Neuronal subtypes and anatomic asymmetry: changes in neuronal number and cell-packing density

The combined volume of an asymmetric cytoarchitectonic area is smaller than that of symmetric homologs. Asymmetry reflects fewer numbers of neurons in the smaller of the two sides. In this study we examined two types of neurons to check whether lateral differences in neuronal numbers affect different types of neurons comparably in the neocortex of the rat. As with overall neuronal numbers, both parvalbumin-immunoreactive (mostly long projection) neurons, and vasoactive intestinal peptide-immunoreactive interneurons increase in number in the larger of the two sides. Moreover, the concentration of parvalbumin- but not vasoactive intestinal peptide-immunoreactive neurons also increases on the larger side. Thus, there may be qualitative as well as quantitative differences in the connectivity of the larger side of an asymmetric architectonic region.

[1]  N. Geschwind,et al.  Hemispheric differences in the brains of great apes. , 1975, Brain, behavior and evolution.

[2]  J A Wada,et al.  Cerebral hemispheric asymmetry in humans. Cortical speech zones in 100 adults and 100 infant brains. , 1975, Archives of neurology.

[3]  M. Diamond,et al.  Age-related morphologic differences in the rat cerebral cortex and hippocampus: Male-female; right-left , 1983, Experimental Neurology.

[4]  V. Denenberg.  Hemispheric laterality in animals and the effects of early experience , 1981, Behavioral and Brain Sciences.

[5]  A. Galaburda,et al.  Neocortical asymmetry and open-field behavior in the rat , 1984, Experimental Neurology.

[6]  A M Galaburda,et al.  La région de Broca: observations anatomiques faites un siècle après la mort de son découvreur. , 1980 .

[7]  N. Geschwind,et al.  Human Brain: Cytoarchitectonic Left-Right Asymmetries in the Temporal Speech Region , 1978 .

[8]  Marjorie LeMay,et al.  MORPHOLOGICAL CEREBRAL ASYMMETRIES OF MODERN MAN, FOSSIL MAN, AND NONHUMAN PRIMATE , 1976, Annals of the New York Academy of Sciences.

[9]  B. Pakkenberg,et al.  An efficient method for estimating the total number of neurons in rat brain cortex , 1990, Journal of Neuroscience Methods.

[10]  A. Galaburda,et al.  [Broca's region: anatomic remarks made a century after the death of its discoverer]. , 1980, Revue neurologique.

[11]  G. D. Rosen,et al.  Ontogenesis of neocortical asymmetry: A [3H]thymidine study , 1991, Neuroscience.

[12]  W. Krieg.  Connections of the cerebral cortex , 1963 .

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

[14]  C V Howard,et al.  The total number of neurons in the human neocortex unbiasedly estimated using optical disectors , 1990, Journal of microscopy.

[15]  Glenn D. Rosen,et al.  Brain volume estimation from serial section measurements: a comparison of methodologies , 1990, Journal of Neuroscience Methods.

[16]  N. Geschwind,et al.  Developmental dyslexia: Four consecutive patients with cortical anomalies , 1985, Annals of neurology.

[17]  Lutz Jäncke,et al.  Anatomical left‐right asymmetry of language‐related temporal cortex is different in left‐ and right‐handers , 1991, Annals of neurology.

[18]  M. LeMay,et al.  Human brain--morphologic differences in the hemispheres demonstrable by carotid arteriography. , 1972, The New England journal of medicine.

[19]  R. Sperry.  Lateral specialization in the surgically separated hemispheres. , 1974 .

[20]  J. van Pelt,et al.  Sex-difference and left-right asymmetries in the prefrontal cortex during postnatal development in the rat. , 1984, Brain research.

[21]  C. Heizmann,et al.  Calcium-binding protein parvalbumin as a neuronal marker , 1981, Nature.

[22]  W. Krieg.  Connections of the cerebral cortex. I. The albino rat. A. Topography of the cortical areas , 1946 .

[23]  K Zilles,et al.  Cerebral asymmetry: MR planimetry of the human planum temporale. , 1989, Journal of computer assisted tomography.

[24]  V. Braitenberg,et al.  Exceptions to bilateral symmetry in the epithalamus of lower vertebrates , 1970, The Journal of comparative neurology.

[25]  M. Kemali,et al.  The asymmetry of the habenular nuclei of female and male frogs in spring and in winter , 1990, Brain Research.

[26]  M W Mahowald,et al.  Asymmetry of the lateral (sylvian) fissures in man , 1976, Neurology.

[27]  F. Hochberg,et al.  Arteriographic correlates of handedness , 1975, Neurology.

[28]  Bryan Kolb,et al.  Asymmetry in the cerebral hemispheres of the rat, mouse, rabbit, and cat: The right hemisphere is larger , 1982, Experimental Neurology.

[29]  J. Juraska,et al.  Sex differences in neuron number in the binocular area of the rat visual cortex , 1992, The Journal of comparative neurology.

[30]  S. P. Springer,et al.  Left brain, right brain , 1981 .

[31]  M. Naeser,et al.  Computed tomographic scan cerebral asymmetries and morphologic brain asymmetries. Correlation in the same cases post mortem. , 1984, Archives of neurology.

[32]  J. Cheverud,et al.  Advanced computer graphics technology reveals cortical asymmetry in endocasts of rhesus monkeys. , 1986, Folia primatologica; international journal of primatology.

[33]  P. Rakić,et al.  Elimination of neurons from the rhesus monkey's lateral geniculate nucleus during development , 1988, The Journal of comparative neurology.

[34]  G. D. Rosen,et al.  Histological Asymmetry in the Primary Visual Cortex of the Rat: Implications for Mechanisms of Cerebral Asymmetry , 1986, Cortex.

[35]  S. F. Witelson,et al.  Left hemisphere specialization for language in the newborn. Neuroanatomical evidence of asymmetry. , 1973, Brain : a journal of neurology.

[36]  W. Krieg.  Connections of the cerebral cortex. I. The albino rat. B. Structure of the cortical areas , 1946, The Journal of comparative neurology.

[37]  N. Brecha,et al.  The morphology and distribution of peptide-containing neurons in the adult and developing visual cortex of the rat. II. Vasoactive intestinal polypeptide , 1982, Journal of neurocytology.

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

[39]  A. Peters,et al.  Vasoactive intestinal polypeptide-immunoreactive neurons in rat visual cortex , 1984, Neuroscience.

[40]  A. Galaburda,et al.  The effect of developmental neuropathology on neocortical asymmetry in New Zealand black mice. , 1989, The International journal of neuroscience.

[41]  A. Tzavaras,et al.  [Right-left asymmetry of the planum temporale; apropos of the anatomical study of 100 brains]. , 1972, Revue neurologique.

[42]  D. Kido,et al.  Asymmetries of the cerebral hemispheres on computed tomograms. , 1978, Journal of computer assisted tomography.

[43]  N. Brecha,et al.  The morphology and distribution of peptide-containing neurons in the adult and developing visual cortex of the rat. III. Cholecystokinin , 1982, Journal of neurocytology.

[44]  Glenna A. Dowling,et al.  Morphologic cerebral cortical asymmetry in male and female rats , 1981, Experimental Neurology.

[45]  A. Galaburda,et al.  Inferior parietal lobule. Divergent architectonic asymmetries in the human brain. , 1984, Archives of neurology.

[46]  J. Fahrenkrug,et al.  Vasoactive intestinal polypeptide , 1980, Trends in Neurosciences.

[47]  F. Nottebohm,et al.  Lateral asymmetries and testosterone‐induced changes in the gross morphology of the hypoglossal nucleus in adult canaries , 1991, The Journal of comparative neurology.

[48]  H J Gundersen,et al.  The efficiency of systematic sampling in stereology and its prediction * , 1987, Journal of microscopy.

[49]  M. Diamond,et al.  Morphological changes in the young, adult and aging rate cerebral cortex, hippocampus, and diencephalon. , 1975, Behavioral biology.

[50]  H. Katsumaru,et al.  GABAergic neurons containing the Ca2+-binding protein parvalbumin in the rat hippocampus and dentate gyrus , 1987, Brain Research.

[51]  A. Reiner,et al.  Habenular asymmetry and the central connections of the parietal eye of the lizard , 1981, The Journal of comparative neurology.

[52]  G. Yeni-Komshian,et al.  Anatomical study of cerebral asymmetry in the temporal lobe of humans, chimpanzees, and rhesus monkeys. , 1976, Science.

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

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