands. For the prehistorical man, recognition of other species members was most critical. According to the living conditions of the prehistorical man, people recognition was suppose to answer at least two of the following questions: (1) Does the other individual belong to the

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same species (i.e., is he/she another Homo sapiens individual)?; (2) what is his/her gender?; (3) what is his/her emotional state; i.e., is he/she a friend or an enemy? Is he/she a known (endogroup member; "familiar individual") or unknown (exogroup person; "nonfamiliar individual") person? And (4) what particular individual is he/she?

Own-species members recognition


Recognition of the own species members does not seem so critical for the contemporary man, as it was for prehistorical people. However, for people currently living in the Amazonian jungle and other natural environments, it continues being equally critical as it was during prehistorical times. It is evident that in Bogot, New York or Paris, the possibilities to meet a member of another species (for instance, a bear, a lion, etc.) are quite low. For the prehistorical man, (and it is for a contemporary Tucano Indians living in the Amazonian jungle) a moving animal supposed the question about what species in particular it is. Brain organization of other people recognition has been studied under normal, but pathological, conditions. Its disturbance is usually known as prosopagnosia (e.g., Bodamer, 1947; Busigny & Rossion, 2009; Damasio et al, 1982). Prosopagnosia can be defined as an acquired disturbance in the ability to identify familiar faces. Specialized brain areas involved in face recognition have been studied. Usually, the damage in the occipito-temporal area, either bilateral (e.g., Bruyer et a, 1983; Damasio et al, 1982; Ettlin et al, 1992; Meadows, 1974) or right (e.g. Benton, 1990; De Renzi, 1986a; Landis et al, 1986, 1988; Whiteley & Warrington, 1977) have been associated with disturbances in face recognition. It is usually assumed that a bilateral occipitotemporal network mediates face perception (Minnebusch et al., 2009); when this network is disrupted, face recognition defects are observed. fMRI procedures have significantly contributed to further our understanding on brain

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organization of face perception. It has been found that the brain areas involved in face recognition include the right middle fusiform gyrus, the left inferior occipital gyrus, and in the right posterior superior temporal sulcus. The dorsal part of the lateral occipital complex and the human middle temporal cortex are localized bilaterally (Freeman et al., 2009; Sorger et al., 2007). Marotta et al., (2001) investigated whether patients with prosopagnosia would show functional activation in the fusiform gyrus, -the most important brain area usually regarded as the neural substrate for face processing (Furi et al., 2010)-, when viewing faces. While the patients did show activation in the fusiform gyrus, with significantly more voxels in posterior areas than their control subjects, this activation was not sufficient for face processing. In one of the patients, the posterior activation was particularly evident in the left hemisphere, which is thought to be involved in feature-based strategies of face perception, but not in the global recognition of faces. The authors concluded that an increased reliance on feature-based processing in prosopagnosia leads to a recruitment of neurons in posterior regions of the fusiform gyrus, regions that are not ideally suited for processing faces. Although testing for prosopagnosia is usually carried out using photographs of faces (Benton et al., 1994; Warrington, 1984), this method obviously represents an extremely artificial situation. It is interesting to note that untrained people are unable to recognize individual faces and even everyday objects in photographs. Moldiano et al. (1982) observed in Mexican Indian children an average error rate of 20% in identifying color paintings of everyday objects. There is no question that recognition of individuals in photographs represents a learned and highly trained ability that we usually take for granted. Little children have a great difficulty to recognize even their own parents and siblings in photographs. This ability is usually achieved around the age of two years, if adequate training opportunities are provided (Ellis, 1992). Face recognition disturbances usually present some specific characteristics: (1) prosopagnosic patients most often recognize different human races (caucasian, mongoloid, black), and they can sort human and animal faces (Benton, 1980, 1990; De Renzi, 1986b); (2) they can also distinguish fruits from flowers, and cars from furniture, although they are

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unable to know what specific category member it is (i.e., what particular fruit, flower, car, or furniture is); (3) prosopagnosic patients usually recognize the general category "human face" (or "fruit" or "flower), and they can even separate human faces from their corresponding cartoons (Lopera & Ardila, 1992), but they fail in recognizing the individual members of the category. These clinical characteristics would suppose the existence of a highly specialized brain system adapted to recognize own-species members. Nonetheless, although prosopagnosic patients usually can separate pictures corresponding to people (own species) from picture corresponding to animals (other species), they eventually can fail in performing this task (Benson et al., 1974; Bornstein et al., 1969). This failure supposes an impairment in those specialized own-species brain detector systems. Farah et al. (1991) have pointed that the visual recognition of living and nonliving things can be selectively impaired in cases of brain damage. Patients with prosopagnosia can present an evident difficulty in recognizing animals and plants; nonetheless, they usually present a better preserved ability to recognize inanimate objects. A neural system relatively more important for recognizing living than nonliving things was proposed by the authors; this system can be selectively impaired by brain damage. Higher visual centers would be specialized not just to recognize faces, but for the perception of biological forms. One subsystem of this higher system specialized in the perception of biological forms would correspond to "human face recognition". Farah et al (1991) point of view in general supports the perceptual model proposed by Konorski (1967). This perceptual model postulates the existence of different gnosic brain areas specialized in the recognition of manipulable and nonmanipulable objects, human faces, emotional facial expressions, and animated objects. By the same token, in cases of anomia associated with brain damage, it has been observed that some specific semantic categories can be selectively impaired, while others are better preserved (Ardila & Rosselli, 2007; Warrington & Shallice, 1984). This specificity has been also shown in memory (Farah et al., 1989). Human species members recognize one another basically (although, not exclusively) based in some visual information. Ethology has carefully studied different species' "sign

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stimuli" (Eibl-Eibesfeldt, 1970; Mazur, 2005; Tinbergen, 1951). A sign stimulus refers to some features of the objects that have been shown to be of major importance in eliciting responses (Hinde, 1970). The human face evidently could be considered as a "sign stimulus". The visual recognition of own species members, as well as the auditory recognition of own species calls, in several animal species (including mankind) have been shown to be somehow biologically programmed (Martinez & Matsuzawa, 2009). Some neurons in different animals' auditory cortex only fire when using the same species calls (Brugge & Reale, 1985), and probably, this also holds true when visually perceiving members of the own species (Gross et al, 1972; Rolls, 1984). Perret et al. (1982) found that about 10% of the neurons they sampled in the superior temporal sulcus of the macaque monkey selectively respond to faces and not to other stimuli. Desimone et al (1984) found in the inferior temporal cortex a population of cells that responded selectively to faces. The responses of these cells were dependent on the configuration of specific face features, and their selectivity was maintained over changes in stimulus size and position. A particularly high incidence of such cells was found deep in the superior temporal sulcus. Baylis et al. (1985) observed that 77% of 44 face-neurons in this temporal area reliably responded more to some specific faces than to others. Perret et al. (1984) claimed to have found cells that are peculiarly responsive to a particular human face often seen by the monkey. And Heywood and Cowey (1992) described cortical neurons that are selectively sensitive to faces, part of faces and particular facial expressions concentrated in the banks and floor of the superior temporal sulcus in macaque monkeys. The neurons of the superior temporal sulcus of monkeys would be, in consequence, part of a system specialized in faces. Ojemann et al (1992) recorded neuronal activity in adult human subjects and observed that 62% of the studied neuronal populations in the nondominant temporal lobe presented significant changes in activity during matching of faces and 52% during labeling of facial emotional expressions. These results would support the specificity of a highly specialized neuronal face-recognition brain system.

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Although the overwhelming majority of cases of prosopagnosia reported in the literature presented in addition to the face recognition impairments, some associated deficits in the recognition of individual members belonging to other visual categories (most often, living things -fruits, flowers, etc., but also nonliving things -buildings, cars, furnitures, etc.) prosopagnosia can be occasionally restricted only to the recognition of faces (De Renzi, 1986; De Renzi et al, 1992; Farah, 1990). Conversely, there are patients with severe visual agnosia for real objects without any evident defect in face recognition (Feiberg et al., 1986; Hecaen & Ajuriaguerra, 1956). Furthermore, prosopagnosic patients can be able to perform very complex perceptual tasks and can perceive and recognize many stimuli that are visually more complex than human faces (Benton & Van Allen, 1972; Busigny et al., 2010; Damasio, 1985). This supposes specificity in face recognition defects. Busigny et al. (2010) tested a prosopagnosic patient in three delayed forced-choice recognition experiments in which visual similarity between a target and its distractor was manipulated parametrically: novel 3D geometric shapes, morphed pictures of common objects, and morphed photographs of a highly homogenous familiar category (cars). In all experiments, the patient showed normal performance and speed, and there was no evidence of a steeper increase of error rates and RTs with increasing levels of visual similarity when compared to controls. According to the authors, these data rule out an account of acquired prosopagnosia in terms of a more general impairment in recognizing objects from visually homogenous categories. They assume that overall, these observations allow for the conclusion that brain damage in adulthood may lead to selective recognition impairment for faces, perhaps the only category of visual stimuli for which holistic/configural perception is not only potentially at play, but is strictly necessary to individualize members of the category efficiently. In conclusion, it seems reasonable to suppose the existence of some brain neuronal subsystems specialized in the recognition of own-species members. These subsystems would participate in a higher neuronal system specialized in the recognition of biological forms. Individual members (individual faces) would be encoded into the "face recognition subsystem". The record of neuronal activity would affirm the existence of highly specialized

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neuronal subsystems involved in the perception of faces (Desimone et al, 1984; Gross et al, 1972; Heywood & Cowey (1992); Ojemann et al, 1992; Perret et al, 1982; Righart et al., 2010; Rolls, 1984).

Gender recognition
Gender recognition (filognosis; from the Greek, filo = gender) represents a crucial perception that will define further social behavior (100,000 years ago, and even nowadays). Taking into account that in mankind a moderate sexual dimorphism exists (females usually have an average smaller height and possess sexual signals that can be easily recognized either by the front or by the back; additionally, gait is different), it is easy to suppose that visual signals were for the pre-historical man, and continue being for contemporary man, relevant and effective (Morris, 1977). Furthermore, not only body configuration but also male's and female's clothes are quite different and identifiable in their construction, shape, and even colors. Some female primates have areas of "sexual skin" which swell and/or change in color with changes in the reproductive state of the animal (Hinde, 1974) representing an evident visual identification mark. Prosopagnosic patients may be unable to identify male and female faces (Bruyer, 1986; Damasio et al., 1990; Lopera & Ardila, 1992), and it can be proposed that they will also present general defects in recognizing males and females according to other (not facial) sexual signals. They can also present kind of whole-body recognition defect. Indeed, in prosopagnosia a defect not only in face but also in body perception can be found (Righart & de Gelder, 2007). The prosopagnosic patient described by Bauer (1982) decided to cancel his subscription to the journal Playboy after becoming prosopagnosic; Bauer suggested the possibility that his patient could present an agnosia for individual nudes, analogous to the defect in the recognition of individual faces. Conversely, the author of this paper studied a prosopagnosic patient with a virtually complete inability to recognize any face, and even to sort males and females faces. However, he easily and accurately

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distinguished male and female bodies. This implies that facial and whole-body males-females distinction can become dissociated. Or at least, that body recognition can be preserved, while face recognition is impaired. If this last assumption were true, it would imply a "sensitivity hierarchy": it is easier (and better preserved in brain-damaged patients) to recognize males-females using whole-body than facial signals. The idea that gender differences aid in the ability to recognize human faces has been suggested. Ino et al. (2010) performed a fMRI experiment in which participants encoded and recognized male and female faces. Behaviorally, the facial recognition ability of men and women was similar and was superior for female faces compared to male faces. At the neural level, widespread areas showed greater responses for men vs. women during the encoding and recognition phase, and several areas, including the hippocampal region, showed greater responses to female vs. male faces during recognition. The authors proposed that the reduced activation of women's brains during encoding and recognition suggests that the relevant neural systems were more efficiently recruited in women than in men. Noteworthy, visual signals are not the only ones used in gender recognition: there are also auditory signals resulting from a different voice timbre, and additionally, distinctive olfactory signals. Auditory and olfactory signals are probably more readily used in low illumination conditions, while visual signals are easily available in daytime conditions. These visual, auditory, and olfactory gender signals remain in our contemporary mankind members, despite the differences in cultural backgrounds. Visual marks have not changed, although usually they can be covered. Height differences remain, although women may use higher shoes for increasing their heights. The differences in gait are evident. Voice-timbre differences supposedly have not changed during the last 150,000 years. And olfactory signals can be artificially covered and replaced by other new olfactory signals, but anyhow they remain as gender marks. Olfactory recognition deserves some special consideration. Olfactory communication plays a crucial communication role in most animals, including primates (Hinde, 1970; Jolly, 1972; Mundy, 2006). Very often, sexual behavior is partially under olfactory control: a

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pheromone is produced that acts as a powerful attractant to the male (Hoover, 2010). The tendency of women living together to menstruate simultaneously may be mediated by olfactory stimuli (Carlson, 2009). A male pheromone is detected most easily by women of reproductive age, but men can smell it if given oestrogen; and olfactory threshold have been observed to vary during the menstrual cycle (Conform, 1970; Hinde, 1974; Eibl-Eibesfeldt, 1970). So, olfactory signals continue being effective in gender identification. Perfumery industry has become a solid and well-established enterprise. In summary, gender identification can be mediated by different types of signals: facial, whole-body, and even auditory and olfactory signals.

Emotional expression and emotional recognition


Some basic emotional expressions are universals and can be easily recognized by any member of any culture (Ekman, 1972; Kohler et al., 2004). Aggressive gestures, protective gestures, threatening signals, submissive postures, and sexual approach signals are roughly identical in any cultural group, and they are quite similar to those observed in non-human primates (Eibl-Eibesfeldt, 1970; Morris, 1977). It can be supposed that they existed in a similar form in the pre-historical man. Some other emotional expressions present major or minor variations across different cultural groups. Surprise, joy, mourning, etc., can present important cross-cultural differences. Special ornaments are often used to make a special emotional state even more easily identifiable: aggression, sexual interest, mourning, etc. (Ekman, 1972; Eibl-Eibesfeldt, 1973). During child development, the face represents the earliest visual stimulus capable to release an emotional response (Fantz, 1961). Facial identification and emotional recognition can be dissociated in brain-damaged individuals. In some cases of prosopagnosia the recognition of facial expression can be preserved while face identification is impaired (Bates et al., 2009; Bruyer et al., 1983; Shuttleworth et al., 1982).

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Conversely, some brain-damaged patients can preserve the ability to identify faces, but fail in recognizing facial emotional expressions. Most often, right hemisphere-damaged patients present serious difficulties to identify, match and comprehend emotional expressions (Feyereisen, 1986). Kurucz and Feldmar (1979) found that some patients could recognize photographs of famous faces, but they were unable to identify their facial expressions. By the same token, the patient reported by Lopera and Ardila (1992) did not recognize facial emotional expressions, but usually was able to deduce them (e.g., "This must be a smiling and joy face, because the teeth are seen through the mouth"). It becomes plausible that facial identification and the recognition of emotional expressions depend on, at least partially, different brain subsystems (Peelen et al., 2009; Stephan & Breen, Caine, 2006). Thus, two different visual agnosic syndromes could be found in brain-damaged patients: agnosia for faces (prosopagnosia) and agnosia for emotional expressions (prosopo-affective agnosia). Konorski (1967) proposed the existence of different brain systems (different "gnostic areas") to recognize human faces and to recognize emotional facial expressions. Recently it has been shown that whereas face recognition defects are associated with cortical damage (very specially, the right fusiform gyrus) the recognition of the facial expression of emotion depends on white matter association tracts, very specially the inferior fronto-occipital fasciculus (Philippi et al., 2009). Etcoff (1984) postulated the existence of different "modules" for the visual identification of faces and facial expressions. She observed that the speed and accuracy with which normal subjects perform a sorting task (to put photographs of faces in different piles according to either their identity or their expression) is not affected by whether facial identity is correlated with facial expression, implying that these two proprieties of faces are processes independently. Etcoff postulated that two separate brain modules underlie the recognition of facial identity and facial expression but that they are neuroanatomical neighbors. It has also been shown that prosopagnosic patients can retain some covert recognition of faces. These patients present a physiological response for familiar, but not for unfamiliar faces (Barton et al., 2001; Bates et al., 2009; Bauer, 1984; De Haan & Young,

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1987; De Haan et al, 1992; Tranel & Damasio, 1985; Young & De Haan, 1988). By the same token, in associative learning tasks, performance is better if familiar faces are used (Bruyer et al., 1983). These findings suggest that despite unawareness in face recognition, some covert face recognition can remain in prosopagnosia syndrome. However, this not surprising at all. Everyday experience discloses that very often, when seeing a particular face, we can be totally unable to identify who he/she is, despite having the "feeling" that we really know that particular individual; we simply have a "feeling of familiarity". The recognition of the individual member can be impossible in this everyday experience (and can be impaired in cases of brain-damage), but the distinction "familiar" and "not familiar" remains. Valds-Sosa et al. (2011) observed in a prosopagnosic patient face-selective activations bilaterally in his occipital gyri and in his extended face system (posterior cingulate and orbitofrontal areas), the latter with larger responses for previously-known faces than for faces of strangers. In the right hemisphere, these surviving face selectiveareas were connected via a partially persevered inferior fronto-occipital fasciculus. According to the authors, this suggests an alternative occipito-frontal pathway, absent from current models of face processing, that could explain the patient's covert recognition while also playing a role in unconscious processing during normal cognition.

Individuals' recognition
Endogroup members are usually very alike (resulting from endogamy) in their height, body contexture, skin color, and additionally, in the clothes and make-up they wear. Usually, they can be visually identifiable even at long-distances. Erroneously, we have learned that individuals are recognized just by their faces. This can be partially true in our urban societies, where we have very limited possibilities to perceive other individual characteristics (e.g., his/her body configuration, his/her gait, etc). In a survey of 1,000 peoples photographs (excluding commercial announcements)

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randomly taken from the two most influential newspapers and the two most influential magazines in Colombia, it was found that face photographs were about four times more frequently published than whole-body photographs. Evidently, we are over trained in individuals' recognition relying only on facial cues. However, facial information is quite insufficient to recognize individuals for anybody living in rural areas, in open fields or in savannas. People living in Argentinean Pampa or Paraguayan Chaco easily recognize approaching or passing-by people when they are still 500 meters or farther away. They do not depend, of course, solely upon face recognition to identify individuals (face can be recognized only within very short distances) but upon a broader diversity of signals, such as body configuration, gait, and even clothes. The human brain should possess not simply a system for encoding and memorizing faces (prosopognosis) but also for encoding and memorizing body configurations and general personal features (by the way, "prosopos" in Greek means not only face, but also person, and prosopagnosia should be understood as the inability to identify not simply faces, but persons). Thus, recognition of individuals and recognition of faces is not equivalent. The face is only one of the visual characteristics used to recognize individuals, but it is not the only one, and eventually, it was not the most important one for the prehistorical man (or for the current jungle inhabitants, for the inhabitants of the Argentinean Pampa or for army members), although evidently it is the most important one in our current city-living conditions. It could be conjectured that that in addition (or superimposed) to the ability to recognize faces, the human brain should possess an ability to recognize individual body configurations and body marks. Furthermore, faces yield information not only about the individual, but also (and eventually even more importantly) about his/her specific emotional state. By the same token, in everyday conditions, faces are not static but continuously moving. Interestingly, prosopagnosic patients may recognize faces on the basis of their idiosyncratic facial movements (Steede et al., 2007). To identify individual members one should be able to recognize body marks and general configuration (somagnosis, that is, body recognition), and face signals (prosopognosis). Patients with prosopagnosia cannot discriminate individuals members in a

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group, but they can use sufficiently evident visual marks (e.g., a face with wrinkles means that it should correspond to an elderly person; a face with a beard should correspond to a male, etc). Somagnosis has not been systematically analyzed in neuropsychology yet. Furthermore, it does not seem easy, considering that currently the most important body marks are the clothes (changing from one day to another), although it seems evident that some people possess a tremendous ability to identify individuals by their clothes. Our knowledge about other people's body configuration is in most cases just approximate. However, it is evident that in addition to memory for people's faces, we also have some memory for people's height, contexture, gait, etc. It is reasonable to suppose that patients presenting face recognition deficits may also present body recognition defects. Interestingly, patients with prosopagnosia usually also present difficulties recognizing animals, either animal faces or whole body recognition (Farah, 1989). Damasio et al (1982) reported a prosopagnosic patient with difficulties to identify people's gaits, but usually patients with prosopagnosia are not tested in recognizing people when using diverse visual characteristics, such as body configuration and gait. Different anatomical substrates have been suggested for the recognition of familiar and nonfamiliar faces (Warrington & James, 1967). Nonaphasic patients with right posterior lesions present the most remarkable difficulty in discriminating familiar faces. Lopera and Ardila (1992) proposed further to distinguish two different neuropsychological syndromes: prosopagnosia (as a more or less isolated perceptual defect in face recognition), and prosopamnesia (as a memory defect for faces). In the first case (prosopagnosia) right occipital-temporal damage would be sufficient; prosopamnesia would be associated with bilateral lesions. Individuals' face recognition would correspond to the specific elements (or items) of this "familiar faces" subsystem. De Renzi et al (1991) introduced a similar distinction and separated two forms of prosopagnosia: apperceptive (as a disorder in face identification), and associative (as amnesia for faces) forms of prosopagnosia. Wilkinson et al. (2009) observed that unilateral damage to the right cerebral hemisphere disrupts the apprehension of whole faces and their component parts.

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Barton (2008) proposed that, (1) prosopagnosia is more severe with bilateral than unilateral lesions, indicating a minor contribution of the left hemisphere to face recognition, (2) perception of facial configuration critically involves the right fusiform gyrus and (3) access to facial memories is most disrupted by bilateral lesions that also include the right anterior temporal lobe. According to the author, this supports assertions that more apperceptive variants of prosopagnosia are linked to fusiform damage, whereas more associative variants are linked to anterior temporal damage. It has been also further suggested that (a) the most specific forms of prosopagnosia are due to lesions of a right posterior network including the occipital face area and the fusiform face area, whereas (b) the face identification defects observed in patients with left temporo-occipital lesions seem due to a semantic defect impeding access to person-specific semantic information from the visual modality. Furthermore, face recognition defects resulting from right anterior temporal lesions can usually be considered as part of a multimodal people recognition disorder (Gainotti, G. & Marra, 2011). Probably, we have learned to identify faces in the same way that an ornithologist has learned to identify birds or a farmer to identify individual animals. Some reports point to the possibility of a prosopagnosic deficit restricted to a very specific visual subcategory. Assal et al. (1984) reported a case of a peasant devoted to caring for cows with a restricted agnosia for cows, associated with a transient prosopagnosia for human faces, anterograde and retrograde amnesia, and topographic amnesia. The patient had difficulty in visual imagery for cows but not for other visual categories, and visual hipoemotionality for cows faces ("the cows have lost their personality and colorfulness"). This case of restricted zooagnosia supports the specificity in learned visual recognition of individuals within a particular visual subcategory. Difficulties in recognizing faces belonging to a different racial group are well known to everyone, whereas twins are easily and errorless recognized by their own parents and siblings. It has been suggested that prosopagnosia arises due to an impairment of a process that reduces uncertainty about the nature/location of the diagnostic cues for face individualization: the ability to perceive multiple elements of a face as a single global

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representation (holistic processing) (Ramon & Rossion, 2010). Being impaired at processing individual faces holistically, prosopagnosic patients would tend to perform relatively worse for processing facial areas containing multiple elements (i.e., the eyes), and for elements that are widely spaced apart. Prosopagnosic patients usually recognize people when hearing their voices (e.g., Bodamer, 1947; Damasio et al., 1982). Voice recognition disorders impair the ability to recognize individuals. Phonagnosia has been defined as the acquired inability to recognize and discriminate voices (Van Lancker & Carter, 1982). A further distinction has been introduced between the discrimination of familiar and unfamiliar voices (Van Lancker et al., 1988; Van Lancker et al., 1989). Deficits in recognizing familiar voices are significantly correlated with damage to the inferior and lateral parietal regions of the right hemisphere, whereas impairment of voice discrimination abilities is associated with temporal damage to either hemisphere. This distinction clearly parallels the distinction between prosopagnosia and prosopamnesia (Lopera & Ardila, 1992) (or between apperceptive and associative prosopagnosia). It is important to point out that voices (like faces) also convey emotional information. Occasionally, only auditory (but not visual) information is used to recognize a particular individual (e.g., by phone). A whole array of neuropsychological syndromes could have been associated with defects in the recognition of individuals: some types of visual agnosia (prosopagnosia, afilognosia, asomagnosia), deficits in voices recognition (phonagnosia), and even eventually, disturbances in smell perception (hiposmia, anosmia, and potentially osmagnosia). In summary, it can be proposed that people recognition is based, predominantly but not exclusively, in some visual information. Different subsystems or modules can be distinguished. A first level analysis implies separating living (people, animals, plants) from nonliving things (furnitures, cars, etc). Individual identification supposes the distinction of familiar and nonfamiliar individuals. Additionally, gender and emotional states are to be recognized in order to achieve a unitary individual perception.

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Conclusions
A great effort has been devoted in neurology and neuropsychology to the analysis of face recognition under normal, and specially, under pathological conditions. However, cultural differences in people recognition show that, not only facial perception can be relevant in individuals' identification, but also other visual signals, such as body and gait characteristics. Furthermore, not only visual information may be relevant for people recognition; auditory and even olfactory information can be also important in people identification. Visual information can be more important in daylight conditions, while auditory and olfactory signals can become relevant in dim conditions. In cases of brain damage, sometimes one category or type of information can be preserved, whereas others are impaired. At least the following perceptual dissociations have been observed in brain-damaged patients: 1. Perception of living and non living things (Farah et al., 1991); 2. Perception of own-species and other species members; that is, people and animals (e.g., Benton, 1980, 1990; De Renzi, 1986; Farah, 1990); 3. Perception of familiar and nonfamiliar faces (e.g., Bauer, 1984; De Haan & Young, 1987; De Haan et al., 1992; Lopera & Ardila, 1992; Warrington and James, 1967); 4. Face identification and recognition of emotional expressions (e.g., Bruyer et al., 1983; Feyereisen, 1986; Shuttleworth et al., 1982); 5. Facial gender-identification and whole-body gender-identification (Ardila & Rosselli, unpublished); and

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6. Visual and auditory people recognition (e.g., Bodamer, 1947; Van Lancker et al., 1988; Van Lancker et al., 1989); Different subsystems (or "modules") could be involved in people recognition. "People" could represent a subsytem included within the higher level "living things" system. One subgroup of this "people" subsystem includes "familiar individuals" (versus "nonfamiliar individuals"). "Familiar individuals" includes all the stock of known people, perhaps, several thousands. Face can be enough to recognize an individual (although voice, gait, body configuration signals, etc., can be also enough to recognize the very same individual). Additionally, gender and emotional expression are conferred to familiar, but also to nonfamiliar persons. Gender and emotional expression can be recognized not only departing from visual, but also auditory information. Individual's recognition represents the final step in this people processing system. Individual's recognition (as it is the meaning of a particular word) represents a complex perception, including multiple association systems (especially visual, but also auditory and even olfactory), and maintaining some specific emotional, memory, and even verbal (individual's name) relationships.

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Modiano, N., Maldonado, L.M. & Villasana, S. (1982). Accurate perception of color illustrations: Rate of comprehension in Mexican Indian children. Journal of Cross-Cultural Psychology, 13, 490-495. Morris, D. (1977). Manwatching. A field guide to human behavior. New York: Elsevier. Mundy, N.I. (2006). Genetic basis of olfactory communication in primates. American Journal of Primatology, 68(6), 559-67. Noordzij, M.L., Newman-Norlund, S.E., de Ruiter, J.P., Hagoort, P., Levinson, S.C. & Toni, I. (2009). Brain mechanisms underlying human communication. Frontiers in Human
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Ojemann, J.G., Ojemann, G.A. & Lettich, E. (1992). Neural activity related to faces and matching in human right nondominant temporal cortex. Brain, 115, 1-14. Peelen, M.V., Lucas, N., Mayer, E. & Vuilleumier, P (2009). Emotional attention in acquired prosopagnosia. Social Cognitive and Affective Neuroscience, 4, 268-77. Perret, D., Rolls, E.T. & Caan, W. (1982) Visual neurons responsive to faces in the monkey temporal cortex. Experimental Brain Research, 47, 329-342. Perret, D., Smith, P.A., Potteer, D.D., Mistlin, A.J., Head, A.S., Milner, A.D. & Jeeves, M.A. (1984). Neurons responsive to faces in temporal cortex: studies of functional organization, sensitivity of identity and relation to perception. Human Neurobiology, 3, 197-208. Philippi, C.L., Mehta, S., Grabowski, T., Adolphs, R., & Rudrauf, D. (2009). Damage to association fiber tracts impairs recognition of the facial expression of emotion. Journal of

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Neurosciences, 29, 15089-99. Ramon, M. & Rossion, B. (2010). Impaired processing of relative distances between features and of the eye region in acquired prosopagnosia--two sides of the same holistic coin? Cortex, 46(3), 374-389. Ridley, M. (1986). The number of males in a primate troop. Animal Behaviour, 34, 18481858 Righart, R. & de Gelder, B. (2007). Impaired face and body perception in developmental prosopagnosia. Proceedings of the National Academy of Sciences of the United States of America, 104(43), 17234-8. Righart, R., Burra, N. & Vuilleumier, P. (2010). Face Perception in the Mind's Eye. Brain Topography Rolls, E.T. (1984). Neurons in the cortex of temporal lobe and in the amygdala of the monkey with response selective for faces. Human Neurobiology, 3, 209-222. Rssler, W. & Zube, C. (2010). Dual olfactory pathway in Hymenoptera: evolutionary insights from comparative studies. Arthropod structure and development Shuttleworth, E., Syring, V. & Allen, N. (1982). Further observations on the nature of prosopagnosia. Brain and Cognition, 1, 307-322. Sorger, B., Goebel, R., Schiltz, C. & Rossion, B. (2007). Understanding the functional neuroanatomy of acquired prosopagnosia. Neuroimage, 35, 836-52.

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Stephan, B.C., Breen, N. & Caine, D. (2006).The recognition of emotional expression in prosopagnosia: decoding whole and part faces. Journal of the International Neuropsychological Society, 12, 884-95 Steede, L.L., Tree, J.J. & Hole, G.J. (2007). I can't recognize your face but I can recognize its movement. Cognitive Neuropsychology, 24, 451-66. Tranel, D. & Damasio, A.R. (1985). Knowledge without awareness: an autonomic index of facial recognition by prosopagnosics. Science, 228, 1453-1454. Van den Berghe, P.L. (1979). Human family systems. New York: Elsevier. Van Lancker, D.R. & Carter, G.J. (1982). Impairment of voice and face recognition in patients with hemispheric damage. Brain and Cognition, 1, 185-195. Van Lancker, D.R., Cummings, J.L., Kreiman, J. & Dodkin, B.H. (1988). Phonoagnosia: a dissociation between familiar and unfamiliar voices. Cortex, 24, 195-210. Van Lancker, D.R., Kreiman, L. & Cummings, J.L. (1989). Voice perception deficits: neuroanatomical correlates of phonoagnosia. Journal of Clinical and Experimental Neuropsychology, 11, 665-674 Valds-Sosa, M., Bobes, M.A., Quiones, I., Garcia, L., Valdes-Hernandez, P.A., Iturria, Y., Melie-Garcia, L., Lopera, F. & Asencio, J. (2011). Covert face recognition without the fusiform-temporal pathways. Neuroimage, 57(3), 1162-1176. Warrington, E. K. (1984). Recognition Memory Test. Windsor, England: NFER-Nelson. Warrington, E.K. & James, M. (1967). An experimental investigation of facial recognition in

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8. Culture and Cognitive Testing4

Introduction
In neuropsychology, cognitive disturbances associated with brain pathology of a limited subsample of the human species --contemporary Western, and most often, urban middle-class and literate brain-damaged individuals-- have been relatively well analyzed. Our understanding about the brain's organization of cognitive abilities, and the disturbances in cases of brain pathology, is therefore not only partial but, undoubtedly, culturally biased (Ardila, 1995; Fletcher-Janzen, Strickland & Reynolds, 2000; Uzzell, Pontn & Ardila, 2007). Cultural and linguistic diversity is an enormous, but frequently overlooked, moderating variable. Several thousands of different cultures have been described by anthropology (e.g., Bernatzik, 1957; Rosaldo, 1993), and contemporary humans speak over 6,800 different languages (Grimes, 2000; www.ethnologue.com). Norms for performance in a sufficiently broad array of neuropsychological tests and an extended analysis of cognitive disturbances in different cultural and ecological contexts are necessary for us to understand the brain organization and evolution of cognition. A significant interest in understanding cultural variables in neuropsychology has been observed since the 1980s and particularly since the 1990s (e.g., Ardila, 1993, 1995; Boivin & Giordani, 2009; Chen et al., 2009; Choudhury et al., 2010; Ferraro, 2002; FletcherJanzen et al., 2000; Nell, 2000; Rendell et al., 2011; Uzzell et al., 2007). Different questions have been approached including but not limited to: Bilingualism research; historical origins of cognition; studies on illiteracy; cross-linguistic analysis of

4 A previous version of this chapter was published in: Uzzell, B., Pontn, M. & Ardila A. (eds). (2007). International Handbook of Cross-Cultural Neuropsychology. Mahwah, NJ: Lawrence Erlbaum Associates, pp. 23-45

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aphasia, alexia and agraphia; research about the influence of socioeducational factors in neuropsychological performance; norms in different national and cultural groups; studies on cultural variables on handedness; neuropsychological assessment and treatment in diverse human groups; analysis of neuropsychological test bias; cultural application of different neuropsychological test batteries; legal and forensic significance of cultural factors; and cognitive abilities in different cultural contexts. In this chapter, an attempt will be made to summarize the major cultural variables affecting cognitive test performance. I will attempt to integrate some ideas previously presented in different publications (Ardila, 1993, 1995, 1996, 1999, 2003, 2007; Ardila et al., 2000a, 2000b, 2010; Ardila, Rodriguez & Rosselli, 2003; Harris et al., 2001; Ostrosky et al., 1998; Puente & Ardila, 2000).

What is culture?
Culture refers to the set of learned traditions and living styles, shared by the members of a society. It includes the ways of thinking, feeling and behaving (Harris, 1983). The minimal definition of culture could simply be, culture is the specific way of living of a human group. Three different dimensions of culture can be distinguished: (1) The internal, subjective or psychological representation of culture, including thinking, feeling, knowledge, values, attitudes, and beliefs. (2) The behavioral dimension, including the ways to relate with others, ways of behaving in different contexts and circumstances, festivities and meeting, patterns of associations, etc. (3) Cultural elements: the physical elements characteristic of that human group such as symbolic elements, clothes, ornaments, houses, instruments, weapons, etc. Culture represents a particular way to adapt to and survive in a specific context. Cultural differences are strongly related with environmental differences. Eskimo and Amazonian jungle culture differences are in a significant extent due to the geographical and

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environmental differences between the Arctic region and the Amazonian jungle. Cultures, however, are usually in some contact and a significant cultural diffusion is generally observed. Cultural evolution and cultural changes are found throughout human history, depending upon, (a) new environmental conditions, (b) contact with other cultures, and (c) internal cultural evolution. For example, Gypsies in Russia and Gypsies in Spain have many cultural commonalties, but also many differences. Cultures can be grouped into branches using different criteria, but mainly, their origins (e.g., Latin cultures, Anglo-Saxon cultures, Islamic cultures, Amerindian cultures, etc.). When comparing two cultures, certain relative distance could be assumed. For instance, the cultural distance between Mediterranean cultures and Anglo-Saxon cultures is lower than the cultural distance between the Mediterranean cultures and the Amerindian cultures. This means that Mediterranean people have more attitudes, beliefs, behaviors, and physical elements in common with Anglo-Saxons than with Amerindians. Certain cultural elements have been particularly successful and have tended to strongly diffuse across cultures. For instance, science and technology have been extremely successful in solving different human problems and have, in consequence, tended to spread throughout virtually all-existing worldwide cultures. In this regard, contemporary man has tended to become more homogeneous and to share the culture of science and technology. To live in Peking and New York is not so different today as it was living in Tashkent and Rome several centuries ago. Furthermore, communication is faster today than it was anytime in history and cultural diffusion has become particularly fast. Formal education and school have played a crucial role in the diffusion of science and technology and in the contemporary trend toward the relative cultural homogenization. In this regard, school can be considered as a subculture, the subculture of school (Ardila, Ostrosky & Mendoza, 2000). School not only provides some common knowledge but also trains some abilities and develops certain attitudes. Cognitive testing is obviously based on those assumptions as well as values of scientific and technologically-oriented societies. Schooled children usually share more scientific and technological values and attitudes than their lower educated parents, and schooled subjects significantly outperform illiterate

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individuals in cognitive testing (e.g., Ardila et al., 2010; Ostrosky, Ardila, Rosselli, Lpez-Arango & Uriel-Mendoza, 1999; Reis, Guerreiro & Petersson, 2003; Rosselli, 1993).

Why culture affects cognitive test performance?


Cross-cultural cognitive testing has been a polemic matter because cognitive assessment uses certain strategies and elements that are not necessarily shared by every culture (Laboratory of Comparative Human Cognition, 1983). Greenfield (1997) has pointed out that there are three different reasons to account why cognitive ability assessments do not cross cultures: (1) Values and meanings, (2) modes of knowing, (3) and conventions of communication. Values and meanings means that there is not a general agreement on the value or merit of particular responses to particular questions. For example, some people may consider that in the Ravens Progressive Matrices test, it is a better answer that one following an aesthetic principle (i.e., the figure that looks better in that position) than the one according to a conceptual principle (i.e., the figure that continues the sequence). Furthermore, the same items do not necessarily have the same meaning in different cultures, regardless of how appropriate and accurate the translation is. An item referring to the protection of animals may have a rather different meaning in Europe than in a hunting society. The question Why should people pay taxes? may trigger quite different associations in a society where people consider that taxes are fairly expended than in a society where people think that taxes are misused. Knowing may be a collective endeavor and not an individual task. Many collective societies find it surprising that the testing situation requires individuals responses without the participation of the social group. If most activities are carried out in a collective way, why should answering a test be the exception? Many cultures, on the other hand, do not make a distinction between the process of knowing and the object of knowing. In

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consequence, questions such as why do you think?, or why do you consider? may be incomprehensible. The point is not what I think or I consider; the point is how it is. Conventions of communication are highly culture-dependent. The test questions assume that a questioner who already has a given piece of information can sensibly ask a listener for the same information. To ask or to answer questions can be highly variable among cultures. American children, for example, learn that they should not talk to strangers, but they also learn that they should answer questions to the doctor, regardless that the doctor is a stranger. In many societies adults rarely talk with children (What could you talk about with a child?), and it is not considered appropriate for children to participate in adults conversations. Furthermore, relevant information is not always the same in every culture. Many types of questions can be difficult to understand. To copy nonsense figures (e.g., Rey-Osterrieth Complex Figure) can be suspicious for many people. It may be a relevant item for an American school child, but it is absurd for somebody living in a nonpsychometrically oriented society. Certain question formats used in testing can be unfamiliar or less familiar in many cultures. For instance, after his first multiple-choice test, a college Haitian student in the US returned it to the instructor pointing out I simply do not have the minimal idea of what I am supposed to do. Conversely, I have found that American university students score notoriously lower in open-question exams than in multiple-choice formats. Effect of culture is not limited to verbal abilities, but is also clearly found on nonverbal abilities too (Rosselli & Ardila, 2003). When nonverbal test performance in different cultural groups is compared, significant differences are evident. Performance on non-verbal tests such as copying figures, drawing maps or listening to tones can be significantly influenced by the individuals culture. Five different cultural aspects potentially affecting neuropsychological test performance will be emphasized: (1) patterns of abilities, (2) cultural values, (3) familiarity, (4) language, and (5) education.

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Patterns of abilities While basic cognitive processes are universal, cultural differences in cognition reside more in the situations to which particular cognitive processes are applied than in the existence of the process in one cultural group and its absence in the other (Cole, 1975). Culture prescribes what should be learned, at what age and by which gender. Consequently, different cultural environments lead to the development of different patterns of abilities (Ferguson, 1956). Cultural and ecological factors play a role in developing different cognitive styles (Berry, 1979). Cognitive abilities usually measured in neuropsychological tests represent, at least in their contents, learned abilities whose scores correlate with the subject's learning opportunities and contextual experiences. Cultural variations are evident in test scores, as culture provides us with specific models for ways of thinking, acting and feeling (Ardila, 1995; Berry, 1979).

Cultural values Culture dictates what is and what is not situationally relevant and significant. What is relevant and worth to learn or to do for an Eskimo does not necessarily coincide with what is relevant and worth learning or doing for an inhabitant of the Amazonian jungle. A culture provides specific models for ways of thinking, acting and feeling, and cultural variations in cognitive test scores are evident (Anastasi, 1988). Current neuropsychological testing uses specific conditions and strategies that may not be only unfamiliar to many people, but also may violate some cultural norms. At least the following cultural values underlay psychometrically oriented cognitive testing (Ardila, 2005):

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1. One-to-one relationship. There is a tester and there is a testee. Hence, it is a oneto-one relationship between two people that very likely have never met before, are aliens, and will not meet again in the future.

2. Background authority. The testee will follow (obey) the instruction given by the tester, and hence, the tester has a background or situational authority. It is not so easy, however, to understand who and why this authority was conferred.

3. Best performance. The testee will perform at best. Performance at best is only done in those endeavors that are perceived and regarded as extremely important and significant. It is supposed in consequence that the testee has to perceive testing as a most important and significant endeavor. It may not be clear enough in many cultural groups why it is so important and relevant to repeat a series of nonsense digits or to draw an absurd figure.

4. Isolated environment. Testing is done in an isolated room. The door is closed and even locked. Usually, nobody else is allowed to be present, and in this regard it is a private and intimate situation. Private appointments with aliens may be quite inappropriate in many cultures. The testee has to accept this type of unusual social relationship.

5. Special type of communication. Tester and testee do not maintain a normal conversation. Tester uses a stereotyped language, repeating over and over again the same phrases in a rather formal language. Testee is not allowed to talk about him/herself. Nothing points to a normal social relationship and usual conversation. This is a type of relationship that can be different from any type of relationship existing in the subjects past experience. For Hispanics, as an example, the personal

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relationship with the examiner may be more important than the test results (Geisinger, 1992). Dingfelder (2005) points out that The detached professional relationship that many therapists cultivate with their clients may seem alien to those Latinos that adhere to the value of close interpersonal relationship. Therapist might consider sharing some minor details of their lives with these clients, to make the clients feel more comfortable and welcome (p. 59).

6. Speed. In many tasks the tester warns that the testee must perform as fast as possible and even time is measured. In the middle of the task, however, the tester frequently interrupts saying, stop! For many cultural groups speed tests are frankly inappropriate. Speed and quality are contradictory, and good products are the results of a slow and careful process. Speed, competitiveness and high productivity are most important cultural values in literate Anglo-American society, but that is not true in other cultural groups.

7. Internal or subjective issues. The tester may ask questions that can be perceived as a violation of privacy. Questions about cognitive issues (e.g., How is your memory?) are also questions about internal subjective representations, the most personal private sphere. Frequently, intellectual or cognitive testing may be perceived as aversive in some cultures. In Latin America, usually highly educated people dislike and try to avoid cognitive testing. Intellectual testing may even be perceived as kind of humiliating situation and disrespect to the privacy.

8. Use of specific testing elements and testing strategies. The tester uses figures, blocks, pictures, etc., and the reason for presenting them may not be easy to understand. That is, the reason may be evident for the tester (e.g., to assess memory) but not for the testee. Sometimes the tester explains that it is like a game, but there is no evident reason to come to play with this alien tester. Sometimes the

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tester refers to exercises, but exercises are by definition useless activities without any evident goal. Exercises are indeed preparation for something. Preparation for what? Furthermore, it they are just exercises why to perform at best? In brief, it is not easy to understand (and to explain) the reason to memorize meaningless digits or saying aloud as many animal names as possible in one minute, etc.

In summary, the rationale and the procedures used in cognitive testing rely on a whole array of cultural values that in no way can be regarded as universal values. When testers use tests developed in their own culture to test members of a different culture, testees often do not share the presumptions implicitly assumed by the test (Greenfield, 1997; p. 1115). It is not surprising that the members of the culture where the test was developed usually obtain the highest scores.

Familiarity Familiarity with the testing situation includes not only the elements used in testing (bikes, houses, figures, stories, etc.) but also the testing environment (see above), and the cultural relevance (meaningfulness) of the elements of the test (Ardila & Moreno, 2001). Familiarity also refers to the strategies needed to solve the task and the attitudes required to succeed. Competitiveness, for example, in many societies is viewed with suspicion. Cooperation and social ability may be far more important. The Boston Naming Test (even the version adapted in Spain) includes naming a beaver and an acorn, an animal unfamiliar for people living in South America and a virtually unknown plant. North American people very likely would consider it unfair to be tested by naming South American animals and plants. The Boston Naming Test also includes a pretzel, a most typical American element but totally unknown in most countries. Obviously, it would also be frankly unfair to test naming ability in American subjects using tortillas or

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tacos as stimuli. Figures representing snow may be unfamiliar for people living in tropical and sub-tropical areas. Cultural relevance (meaningfulness) may be another significant confounding factor in cross-cultural neuropsychological testing. Items developed in a particular cultural context do not have the same relevance when translated to another culture. Spelling out words (frequently included in the Mini-Mental State Exam) is not used in languages with phonological writing systems (such as Russian, Italian or Spanish), and hence it is perceived as an artificial task. In many world cities, people get oriented using cardinal points (North, South, West, and East) but in no way is this strategy found in every culture. I personally do not know where is North, South, West, and East in my Colombian hometown simply because I never used it. People in Barcelona (Spain) use to spatial directions: toward the sea and toward the mountain. People in Colombia frequently use up and down, referring to the numbering system, but up and down in Guadalajara (Mxico) mean from downtown and toward downtown. The Picture Arrangement subtest from the Wechsler Intelligence Scale may have different levels of difficulty in different cultural contexts, depending on the familiarity with the storys elements. Something may be obvious in a culture, but unusual and weird in another.

Language Language plays an instrumental role in cognition (Vygotsky, 1962, 1989). As a matter of fact, it represents the major cognitive instrument. Different languages differ in phonology, lexicon (semantic field of the words), grammar, pragmatic, and reading systems. These differences may affect language test performance. Different languages conceptualize the world in a different way (Whorf, 1956). For instance, the notion of time is quite different in Latin languages than in Germanic ones. Latin languages have a significantly high number of tenses pointing to some temporal nuances. Slavic languages use perfective and non perfective tenses in verbs. Space and casualty are also coded different in different languages.

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Language usage differs according to the cultural (and subcultural) background and strongly correlates with the subject's educational level. Sometimes, test instructions (and in general, the language used in testing) are given in a formal language, which may be very difficult to understand for individuals with limited education. Formal language represents a sort of academic language, most often found in a written form that many people neither use nor completely understand. A permanent effort is required to make test instructions and, in general, test language understandable for less educated people and appropriate for different cultural and subcultural groups.

Education Education plays a double role in test performance: school, on one hand, provides some contents frequently included in cognitive tests; and school, on the other hand, trains some learning strategies and develops positive attitudes towards intellectual matters and intellectual testing. In consequence, school could be considered as a subculture into itself. Greenfield (1997) has emphasized that A major (probably the major) factor that makes a culture more or less different from the cultural conventions surrounding ability testing is the degree of formal education possessed by the participants (p. 1119). Learning to read reinforces certain fundamental abilities, such as verbal memory, phonological awareness, and visuospatial discrimination (Ardila, Ostrosky & Mendoza, 2000; Ardila et al., 2010). It is not surprising that illiterate people underscore in cognitive tests tapping these abilities. Furthermore, attending school also reinforces certain attitudes and values that may speed the learning process, such as the attitude that memorizing information is important, knowledge is highly valuable, learning is a stepwise process moving from the simpler to more complex, etc. It has been emphasized that schooling improves an individuals ability to explain the basis of performance on cognitive tasks (Laboratory of Comparative Human Cognition, 1983). The fundamental aims of schools are equivalent for all schools and school reinforces certain specific values regardless of where they are located. Hence, school could be seen as a culture unto itself, a transnational

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culture, the culture of school. School not only teaches, but also helps in developing certain strategies and attitudes that will be useful for future new learnings. Ciborowski (1979) observed that schooled and non schooled children can learn a new rule equally well, but once acquired, schooled children tend to apply it more frequently in subsequent similar cases. Interestingly, education is not related with the ability to solve everyday problems. Cornelious and Caspi (1987) found that educational level has a substantial relationship with performance on verbal meaning tests but was not systematically related to everyday problem solving (i.e., functional criterion of intelligence). Craik, Byrd, and Swason (1987) observed that differences in memory loss during aging are related to socioeconomic status. Ardila and Rosselli (1989) reported that during normal aging the educational variable was even more influential on neuropsychological performance than the age variable. Albert and Heaton (1988) argue that, when education is controlled, there is no longer evidence of an age-related decline in verbal intelligence. A significantly decreased neuropsychological test performance has been documented in illiterate individuals (Ardila, 2000; Ardila et al., 1989, 2010; Goldblum & Matute, 1986; Lecours et al. 1987a, 1987b, 1988; Manly et al., 1999; Matute et al., 2000; Ostrosky et al., 1998; Reis & Castro-Caldas, 1997; Reis, Guerreiro & Petersson, 2003). Rosselli, et al., 1990). Lower scores are observed in most cognitive domains, including, naming, verbal fluency, verbal memory, visuoperceptual abilities, conceptual functions, and numerical abilities. Language repetition can be normal for meaningful words, but abnormal for pseudowords (Reis & Castro-Caldas, 1997; Rosselli et al., 1990). Similarly, copying meaningful figures can be easier than copying nonsense figures (Ostrosky et al., 1998). Furthermore, for illiterate people to use concrete situations can be notoriously easier than using non-real and abstract elements. When the information is related to real life, it can be significantly easier to understand. Thus, for the illiterate person, it is easier to solve the arithmetical operation If you go to the market and initially buy 12 tomatoes and place them in a bag and later on, you decide to buy 15 additional tomatoes, how many tomatoes will

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you have in your bag? than the operation: How much is 12 plus 15? Semantic verbal fluency is easier than phonological verbal fluency (Reis & Castro-Caldas, 1997; Rosselli et al., 1990), seemingly because phonological abstraction is extremely difficult for the illiterate person. Semantic verbal fluency requires the use of concrete elements (animals, fruits) whereas phonological fluency is tapping a metalinguistic ability. The very low scores observed in neuropsychological tests in illiterates can be partially due to differences in learning opportunities of those abilities that the examiner considers most relevant, although, they are not the really relevant abilities for illiterates' survival. They can be also due to the fact that illiterates are not used to being tested. Furthermore, testing itself represents a nonsense situation that illiterate people may find surprising and absurd. This lack of familiarity with a testing situation represents a confounding variable when testing individuals with limited education. Several studies have demonstrated a strong association between educational level and performance on various neuropsychological measures (e.g., Ardila, Rosselli & Ostrosky, 1992; Bornstein & Suga, 1988; Finlayson, Johnson & Reitan, 1977; Heaton, Grant & Mathews, 1986; Leckliter & Matarazzo, 1989; Ostrosky et al., 1985, 1986). However, some tests are notoriously more sensitive to educational variables (e.g., language understanding tests) than others (e.g., orientation tests). Extremely low scores in current neuropsychological tests are observed in illiterate people (e.g., Ardila, Rosselli & Rosas, 1989; Rosselli, Ardila & Rosas, 1990). Low scores in neuropsychological tests observed in illiterates can be partially due not only to differences in learning opportunities of those abilities that the examiner considers relevant (although, evidently, they are not the really relevant abilities for illiterates' survival) and to the fact that illiterates are not used to being tested (i.e., they have not learned how to behave in a testing situation), but also, that testing itself represents a nonsense (non-relevant) situation (Ardila, 1995). This educational effect, nonetheless, is not a linear effect, but rather it is a negatively accelerated curve, ending in a plateau. Differences between zero and three years of education are highly significant; differences between three and six years of education are

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lower; between six and nine are even lower; and so forth. And virtually no differences are expected to be found between, for example, 12 and 15 years of education. The reason is simple: the ceiling in neuropsychological tests is usually low (Ardila, 1998). Table 8.1 presents the differences in some cognitive tests between illiterates and subjects with onetwo and three-four years of education and Figure 8.1 illustrates a specific example.

_______________________________________________________________________________

Years of education

Test

1-2

3-4

_________________________________________________________________ Digits backwards Verbal memory Copy of a figure Naming Comprehension Semantic fluency Phonologic fluency 2.4 4.2 7.5 7.3 3.7 13.5 3.3 2.6 4.2 8.8 7.3 4.4 14.6 6.5 2.7 4.3 9.4 7.5 4.6 15.4 7.0

________________________________________________________________________________ Note: mean scores are presented

Table 8.1. Effect of education on test performance in some selected subtests of the NEUROPSI neuropsychological test battery (n=807) (adapted from Ostrosky et al., 1999).

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Figure 8.1. The educational effect is not a linear effect, but rather it is a negatively accelerated curve, ending in a plateau. Example of the Copy of a Semi-Complex Figure test (adapted from Ostrosky et al., 1999).

Although it is well established that there a significant correlation between cognitive test scores (e.g., IQ) and school attendance (e.g., Matarazzo, 1972) interpreting this correlation has been polemic (Brody, 1992; Finch et al., 2011; Neisser et al., 1996). The really crucial question is: Do cognitive (intelligence) tests indeed predict school performance? Or rather, does school train those abilities appraised in intelligence tests? To answer these questions is not easy, even though frequently the interpretation has been that IQ predicts school performance (e.g., Hunter, 1986). Other researchers, however, consider that IQ scores are to a significant extent a measure of direct and indirect school learning (e.g., Ardila, 1999; Ceci, 1990, 1991). Ceci and Williams (1997) presented an impressive and detailed review of the available data in this area. Seven types of historical evidence for the effect of schooling on IQ were examined:

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(1) The effect of intermittent school attendance: several studies have provided converging evidence that the longer youngsters stay out of school, the lower their IQs. (2) The effect of delayed school start-up. Different studies have demonstrated that children whose schooling was delayed experienced a decrement in several IQ points for every year that their schooling was delayed. (3) The effect of remaining in school longer. As a result of extra schooling (to avoid military service), men born on a particular date (July 9 instead of July 7) earned approximately a 7% rate of return on their extra years of schooling. The authors point out that this figure of 7% is very close to the estimate of the return on an extra year of schooling derived from studies of being born early or late in a given year. (4) The effect of discontinued schooling. There is a well-established detrimental effect of dropping out of school before graduating. For each year of high school not completed, a loss of 1.8 IQ points has been observed. (5) The summer school vacations. A systematic decline in IQ scores occurs during summer months. With each passing month away from school, children lose ground from their end-of-year scores on both intellectual and academic scores. (6) The effect of early-year birth dates. Given the age limits to enter school in the US, within a given year, the number of years of schooling completed is the same for those born during the first nine months of the year. But the amount of school attendance drops off for those born during the final three months of the year. After coming of age, some individuals leave school, and students with late-year births are more likely to stay in school one year less than students with early-year births. It has been observed that for each year of schooling that is completed there is an IQ gain of approximately 3.5 points.

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(7) Cross-sequential trends. A correlation between the length of schooling completed and intellectual performance among same-age, same-SES children has been observed. The general conclusion is that school attendance accounts not only for a substantial portion of variance in children's IQ but also apparently some, though not all, of the cognitive processes that underpin successful performance in IQ tests. The magnitude of this influence ranges between 0.25 to 6 IQ points per year of school (Ceci, 1991). In consequence, the association between IQ and education cannot be interpreted assuming that IQ predicts school success. Intelligence and schooling have complex bi-directional relationships, each one influencing variations in the other (Ceci & Williams, 1997). According to our results (e.g., Ardila et al., 2000b) even though bi-directional relationships between intellectual test performance and schooling may exist, the really significant relationship is between schooling and cognitive test performance. That is, attending school significantly impacts cognitive test performance.

Culture minorities groups


Cognitive testing of so-called minority groups represents a special situation in neuropsychology assessment. Minority groups constitute a culture or subculture within a mainstream culture. Quite often, the tester belongs to the majority culture and may have a limited understanding of the minority culture or subculture. Testing is likely interpreted from the majority culture perspective. To be a member of a minority group, however, has significant implications that can affect the testing situation and the testing results.

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There are over 120 million people living in a country different from that one where they were born. They are "minorities in the new host country: Turkishes in Germany, Moroccans in Spain, Hindus in England, Colombians in Venezuela, Greeks in Switzerland, Rwandans in Zaire, Mexicans in US, Greeks in France, etc. There are also some ethnic groups that are minorities in their own countries: African-Americans in US, Kurds in Turkey, Ameridians in Colombia (and virtually in every country), etc. Finally, there are some groups that are minorities everywhere because they do no have a country. Currently Gypsies are the best example, but until recently, Jews were also a peoplehood without a country. To be different from the mainstream people has a significant psychological impact. Patterns of behavior, beliefs, and attitudes may be different. Language can impair normal communication with the majority group. Even physical appearance and dressing can separate and distinguish the minority people. In the US there are hundreds of groups that can be regarded as minorities. At least six different variables can potentially distinguish the minorities groups. They may also affect intellectual test performance and the psychology of minority: 1. Nationality: is that person regarded or not as an alien? Intermediate

possibilities can exist. For instance, Hispanics in the US have five different possibilities: US born (2 possibilities: from the mainland or from Puerto Rico), acquired citizenship, legal immigrant, and illegal immigrant. It makes a significant difference if the country where you are living in is legally your country or you are a non invited alien. 2. Culture (relative distance). Irish immigrants in US have a closer culture to mainstream American way of life than Ethiopians. The larger the cultural distance, the more separated you are to understand the new culture and appropriately behave in it.

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3. Language (relative distance). Minorities may speak a different language, may speak a dialect of the majority language, or may simply speak the same language. The ability to communicate, and hence, participate (e.g., to have a job) in the host culture highly depends on the ability to speak. Language distance between English and German is lower than language distance between English and Spanish. Language distance between English and Chinese is huge. Age also plays a crucial role in the ability to learn the new language. Young Moroccan people in Spain can easily learn Spanish and improve in social status, whereas adults have to accept low qualified and paid jobs. 4. Normality (how frequent -- normal-- is your group in your living environment). To be different depends on the community you live in. Hispanics are the normal people in Miami, but very unusual people in Fargo. To be unusual may be associated with suspiciousness in the majority group and paranoia in the minority people. 5. Reference group (How many people are like you are). It depends upon with what specific group is the identification. Hispanics for instance, can consider that their reference group is Latin America or other US Hispanics. In the fist case the reference group is even larger than the majority US group. In the second one it is a notoriously smaller and weak social reference group. Finally, 6. Social image: Positive or negative attitudes in the majority group toward the minority people. Even though minorities have in general a low social image (e.g., they are poor, with low education, inappropriate behaviors, etc.) some times positive attitudes are also associated with the minority group. For instance,

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Oriental people are frequently regarded in the US as intelligent and hardworking people. Neuropsychological testing of minority groups have progressively become a more and more important question in neuropsychology, particularly in some countries with a significant immigration flow (e.g., some European countries). It is not easy for a Spanish neuropsychologist to test a Moroccan patient, or for a Danish neuropsychologist to test a Somalian client. There are not obvious answers to questions such as, how to carry the testing, what specific tests to use, and what conclusions can potentially be drawn from the testing results.

Norms in different national and cultural groups


A tremendous effort has been devoted in neuropsychology to obtaining test performance norms (e.g., Ardila et al.., 1994; Lezak, 2004; Spreen & Straus, 1998). Currently, many neuropsychological tests possess relatively solid and reliable norms. Nonetheless, norms have been obtained in most cases in white English-speaking, middle-class subjects with a high-school or college level of education. In cognitive testing it is usually assumed that norms are always required. Otherwise, no comparison is reliable. This idea, however, is more a desideratum than a reality. Furthermore, it does not seem to be a completely realistic idea. As a matter of fact, in the future, the search for norms may be coordinated with the search for understanding the sources of variation. Two evident problems with norms are readily observed: 1. Language. To obtain norms in English or Spanish (each one with about 400 million speakers) seems realistic. But English and Spanish are just two out of the three largest existing languages accounting together for no more than 15% of the worlds

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population.

Worldwide,

there

are

about

6,800

different

languages

(http://www.ethnologue.com/), most of them, with a limited number of speakers. As an example, in Mexico 288 Amerindian languages are currently spoken (http://www.ethnologue.com/). In the USA, over 300 languages are found, when counting both Amerindian and immigrant languages (http://www.ethnologue.com/). To obtain norms for all these 6,800 different languages is simply unrealistic. Furthermore, most of the world languages are small languages, and obtaining a reliable database would mean testing a high percentage of the speakers. If we assume that the average language has one million speakers (the real number is lower), and we want to normalize the neuropsychological instruments using just 200 stratified subjects in each language, it would mean that about one and half million participants would be required. This is a nonrealistic endeavor for contemporary neuropsychology. It seems more realistic to determine the linguistic factors potentially affecting cognitive test performance. A diversity of languages could be selected, comparison established, and significant variables distinguished. Language idiosyncrasies seem most important in understanding potential sources of variations. Obtaining norms is a realistic endeavor in English, Spanish, Quechua or Bengali, but does not seem realistic for the 288 Amerindian languages spoken in Mexico. 2. Culture. There are solid bases to assume significant cultural variations in psychological and neuropsychological test performance (e.g., Ardila, 1995; Fletcher-Janzen et al., 2000; Nell, 2000; Uzzell et al., 2007). Thus, the question becomes, how many cultural groups should be separated? Although several thousand different cultures have been described by anthropology (e.g., Bernatzik, 1957), obviously, there is not a definitive answer to this question. Cultures frequently represent a continuum, and cultures can partially overlap. For example, if asked whether separate norms should be used when testing Caucasians and Hispanics in the US, most neuropsychologists might answer YES. Nonetheless, a diversity of conditions may separate Caucasians and Hispanics: primary language (for many

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Hispanics, their primary language is English; most Hispanics are bilinguals, some are monolingual; the degree of mastery of Spanish and English is tremendously variable), acculturation (degree of assimilation of the modal American culture values is highly variable), etc. So, there does not seem to be an obvious and direct answer. To be Hispanic or Caucasian is not a dichotomy. Another question: In the US, can the norms obtained in San Francisco be used to test people in Boston, San Antonio, Honolulu, or Anchorage? San Francisco is a quite heterogeneous city and the question becomes what specific San Francisco norms are going to be used with what specific population in Boston, San Antonio, Honolulu or Anchorage? The same type of question can be raised everywhere. For instance, can we use the norms obtained in Barcelona, Spain to test people in the Canary Islands, Santiago de Compostela or Bilbao? The answer in all these cases may be, partially yes, partially no. This is indeed an endless question. If we move to the worldwide situation (with thousands of cultural variations!), we may conclude that this is also a nonrealistic endeavor for psychology and neuropsychology. I am proposing that this question has to be re-stated, and instead of looking for norms in every existing human group, we should try to understand why culture may impact and how culture impacts cognitive testing, i.e., which are the specific cultural variables that may affect the performance in a psychological or neuropsychological tests (Ardila, in press). For this purpose, it seems more reasonable to select a series of rather different cultural groups, representing enough cultural dispersion, in an attempt to pinpoint those cultural variables potentially affecting cognitive test performance. In brief, understanding the variables that can affect cognitive test performance seems to be as important as obtaining a large number of norms in different linguistic and cultural groups. (Ardila, Ostrosky & Bernal, 2006). For example, there does not seem to exist any reason to find differences in verbal fluency in pre-school and school children when using an equivalent semantic category in Spanish and English. If the familiarity with the testing condition is equivalent (both are small

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children with little or no familiarity with testing), the level of education is the same (none or whatever), the age is the same, and the semantic category has the very same semantic field in both languages, no differences in performance are expected. Table 8.2 presents the norms obtained by Halperin et al. (1989) in the US and Ardila and Rosselli (1994) in Colombia. Even though the age groups were divided differently (Halperin et al. used one year range; Ardila & Rosselli used two-year range) it is evident that performance was virtually identical. __________________________________________________________________ Halperin et al., 1989 (USA) Age (years) n M SD Ardila and Rosselli, 1994 (Colombia) Age (years) n M SD

__________________________________________________________________

__________________________________________________________________ 6 7 8 9 10 11 12 34 40 32 38 22 28 10 10.74 12.43 12.31 13.76 14.27 15.50 18.90 2.40 2.90 2.70 3.70 3.70 3.80 6.20 11-12 65 16.75 4.64 9-10 56 14.09 3.99 7-8 63 11.49 2.87 5-6 49 9.33 3.65

__________________________________________________________________

Table 8.2. Semantic verbal fluency (ANIMALS) in US and Colombia.

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Table 8.3. compares performance in two verbal fluency tests (phonological and semantic verbal fluency) in Spanish and English monolingual speakers. As anticipated, performance is virtually identical, if confounding variables are controlled. English speakers do a little better when using some letters; Spanish speakers do a little better when using other letters, very likely depending upon the frequency of words beginning with that particular letter in each language, the potential ambiguity existing between homophone letters, and some other uncontrolled confounding variables. Performance in semantic verbal fluency using the category ANIMALS was virtually identical.

____________________________________________________________________

English

Spanish

____________________________________________________________________ F A S Animals 12.9 (5.4) 10.7 (5.1) 13.8 (5.4) 16.8 (5.2) 11.7 (4.1) 11.8 (4.6) 11.4 (3.8) 16.7 (3.8)

Note. Mean scores and standard deviations are presented.

Table 8.3. Semantic verbal fluency (ANIMALS) in Spanish and English monolinguals (60-65 years; 13-16 years of education (according to Rosselli et al., 2000).

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Nonetheless, unexpected confounding variables can exit. Digit span looks like a relatively culture-fair test, and similar performance might be anticipated in people from different human groups. Nonetheless, that is not the case. A significant variability has been observed. Digit span varies from 5.4 (Poland) to 9.0 (China) (Dehaene, 1997; Nell, 2000).The reason for this variability is not totally clear, but both linguistic and training factors seem to exist (Dehaene, 1997). The phonological length of digits (number of phonemes included in digit words) as well as previous exposure to similar tasks (e.g., to say phone numbers using digit-by-digit strategy) may play a significant role in digit span. In the Sikuani language spoken in the Amazon jungle digits are: kae (one) , aniha-behe (two), akueyabi (three), penayanatsi (four), kae-kabe (five), kae-kabe kae-kabesito-nua (six), kae-kabe aniha-kabesito-behe (seven), kae-kabe aniha-kabesito-akueyabi (eight), kae-kabe aniha-kabesito-penayatsi (nine). With such long words, it can be conjectured that digit span will be very low. What is proposed is that understanding the variables potentially affecting (and confounding) test performance may be as important as obtaining norms for different human groups. No doubt, understanding cultural variables in cognition represents a major research area during the twenty-first century.

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