Postnatal development of interhemispheric asymmetry in the cytoarchitecture of human area 4

Abstract The postnatal development of interhemispheric asymmetry was analyzed in the primary motor cortex (area 4) of 20 human brains with quantitative cytoarchitectonic techniques. The volume fraction of cortical tissue occupied by cell bodies (grey level index) was determined by automated image analysis. In children as well as in adults, the volume fraction of cell bodies averaged over all cortical layers was greater on the right than on the left. Thus, the space between cell bodies, i.e. the volume fraction of neuropil containing axons, dendrites and synapses, was greater in the left than in the right primary motor cortex. At the level of single layers, however, interhemispheric asymmetry of the neuropil volume fraction differed between age groups. The supragranular layers were significantly less asymmetrical in children than in adults, whereas the infragranular layers showed a similar degree of asymmetry in both age groups. Thus, the postnatal development of the architectonic asymmetry in the supra- and infragranular layers of area 4 follows the same sequence of maturation as found during neuronal migration, i.e. an inside-to-outside gradient. Comparing the layer-specific developmental pattern with available functional data, it was found that the structural maturation of interhemispheric asymmetry in the supragranular layers correlates with the development of hand preference.

[1]  L Jäncke,et al.  The Hand Performance Test with a Modified Time Limit Instruction Enables the Examination of Hand Performance Asymmetries in Adults , 1996, Perceptual and motor skills.

[2]  G. D. Rosen,et al.  Interhemispheric connections differ between symmetrical and asymmetrical brain regions , 1989, Neuroscience.

[3]  J C Mazziotta,et al.  Somatotopic mapping of the primary motor cortex in humans: activation studies with cerebral blood flow and positron emission tomography. , 1991, Journal of neurophysiology.

[4]  G. I. Poliakov Some results of research into the development of the neuronal structure of the cortical ends of the analyzers in man , 1961, The Journal of comparative neurology.

[5]  P. Yakovlev,et al.  The myelogenetic cycles of regional maturation of the brain , 1967 .

[6]  François Michel,et al.  Hand Performance of French Children on a Finger-Tapping Test in Relation to Handedness, Sex, and Age , 1993, Perceptual and motor skills.

[7]  F. James Rohlf,et al.  Biometry: The Principles and Practice of Statistics in Biological Research , 1969 .

[8]  D Kilshaw,et al.  Right- and left-hand skill I: Effects of age, sex and hand preference showing superior skill in left-handers. , 1983, British journal of psychology.

[9]  M Annett,et al.  The growth of manual preference and speed. , 1970, British journal of psychology.

[10]  J. Kleim,et al.  Synaptogenesis and FOS Expression in the Motor Cortex of the Adult Rat after Motor Skill Learning , 1996, The Journal of Neuroscience.

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

[12]  R. Adams,et al.  Principles of Neurology , 1996 .

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

[14]  G. Schlaug,et al.  Asymmetry of the planum parietale. , 1994, Neuroreport.

[15]  Karl J. Friston,et al.  Regional cerebral blood flow during voluntary arm and hand movements in human subjects. , 1991, Journal of neurophysiology.

[16]  W. Welker,et al.  Why Does Cerebral Cortex Fissure and Fold ? A Review of Determinants of Gyri and Sulci , 2022 .

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

[18]  S P Wise,et al.  Size, laminar and columnar distribution of efferent cells in the sensory‐motor cortex of monkeys , 1977, The Journal of comparative neurology.

[19]  V S Caviness,et al.  Cerebral structural abnormalities in obsessive-compulsive disorder. A quantitative morphometric magnetic resonance imaging study. , 1996, Archives of general psychiatry.

[20]  M. Merzenich,et al.  Neurophysiological correlates of hand preference in primary motor cortex of adult squirrel monkeys , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[21]  K. Brodmann Vergleichende Lokalisationslehre der Großhirnrinde : in ihren Prinzipien dargestellt auf Grund des Zellenbaues , 1985 .

[22]  V. Hömberg,et al.  Development of speed of repetitive movements in children is determined by structural changes in corticospinal efferents , 1992, Neuroscience Letters.

[23]  A. P. Georgopoulos,et al.  Functional magnetic resonance imaging of motor cortex: hemispheric asymmetry and handedness. , 1993, Science.

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

[25]  P. Roland,et al.  Fields in human motor areas involved in preparation for reaching, actual reaching, and visuomotor learning: a positron emission tomography study , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[26]  Susan Hart,et al.  Hand Preference Consistency and Fine Motor Performance in Young Children , 1993, Cortex.

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

[28]  A. Schleicher,et al.  The ontogeny of human gyrification. , 1995, Cerebral cortex.

[29]  W. Greenough,et al.  Learning causes synaptogenesis, whereas motor activity causes angiogenesis, in cerebellar cortex of adult rats. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[30]  G. Schlaug,et al.  In vivo evidence of structural brain asymmetry in musicians , 1995, Science.

[31]  K Zilles,et al.  A quantitative approach to cytoarchitectonics: Analysis of structural inhomogeneities in nervous tissue using an image analyser , 1990, Journal of microscopy.

[32]  Leslie G. Ungerleider,et al.  Functional MRI evidence for adult motor cortex plasticity during motor skill learning , 1995, Nature.

[33]  A. Schleicher,et al.  Motor cortex and hand motor skills: Structural compliance in the human brain , 1997, Human brain mapping.

[34]  M. Marín‐Padilla,et al.  Prenatal and early postnatal ontogenesis of the human motor cortex: a golgi study. I. The sequential development of the cortical layers. , 1970, Brain research.

[35]  A. Schleicher,et al.  Structural Asymmetries in the Human Forebrain and the Forebrain of Non-human Primates and Rats , 1996, Neuroscience & Biobehavioral Reviews.

[36]  A. Davis,et al.  Handedness as a Function of Twinning, Age and Sex , 1994, Cortex.

[37]  S. F. Witelson,et al.  Sylvian fissure morphology and asymmetry in men and women: Bilateral differences in relation to handedness in men , 1992, The Journal of comparative neurology.

[38]  M. Duyme,et al.  Is a dot-filling group test a good tool for assessing manual performance in children? , 1993, Neuropsychologia.

[39]  N. Geschwind,et al.  Human Brain: Left-Right Asymmetries in Temporal Speech Region , 1968, Science.

[40]  David M. Brody TWIN RESEMBLANCES IN MECHANICAL ABILITY, WITH REFERENCE TO THE EFFECTS OF PRACTICE ON PERFORMANCE1 , 1937 .

[41]  J. Donoghue,et al.  Shared neural substrates controlling hand movements in human motor cortex. , 1995, Science.

[42]  Glenn D. Rosen,et al.  Planum temporale asymmetry, reappraisal since Geschwind and Levitsky , 1987, Neuropsychologia.

[43]  W. Greenough,et al.  Glial hypertrophy is associated with synaptogenesis following motor‐skill learning, but not with angiogenesis following exercise , 1994, Glia.

[44]  A. Schleicher,et al.  Asymmetry in the Human Motor Cortex and Handedness , 1996, NeuroImage.

[45]  F. Gallyas Silver staining of myelin by means of physical development. , 1979, Neurological research.

[46]  L. White,et al.  Structure of the human sensorimotor system. II: Lateral symmetry. , 1997, Cerebral cortex.

[47]  W. Greenough,et al.  Exercise and the Brain: Angiogenesis in the Adult Rat Cerebellum after Vigorous Physical Activity and Motor Skill Learning , 1992, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[48]  B. Rockstroh,et al.  Increased Cortical Representation of the Fingers of the Left Hand in String Players , 1995, Science.

[49]  L. White,et al.  Cerebral asymmetry and handedness , 1994, Nature.

[50]  M. Mishkin,et al.  Effects of hemispheric side of injury, age at injury, and presence of seizure disorder on functional ear and hand asymmetries in hemiplegic children , 1996, Neuropsychologia.

[51]  G Schlaug,et al.  Brain (A) symmetry in monozygotic twins. , 1995, Cerebral cortex.

[52]  Samuil Michailovič Blinkov,et al.  Das Zentralnervensystem in Zahlen und Tabellen , 1968 .

[53]  Katrin Amunts,et al.  A method of observer-independent cytoarchitectonic mapping of the human cortex , 1995 .

[54]  N. Marlow,et al.  HANDEDNESS IN VERY‐LOW‐BIRTHWEIGHT (VLBW) CHILDREN AT 12 YEARS OF AGE: RELATION TO PERINATAL AND OUTCOME VARIABLES , 1996, Developmental medicine and child neurology.

[55]  M Annett,et al.  Handedness in families , 1973, Annals of human genetics.

[56]  F. Gilles,et al.  Left-right asymmetries of the temporal speech areas of the human fetus. , 1977, Archives of neurology.

[57]  M Marín-Padilla,et al.  Ontogenesis of the pyramidal cell of the mammalian neocortex and developmental cytoarchitectonics: A unifying theory , 1992, The Journal of comparative neurology.

[58]  P. Rakić Development and modifiability of the cerebral cortex. , 1982, Neurosciences Research Program bulletin.

[59]  J. Cheverud,et al.  Cortical asymmetries in frontal lobes of Rhesus monkeys (Macaca mulatta) , 1990, Brain Research.