Prenatal development of the visual system in rhesus monkey.

Autoradiographic evidence from juvenile rhesus monkeys that had been exposed to a pulse of [3H]thymidine at different embryonic (E) and early postnatal (P) days indicates that all neurons which compose the visual system of this primate have been generated two months before birth. The first retinal ganglion cells (RGC) are generated around E30 preceding by a few days the onset of genesis of neurones destined for the dorsal lateral geniculate body (LGd) and superior colliculus (SC) both of which begin at E36. Production of neurons destined for the primary visual cortex (area 17) begins at approximately E43 and ends by E102. Neurons destined for layer IV, the major target of axons from the LGd, are generated between E70 and E85. The prenatal development of visual connections was studied by the autoradiographic method of anterograde axoplasmic transport in foetuses killed 14 days after unilateral eye injection of a mixture of [3H]proline and [3H]fucose. Initially, in the LGd and in the SC projections from both eyes overlap. Segregation of the axons and/or terminals from the two eyes occurs in the LGd and SC during the middle period of gestation. Transneuronal transport of tritium shows that although LGd axons form the optic radiation before E78, these fibres do not yet enter the developing cortical plate at this foetal age. During the second half of gestation, geniculocortical axons carrying input from each eye invade the cortex but are not yet segregated into ocular dominance columns. Rather, grains are distributed uniformly over the entire layer IV at E124. Three weeks before birth, at E144, segregation of afferents into sublayers IVA and IVC is apparent, and the first hint of ocular dominance columns is displayed by slight differences in grain counts in alternating areas of layer IV. These results show that all neurons in the primate visual system have been generated, reached their final positions and formed their basic connections subserving ocular dominance before birth, i.e. before visual experience. In the SC and LGD, monocular segregation is well established during the middle period of gestation, whereas in the cortex it has begun, but is not fully developed at birth.

[1]  H. P. Jensen.  Department of Obstetrics , 1942 .

[2]  W. Möllendorff,et al.  Handbuch der Mikroskopischen Anatomie des Menschen , 1958 .

[3]  W M Cowan,et al.  Transneuronal cell degeneration in the lateral geniculate nucleus of the macaque monkey. , 1960, Journal of anatomy.

[4]  R. Sidman,et al.  Autoradiographic Study of Cell Migration during Histogenesis of Cerebral Cortex in the Mouse , 1961, Nature.

[5]  D. Hubel,et al.  SINGLE-CELL RESPONSES IN STRIATE CORTEX OF KITTENS DEPRIVED OF VISION IN ONE EYE. , 1963, Journal of neurophysiology.

[6]  Leblond Cp.  CLASSIFICATION OF CELL POPULATIONS ON THE BASIS OF THEIR PROLIFERATIVE BEHAVIOR. , 1964 .

[7]  Angevine Jb.  Time of neuron origin in the hippocampal region. An autoradiographic study in the mouse. , 1965 .

[8]  A. W. Rogers,et al.  The migration of neuroblasts in the developing cerebral cortex. , 1965, Journal of anatomy.

[9]  D. Hubel,et al.  Receptive fields and functional architecture of monkey striate cortex , 1968, The Journal of physiology.

[10]  C. D'amato,et al.  Cell migrations to the isocortex in the rat , 1968, The Anatomical record.

[11]  M. Shimada,et al.  Cell proliferation, migration and differentiation in the cerebral cortex of the golden hamster , 1970, The Journal of comparative neurology.

[12]  R. Sidman.  Autoradiographic Methods and Principles for Study of the Nervous System with Thymidine-H3 , 1970 .

[13]  J. B. Angevine.  Time of neuron origin in the diencephalon of the mouse. An autoradiographic study , 1970, The Journal of comparative neurology.

[14]  R L Sidman,et al.  Histogenesis of cortical layers in human cerebellum, particularly the lamina dissecans , 1970, The Journal of comparative neurology.

[15]  B. Grafstein.  Transneuronal Transfer of Radioactivity in the Central Nervous System , 1971, Science.

[16]  A. Hendrickson,et al.  The autoradiographic demonstration of axonal connections in the central nervous system. , 1972, Brain research.

[17]  P. Rakić.  Mode of cell migration to the superficial layers of fetal monkey neocortex , 1972, The Journal of comparative neurology.

[18]  D. Hubel,et al.  Laminar and columnar distribution of geniculo‐cortical fibers in the macaque monkey , 1972, The Journal of comparative neurology.

[19]  P. Rakić,et al.  Neuronal migration, with special reference to developing human brain: a review. , 1973, Brain research.

[20]  D H Hubel,et al.  Autoradiographic demonstration of ocular-dominance columns in the monkey striate cortex by means of transneuronal transport. , 1974, Brain research.

[21]  P. Rakić,et al.  CLEARANCE RATE OF EXOGENOUS 3H‐THYMIDINE FROM THE PLASMA OF PREGNANT RHESUS MONKEYS , 1974, Cell and tissue kinetics.

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

[23]  D. Hubel,et al.  Mode of termination of retinotectal fibers in macaque monkey: An autoradiographic study , 1975, Brain Research.

[24]  H. B. Barlow,et al.  Visual experience and cortical development , 1975, Nature.

[25]  P. Rakić,et al.  Timing of major ontogenetic events in the visual cortex of the rhesus monkey. , 1975, UCLA forum in medical sciences.

[26]  P. Rakic,et al.  Cell migration and neuronal ectopias in the brain. , 1975, Birth defects original article series.

[27]  M. Sanders.  Handbook of Sensory Physiology , 1975 .

[28]  R. Lund,et al.  Prenatal development of central optic pathways in albino rats , 1976, The Journal of comparative neurology.

[29]  P. Rakić,et al.  Differentiation of Purkinje cells and their relationship to other components of developing cerebellar cortex in man , 1976, The Journal of comparative neurology.

[30]  P. Rakic.  Prenatal genesis of connections subserving ocular dominance in the rhesus monkey , 1976, Nature.

[31]  P. Rakić.  Differences in the Time of Origin and in Eventual Distribution of Neurons in Areas 17 and 18 of Visual Cortex in Rhesus Monkey , 1976 .

[32]  E. G. Jones,et al.  The organization and postnatal development of the commissural projection of the rat somatic sensory cortex , 1976, The Journal of comparative neurology.

[33]  P. Rakic.  Synaptic specificity in the cerebellar cortex: study of anomalous circuits induced by single gene mutations in mice. , 1976, Cold Spring Harbor symposia on quantitative biology.