Epilepsy & Behavior 72 (2017) 161–172

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Epilepsy & Behavior

journal homepage: www.elsevier.com/locate/yebeh

Special Communication

Potential implications of Luria's work for the neuropsychology of epilepsy

and epilepsy surgery: A perspective for re-examination
Panayiotis Patrikelis a,⁎, Giuliana Lucci b, Anna Siatouni a, Anastasia Verentzioti a,
Athanasia Alexoudi a, Stylianos Gatzonis a
a
Epilepsy Surgery Unit, Department of Neurosurgery, School of Medicine, Evangelismos Hospital, University of Athens, Greece
b
University of Rome “G. Marconi”, Rome, Italy

a r t i c l e i n f o a b s t r a c t

Article history: The pioneeristic work of Alexander Romanovic Luria into the field of human neuropsychology offered eminent
Received 6 February 2017 contributions to clinical praxis by providing theory guided methods and instruments for the study of higher cor-
Revised 24 March 2017 tical functions. However, lots of this knowledge corpus either remains untranslated and thus inaccessible, or in
Accepted 25 April 2017
some cases selectively overlooked by academic authorities and consequently not passed to the future generations
Available online 10 June 2017
of experts. Although Luria was not exclusively devoted to the study of epilepsy, his theories and clinical ap-
Keywords:
proaches actually penetrate the whole neuropathology spectrum. His holistic and systemic approach to the
Epileptology brain sounds nowadays more than opportune and consistent with the network approach of the modern neuro-
Preoperative neuropsychological assessment imaging era. As to epilepsy, the logic underlying the Lurian approach (cognitive functions organized into complex
Anatomical data functional systems with intra- and/or inter-hemispheric distribution, as opposed to the modularistic view of the
Lurian idiographic approach brain) seems consistent with our current knowledge in epileptology with respect to epileptic networks, as well as
Materialistic psychology the modern construct of the functional deficit zone. These contributions seem to be highly promising for the neu-
Functional systems theory ropsychology of epilepsy and epilepsy surgery, since they provide clinicians with valuable methods and theories
to assist them in the localization -and lateralization- of cognitive deficits. Consequently they are of great applica-
bility in the context of the preoperative neuropsychological monitoring of patients candidates for epilepsy sur-
gery, where neuropsychologist are called upon to provide surgeons with anatomical data.
© 2017 Elsevier Inc. All rights reserved.

1. Introduction
Summarizing Luria's work is an extremely hard, if not altogether im-
possible undertaking. His deterministic approach to the brain, guided
for the most part by the Zeitgeist of his era (the dialectical and historical
materialism), has contributed significantly to the field of human neuro-
psychology. Although Luria did not devote himself exclusively to the
study of epilepsy, his theoretical assumptions and conceptualizations
have nonetheless penetrated all aspects of neuropathology.
For many decades the neuropsychology of epilepsy has been domi-
nated by modular theories of brain functions (e.g., the material-
specificity theory of memory), which on the one hand have enhanced
our acumen of seizure-induced cognitive dysfunction and its neurobio-
logical correlates, but on the other have dramatically hampered our
clinical understanding. Luria proposed an alternative functional concept
of the brain which states that higher cortical functions result from the
dynamic and coordinated coupling of different brain areas, each
⁎ Corresponding author at: 45-47 Ipsilantou Str., 10676 Athens, Greece.
E-mail address: ppatrik@cc.uoi.gr (P. Patrikelis).
contributing in its own particular and unique fashion within the domain
of a functional system.
According to this model, a brain lesion may compromise a functional
system at any level of its organization, and the nature of the disturbance
will be strongly associated with the anatomical site of the lesion. Thus,
the clinician has the duty to identify the anatomical distribution of the
functional system - or systems - under examination, as well as the role
played in it - them - by different brain regions. This functional brain
model was inconsistent both with the classical localizationism and anti-
localizationism (connectionism) approaches, which attempt to interpret
the spatial construction of the brain in static and non-spatial terms [1].
According to Luria, the concept of the functional system was anti-
thetical to the topographic concept of higher mental processes, shared
by the majority of western scientists of that era. In fact, Luria neither
reduced mental processes to the functional domain of specific brain
regions, nor limited them to one of the two hemispheres. He assumed
that mental operations are the product of the synergic action of different
functional systems, the components of which are localized in different
brain areas and, in many cases, distributed inter hemispherically.
Consequently, the anatomical substrate of neuropsychological
deficits is no longer identified within specific brain areas, belonging to

http://dx.doi.org/10.1016/j.yebeh.2017.04.041
1525-5050/© 2017 Elsevier Inc. All rights reserved.
162 P. Patrikelis et al. / Epilepsy & Behavior 72 (2017) 161–172
the dominant or nondominant hemisphere responsible for the symp-
tom, by means of a simple taxonomic reduction process, but rather
through a qualitative neuropsychological analysis of the syndrome
or symptom-complex. This latter drew upon a solid corpus of theories
regarding various topics, such as memory and executive functions, pro-
duced by Luria's comprehensive and insightful observations of people
suffering brain injuries, although a (see Table 1) shallow view into
Luria's methods may regard them as impromptu or even not susceptible
to quantification.
1.1. The riddle of localization of psychological function
Memory and its anatomo-functional mechanisms could serve to
gain insight into Luria's concept of brain function. There is evidence sug-
gesting a functional relationship between left temporal lobe and verbal
memory [2–4], and right temporal lobe and nonverbal memory, such as
abstract designs, melodic patterns and music tones [5]. Accordingly,
a major functional dissociation has been proposed between memory
for verbal and nonverbal material, assumed to be covered by the domi-
nant (usually left), and the non-dominant temporal lobe respectively.
However, evidence concerning the functional relationship between
right temporal lobe and non-verbal mnemonic processing is weaker
than that with respect to the left temporal lobe and verbal memory
[6]. This could be attributed to the fact that memory for nonverbal
material is a more abstract and psychometrically less documented
construct [7].
Since the 70s there has been an increased awareness about the in-
herent potential of the right cerebral hemisphere in processing lexical
and semantic information, as well as about its property to mediate ver-
bal memory through its ability to represent highly imageable words.
Jones [8], corroborating Patten's position [9], reported that both healthy
controls and also patients with left-sided temporal lobe epilepsy were
likely to improve performance in verbal memory tasks by implementing
a strategy known as imagery mediated verbal recall, whereas patients
with right-sided temporal lobe epilepsy were not. Following studies
[10,11] have demonstrated the crucial role played by the right temporal
lobe in processing verbal material with high imageability (i.e., concrete
words as chair, vase, etc.). This was further supported by the difficulties
that patients with right temporal lobe epilepsy may face, when the ma-
terial to be learned presents high imageability level [12].
The two hemispheres' variable degree of engagement in recalling
verbal information became more obvious through the use of pictorial
stimuli. Jaccarino [13] (cf. Milner [14]) suggested that both right and
left temporal lesions seem to compromise recall for line drawings'
name presented the previous day.
Similarly, Moscovitch [15] showed that right temporal lesions may
impair immediate verbal recall, thus implying that beyond an early
processing stage, each hemisphere code identical information in its
own way, in accordance with its unique characteristics and processing
abilities [16].
Of interest to this point is Pillon and associates' [17] postulation that
left vs. right temporal lobes difference may be reliant on their selective
involvement in various stages of mnemonic processing, rather than on
their specialization for material-specific memory (verbal and nonverbal
respectively).
To Luria [18] psychological functions are not likely to be lateralized:
both cerebral hemispheres are involved in the expression of mental
functions, each of which with its own particular processing mode. This
selective involvement doesn't appear to differ in relation to the stimuli
nature (as in the case of memory for linguistic or nonlinguistic stimuli),
but rather in relation to the mode of processing and the particular
moment in which each hemisphere assumes its functional duties. This
probably implies different stages of processing requiring the specialized
and selective contribution of both cerebral hemispheres, and as such
came in contrast to the quadrant base (modular) approaches to the
brain [1].
Luria adopted a systemic-network approach to the study of the brain,
an issue subject currently of interest to both epileptology (epileptic net-
works) and also the neuropsychology of epilepsy. This neuropsychologi-
cal concept seems to imply an epistemological transition from the logic
of lesions to the logic of cerebral networks, thereby heralding the era of
neuroimaging and neural networks.
Although Luria sees a functional advantage for learning and use of
language code in the dominant hemisphere (usually the left), he argues
that this by no means implies that linguistic functions are exclusively
represented within it.
Departing from Vigotsky's developmental theory of higher psycho-
logical processes, Luria maintains that is not possible to segregate
linguistic activity from its constituent part, i.e., visual impressions, sug-
gesting that complex psychological functions draw upon a dynamic in-
terhemispheric interaction. This is because according to both Vigotsky
and Luria psychological functions build upon the products of sensory
experience and organized by the means of language [19]. More specifi-
cally, in the course of its development, a child typically learns how to
use cultural tools in interactions with others and later independently.
The child develops higher mental functions that are intentional, self-
regulated, and mediated by language and other sign systems [19,20].
1.2. Left-right dissociation of hippocampal memory processes
Particular emphasis was placed on memory function and its
two main typologies (i.e., verbal and nonverbal), which, according
to Luria, underlie the unique contribution of each brain hemisphere in
different memory processing stages. Thus, the dominant hemisphere
has been conceptualized as supporting explicit memory, while the
non-dominant as supporting implicit memory, the latter being a crucial
part of imprinting, a process with evolutionary meaningful implications
for many species; this was further corroborated through the study of pa-
tients suffering left brain lesions and explicit memory deficits and also
patients with right lesions manifesting memory deficits of implicit na-
ture [20]. By studying patients with lateralized hemispheric lesions,
Luria and Simernitskaya [20] reached the conclusion that both hemi-
spheres are involved in the memorization of linguistic information,
but at different time frames (phase difference), as to the various stages
of information processing. It is noteworthy that Luria and Simernitskaya
[20] reached this conclusion at least two decades before Pillon and
collaborates [17].
More explicitly, what Luria proposed was a memory system with a
modality-specific organization, contrary to the modularistic view sug-
gesting a material-specific organization of memory, as suggested by
Penfield and Milner [21]; in the former's view, memorization of linguis-
tic material occurs at a higher order processing stage where memory
meets language function, while memorization of non-linguistic material
occurs at a lower order processing stage, where memory relates to sen-
sory systems.
1.3. Frontal executive-temporal mnemonic dissociation
Another neuropsychologically important subdivision commonly op-
erated by western researchers is that between temporal and frontal-
lobe functions, implying that memory functions reside in the former
and executive functions in the latter. As documented, patients with hip-
pocampal lesions, and particularly with bilateral resection of the hippo-
campal formations, manifest severe amnesia [22], thus underlying the
functional significance of this brain structure for memory [21]. On the
other hand, frontally damaged patients present dysexecutive problems,
e.g. sorting ability deficits in the Wisconsin Card Sorting Test [23].
Based on the above-mentioned studies, a new double dissociation
paradigm is being established, referring to the difference between
areas functionally devoted to memory (temporal areas) and others de-
voted to executive control (frontal areas). As expected these theories
have met with opposition, as there are studies which posit that memory
 P. Patrikelis et al. / Epilepsy & Behavior 72 (2017) 161–172 163

Table 1 Table 1 (continued)

A summary of some Lurian tests juxtaposed to their standard measures analogues.
Naming of fingers on a hand
Evaluation of attention Recognition of objects by touch (key, comb, etc.) Tactile form recognition-
Characteristics of involuntary attention Posner cueing task with the right hand, and with the left hand Halstead-Reitan
—Elements of purposeful behavior (non informative (register the character of tactile exploration: neuropsychological
(echopraxia, echolalia) cueing version) inactive, active without synthesis, etc.) test battery (Reitan
—Uncontrolled emergence of associations (Posner, 1980) and Wolfson, 1985)
Characteristics of voluntary attention Continuous Evaluation of auditory perception and auditory-motor coordination
—Results of clinical examination performance test Sound-pitch relationships Sound recognition test
—Results of correction test (Rosvold et al., 1956) —assessment (Spreen and Benton,
—Results of Kraepelin's test Cancelation and visual —repetition 1963)
—Results of a test of visual attention search tasks Melodies Dichotiv listening:Music
—recognition (Spellacy, 1970)
Evaluation of visual perception and visual-spatial gnosis —repetition
Object perception/gnosis b) Boston Naming Localization of sound in space
a) Recognition of real objects Test-BDAE (Goodglass Study of dichotic listening
b) Recognition of realistic images et al. 1983). Assessment and reproduction of rhythms:
c) Recognition of contour images c) Benton Visual Form Assessment of rhythms Rhythm test
d) Recognition of superimposed images Discrimination II II III III II III (Seashore, 1960)
e) Recognition of Poppelreuter's figures (Benton et al., 1983) III III II II
f) Recognition of conflicting (composite) d) Poppelreuter-Ghent's Reproduction of rhythms from an example
figures (e.g., fish-hare, hare-fish) overlapping figures test II II II III III III
(della Sala et al., 1995) II II II II II II II
Volume or scope of visual perception TVPS, test of II II
—simultaneous comprehension of two visual-perceptual —immediate reproduction of rhythms
or three figures skills (Gardner, 1982). —delayed reproduction (following an
—ignorance of a side (neglect or inattention) Bell test (Gauthier empty pause) of rhythms
et al., 1989). —reproduction following interference
Recognition of faces Face recognition test – Repetition of rhythms to verbal instruction:
—direct Rivermead Behavioral “two at a time,” “three
—familiar portraits (identifying a familiar face) Memory Test II at a time,” “two at a time,” “four at a time”
—identification of portraits by memory traces (Wilson et al., 2003). —immediate reproduction
Benton facial —delayed reproduction (following an empty phase)
recognition (Benton —reproduction following interference
and Van Allen, 1968)
Color perception Ishihara Tests (1917) Evaluation of movement and action
—selection of shades from a standard Execution of simple instructions (with the
—identification from memory traces right hand, left hand)
—naming of colors —clenching of the hand
Optic-spatial perception/gnosis Rey complex figure —finger movements
—reading time from a watch test (Rey 1941) Postural praxis (of the wrist) (with the right
—reading time from a schematic watch hand, left hand)
—arrangement of hands on the watch face —in a horizontal plane
without figures Right-Left orientation —in a vertical plane (in cases of hemianopsia)
—orientation on a geographical map (Benton, 1959) —transfer of posture from one hand to another
(designation of cardinal geographic points, Spatial praxis
well-known cities, rivers, etc.) —one-hand tests (hand-chin)
—drawing a plan of the ward or hospital floor —two-hands tests (hand-hand)
Division (or bisection) of a line Line bisection task Head's tests: one-sided
(presence of asymmetry) (Schenkenberg et al., cross/form
1980) Dynamic praxis (fist-edge-palm, Kaufman hand
Examination of a group of figures and complex Bells Test edge-palm-fist, 1-2-1-5) movements test (Barry
images (unawareness of a side) (Gauthier et al., 1989) and Riley, 1987)
Letter perception/gnosis Reciprocal coordination (Oseretskii)
—recognition of letters in different typefaces Asymmetrical knocking (2-1; 1-2) with the hands
—recognition of letters as a mirror image Implementation of motor programs Rey-Osterrieth complex
—recognition of imposed and superimposed letters a) drawing of a series of geometrical figures figure; copy (Rey and
Figure perception/gnosis b) graphic testing Osterrieth, 1993)
—recognition of figures: Arabic Roman Constructional praxis: Rey-Osterrieth complex
—recognition of figures: superimposed, as a mirror figure; copy (Rey and
image and superimposed Osterrieth, 1993)
Drawing (house, table, cube, man, face) Rey-Osterrieth complex
VI. Evaluation of somatosensory perception/gnosis —independent figure; copy (Rey and
Test for the localization of touch Finger localization —copying Osterrieth, 1993)
—single (Benton, 1994) —outlining
—double (on one hand, on two hands, Actions with objects
or on the face) —fastening of buttons
Test for tactile discrimination (determine the —tying a knot or a bow
number of touches: one or two) —striking a match
Cutaneous-kinesthetic sensitivity Rey's skin writing Symbolic praxis Test of oral and limb
(on the right or the left hand) test (Rey, 1964) —to threaten someone, to beckon someone, apraxia; TOLA
—Foerster's graphesthesia testing (identification to stir tea, etc. (Helm-Estabrooks, 1992)
of a figure or figures written on the palm of the Florida apraxia
right or the left hand) screening test-revised
Transfer of the posture of a hand and wrist from (Fast-R; Rothi, Raymer,
one hand to another with closed eyes and Heilman, 1997)
Determination by the patient of his or her right Apraxia battery for
and left side and the sides of a person sitting adults (Dabul; 2000)
opposite him or her
(continued on next page)
164 P. Patrikelis et al. / Epilepsy & Behavior 72 (2017) 161–172

Table 1 (continued) Table 1 (continued)

Eye movements —“Sshit kolpak ne po kolpakovski, nado ego

—visual fixation (stable, unstable) perekolpakovat' i nikto
—gaze-related movements ego ne perekolpakuet.”
—shifting gaze on instruction [The cone hat is made the wrong way,
—shifting gaze to follow a moving object and no one can do it right.]
—visual limitations (to the right, left, Naming of objects: Boston naming test -
upward, downward) From pictures (10) BDAE (Goodglass
—impairment of the smoothness of movements apple lamp teapot et al. 1983)
—localization of an object in space bottle inkstand etc.
Oral praxis Test of oral and limb Parts of the body
—to imitation apraxia; TOLA brow eye hand
—to instruction (Helm-Estabrooks, 1992) finger elbow shoulder
—praxis of the lips (grin, stretching of the lips) Florida apraxia Understanding of speech: Basic word
—of the tongue (raise, withdraw, to the right, screening test-revised Understanding of words (assisted by discrimination BDAE
to the left) (Fast-R; Rothi, Raymer, showing a picture) (Goodglass et al. 1983)
—of the cheeks (inflate, deflate) and Heilman, 1997) —single element (10)
—of the facial muscles Apraxia battery for —double elements (5 pairs)
—raise the brows adults (Dabul; 2000) —triple elements (5 groups of three)
—knit the brows Word comprehension (without visual
—conventional oral movements assistance: parts of the body)
—to click —show ear-nose-eye
—to whistle —single element (ear, etc.)
—to clatter —double elements (ear-eye, etc.)
—demonstrate spitting and kissing —triple elements (eye-nose-ear, etc.)
Conventional and conflict reactions and actions: Understanding of low-frequency words
Simple conventional reactions (raise a hand (nail, caterpillar, etc.)
following a knock) Understanding of everyday instructions
Conventional choice reactions (raise the right and sentences
hand following one knock and the left hand —Open your mouth; open your eyes; close
following two knocks) your mouth, close your eyes.
Breaking of a stereotype—111,222,121,211 —Put your left hand into the pocket of your
Conflicting conventional reactions—raise a gown.
finger in response to a fist (FF), raise a fist in Understanding of logical-grammatical
response to a finger (Fi), raise lightly in constructions
response to a heavy stroke (1), raise quickly —Indicate: the key with the pencil,
in response to a weak stroke (11) the pencil with the key;
FF Fi Fi FF Fi FF Fi FF FF the key with the pencil.
11 1 1 1 1 1 11 —Demonstrate or follow the instruction: Commands word
The book is under the notebook; comprehension BDAE
Evaluation of speech
the notebook is under the book; (Goodglass et al. 1983)
Spontaneous speech. A conversation with Simple social responses -
the book is on top of the notebook, etc.
the patient (How did you fall ill? etc.) Boston diagnostic
The triangle is under the cross;
aphasia examination
the cross is under the triangle, etc.
(BDAE; Goodglass et al.
—Indicate: which object is lighter,
1983)
darker, less light,
Free conversation –
less dark
BDAE (Goodglass et al.
—Show or explain the meaning of: Token test
1983)
mother's daughter, daughter's mother; Complex ideational
Automatic speech: Automatized
father’s brother, brother's father material - BDAE
—number series from 1 to 10 Sequences - BDAE
I had my breakfast after I read the newspaper. (Goodglass et al. 1983)
—two weeks: Monday, Tuesday… (Goodglass et al. 1983)
What did I do first?
—months: January, February…
Spontaneous narrative speech: Picture description-
Nonautomatic speech:
A story told from a subjective picture BDAE (Goodglass
—backward number series: 10, 9, 8…
Oral composition of a topic et al. 1983)
—days of the week backward: Sunday, Saturday…
“Rest” “The north” etc.
—months backward: January, December…
Repetition of speech: Verbal agility - BDAE Evaluation of writing
Repetition of sounds (Goodglass et al. 1983) Automatic writing (name; first, second names)
a, o, i, u, b, d, k, s Writing of letters
Repetition of disjunctive pairs of sounds —Copying of printed letters (single letters, pairs)
b-i k-s m-r —Writing to dictation (single letters, pairs)
Repetition of opposed phonemes Writing of words Written picture
b-p p-b d-t t-d z-s s-z —Copying of words naming- BDAE
Repetition of a series of sounds —Writing to dictation of simple words: house, (Goodglass et al. 1983)
bi-ba-bo bo-bi-ba ba-bi-ba window, chair
Repetition of words —Words with opposed phonemes: dochka-tochka
—house, window, cat, tailor, cry, elephant [daughter-dot],
—colonel, admirer, ladle zabor-sobor-zapor [fence-cathedral-constipation]
—cooperative, shipwreck —Words with opposite articulemes:
Repetition of a series of words Single word repetition - stol-ston-slon [table-cry-elephant]
—house-forest cat-table BDAE (Goodglass et al. —Complex words: tailor-hemming-shipwreck
—oak-night-needle orchard-cupboard-day 1983) Writing of phrases (copying, writing to dictation) Narrative writing BDAE
Repetition of phrases The boy sleeps, the girl weeps; (Goodglass et al. 1983)
—The boy is sleeping; the girl is crying. It is raining outside.
—The boy already beat a dog; the girl is
drinking tea. Evaluation of memory
Repetition of tongue twisters3 Repetition of sentences - Repetition of a series of words Rey auditory verbal
—“Iz pod topota kopyt pyl' po polyu letit.” BDAE (Goodglass et al. —Direct recall learning test (Rey, 1964)
[The dirt is flying off the horse's hooves.] 1983)
 P. Patrikelis et al. / Epilepsy & Behavior 72 (2017) 161–172 165

Table 1 (continued) Table 1 (continued)

—Delayed recall Recall ?/I ?/II

house-night-needle Interference by counting ?/I ?/II
table-ringing-leaf-cupboard 4. “The Lion and The Mouse”
onion-bridge—umbrella-peace A lion was sleeping. A mouse ran over his body, but
cat-knocking-ball-night-dust-sound the lion woke up and caught her. The mouse began
Learning of a series of words (over 10 trials): to plead: “Let me go and I'll be useful to you.” The lion
house forest table cat night needle pie ringing burst out laughing but let her go. The next day,
bridge cross hunters trapped the lion and tied him to a tree with
I ropes. The mouse heard the lion's roar, ran to him, bit
II through the ropes, and saved the lion.
III Recall ?/I ?/II
IV
Evaluation of the system of computation
V
Assessment of the concept of quantity
VI
(counting of a group of dots)
VII
Reading and writing of simple figures
VIII
Reading of complex figures: 78 87 19 91 107
IX
4807 10126
X
Reading of figures written vertically: 123 3456
Delayed recall after 2 min
Writing of complex figures: 86 68 96 203 1026
Memorization of two groups of elements Wechsler memory scale
1003 10125
—Memorization of a group of words (WMS-R, WMS-III,
Performance of simple computational operations: Arithmetic- WAIS-III
WMS-IV)
Repetition of the multiplication tables (orally); (WAIS, 1997)
Series A I circle chair
written performance of arithmetic operations:
II day eye
addition, subtraction, multiplication, division
Series B I day pinetree cupboard
2 + 7 = 6 − 4 = 11 − 2 = 9 + 5 =
II book hat circle
16 184 31 1003 16 42
1) first reproduction
+ 23 −77 −17 −934 × 9 × 13
2) second reproduction
729/9125/4
3) third reproduction
Performance of three-part computations
?/I ?/II ?/I ?/II
(13 + 7 − 2, etc.)
—Memorization of a group of pictures Rey-Osterrieth complex
Performance of serial subtractions:
Series A figure test (recall)
100–7 = … 100 − 2, −1 = …
I telephone glasses tomato
II mushroom bottle shoes Evaluation of intellectual processes
1) first reproduction Understanding of stories:
2) second reproduction “The Crow and the Doves” (see Section XII)
3) third reproduction “The Lion and the Mouse” (see Section XII)
?/I ?/II ?/II ?/II “The Ant and the Dove” (see Section XII)
Memorization of two logical series “The Hen and the Golden Eggs” (see Section XII)
(phrases, stories) Understanding of thematic pictures (from a Pictures arrangement
Series A I The dog barks. neuropsychological manual or picture booklet): WAIS-III (WAIS, 1997)
II The house is on fire. “An Ice Hole”
Series B I The boy hit a dog. “A Broken Window”
II The girl drinks tea. “The Last Spring,” etc.
Series C I The apples were in the orchard Solution of problems: Arithmetic WAIS-IV
behind a high fence. A housewife uses 15 l of milk for each of 5 days. (WAIS, 2008)
II The hunter killed a wolf on the edge of a forest. How much does she use in a week?
1) first reproduction Repetition
2) second reproduction Solution strategy
3) third reproduction There are 18 books on two shelves, but the
4) fourth reproduction number on each shelf is different: There are
Interference by counting twice as many on one shelf as on the other.
?/I ?/II How many books are on each shelf?
Memorization of two stories Logical Repetition
1. “The Hen and the Golden Eggs” memory-WMS-III Solution strategy
A man had a hen that laid golden eggs. The (Wechsler, 1997). There are 18 books on two shelves, but there are
man wanted to have more two more books on one shelf than on the other.
gold, so he killed the hen, assuming she had How many books are on each shelf?
more gold inside her. But Repetition
there was nothing inside, for she was just an Solution strategy
ordinary hen. There are 24 kg of sugar in two boxes, but one
2. “The Crow and the Doves” box has three times more sugar than the other.
A crow heard that doves are well fed. She dyed How much sugar is in each box?
herself white and flew into the dovecote. The Repetition
doves accepted her. But she could not restrain Solution strategy
herself and crowed the way crows do. Then A son is 5 years old. In 15 years his father will be
the doves drove her away. She went to join three times as old as the son. How old is the
her flock, but they thought she was a stranger father now?
and drove her away. Repetition
3. “The Ant and the Dove” Solution strategy
An ant ran down to a rivulet to drink. A wave rushed A candle is 15 cm long, the shadow is 45 cm longer.
over him and he began to sink. A dove flew by. She How many times longer is the shadow than
saw the sinking ant and threw him a straw. He the candle?
caught the straw and climbed ashore. The next day, Repetition
a hunter wanted to trap the dove. The ant sneaked Solution strategy
up and bit the hunter on the finger. The hunter Completion of a phrase:
cried out and dropped the net, and the dove took High-probability words:
to the air and flew away. A strong blew from the sea.

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Table 1 (continued) Table 1 (continued)

The was shining brightly in the sky. 2. Give every man thine ear, but few thy voice.
Low-probability words: 3. A man is valued for his qualities.
I had my breakfast after I. Classification of objects (from a neuropsychological
There was a on the table. manual or picture booklet)
Completion of omitted words: 1. seesaw-ax-spade-log
High-probability words in a phrase: 2. shoe-foot-boot, etc.
I wore a because it was raining.
It is to cross the street here because of the
heavy traffic.
Low-probability words in a phrase:
I was the whole day and got very tired. disorders are linked to lesions of structures other than the hippocampus
One could see in the distance; it ran farther and medial temporal-lobes, i.e. [24]. Moreover, it has also been sug-
and farther. gested that the hippocampus is likely to support functions beyond the
Flow of associations (for 2–3 min) Word, animal, or mere domain of memory, such as self-monitoring and inhibition of
—Name as quickly as possible seven red figural fluency
(sharp) objects.
inappropriate behavioral responses [25], as well as linking perception
—Name as quickly as possible seven to action [26].
objects that begin with the letter T. A great deal of research has challenged the double dissociation view
Selection of opposites: between memory (temporal areas) and executive functions (frontal
Passive
areas). For instance, Giovagnoli [27] showed that left MTLE patients
Big-
Weak- and hippocampal sclerosis along with left frontal-lobe epilepsy patients
Warm- manifest severe executive deficits in the Modified Wisconsin Card
Low- Sorting Test, as to their counterparts with right sided foci. This paradox
Dear- has been interpreted in the light of hippocampal contribution to encode
Cheap-
new information and form associations, the latter also being a function
Active
Give two pairs of words, opposite in meaning. the frontal cortex. Likewise, there is recent evidence suggesting a hippo-
Selection of analogies Similarities - Wechsler campal involvement in working memory [28], traditionally conceptual-
a) Free associations adult intelligence ized as a prefrontal function.
rose-flower raspberry-berry scales IV (WAIS, 2008)
Other studies have demonstrated the direct hippocampal involve-
horse-foal dogegg-
shell potatodog- ment in executive functions in both patients with MTLE and schizophre-
wool pikebird- nia [29,30], while others regard the hippocampus as a structure linking
nest mankey- numerous and anatomically heterogeneous cortical areas, and possessing
iron tablescythe- anatomo-functional rapports well beyond the medial temporal-lobe
grass razorcupboard-
domain [31,32].
dishes purse-:
doctor-treatment tailor-:
grief-tears joysky-
clouds stageriver- 2. Some reflections on simple partial seizures manifest as
bank streetb) cognitive/psychic symptoms in light of Luria's conceptualization
Choosing from alternatives:
Explanation according to an example:
high thick low hungry, thin, fat Although neuropsychological analysis of cognitive/psychic symp-
thin ugly thick fat, dirty, beautiful, monster, toms arising in the context of simple partial seizures is beyond the
merry pigs fluff scope of this paper, we will briefly attempt to approach this complex
heavy difficult, feather bed, feathers,
topic in the light of Luria's conceptualization.
light, hens
horse cow Classification of psychic seizures is an arduous endeavor, due to the
foal pasture, horns, milk, calf, ox subjective nature of such phenomena. Although temporal lobes are for
spoon fork the most part likely to represent the neurological underpinnings of psy-
porridge butter, knife, plate, meat, dishes chic seizures, they are not necessarily localized, while conceivably some
ear teeth
to hear to see, treat, mouth, brush, chew
of them are expressed through extensive and interconnected networks
son mother within and around the temporal lobes [33]. Such latter and relatively
father housewife, daughter, grandmother, husband recent MEG finding is to some extent contrary to the key role attributed
Interpretation of the meaning of sayings and Proverbs - WAIS-R to temporo-limbic dysfunction in the genesis of psychic seizure, as sug-
proverbs (WAIS, 1981)
gested by traditional studies.
a) Free association:
Feeding dogs is very fine, but not too close to This network view of psychic/cognitive seizures is consistent with
hunting time! the Lurian systemic-holistic approach to the study of the brain. Accord-
All that glitters is not gold. ing to this approach, symptoms and even complaints present in the con-
b) Multiple choice: test of psychosensory disorders and seizures with a distinctive pattern
Strike while the iron is hot.
1. A blacksmith should hammer iron well.
of aura may be of direct topical-localizing value [18].
2. There are power hammers nowadays at In particular, auditory and visual hallucinations and the degree to
forge shops. which they assume complex forms may inform the clinician regarding
3. Never put off till tomorrow what you can the hemispheric side these hallucinations emanate from and the partic-
do today.
ular projection or association areas (according to Luria's theory the spe-
Don't count your chickens before they are hatched.
1. Chickens grow fast by autumn. cific cortical analyzer-s and the functional unit-s affected) involved,
2. Poultry-raising is profitable. respectively. For instance, simple hallucinations may result from stimu-
3. You can never be sure of success. lation of either peripheral receptors, of the conducting tracts or cortical
A house is not known for how it looks but for the projection areas, whereas more formed hallucinations (e.g., visual
things it cooks.
1. You cannot eat pies every day, so have brown
images, micropsia, macropsia etc.) and even more complex, like experi-
bread for a change. ential hallucinations in the form of scenes, point to the deeper divisions
of the temporo-diencephalic region [18].
 P. Patrikelis et al. / Epilepsy & Behavior 72 (2017) 161–172
Other psychic ictal manifestations such as autoscopic hallucinations,
which may be regarded as originating from the parieto-occipital lobes
preferentially of the right side [34], are consistent with Luria's descrip-
tions of episodic changes in the concept of body scheme (e.g., such as
sensations of excessive growth of the hands and feet etc.) are valuable
symptoms, pointing to the effect of a pathological process of the parietal
areas. Of comparable value are perceptual illusions manifested as
psychic seizures which induce changes in the perception of external
objects, for example decrease and increase of their size and shape
(micropsia, macropsia, and metamorphopsia), suggesting visuo-spatial
aberrations of parieto-occipital origin.
Subsequently, ictal auditory phenomena (hyperacusia, paroxysmal
disturbances of the understanding of speech) can be understood as dys-
functions of higher sensory processing occurring in the temporal neo-
cortex. Déjà vu and the paroxysmal visions of catastrophe and terror
indicate a pathological process of mesial temporal origin.
Epileptic personality changes, i.e. anger or irritability, sadness or
depression may also be indicative of dysfunction of the temporal or
frontobasal region [18].
A recent case study suggested that presumed persistent seizure ac-
tivity confined around the right amygdala may lead to the development
of acute psychosis and rapid development of epileptic personality
change [35]. Accordingly, Luria [36] proposed that decreased inhibitory
control of the orbito-frontal cortex on deeper limbic structures, the
amygdala in particular, may induce impulsive, aggressive, and at times
psychopathic types of behavior. Finally, seizures implying a sudden,
sharp lowering of tone and those inducing an immediate and deep un-
conscious state without premonitory signs (aura) are of great localizing
value suggesting pathological processes involving the deep portions of
the brain or the frontal lobes [18].
All these psychosensory disorders are by no means the direct conse-
quence of a lesion of a circumscribed area, but rather their localizing
value can only be proven by taking into account the whole syndrome
(through a syndrome analysis approach) of which these manifestations
are part.
Syndrome analysis refers to the comparative analysis of neuropsy-
chological evidence collected by means of various tests and the determi-
nation of general signs among them, hopefully leading to a unified
syndrome. In Luria's view a syndrome is conceived as a structure
emerged by constellations of causally related, multi-level symptoms
(primary and secondary); thus understanding the different nature of
the latter is of crucial importance in determining the source of a neuro-
logical breakdown and also in advancing the localization hypothesis.
2.1. Translating clinical issues relevant to the neuropsychology of epilepsy
into Luria's terms
Luria theorizes that a particular cerebral area usually stands for a sin-
gle factor subserving different systems and supporting various psycho-
logical functions. The specific pattern of interacting factors leading to
a particular behavior represents what Luria defined as a functional sys-
tem. It should be noted that each area of the brain can be involved in
more than one functional system, something which has also been dem-
onstrated by recent investigations using functional magnetic resonance
imaging (fMRI) [37–39]. Indeed, epilepsy is a network disease [40].
Over recent years, the concept of “epileptic focus” has progressively
been substituted by that of “epileptic network” [41,42]. In fact, multiple
studies implementing functional neuro-imaging techniques, have con-
firmed that the epileptic zone can rarely be reduced to a circumscribed
brain area [43], as it regularly involves distinct brain regions generating
both interictal [44] and ictal activity [45]. Accordingly, functional con-
nectivity has been widely implemented to depth-EEG data to predict
seizures [46] and identify epileptic networks in patients with partial
epilepsies [47], suggesting alterations of synchronization in brain
networks both during ictal [48–50] and interictal to ictal shifts [51]. Dis-
ruptions of epileptic networks may be associated with neuro-cognitive
167
and behavioral deficits, regularly encountered among patients with
chronic epilepsy. In the study of epilepsy, network analysis (or network
theory) is gaining ground as it provides a theory structure for the study
of the organization of brain networks , e.g. [52,53] and also serves to im-
prove our understanding of comorbidities of chronic epilepsy, such as
behavioral problems and cognitive decline [54,55].
In addition, modern neuro-imaging data suggests that cognition
emerges as a result of neural dynamics, meaning interactions among
distributed brain regions through phase synchronization laying the
ground for cognitive processing. Thus cognition and consciousness are
believed to emerge from the activity of widespread brain regions coor-
dinated by phase synchronization [56–59]. Such neural interactions are
extremely dynamic, leading to temporary establishment and dissolu-
tion of functional networks in the time frame of tens of milliseconds.
Contemporary neuroscience leans towards a network-based ap-
proach to the study of cognition in general, and cognition in epilepsy
in particular, legitimating Luria's classical concept of the systemic orga-
nization of cognitive functions. Thus, to some extent, Luria anticipated
the direction of neuro-scientific research, as he claimed that psycholog-
ical functions are dynamic systems with their interacting constituent
parts being non-linearly organized into spatio-temporal patterns [60].
The major advantages of the Lurian approach are its well-structured
and well-defined integrative cognitive components and its ability to
provide valuable information concerning their interactions [60].
2.2. Examples
Luria's neuropsychological procedures have been thoroughly
discussed in both Higher Cortical Functions in Man [18] as well as in
Luria's Neuropsychological and Neurolinguistic Testing [61]. His sys-
temic approach may provide a conceptual framework for neuropsycho-
logical praxis in general and for epilepsy in particular. What follows are
some clinical examples through which the reader can gain a better un-
derstanding of the Lurian approach and its possible applications to the
neuropsychology of epilepsy (see Table 1).
I. Investigation of the learning process may yield valuable results
for the neuropsychological study of local brain lesions, since
analysis of methods implemented in the learning process may in-
form clinicians as to the amount of retained information, as well as
to the patient's attitude towards mistakes he/she may make [18].
Procedure: a series of completely unrelated words that are too long
(10–12 words or alternatively 8–10 numbers) are presented and
the examinee is required to reproduce them in any order. This is re-
peated 8 to 10 times, with the examinee writing down what he/she
recalls after each consecutive presentation and the examiner noting
the words recalled each time by numbers corresponding to their
reproduction order, and also tracking the subject's aspiration level
for subsequent clinical interpretations.
Patients with posterior lesions present the same qualitative
features as those found in healthy subjects (their aspiration lies
rather higher than the amount of words they are able to recall in
each consecutive trial; they recall items in a particular order; they
pay attention to the missing items), although their learning curves
are likely to rise very slowly as compared to those of healthy sub-
jects. Quite different is the learning profile of patients with frontal
lesions exhibiting pathological features in their level of aspiration,
as they may state any number when requested to predict their
next series performance without being aware of their real poten-
tial. Moreover, they continue to inertly repeat a low number of
items, even if they have previously showed that their actual per-
formance is higher; they memorize words in a random way (lack
of strategies) without paying attention to words they were not
able to recall the previous time (impaired self-monitoring); their
recalled series may be either stereotyped or non-repetitive; they
regularly repeat previous mistakes with no attempt to correct,
168 P. Patrikelis et al. / Epilepsy & Behavior 72 (2017) 161–172
while within a series reproduction they often repeat the same
word. Their learning curve often reflects the inactive character of
their memory processes, which doesn't rise above a specific num-
ber of items (plateau). Frontal patients often are not able to make
use of logical connections as a memory aid; for instance, if they are
given a picture to form an association with the word to be remem-
bered, they often produce independent associations unconnected
to the word [18]. Problems in taking advantage of memory aids
seem to characterize frontal syndromes in general, and patients
suffering frontal lobe seizures in particular [62,63].
II. The above-mentioned methodology seems to be a good fit with is-
sues of differential diagnosis between patients suffering frontal-
and those with extra-frontal- seizure origin, particularly when
examining the domain of learning, as it provides qualitative-
semeiotic neuro-behavioral information which points clinicians
towards the anatomical source (meaning the specific functional
systems) of neurological breakdowns.
Our knowledge with respect to partial epilepsies of posterior ori-
gin, and in particular to occipital-lobe epilepsy, is quite limited as
these epilepsies have neither been studied extensively nor on a
large sample of patients. Of particular significance to neuropsy-
chology is that occipital seizures often spread the temporal-, sup-
plementary motor- or parietal-areas, with their clinical
semiology often resembling that of the above areas. Furthermore,
seizure activity in the occipital areas may spread to the frontal divi-
sions of the cortex (1/3 of cases), as well as to other multiple cortical
sites simultaneously (1/3 of cases) [64]. Both parietal and occipital-
lobe epilepsy present a rather diffuse and generalized pattern of
cognitive dysfunction, often mimicking neurocognitive deficits pres-
ent in TLE, because of the propagation of seizures beyond the parie-
tal or occipital lobes [65,66]. Also EEG findings in posterior epilepsies
may resemble temporal or frontal anomalies [66]. Consequently,
neuropsychological differential diagnosis may prove problematic.
What Luria proposes for cases of patients with suspected occipital-
lobe pathology is the study of the direct impression of traces in
order to elicit focal deficits [18]. This is based on the fact that each
stimulus induces excitation that persists for some time even after
the stimulus itself has ceased to act. The immediate after-effect of
this stimulus (in our case visual) may be investigated to reveal oc-
cipital lobe dysfunction.
Procedure: “If a subject is shown a bright red figure (a square or
circle) superimposed on a homogeneous gray (or white) background
for 15 to 20 seconds, he will continue to see a trace of this figure for
a short time after the figure itself has been removed. As a rule, it re-
tains well-defined outlines, which only gradually fade. The image
persists for a short time and then gradually disappears, sometimes
reappearing once or twice. In healthy subjects, the visual after-
image is present between 15 and 30 s, after which it loses its defini-
tion and disappears. Its duration and intensity depend on the individ-
ual peculiarities of the subject, the brightness of the stimulus, and the
duration of its fixation” (p. 441) [18].
Stimulation parameters such as brightness and duration of after-
images may be considerably altered in pathological states,
reflecting general changes in cortical excitability. In patients in-
clined towards hallucinations, the brightness and persistence of
the afterimages may be enhanced [18]. Accordingly, since dis-
turbed cortical excitability is an inherent patho-physiological
feature of epilepsy, we posit that the above-mentioned experi-
mental paradigm may apply to patients with suspected seizures
of occipital origin to unmask their primary cognitive deficits
from secondary epiphenomenal-cognitive manifestations of
temporal or frontal-like type.
III. A special method used to study the direct impression of traces in
the somato-sensory domain concerns the phenomenon of “fixed
orientation” or “set,” which has been studied in detail by the so-
viet psychologist Uznadze [67].
Procedure: “If a subject is instructed to grasp different size spheres
10 to 15 times with both hands, each time taking the larger sphere
in the right hand and the smaller in the left, and if then, in a control
experiment, spheres of identical size are placed in both hands, the
subject usually has an illusion of contrast, known as”Charpentier's
illusion“(i.e., the sphere in the right hand seems smaller than that
in the left). This illusion, a phenomenon of after-contrast in the
sphere of cutaneous and kinesthetic sensation, may persist for a
considerable period of time. It is then gradually extinguished, the
course of its extinction typically fluctuating so that it may some-
times be observed after considerable intervals of time” (p. 443) [18].
What is important to our discussion is that according to Luria pa-
tients with seizures originating in the somato-sensory cortex
(parietal seizures) may show a sharp increase in the stability
of their fixed orientation or set [18], thus implying somato-
sensory cortex dysfunction and consequently enabling clinicians
to further corroborate the hypothesis of a possible parietal
seizure onset.
IV. Another method proposed for the study kinetic apraxia - which
can also applied to epilepsy - is that of motor paradigms like
the Fist-Edge-Palm test requiring the execution of sequential
movements. Disturbances of kinetic praxis may give rise to defi-
cits in executing sequential motor acts in a fluid manner (Luria's
kinetic melodies). Typically, lesions of the premotor areas are
likely to compromise motor sequencing. However, many other
cortical divisions seem to contribute to the construction of com-
plex movements each with its own functional duty; for instance,
an intact visuo-spatial afferent system is required for a complex
motor act to be normally performed, since this system provides
the external space coordinates (up, down; right, left; near, far)
to ensure the correctness of movement [18]. Visuo-spatial coor-
dination is carried out by the occipito-parietal divisions of the
cortex. Thus, it is extremely important to disentangle such com-
ponents, as well as others, which contribute to the construction
of complex motor acts to understand the anatomical origin of
disturbed motor-behavior. Moreover, at a behavioral level, fur-
ther observations such as the patient's inability to correct the
number and type of errors i.e., errors of serial organization, un-
stable tendencies of motor program expansion, inert reproduc-
tion of a motor program and perseverance, de-automatization
and echopraxic movements, may be of value in understanding
both the nature and also the anatomical origin of cognitive
disturbances. Thus, in case of impaired motor sequencing, the
above clinical signs may inform the clinician of the potential in-
volvement of areas beyond the supplementary motor cortex,
such as executive-dependent prefrontal territories; for instance,
in such patients, euchopraxic movements may be attributed to
a disruption of the inferior frontal gyrus that may influence imi-
tative behavior. Recent fMRI studies in humans have demon-
strated a putative role of the mirror neurons activity in the
ventral premotor cortex, inferior frontal gyrus, inferior parietal
lobule and insula [68]. Hence, semeiotic analysis of a patient's
neuropsychological presentation should be considered in order
to define the functional deficit zone, when for instance assessing
patients with seizures of suspected supplementary motor origin,
resulting from the individuation of the functional system(s) in-
volved and their components.
Another valuable paradigm to study the visuo-kinesthetic organiza-
tion of a complex movement is to ask the patient to reproduce the
different finger positions demonstrated by the experimenter. To this
purpose the patient is asked to reproduce one of the positions of the
hand, or, he is asked to place the index over the middle finger, etc. It is
important that the patient has as little visual control over his movement
as possible; for this purpose, his hand may be placed through a hole in a
screen.
 P. Patrikelis et al. / Epilepsy & Behavior 72 (2017) 161–172
A true disorder of the kinesthetic basis of movement will also be re-
vealed by this test when the patient is not immediately able to achieve
the necessary selection of movements (e.g., movements are diffuse in
character, often instead of extending the index and little fingers the pa-
tient continues to extend the middle and ring fingers, or he may be un-
able to perform the test with the corresponding hand, trying to help
himself by bending the fingers with his other hand). The above analysis
of a patient's motor behavior is indicative of a disturbance of the kines-
thetic basis of action and in the words of Luria, of afferent (kinesthetic)
apraxia. Apraxia constitutes one of the principal seizure somato-sensory
symptomatologies in both occipital and parietal-lobe epilepsy [69].
It is noteworthy that the study of motor behavior using Lurian proce-
dures has proved valuable in epilepsy, since early studies suggested that
impaired motor dexterities represent a salient neuropsychological fea-
ture of patients suffering frontal seizures [70,71]. In our opinion this is
not an incidental finding, but rather one attributed to the use of simple,
but rather process-oriented, motor tests to elicit motor impairments
that would otherwise remain concealed, given the inherent complexity
of frontal seizures.
2.3. Language lateralization: the Wada Test versus the fMRI
The Wada Test is an invasive technique, which enables assessment
of language in one hemisphere, without the influence of the other, by
producing a fairly diffuse, unilateral functional arrest, and as such
doesn't provide specific information regarding the inter-hemispheric
organization of language. Instead, the fMRI serves as a non-invasive
activation method that enables detailed investigation of both hemi-
spheres simultaneously. Thus, in examining hemispheric lateralization
of language functions, the fMRI goes well beyond the dichotomic way
of thinking concerning a leftward, rightward or mixed representation
of language, by adopting a network view with often bilateral distribu-
tion [72]. As a result, the Wada Test approaches to language lateraliza-
tion find less evidence for bilateral language functioning than the
fMRI approaches do. This is supported by imaging studies reporting ac-
tivation in the homologous (with respect to the left hemisphere) areas
of the right-hemisphere for a variety of language tasks, suggesting
that the right hemisphere also plays some role in language processing
[73,74]. More recent functional neuro-imaging studies have extended
these findings by demonstrating the wide-range spatial distribution
of language systems, probably spanning the frontal, temporal, and
parietal cortices [73,75]. This is consistent with earlier views on the
topic [76,77].
Luria states, “The study of the system of localization of higher psycho-
logical functions in the cortex, by such means, overcomes the ideas of nar-
row localization and the conceptualization of the brain as a unitary whole.
Every specific function ceases to be thought of us a product of some kind of
center; on the other hand the function of the brain as a whole ceases to be
conceived of as the work of a homogeneous mass of nervous tissue. In the
place of both these conceptions there is the position of a system of highly
differentiated zones of the cortex working together, accomplishing new
tasks by means of new “inter-areal” relations” (p. 391) [76].
This may explain why the fMRI protocols, which investigate mental
factions as distributed networks, provide a more distributed and often
bilateral representation of language function, a fact consistent with ear-
lier interpretations of higher cortical functions as complex functional
systems with both intra and inter-hemispheric distributions [18,77],
with their elements non-linearly organized in patterns with variable
time and space distribution [60].
2.4. Limitations
Despite the important theoretical contributions and the clinical ad-
vantages of the Lurian approach, it has been widely criticized for its
lack of a direct evaluation of the tests and of controlled scoring, since
the latter is mainly based upon the clinician's level of expertise rather
169
than on normative data. Instead, standardized psychometric tests have
proven to be more valid and reliable in cases of focal, well-defined
brain insults. Their value, however, is limited when assessing patients
suffering ill-defined brain impairments (as is the case in many epilepsy
cases) and severe or diffuse neuro-behavioral disorders [78]. For in-
stance, when assessing cognitive functions using a standard neuropsy-
chological test on two different patients who have been assigned the
same degree of severity, they may manifest qualitatively different cog-
nitive deficits. In fact, an ambiguity of well-known cognitive constructs
becomes evident in the weak correlation between paradigms, including
multiple cognitive factors, and performance in different cognitive tasks
[79]. Luria's approach instead focuses on the process (not on test
achievement) allowing for error analysis and detecting commonalities
of deficits across the tasks, to enable clinicians to identify the impaired
network. As such this approach is of particular value in tracking diffuse
cognitive deficits caused by the disconnection of brain networks, a
fact which also applies to epilepsy given seizures' disconnecting-
interfering effects on functional networks.
Ever since, various attempts have been made to standardize Luria's
tests, with the that of Glozman most notably [80], and many neuropsy-
chologists have begun to adopt rather flexible approaches to assessment
by choosing tests from separate batteries and of both quantitative and
qualitative nature, targeting (in accordance to Luria) a synthetic evalu-
ation of mental processes and making it possible to dissect them into
several functional domains.
Future studies should address the still unresolved issue of integra-
tion between quantitative and qualitative assessment methods, to fur-
ther enhance the potential of Luria's neuropsychological examination
paradigms.
3. Perspective
Clinical neuropsychological praxis in the context of epileptology
advises for an inability of a clear-cut distinction of seizures anatomical
origin on the basis of patient's cognitive deficits, a fact further corrobo-
rating a network view of mental functions, instead of a reductionist
localization approach. For instance, the negative effects of seizures
spread from temporo-limbic to frontal brain regions have been reported
by the literature and may explain the secondarily induced frontal dys-
function often seen in TLE patients, as well as a temporal like pattern
in frontal lobe epilepsy patients [81–83].
However, this type of dichotomic and rigid view seems to impact the
way clinicians regard mental functions and their purported direct link to
specific brain areas. This leads to arbitrary and oversimplified interpre-
tations of cognitive performance based on the distinction between fron-
tal and temporal, or even exclusively hippocampal, tasks.
On the one hand, the illogic and selective overlook of eminent
figures' theorizing in the field of neuroscience, like Nauta [84] and
Pribram [85], who view the hippocampus and the frontal brain areas
as a unitary integrative system, and on the other hand, the success of
dichotomic and modularistic views of brain function, both considerably
limit clinical thought in their epistemic blind alleys.
In the area of epilepsy, neuropsychology of focal epilepsies and espe-
cially of MTLE, has been dominated for many decades by the material-
specificity theory of memory, which urges for a clear-cut lateralization
of cognitive functions and especially of memory. Thus, for instance,
verbal memory was attributed to the functional domain of the domi-
nant (usually left) temporal-lobe and non-verbal memory to the non-
dominant (right) temporal-lobe. This model has been proposed as a
sort of diagnostic panacea to solve the riddle of lateralization and local-
ization of seizures.
Although this theory draws its roots to the early interpretations of
post-resection studies of memory in MTLE, current findings on post-
surgery epilepsy cases are not likely to be consistent with that. For in-
stance, a weak functional relation has been reported between right
temporal-lobe and spatial memory, as many aspects of this cognitive
170 P. Patrikelis et al. / Epilepsy & Behavior 72 (2017) 161–172
domain are affected also in patients with left MTLE and those with hip-
pocampal sclerosis undergoing anterior temporal lobectomy [86,87].
Recent neuro-imaging findings have raised further concerns about the
material specificity theory of memory [88], which advises for a dynamic
interaction between left and right temporal regions, with their selective
contribution depending on the demands imposed by the task in hand
[89–93].
By working with patients suffering frontal injuries, Luria emphasized
the notion of executive functions and deepened understanding of what
is currently known as dysexecutive syndrome. He provided detailed de-
scriptions and neuropsychological analyses of these patients, showing
that their difficulties are not strictly related to what we call “frontal
symptoms”, but rather concern functions such as memory, usually
attributed to the integrity of temporo-limbic regions.
Memory problems encountered in patients with frontal syndromes
are qualitatively different from those of patients suffering from tempo-
ral lesions; frontal injuries likely compromise the selective character of
mental activity, which is rather substituted by inert stereotypes of be-
havior which lacks goal-direction [94]. For instance, in a word list recall
task frontal patients usually show a sort of ceiling effect (plateau) in the
learning curve, reflecting the inactive and inert character of their mem-
orization process. They seem to lack the internal drive to progressively
increase the number of items recalled, something that would normally
occur in persons with intact frontal systems which in each recall trial ac-
tively compare currently recalled items with those omitted.
The inert character of old memorizations, such as a word lists
or other information, is likely to interfere with new learning, thereby
causing intrusions in the current patient's recall, which take the form
of unrelated associations and confabulations, i.e., words or phrases
invented by the person without any relation to the material to be
learned. Consequently, difficulties in inhibiting such inappropriate and
pathological responses in the form of inert stereotypes lacking selec-
tivity of normal memory traces, transform memory from a close logical
system to an open system susceptible to external interferences, sensory
impressions and unrelated associations [94].
It is widely known that investigations of focal epilepsies and MTLE in
particular, have shed light to the neurobiological substrate of memory
systems, and their relevant pathophysiology as well. For instance, pa-
tients with medial temporal pathology typically manifest difficulties
in conserving newly encoded memory traces and as such as present
fast rates of forgetting. According to Luria, this reflects difficulty in
stabilizing mnemonic traces, a phenomenon not encountered among
patients with lateral temporal lesions which, by contrast, suffer from
impaired encoding of auditory information. Patients with medial tem-
poral pathology are more prone to exhibiting proactive interference,
i.e., they are unable to recall a recently encoded story after being read
a new one, while they are quite able to grasp the general meaning of
the information presented for learning.
Another of Luria's major contributions to neuropsychology concerns
the diagnostic localization methods, as those, for instance, introduced in
his work “A neuropsychological analysis of problem solving” [95], with
respect to the evaluation and interpretation of cognitive disorders and
their anatomo-functional correlates, meaning the functional systems
involved in their clinical expression. In this latter work, Luria aimed to
assess mental activity as a whole in simple experimental conditions
utilizing procedures based on theoretically solid grounds. To this end,
the experimental paradigm he adopted was that of the solving of arith-
metic problems of various nature and complexity, given that the struc-
ture of mathematical problems offers an ideal chance to study higher
cortical functions. This is because the structure of mathematical
problem-solving promotes a clinician's understanding of the nature
of impairments in the course of thorough observations of a patient's
solving attempts and the cognitive mechanisms recruited in these
attempts.
In this manner, different types of problems, such as difficulty
comprehending a problem's initial statement, concentration and
attention problems, trouble with programming and maintenance of an
action plan, difficulty going through the required steps to solve prob-
lems, as well as the comparison of the outcome with the initial state-
ment of the problem, may inform the clinician on the nature of
cognitive disturbances and the underlying functional systems.
As a result, Luria was able to describe specific patterns of neuropsy-
chological dysfunction in patients suffering from lesions of variable
location and attribute them to the domain of different functional
system/s. Thus, through his writings we are able, for instance, to recog-
nize the specific characteristics of patients suffering parieto-occipital,
basal frontal or massive frontal-lesions, left frontal pathology, temporal
lesions etc., [95].
The above contributions seem to be highly promising for the
neuropsychology of epilepsy and epilepsy surgery, since they provide
clinicians with valuable methods and theories to assist them in the lo-
calization -and lateralization- of cognitive deficits. A cognitive deficit is
no more attributed to a single brain region, but rather to the functional
breakdown of one or more functional systems. The logic underlying this
approach seems consistent with our current knowledge in epileptology
with respect to epileptic networks, therefore constellations of areas pre-
senting seizure activity but no more isolated seizure foci. Additionally,
consistent with Luria's systemic view of the brain is the modern
construct of the functional deficit zone [96], i.e., the part of the brain
showing dysfunction interictally, as suggested by objective neurological
examination, neuropsychological screening and fMRIs, which is of great
importance for the neuropsychology of epilepsy and the pre-operative
neuropsychological monitoring of patients who are candidates for
epilepsy surgery, in particular.
We herewith address the necessity for the neuropsychology of
epilepsy and epilepsy surgery to crush the shackles imposed by the
quadrant-based logic of the modular approach to the brain, in favor
of a systemic view inspired by Luria's clinical work and theorizing,
i.e. the qualitative syndrome analysis. Luria's idiographic neuropsycho-
logical approach through thorough and insightful evaluations and
theory- guided methods may prove to be invaluable in the context of
the preoperative monitoring of epilepsy surgery candidates, particularly
when neuropsychologists are called upon to provide anatomical data
concerning the lateralization and localization of seizures.
Disclosure of conflicts of interest
We confirm that we have read the Journal's position on issues in-
volved in ethical publication and affirm that this report is consistent
with those guidelines. None of the authors report any conflict of interest.
There are no sources of financial support.
Acknowledgments
This research did not receive any specific grant from funding agen-
cies in the public, commercial, or not-for-profit sectors.
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