Lateral Asymmetries in Infancy: Implications for the Development of the Hemispheres

Cerebral asymmetry of cognitive processing of stimulus information is commonly viewed as a neocortical phenomenon. However, a number of lines of evidence give innate asymmetry of brainstem motivating systems, which anticipate experience, a key role. Spontaneous asymmetries of gesture and emotion can be observed in infants, who entirely lack language and visuo-constructive skills. Motives for communication in early life may direct subsequent development of complementary cognitive systems in left and right hemispheres. In split-brain monkeys, lateralized motive sets, intentions for manipulation by one hand, can determine which hemisphere will see and learn. Evolutionary antecedents of cerebral asymmetry appear to affect motivation, social signalling and bimanual coordination, with secondary effect in perceptual processing and learning. The hemispheres of adult humans differ in links with neurochemical system that regulate motor initiatives, exploration and attention, and the approach/withdrawal balance in social encounters. Asymmetries in emotional and communicative behaviour in infancy support evidence that an Intrinsic Motive Formation emerging in the embryo human brain stem regulates asymmetries in development and in functioning of the cerebral cortex.

[1]  A. Young,et al.  Infants' Hand Preferences for Actions and Gestures , 1985 .

[2]  Wittrock The Brain and Psychology , 1980 .

[3]  D. Pandya,et al.  Architecture and Connections of Cortical Association Areas , 1985 .

[4]  J. Graham Beaumont,et al.  Hemisphere Function in the Human Brain , 1974 .

[5]  Elizabeth C. Crosly,et al.  The Brain of the Tiger Salamander. , 1949 .

[6]  G. C. Quarton,et al.  The Neurosciences;: Second study program , 1970 .

[7]  G. Humphrey,et al.  Sex differences in infant reaching , 1987, Neuropsychologia.

[8]  N. Geschwind Cerebral interhemispheric relations , 1974 .

[9]  A. Fernald Intonation and Communicative Intent in Mothers' Speech to Infants: Is the Melody the Message?. , 1989 .

[10]  M. Piercy Functions of the corpus callosum: Ciba Foundation Study Group No. 20. Edited by E.G. Ettlinger. J. and A. Churchill, London. 156 pp. 20s , 1966 .

[11]  N. Fox,et al.  If it's not left, it's right. Electroencephalograph asymmetry and the development of emotion. , 1991, The American psychologist.

[12]  A. Oke,et al.  Lateralization of norepinephrine in human thalamus. , 1978, Science.

[13]  Joseph E LeDoux Brain mechanisms of emotion and emotional learning , 1992, Current Opinion in Neurobiology.

[14]  P. Mackinnon,et al.  Sexual Differentiation of the Brain , 1979 .

[15]  D. Ploog Neuroethological Perspectives on the Human Brain: From the Expression of Emotions to Intentional Signing and Speech , 1992 .

[16]  P. Goldman-Rakic Dopamine-mediated mechanisms of the prefrontal cortex , 1992 .

[17]  M. Jeannerod The representing brain: Neural correlates of motor intention and imagery , 1994, Behavioral and Brain Sciences.

[18]  F. Plooij,et al.  Distinct periods of mother-infant conflict in normal development: sources of progress and germs of pathology. , 1993, Journal of child psychology and psychiatry, and allied disciplines.

[19]  F H Previc,et al.  A general theory concerning the prenatal origins of cerebral lateralization in humans. , 1991, Psychological review.

[20]  M. Kinsbourne The mechanism of hemispheric control of the lateral gradient of attention , 1975 .

[21]  J. Shucard,et al.  The Development of Cerebral Specialization in Infants , 1984 .

[22]  C. Hofsten Catching Skills in Infancy , 1983 .

[23]  D I Perrett,et al.  Frameworks of analysis for the neural representation of animate objects and actions. , 1989, The Journal of experimental biology.

[24]  D. Kimura Sex differences in the brain. , 1992, Scientific American.

[25]  P. Hepper,et al.  Origins of fetal handedness , 1990, Nature.

[26]  H. Prechtl,et al.  Continuity of neural functions from prenatal to postnatal life , 1984 .

[27]  R. Doty,et al.  Lateralization in the nervous system , 1977 .

[28]  Marie T Banich,et al.  Asymmetry of perception in free viewing of chimeric faces , 1983, Brain and Cognition.

[29]  C. Geula,et al.  Architecture of connectivity within a cingulo-fronto-parietal neurocognitive network for directed attention. , 1993, Archives of neurology.

[30]  N. Fox,et al.  Social perception in infants , 1985 .

[31]  J. Bradshaw,et al.  The nature of hemispheric specialization in man , 1981, Behavioral and Brain Sciences.

[32]  G. Visser,et al.  Fetal motility in the first half of pregnancy , 1984 .

[33]  M. Studdert-Kennedy,et al.  Primate handedness reconsidered , 1987, Behavioral and Brain Sciences.

[34]  C. Trevarthen Development of Early Social Interactions and the Affective Regulation of Brain Growth , 1989 .

[35]  R. Harmon,et al.  Continuities and Discontinuities in Development , 2012, Topics in Developmental Psychobiology.

[36]  A. Georgopoulos,et al.  Cognitive neurophysiology of the motor cortex. , 1993, Science.

[37]  A. Young,et al.  Aspects of face processing , 1986 .

[38]  Richard J. Davidson,et al.  Temperament, affective style, and frontal lobe asymmetry. , 1994 .

[39]  W. Crowley,et al.  Neuroendocrine Control of the Onset of Puberty , 1986 .

[40]  A. Harrington So Human a Brain , 1992, Birkhäuser Boston.

[41]  C. Trevarthen,et al.  Perceptual, semantic and phonetic aspects of elementary language processes in split-brain patients. , 1977, Brain : a journal of neurology.

[42]  C. Hamilton,et al.  Hemispheric differences in split-brain monkeys viewing and responding to videotape recordings. , 1984, Behavioral and neural biology.

[43]  R. Myers,et al.  Neural control of social behavior: prefrontal and anterior temporal cortex. , 1973, Neuropsychologia.

[44]  P Bakan,et al.  Visual asymmetry in perception of faces. , 1973, Neuropsychologia.

[45]  J. Beaumont Cerebral Lateralization: Biological Mechanisms, Associations, and Pathology , 1987 .

[46]  S. de Schonen,et al.  Hemispheric Asymmetry in Face Processing in Infancy , 1986 .

[47]  Lori A. Roggman,et al.  Infants' differential social responses to attractive and unattractive faces , 1990 .

[48]  Douglas S. Ramsay,et al.  Onset of unimanual handedness in infants , 1979 .

[49]  J. H. Dewson 4 – Preliminary Evidence of Hemispheric Asymmetry of Auditory Function in Monkeys , 1977 .

[50]  M. Halliday,et al.  Language topics : essays in honour of Michael Halliday , 1989 .

[51]  Jacqueline Nadel,et al.  New Perspectives in Early Communicative Development , 1993 .

[52]  R. Joseph,et al.  The right cerebral hemisphere: emotion, music, visual-spatial skills, body-image, dreams, and awareness. , 1988, Journal of clinical psychology.

[53]  S. Dornič,et al.  Attention and performance V , 1976 .

[54]  E. Ross,et al.  Nonverbal aspects of language. , 1993, Neurologic clinics.

[55]  C. Trevarthen Development of Intersubjective Motor Control in Infants , 1986 .

[56]  C. Trevarthen,et al.  Two mechanisms of vision in primates , 1968, Psychologische Forschung.

[57]  L. Rönnqvist A critical examination of the Moro response in newborn infants—Symmetry, state relation, underlying mechanisms , 1995, Neuropsychologia.

[58]  D. Ottoson Duality and Unity of the Brain , 1987, Wenner-Gren Center International Symposium Series.

[59]  H. Whiting,et al.  Motor development in children : aspects of coordination and control , 1986 .

[60]  N. Geschwind,et al.  Neuroanatomical asymmetries in non-human species , 1982, Trends in Neurosciences.

[61]  L. Murray The sensitivities and expressive capacities of young infants in communication with their mothers , 1980 .

[62]  C. Hofsten,et al.  Neonatal finger and arm movements as determined by a social and an object context , 1994 .

[63]  C. Hamilton,et al.  Hemispheric differences in split-brain monkeys learning sequential comparisons , 1982, Neuropsychologia.

[64]  W. R. Hess Diencephalon : autonomic and extrapyramidal functions , 1955 .

[65]  H. Papoušek,et al.  Musical elements in the infant's vocalization: Their significance for communication, cognition, and creativity. , 1981 .

[66]  R W Sperry,et al.  Reception of bilateral chimeric figures following hemispheric deconnexion. , 1972, Brain : a journal of neurology.

[67]  J. Mehler,et al.  Neonate Cognition: Beyond the Blooming Buzzing Confusion , 1985 .

[68]  Joel L. Davis,et al.  Modeling the Roles of Basal Ganglia in Timing and Sequencing Saccadic Eye Movements , 1994 .

[69]  G. Dawson,et al.  Human behavior and the developing brain , 1994 .

[70]  Alan Peters,et al.  Association and Auditory Cortices , 1985, Cerebral Cortex.

[71]  E. Rolls A Theory of Emotion, and its Application to Understanding the Neural Basis of Emotion , 1990 .

[72]  J. Bruner Child's Talk: Learning to Use Language , 1985 .

[73]  D. Kimura,et al.  Manual activity during speaking. I. Right-handers. , 1973, Neuropsychologia.

[74]  Joel L. Davis,et al.  Adaptive Critics and the Basal Ganglia , 1995 .

[75]  E. Nordeen,et al.  Hemispheric asymmetries in the behavioral and hormonal effects of sexually differentiating mammalian brain. , 1982, Science.

[76]  Brain Asymmetry, Functional Aspects , 1988 .

[77]  G. Berlucchi Two hemispheres but one brain , 1983, Behavioral and Brain Sciences.

[78]  C. Trevarthen,et al.  Voluntary emotional facial expressions in patients with focal cerebral lesions , 1990, Neuropsychologia.

[79]  A. Schore Affect Regulation and the Origin of the Self: The Neurobiology of Emotional Development , 1994 .

[80]  P. Maclean CEREBRAL EVOLUTION AND EMOTIONAL PROCESSES: NEW FINDINGS ON THE STRIATAL COMPLEX , 1972, Annals of the New York Academy of Sciences.

[81]  G. Butterworth,et al.  Origins of Handedness in Human Infants , 1993, Developmental medicine and child neurology.

[82]  C. Trevarthen,et al.  Brain development, infant communication, and empathy disorders: Intrinsic factors in child mental health , 1994, Development and Psychopathology.

[83]  G. Dawson,et al.  Infants of mothers with depressive symptoms: Electroencephalographic and behavioral findings related to attachment status , 1992, Development and Psychopathology.

[84]  M. Lamon,et al.  Unilateral Facial Contractions Produce Mood Effects on Social Cognitive Judgements. , 1992, Cognition & emotion.

[85]  Dahlia W. Zaidel,et al.  She is not a beauty even when she smiles: Possible evolutionary basis for a relationship between facial attractiveness and hemispheric specialization , 1995, Neuropsychologia.

[86]  F. Beck,et al.  Developmental Stages in Human Embryos. , 1988 .

[87]  A. Minkowski,et al.  Physiological and biochemical basis for perinatal medicine. , 1981 .

[88]  J. Panksepp A critical role for "affective neuroscience" in resolving what is basic about basic emotions. , 1992, Psychological review.

[89]  M Mishkin,et al.  Amygdalectomy impairs crossmodal association in monkeys. , 1985, Science.

[90]  N. Geschwind,et al.  Cerebral lateralization. Biological mechanisms, associations, and pathology: I. A hypothesis and a program for research. , 1985, Archives of neurology.

[91]  E. Strauss,et al.  The neurobiological basis of lateralized cerebral function. A review. , 1983, Human neurobiology.

[92]  N. Fox,et al.  Asymmetrical brain activity discriminates between positive and negative affective stimuli in human infants. , 1982, Science.

[93]  S. D. Glick,et al.  Lateralization of function in the rat brain Basic mechanisms may be operative in humans , 1981, Trends in Neurosciences.

[94]  M. Diamond Asymmetry in the Cerebral Cortex: Development, Estrogen Receptors, Neuron/Glial Ratios, Immune Deficiency and Enrichment/Overcrowding , 1987 .

[95]  M Studdert-Kennedy,et al.  Infant intermodal speech perception is a left-hemisphere function. , 1983, Science.

[96]  C. Trevarthen Double Visual Learning in Split-Brain Monkeys , 1962, Science.

[97]  S. Dimond The brain is not a simple seesaw , 1983, Behavioral and Brain Sciences.

[98]  Colwyn Trevarthen,et al.  Sharing makes sense: intersubjectivity and the making of an infant’s meaning , 1987 .

[99]  J. T. Massey,et al.  Mental rotation of the neuronal population vector. , 1989, Science.

[100]  P. Rakic Specification of cerebral cortical areas. , 1988, Science.

[101]  P. Goldman-Rakic,et al.  Gonadal hormones influence the emergence of cortical function in nonhuman primates. , 1989, Behavioral neuroscience.

[102]  J. Cummings Frontal-subcortical circuits and human behavior. , 1993, Journal of psychosomatic research.

[103]  M. Posner,et al.  Orienting in normal and pathological development , 1994, Development and Psychopathology.

[104]  M. Lamon,et al.  Inducing emotion by unilateral contraction of facial muscles: A new look at hemispheric specialization and the experience of emotion , 1989, Neuropsychologia.

[105]  A. Lecours,et al.  The Biological foundations of gestures : motor and semiotic aspects , 1986 .

[106]  S E Trehub,et al.  Music and speech processing in the first year of life. , 1993, Advances in child development and behavior.

[107]  E. Clark,et al.  The Child's Path to Spoken Language. , 1994 .

[108]  R W Sperry,et al.  Perceptual unity of the ambient visual field in human commissurotomy patients. , 1973, Brain : a journal of neurology.

[109]  G. Innocenti General Organization of Callosal Connections in the Cerebral Cortex , 1986 .

[110]  M. Banich,et al.  Are variations among right-handed individuals in perceptual asymmetries caused by characteristic arousal differences between hemispheres? , 1983, Journal of experimental psychology. Human perception and performance.

[111]  Kenneth M. Heilman,et al.  Neuropsychology of human emotion , 1983 .

[112]  A. L. Beckman The Neural Basis of Behavior , 1982, Springer Netherlands.

[113]  M. Hauser Right hemisphere dominance for the production of facial expression in monkeys. , 1993, Science.

[114]  W. S. Condon,et al.  Neonate Movement Is Synchronized with Adult Speech: Interactional Participation and Language Acquisition , 1974, Science.

[115]  Pierluigi Zoccolotti,et al.  Left/right and cortical/subcortical dichotomies in the neuropsychological study of human emotions , 1993 .

[116]  W. Nauta,et al.  Neural Associations of the Limbic System , 1982 .

[117]  D. Tucker,et al.  Emotion and brain lateralization. , 1989 .

[118]  D. McNeill Hand and Mind: What Gestures Reveal about Thought , 1992 .

[119]  R. Thatcher,et al.  Human cerebral hemispheres develop at different rates and ages. , 1987, Science.

[120]  Nathan A. Fox,et al.  Brain development over the first year of life: Relations between electroencephalographic frequency and coherence and cognitive and affective behaviors. , 1994 .

[121]  P. D. Eimas,et al.  Speech Perception in Infants , 1971, Science.

[122]  N. Fox,et al.  The relations between frontal brain electrical activity and cognitive development during infancy. , 1992, Child development.

[123]  A. Meltzoff,et al.  Early Imitation Within a Functional Framework: The Importance of Person Identity, Movement, and Development. , 1992, Infant behavior & development.

[124]  D. Kimura,et al.  Left-hemisphere control of oral and brachial movements and their relation to communication. , 1982, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[125]  D. Oller,et al.  Phrasing in prelinguistic vocalizations. , 1995, Developmental psychobiology.

[126]  Marcel Kinsbourne,et al.  Hemispheric disconnection and cerebral function , 1974 .

[127]  C. Darwin,et al.  The Expression of the Emotions in Man and Animals , 1872 .

[128]  P. A. Williamson,et al.  Asymmetric neural control systems in human self-regulation. , 1984, Psychological review.

[129]  C. Trevarthen Chapter II – Functional Organization of the Human Brain , 1980 .

[130]  Kurt W. Fischer,et al.  Dynamic development of coordination of components in brain and behavior: A framework for theory and research. , 1994 .

[131]  C. Trevarthen,et al.  Metacontrol of hemispheric function in human split-brain patients. , 1976, Journal of experimental psychology. Human perception and performance.

[132]  S. Trehub The perception of musical patterns by human infants: The provision of similar patterns by their parents. , 1990 .

[133]  Jordan Grafman,et al.  Handbook of Neuropsychology , 1991 .

[134]  G. Michel,et al.  Right-handedness: a consequence of infant supine head-orientation preference? , 1981, Science.