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Inf. Child. Dev. 20: 319 (2011) Published online 14 May 2010 in Wiley Online Library (wileyonlinelibrary.com). DOI: 10.1002/icd.683
Although neonatology, the study of the newborn, is well established in medical science, psychological research on the newborn is relatively scarce. Can we justify this period as a distinct stage of human development in Psychology? This introductory article considers the unique characteristics of the neonatal period, the impact of the transition to extrauterine life, including the impact of birth itself, and the stages of brain development that characterize this period. It presents evidence of an intentional, intersubjective neonate, and uses behavioural and neuroscientic evidence to argue that the neonates early social preferences and responses indicate a unique, sensitive, experience-expectant stage of development. The authors of this issue agree in proposing that the newborn infant is prepared, evolutionarily and psychobiologically, to be born intersubjective. The notion of an intersubjective newborn infant, however, is virtually impossible to support without data and models from neuroscience, medicine, perinatology, physiology, ethology, evolutionary psychology and cognitive science. This issue is an attempt to bring scientists together from many of these elds to explore the unique characteristics of the rst weeks of life. Copyright r 2010 John Wiley & Sons, Ltd. Key words: neonate; intersubjectivity; brain development
*Correspondence to: Emese Nagy, School of Psychology, University of Dundee, Park Place, Dundee DD1 4HN, Scotland. E-mail: E.Nagy@dundee.ac.uk
Copyright r 2010 John Wiley & Sons, Ltd.
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and adulthood all span years rather than days, the neonatal period is much shorter. How can we justify this 4-week-long period as a distinct stage of human development in psychology? Infancy itself is a heterogeneous stage characterized by multiple developmental and regression periods for different psychological functions (Heimann & Plooij, 2003). Is the neonatal period so well marked within infancy that we can justify the neonatal period as a stage? In fact, recognition of the newborn in developmental psychology is far from consistent. The stage has gained some interest, but recognition has been considerably delayed and less emphasized compared with the well-established medical sub-discipline of neonatology. Neonatology as a specialty emerged a few years after paediatricians took over the care of the newborn from obstetricians in the mid 20th century. Concurrently, neonatal mortality decreased from 40 in every thousand live births in 1900 to 4 or 5 in every thousand in 2000 (Levene, Tudehope, & Sinha, 2008). Newborns became a special paediatric population, and further elds evolved rapidly to address issues specic to this stage of development, such as neonatal intensive care, neonatal nursing, neonatal physiology or neonatal ultrasound. In medicine, at least, the neonatal period is distinct, and professionals are provided with specialized training to help infants at this stage. The World Health Organisation has further demarcated a perinatal stage within the neonatal period. Perinatal, according to the WHO, refers to the period from the 22nd completed gestational week to the end of the 7th day after birth (WHO Geneva, WHA20.19, WHA43.27, Article 23). While demarcation of the rst week of life as perinatal is rarely used, and perinatal generally refers to the neonatal period, mortality indices are commonly reported separately for the two stages. Perinatal mortality rates reect deaths occurring up to 7 days (the 6th full day) after birth, while neonatal mortality refers to deaths occurring within 28 days after birth, and infant mortality refers to deaths occurring within 1 year after birth. The large differences in these indices justify the terminology: a 10/1000 death rate has been reported in the rst week of life, while it is half this rate (5/1000) for the late perinatal period in developed countries (WHO, 2005), and mortality rates for the remainder of the rst year of life are equal to or less than those of the neonatal period alone. These numbers may indicate the distinctness of the rst 4 weeks of life within the period of infancy, and reect a highly vulnerable period of transition as the infant adapts to extrauterine life.
birth (Lagercrantz & Herlenius, 2002) that activate the metabolism of glycogen to glucose, and further metabolic pathways for conversion of alanine, pyruvate and lactate to glucose. When all these adaptive processes become insufcient, the newborn starts to convert fat to glucose (Diderholm, Stridsberg, Ewald, Lindeberg-Norden, & Gustafsson, 2005). The loss of body fat, however, challenges the newborn with a further decrease in body temperature, which is already about 151C colder than the intrauterine environment. Taken together, even healthy newborns born in uncomplicated deliveries need to rapidly mobilize adaptive physiological processes during their transition from the intrauterine to the extrauterine world. Although this transition renders the newborn vulnerable, benecial effects of the stress of being born have been proposed by Lagercrantz and Slotkin (1986). Before birth, aided by a downregulated sympathetic nervous system, the foetus responds to stress with bradycardia and stillness (Lagercrantz & Herlenius, 2002). The mechanical tactile and proprioceptive pressure during vaginal delivery and the overwhelming visual and auditory input from the extrauterine environment result in a sudden activation of the sympathetic nervous system, such as increased levels of noradrenaline, for example, that facilitate breathing and the co-regulation of the cardio-respiratory system. Such changes also increase behavioural arousal in the rst hours of life, and a wide-awake newborn is available and ready for the rst extrauterine social interactions.
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microanalytic observations of a pair of twins by Stern (1971), and the recognition that neonate actions are intentional even when they appear random (e.g. Meltzoff & Moore, 1977; Van der Meer, Van der Weel, & Lee, 1995). While testing the validity of neonatal imitation, Fontaine (1984) could not help noting how much we try to avoid attributing intentionality to the infant. These ndings, however, have led to a wider recognition of the emotionally attuned, intersubjectively engaged infant, and rekindled an interest in neonates beyond the reactive, reexive, subcortical and vulnerable infant (e.g. Field et al., 1983; Heimann & Schaller, 1985; Kugiumutzakis, 1985; Meltzoff & Moore, 1983).
REFLEXIVE OR INTENTIONAL?
Reactive, reexive and subcortically guided are all terms commonly used to describe the neonate. A number of primitive reexes aid the neonate; for example, to free up their airways or to grasp strongly onto any object, a response that is active well before birth (Petrikovsky & Kaplan, 1993) and that which may have evolved to ensure safety. At tactile stimulation of the cheeks, newborns start moving their heads rhythmically sidewise in search of the stimulus, and then start sucking it vigorously. This well-coordinated rooting and sucking behaviour enables newborns to respond very quickly and efciently to the maternal breast if it is close by. The use of the term reex is justied by the view that the very young infants central nervous system is far too immature for voluntary control of such complex, functional, well-organized behaviours. These reexes displayed by the neonate, which are in fact complex, highly organized behaviours, frequently resemble later purposeful behaviours. Since a great number of reexes can be elicited in the young infant while higher brain activity cannot yet be observed, the conclusion has been drawn that the infants brain activity consists only of reexes. This opinion does not at all do justice to the facts as Peiper pointed out in 1963 (p. 248). Several neonatal reexes disappear temporarily and then reappear later in a reorganized form, thus leading to speculation that brain development is hierarchically organized with an immature subcortical brain in the newborn, (sometimes even labelled archaic). Indeed, it has been suggested that newborns are in a state of extrapyramidal cerebral palsy (e.g. Capute, Accardo, Vining, Rubenstien, & Harryman, 1978). According to this model, the subcortical primitive functions become inhibited by the subsequent maturation of the higher cerebral cortical areas, and the transition coincides with the emergence of infant intentionality. Thelens studies on the continuity of newborn stepping and later walking support a very different model. Instead of being two different behaviours, distinct not only by developmental stage but the underlying neural structures; Thelens studies found that walking develops gradually from patterns of stepping and walking that are available already at birth (Thelen & Coke, 1987). Seven-month infants, who showed no stepping movements while stationary, displayed mature stepping patterns when supported on a treadmill (Thelen, 1986). Thelen suggested the neural structures for stepping and walking are the same from birth. As infants gain strength, increase balance control, newborn stepping gradually evolves to a more mature walking. Primitive reexes may not disappear, after all. Although Sherrington (1906) and later Prechtl (1956) and Touwen (1976) questioned whether these early complex behaviours were primitive or indeed
Copyright r 2010 John Wiley & Sons, Ltd. Inf. Child. Dev. 20: 319 (2011) DOI: 10.1002/icd
reexes, the concept is still in use. The examination of primitive reexes as part of the standard neurological examination of the newborn provides invaluable behavioural measures of the integrity of the nervous system in the newborn; at the same time, it remains part of the conceptual framework of how the newborn nervous system is organized. The existence of these complex behaviours in the neonate does not imply, however, the lack of intentionality in the neonate. Physiological indicators, such as the heart rate changes and heart rate variability, have long been suggested to indicate attentional responsivity of the newborn infant (Porges, 1972). Newborns were found not only to be able learn (Clifton, 1974; Porges, 1972, Stamps & Porges, 1975), but anticipated the upcoming stimuli, indexed by heart rate deceleration (Porges, 1972). Recent evidence suggests a neurophysiological link between, for example, early complex behaviours, states of consciousness, self-other regulatory functions and social engagement. Self-regulatory behaviours, such as non-nutritive sucking in the neonate, are known to activate the vagal system (Marchini, Laggercrantz, Feuerberg, Winberg, & Uvnas-Moberg, 1987) and cause a threefold surge in insulin levels within a minute. The increased vagal tone, in turn, stimulates growth, increases anabolic activity (Uvnas-Moberg, Widstrom, Marchini, & Winberg, 1987) and facilitates physiological stability. The increase in vagal tone also enhances afliative behaviours and sensitizes and prepares the newborn for the auditory, perceptual, visual and motor aspects of participation in intersubjective interaction (Porges & Furman, this issue; Trevarthen, this issue).
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Nagy & Molnar, 1998; Nagy, Orvos, & Pal, 2009). When the experimenter raised her index and middle ngers, newborns raised these two ngers, and when the experimenter raised her thumb, index nger and middle nger together, babies raised these three ngers but not the others (Nagy et al., 2009). It has been suggested that the voluntary production of such ne motor movements appears only in the second half of the rst year when the motor pathways become sufciently myelinated (Eyre, Miller, Clowry, Conway, & Watts, 2000). Indeed, neural conduction time from the motor cortex is about three times longer in neonates than in adults, yet the speed of the actual movement was not different (Schieber, 1996). Despite the expectations based on the neurophysiological literature, neonates were found to voluntarily show such ne nger movements in their rst days of life, and the study has been repeated (Nagy et al., 2005, 2009). Although we have evidence that even complex social behaviours can be guided purely by subcortical areas, such as a smile reported in an anencephalic neonate by Luyendijk and Treffers (1992), neonates are far from subcortical. Studies using event-related potential (ERP) measures reported the functional activity of several cortical areas in neonates and young infants. Newborn infants activated the fronto-central areas and the left superior temporal gyrus during categorical perception of phonemes, a network for phonetic perception similar to that of adults (Dehaene-Lambertz & Pena, 2001). The mismatch negativity ERP component, an index of the perception of a stimulus that deviates from the stream of other stimuli, was measured over the temporal areas in newborns (Dehaene-Lambertz & Pena, 2001). The newborn brain therefore processed these stimuli similarly although a little slower than adults (292 ms in the newborn, 80160 ms in the adult) (Naatanen, Gaillard, & Mantysalo, 1978). Many further ERP components known from studies with adults (such as P150, N250, P350 and N450) have been found in neonates (Kushnerenko et al., 2002). The cortex is functionally active at birth, with the somatosensory and motor areas particularly active, yet the hippocampus, thalamus and brainstem have the highest glucose metabolism in the newborn brain (Chugani, 1998). As the studies cited above demonstrate, behaviours in the neonate may be guided by additional subcortical pathways that differ from those in adults. The cortical contribution to a function will certainly differ between the young infant and the adult, as demonstrated in a study by Tzourio-Mazoyer et al. (2002), in which 2-month-old infants activated their left superior temporal and inferior frontal regionsassociated with language processing in adultswhile watching pictures of the faces of women. The activity of the brain indicates that perceiving and performing speech develops in regions that aid communicative responses to non-verbal expressions.
throughout infancy and childhood, and a subsequent decline in synaptogenesis from puberty through adulthood. Until the perinatal stage, the process proceeds independently of experience. Synaptogenesis in the perinatal period, however, becomes experience-expectant; that is, external stimuli are needed to ne-tune the neural circuits in most brain areas. The critical periods are different for different functions. In the visual cortex, synaptogenesis progresses independently of input from the periphery for about 4 months in the rhesus monkey (Bourgeois, Jastreboff, & Rakic, 1989; Bourgeois & Rakic, 1996). Other neural systems, however, as if pre-wired earlier, appear in full complexity in the perinatal period, possibly laying the foundation for further experience-expectant and dependent synaptogenesis. Infants born prematurely, for example, showed weaker discrimination between the voice of a stranger and their mothers, and the difference could not be attributed to post-natal experience (Black, deRegnier, Long, Georgieff, & Nelson 2004). Infants visually deprived in their rst 7 weeks of life showed impaired facial identity processing, but intact processing of facial movement and expressions, even as adults (Geldart et al., 2002). Newborns show similar predispositions such as attending to biological motion (Simion, Regolin, & Bulf, 2008), human faces (Johnson, Dziurawiec, Ellis, & Morton, 1991; Goren, Sarty, & Wu, 1975) and human speech (Vouloumanos & Werker, 2007). They learn the characteristics of the face (Field, Cohen, Garcia, & Greenberg, 1984), the voice (Mehler, Bertoncini, & Barriere, 1978; deCasper & Fifer, 1980) and the odour (Cernoch & Porter, 1985) of their mothers surprisingly rapidly. Bednar and Miikkulainen (2000) suggested that the emergence of these preferences in the newborn brain resemble the formation of untrained articial networks with initial predispositions. These networks actively seek further encounters after an initial encounter with the stimulus. The rst encounter, as Miikulainen and Bednar propose, may induce the experience-expectant netuning of the neural circuit, and through further repeated exposures the neural circuit learns the properties of the stimulus. Pre-wired predispositions therefore evoke, and interact with, rapid learning. Social behaviours of the human neonate (i) are similarly sensitive to certain features of the stimulus without prior exposure (human face, movement), (ii) usually involve a rapid learning component (such as of the odour or the face of the mother after birth, or learning as a component of imitation (Nagy et al., 2009), and (iii) may appear during the window of a sensitive period, as suggested by the U-shaped developmental curve of some early predispositions. In summary, these characteristics of neonate social response resemble the model of lial imprinting described in avian species by Bolhuis and Honey (1998). In other words, the neonatal period is not merely a period of increased vulnerability important for the medical profession, but is a fascinating stage characterized by processes qualitatively distinct from earlier and later development.
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disturbances such as the still face paradigm (Nagy, 2008), just as older infants do (Murray & Trevarthen, 1985; Tronick, Als, Adamson, Wise, & Brazelton, 1978). Still, the experimental evidence of social-communicative abilities of the neonate continues to be debated. A few researchers have failed to replicate the results (e.g. Anisfeld et al., 2001; Jones, 2006), even suggesting that some of these skills do not develop until the second year of life (Jones, 2009). The purpose of this special issue is, in part, to provide further evidence and theoretical frameworks to support the notion of the intersubjective newborn who is keen to engage, respond to and initiate interpersonal encounters shortly after birth (Nagy & Molnar, 1994, 2004).
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However, as data on human neonate sleep and the newborns level of availability (such as attention, learning) during different sleep stages are still scarce in the literature, Tarullo, Balsam, and Fifer present an up-to-date review of neonatal sleep in this Special Issue. It has frequently been cited that newborns spend approximately 70% of their time sleeping (So, Adamson, & Horne, 2007), and their narrow window of wakefulness may contribute to the view of perinatal infants as passive and reactive, and in part explain why the newborns interpersonal engagements have not been researched more widely. Although newborns do indeed spend most of their time in different stages of sleep, as Tarullo et al. point out in this issue, neonatal sleep is organized differently from sleep in adults. Furthermore, there is evidence that neonates do pay attention, are available to external stimulation and show extensive learning while asleep. Additionally, sleep, particularly active sleep, promotes the maturation of the nervous system, memory consolidation and synaptic remodelling in the brain. The range and rapid uctuation of states of consciousness in the perinatal infant, as Tarullo et al. explain, are therefore of signicant practical and theoretical importance. Bard has been invited in this Special Issue to highlight the insights comparative psychology can offer to human developmental researchers in understanding the perinatal period. Bard is one of the only two researchers who have demonstrated that newborn chimpanzees are able to imitate facial gestures (Bard, 2007; Myowa, 1996), just as human neonates do, using the same paradigm as with human neonates. Along with evidence of imitation in newborn rhesus monkeys (Ferrari et al., 2006), Bards and Myowas works highlight the evolutionary continuity of perinatal social responsiveness, and demonstrates an inborn intersubjectivity across species. In this Special Issue, Bard and her co-authors investigate the neurobehavioural organization of chimpanzee and human neonates using the NBAS (Brazelton, 1984; Brazelton & Nugent, 1995). Although this scale was originally designed to assess human neonates, Bard and her co-authors have applied the technique to neonatal chimpanzees. By so doing, they have made comparative studies on bio-behavioural organization, self-regulation, social orientation and motor maturity between humans and chimpanzees possible. Although a signicant body of our knowledge of the bio-behavioural regulation of the infant comes from animal research (e.g. Kraemer, 1992, 1997; Moriceau, Shionova, Jakubs, & Sullivan, 2009; Sullivan, 2003), substantial differences in pre- and early post-natal development between rats, rhesus monkeys and humans call for caution when translating the results to human development. Bard and her colleagues have innovatively applied methods designed to study human infants to chimpanzees, such as the NBAS (Bard et al., current issue), or the Ainsworth Strange Situation (Van Ijzendoorn, Bard, Bakermans-Kranenburg, & Ivan, 2009). This methodological innovation presented in the current issue has made cross-species comparison possible. Tiffany Field has led one of the most active laboratories in behavioural and psychophysiological research on the human neonate. As author of over 500 research articles and book chapters and 23 books, she has dened the eld and built a substantial body of our current knowledge of the psychological and psychophysiological functioning of the healthy and the high-risk human neonate. Among her extensive and by now text-book data is the description of the neonates ability to imitate facial emotional expression (Field, Woodson, et al., 1982; Field et al., 1983), neonates face, and gaze perception (e.g. Field et al., 1984), facial expressions (e.g. Field, Greenberg, Woodson, Cohen, & Garcia, 1984), neonatal crying behaviour (Field, Diego, Hernandez-Reif, & Fernandez, 2007), heart
Copyright r 2010 John Wiley & Sons, Ltd. Inf. Child. Dev. 20: 319 (2011) DOI: 10.1002/icd
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rate changes as indicators of social perception (e.g. Field, Dempsey, Hatch, Ting, & Clifton, 1979) and as predictors of well-being (Field, Ignatoff et al., 1982; Field et al., 1983), behavioural pain and stress management in the neonate (e.g. Field, 1987, 1990), and the effects of various stimulations on preterm neonates (Field, 1980; Field et al., 1986), including touch and massage (e.g. Field, Scadi, & Schanberg, 1987). Field et al. have further explored the bidirectional relationship, how the mother affects her neonate using biochemical markers (Field et al., 2004a) and neurophysiological markers (Field et al., 2004b), how neonates affect their mothers (Widmayer & Field, 1980), as well as the impact of various disorders such as respiratory distress syndrome, HIV and maternal cocaine abuse on the neonatal infant (Eisen et al., 1991; Field, 1998; Scadi et al., 1996). Field and her laboratory have also built substantial expertise in studying the effect of maternal depression on the developing newborn. In this special issue, Field, Hernandez-Reif, and Diego give us an up-to-date review of their substantial research in this eld. Stephen Porges has been researching in the eld of developmental psychobiology for 40 years, and has published about 200 major scientic papers and chapters. He has been exploring psychophysiological indices of psychological processes, such as EEG, heart rate, and respiratory sinus arrhythmia, and made numerous theoretical and methodological innovations in the eld. He has proposed that cardiac vagal tone is strongly related to stress reactivity and selfregulation (1991, 1992, 1995), and indeed, his series of studies has conrmed that healthy newborns have higher vagal tone (e.g. Porges, 1992), and that infants with higher vagal tone are more socially competent (Doussard-Roosevelt, Porges, Scanion, Alemi, & Scanion, 1997). Aided by the wealth of his data and his analysis of the evolution of the autonomic nervous system, he has developed the polyvagal theory (Porges, 1995, 2007), which places mammalian social afliative behaviours within a new theoretical framework. Porges has proposed that the myelinated ventral vagal system, a mammalian evolutionary innovation, provides the neuroanatomical substrate and physiological foundation for the social engagement system that is actively utilized in intersubjective interactions. Within the system he has described the vagal brake, which enables mammals to a rapid regulatory control needed in social interactions, and the contribution of the myelinated vagus to the regulation of the striatal muscles of the face, neck and middle ear: the eyelid muscles that control social gaze, the muscles of facial expressions, the muscles of the middle ear that extract the human voice from environmental noise, and the neck muscles that tilt or turn the head, establish gestures and contribute to posture. In this Special Issue, Stephen Porges and Senta Furman propose that the development of the autonomic system in the last trimester provides a neural platform that enables young infants to socially engage. This theory provides a new insight into foetal and perinatal psychology, and calls the elds attention to the consequences of the maturational changes taking place at these stages in the autonomic nervous system. Colwyn Trevarthen, a biologist, psychologist and pioneer, established the foundations of a descriptive microanalytic technique for young infants in the 1970s (Trevarthen, 1977), proposed the inuential developmental theory of intersubjectivity (Trevarthen, 1974b, 1979a, 1980a, 1993, 1998, 1999, 2001; Trevarthen & Aitken, 2001; Trevarthen & Hubley, 1978) that continues to inspire generations of researchers in their work with young infants and neonates, and has published about 300 research articles, chapters and books on brain development and infancy over the last 40 years.
Copyright r 2010 John Wiley & Sons, Ltd. Inf. Child. Dev. 20: 319 (2011) DOI: 10.1002/icd
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Trevarthen has identied two distinct phases of primary and secondary intersubjectivity to describe how infants interact with their caretakers and the world well before language develops. The theory of intersubjectivity, however, is not a descriptive, stage-based theory of social-communicative development. Trevarthen has extensively researched the psychobiological foundations of infant development (Trevarthen, 1979b, 1980b, 1980c, 1985), and the theory of intersubjectivity is a neurobiologically, and ethologically grounded theory of the creative process of early development (Trevarthen, 1986, 2001; Trevarthen & Aitken, 2003). In this Special Issue, Trevarthen proposes that neurobiological preparedness enables the human neonate to participate and share meanings with others with coherent, rhythmic purposeful consciousness, and he provides a wealth of evidence that neonates are born with motives and emotions for actions that sustain human intersubjectivity. His rich, thought-provoking inter-disciplinary analysis closes this Special Issue and hopefully signs the beginning of inspirational, new research on the intersubjective newborn. As clearly demonstrated by all papers presented, this eld is widely interdisciplinary. The major conclusion of the Issue is that the newborn infant is prepared evolutionarily (Porges & Furman, this issue), and psychobiologically (Trevarthen, this Issue) to be born intersubjective. The notion of the intersubjective infant is, however, virtually impossible to maintain without incorporating new data and models from neuroscience, medicine, perinatology, physiology, ethology, evolutionary psychology and cognitive science. This Special Issue has attempted to bring together scientists from some of these elds to explore the unique characteristics of the rst weeks of life.
ACKNOWLEDGEMENTS
The writing of this manuscript and editing this Special Issue was supported by the ESRC (RES-062-23-1779), the Nufeld Foundation (SGS/36565) and the British Academy (SG/54514).
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