Topographic and laminar maturation of striate cortex in early postnatal marmoset monkeys, as revealed by neurofilament immunohistochemistry.

The maturation of pyramidal neurons in the primary visual cortex (V1) of marmoset monkeys was investigated using an antibody (SMI-32) to non-phosphorylated neurofilament protein (NNF). Analysis of animals aged between birth and postnatal day 91 (PD 91, which corresponds approximately to the peak of synaptogenesis in this species) revealed discrete changes in both the laminar and the areal distribution of NNF. At PD 0, the upper part of layer 6 contained darkly labelled neurons and associated neuropil, including axons. In this layer a centroperipheral gradient, with more labelled cells in the foveal representation, was apparent at PD 0. This topographic gradient gradually disappeared, and by PD 91 a similar density of labelled layer 6 cells was observed throughout V1. Labelled cells were not apparent in layer 3C until PD 7, and were not distributed according to a topographic gradient. Labelled cells were first observed in layer 3B(alpha) at PD 28, when they formed a centroperipheral gradient similar to that seen in layer 6. This gradient was still evident in an adult animal. These results demonstrate an inside-out profile of postnatal cortical development, with the topographic pattern of maturation of V1 mimicking the centroperipheral gradient of maturation in the retina.

[1]  Synaptic development in macaque monkey retina and its implications for other developmental sequences. , 1996 .

[2]  A. Cowey,et al.  Fibre organization of the monkey's optic tract: I. Segregation of functionally distinct optic axons , 1990, The Journal of comparative neurology.

[3]  R. Lasek The dynamic ordering of neuronal cytoskeletons. , 1981, Neurosciences Research Program bulletin.

[4]  D. Munoz,et al.  SMI-32 immunoreactivity in human striate cortex during postnatal development. , 1991, Brain research. Developmental brain research.

[5]  L. Sternberger,et al.  Varying degrees of phosphorylation determine microheterogeneity of the heavy neurofilament polypeptide (Nf-H) , 1987, Journal of Neuroimmunology.

[6]  T. Nag,et al.  Calbindin and parvalbumin immunoreactivity in the developing and adult human retina. , 1996, Brain research. Developmental brain research.

[7]  J. Stone,et al.  The area centralis of the retina in the cat and other mammals: Focal point for function and development of the visual system , 1984, Neuroscience.

[8]  S. Schein,et al.  Mapping of retinal and geniculate neurons onto striate cortex of macaque , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  V. Caviness,et al.  Sequence of Neuron Origin and Neocortical Laminar Fate: Relation to Cell Cycle of Origin in the Developing Murine Cerebral Wall , 1999, The Journal of Neuroscience.

[10]  I. Kovács,et al.  Late maturation of visual spatial integration in humans. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[11]  M. Cynader,et al.  Differential expression of neurofilament protein in the visual system of the vervet monkey , 1996, Brain Research.

[12]  J. Morrison,et al.  Monoclonal antibody to neurofilament protein (SMI‐32) labels a subpopulation of pyramidal neurons in the human and monkey neocortex , 1989, The Journal of comparative neurology.

[13]  J. Hearn The Common Marmoset (Callithrix jacchus) , 1983 .

[14]  J R Wolff,et al.  Pre‐ and postnatal development of the primary visual cortex of the common marmoset. II. Formation, remodelling, and elimination of synapses as overlapping processes , 1993, The Journal of comparative neurology.

[15]  V. Casagrande,et al.  Development of primate retinogeniculate axon arbors , 1988, Visual Neuroscience.

[16]  S. Rumpel,et al.  Silent synapses in the immature visual cortex: layer-specific developmental regulation. , 2004, Journal of neurophysiology.

[17]  Daniel C. Kiper,et al.  Development of contrast sensitivity across the visual field in macaque monkeys (Macaca nemestrina) , 1996, Vision Research.

[18]  M. Rosa,et al.  Neurofilament protein expression in the geniculostriate pathway of a New World monkey (Callithrix jacchus) , 2003, Experimental Brain Research.

[19]  M. Blue,et al.  The formation and maturation of synapses in the visual cortex of the rat. I. Qualitative analysis , 1983, Journal of neurocytology.

[20]  Michel Imbert,et al.  Vascularization in the primate visual cortex during development. , 2002, Cerebral cortex.

[21]  C. Blakemore,et al.  Development of contrast sensitivity and temporal-frequency selectivity in primate lateral geniculate nucleus , 1997, Experimental Brain Research.

[22]  I. Fujita,et al.  Distribution of α‐amino‐3‐hydroxy‐5‐methyl‐4‐isoxazolepropionate‐type glutamate receptor subunits (GluR2/3) along the ventral visual pathway in the monkey , 2003, The Journal of comparative neurology.

[23]  Vivien A. Casagrande,et al.  The Afferent, Intrinsic, and Efferent Connections of Primary Visual Cortex in Primates , 1994 .

[24]  W. Burke,et al.  Laminar differences in plasticity in area 17 following retinal lesions in kittens or adult cats , 2003, The European journal of neuroscience.

[25]  Lasek Rj,et al.  The dynamic ordering of neuronal cytoskeletons. , 1981 .

[26]  A. Matus Neurofilament protein phosphorylation - where, when and why , 1988, Trends in Neurosciences.

[27]  M P Stryker,et al.  Emergence of ocular dominance columns in cat visual cortex by 2 weeks of age , 2001, The Journal of comparative neurology.

[28]  P. Rakić,et al.  Early developmental events: cell lineages, acquisition of neuronal positions, and areal and laminar development. , 1982, Neurosciences Research Program bulletin.

[29]  P. Rakić,et al.  Cytogenesis in the monkey retina , 1991, The Journal of comparative neurology.

[30]  P. Rakic Evolving concepts of cortical radial and areal specification. , 2002, Progress in brain research.

[31]  C. Blakemore,et al.  Organization and post‐natal development of the monkey's lateral geniculate nucleus. , 1986, The Journal of physiology.

[32]  J. Tigges,et al.  Subcortical projections, cortical associations, and some intrinsic interlaminar connections of the striate cortex in the squirrel monkey (Saimiri) , 1970, The Journal of comparative neurology.

[33]  Leslie G. Ungerleider,et al.  Neurofilament protein is differentially distributed in subpopulations of corticocortical projection neurons in the macaque monkey visual pathways , 1996, The Journal of comparative neurology.

[34]  P. Rakić,et al.  Early divergence of magnocellular and parvocellular functional subsystems in the embryonic primate visual system. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[35]  W. B. Spatz The retino-geniculo-cortical pathway in Callithrix. II. The geniculo-cortical projection , 1979, Experimental Brain Research.

[36]  W. B. Spatz,et al.  Morphology and connections of neurons in area 17 projecting to the extrastriate areas mt and 19DM and to the superior colliculus in the monkey Callithrix jacchus , 1995, The Journal of comparative neurology.

[37]  P. Pasik,et al.  Early postnatal development of the monkey visual system. I. Growth of the lateral geniculate nucleus and striate cortex. , 1985, Brain research.

[38]  J. Morrison,et al.  Neurofilament protein defines regional patterns of cortical organization in the macaque monkey visual system: A quantitative immunohistochemical analysis , 1995, The Journal of comparative neurology.

[39]  M. Cynader,et al.  The correlation between cortical neuron maturation and neurofilament phosphorylation: a developmental study of phosphorylated 200 kDa neurofilament protein in cat visual cortex. , 1994, Brain research. Developmental brain research.

[40]  L. Sternberger,et al.  Monoclonal antibodies distinguish phosphorylated and nonphosphorylated forms of neurofilaments in situ. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[41]  P. Rakić,et al.  Changes of synaptic density in the primary visual cortex of the macaque monkey from fetal to adult stage , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[42]  M. Black,et al.  Phosphorylation of neurofilament proteins in intact neurons: demonstration of phosphorylation in cell bodies and axons , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[43]  Aaron R. Seitz,et al.  Laminar development of receptive fields, maps and columns in visual cortex: the coordinating role of the subplate. , 2003, Cerebral cortex.

[44]  N. Hasgekar,et al.  Developmental expression of neurofilament and glial filament proteins in rat cerebellum. , 1994, The International journal of developmental biology.

[45]  H. Kennedy,et al.  Cytochrome oxidase activity in the striate cortex and lateral geniculate nucleus of the newborn and adult macaque monkey , 2004, Experimental Brain Research.

[46]  P. Rakic DNA Synthesis and Cell Division in the Adult Primate Brain a , 1985, Annals of the New York Academy of Sciences.

[47]  J. Lund,et al.  The origin of efferent pathways from the primary visual cortex, area 17, of the macaque monkey as shown by retrograde transport of horseradish peroxidase , 1975, The Journal of comparative neurology.

[48]  A. Chaudhuri,et al.  Developmental profiles of SMI-32 immunoreactivity in monkey striate cortex. , 2000, Brain research. Developmental brain research.

[49]  M. Blue,et al.  The formation and maturation of synapses in the visual cortex of the rat. II. Quantitative analysis , 1983, Journal of neurocytology.

[50]  W. B. Spatz,et al.  Distribution of cytochrome oxidase in layers IV and V of the striate cortex in neonate monkeys , 2004, Experimental Brain Research.

[51]  J R Wolff,et al.  Pre‐ and postnatal development of the primary visual cortex of the common marmoset. I. A changing space for synaptogenesis , 1993, The Journal of comparative neurology.

[52]  P. Rakić Neurons in Rhesus Monkey Visual Cortex: Systematic Relation between Time of Origin and Eventual Disposition , 1974, Science.

[53]  M G Rosa,et al.  Visuotopic organisation of striate cortex in the marmoset monkey (Callithrix jacchus) , 1996, The Journal of comparative neurology.

[54]  L. Arckens,et al.  Neurofilament protein: A selective marker for the architectonic parcellation of the visual cortex in adult cat brain , 2001, The Journal of comparative neurology.

[55]  J. Lund,et al.  Development of neurons in the visual cortex (area 17) of the monkey (Macaca nemestrina): A Golgi study from fetal day 127 to postnatal maturity , 1977, The Journal of comparative neurology.

[56]  L. Garey,et al.  Quantitative changes in morphological parameters in the developing visual cortex of the marmoset monkey. , 1986, Brain research.

[57]  W. B. Spatz Loss of ocular dominance columns with maturity in the monkey, Callithrix jacchus , 1989, Brain Research.

[58]  A. Mikami,et al.  Development of the ability to detect visual motion in infant macaque monkeys. , 1992, Developmental psychobiology.

[59]  M. Wong-Riley Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry , 1979, Brain Research.

[60]  M. Kirby,et al.  Early dendritic outgrowth of primate retinal ganglion cells , 1991, Visual Neuroscience.

[61]  Synaptic development in macaque monkey retina and its implications for other developmental sequences. , 1996, Perspectives on developmental neurobiology.

[62]  A. Hendrickson,et al.  Development of synapses in macaque monkey striate cortex , 1992, Visual Neuroscience.