Changes of synaptic density in the primary visual cortex of the macaque monkey from fetal to adult stage

The kinetics of synaptogenesis in the primary visual cortex (Brodmann's area 17) were analyzed by electron microscopy in 33 rhesus monkeys, ranging in age from the 50th embryonic day (E50) to 20 years. A series of overlapping electron micrographs (vertical probes) were examined at each age on sections of the upper bank of the calcarine fissure. Synaptic contacts were first observed in the E50 specimen in the subplate and marginal zone (prospective layer I). In the cortical plate itself, synapses appear between E65 and E89 starting in the prospective layer VI. By E112, after all cortical neurons have assumed their laminar positions, synapses situated predominantly on dendritic shafts were present at a low density throughout the full thickness of the cortical plate. Thereafter, synapses accumulate more rapidly on dendritic spines and by E144 an equal number of contacts are found on both spines and shafts. The density of synapses continues to increase exponentially in all layers and reaches the mean maximum density of about 90 synapses per 100 microns 3 of neuropil by the third postnatal month. During the next 2 postnatal years the density of synaptic contacts decreases only slightly to a mean of 80/100 microns 3 of neuropil. Around the time of puberty, however, synaptic density decreases more rapidly to reach the adult level of about 40–50/100 microns 3 of neuropil. The 40% decrease in the density of synaptic contacts occurring between 2.7 and 5 years represents a loss of about 5000 synapses per second in the primary visual cortex of the two hemispheres, due primarily to the loss of asymmetric synapses situated on dendritic spines. The transient phase of high density of synaptic contacts located on dendrospines is shorter in thalamo-recipient layer IV than in either supra- or intragranular layers and is completed within the first postnatal year. It ends earlier in sublayer IVC than in layers IVAB and II-III, for example, reflecting biochemical and functional maturation of the different visual subsystems.

[1]  F E Bloom,et al.  The formation of synaptic junctions in developing rat brain: a quantitative electron microscopic study. , 1967, Brain research.

[2]  P. Rakić,et al.  Development of the corpus callosum and cavum septi in man , 1968, The Journal of comparative neurology.

[3]  R. Coupland Determining Sizes and Distribution of Sizes of Spherical Bodies such as Chromaffin Granules in Tissue Sections , 1968, Nature.

[4]  H. R. Catchpole,et al.  A Handbook of Living Primates , 1968, The Yale Journal of Biology and Medicine.

[5]  M. Colonnier Synaptic patterns on different cell types in the different laminae of the cat visual cortex. An electron microscope study. , 1968, Brain research.

[6]  J. Napier,et al.  A Handbook of Living Primates , 1969 .

[7]  V. Tennyson The Fine Structure of the Nervous System. , 1970 .

[8]  M. Carpenter The Fine Structure of the Nervous System , 1970, Neurology.

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

[10]  P. Rakić Kinetics of proliferation and latency between final cell division and onset of differentiation of cerebellar stellate and basket neurons , 1973, The Journal of comparative neurology.

[11]  J. Lund Organization of neurons in the visual cortex, area 17, of the monkey (Macaca mulatta) , 1973, The Journal of comparative neurology.

[12]  B. Cragg,et al.  Estimation of the number of synapses in a volume of nervous tissue from counts in thin sections by electron microscopy , 1974, Journal of neurocytology.

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

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

[15]  B. Cragg,et al.  The development of synapses in the visual system of the cat , 1975, The Journal of comparative neurology.

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

[17]  C. Gilbert,et al.  Laminar patterns of geniculocortical projection in the cat , 1976, Brain Research.

[18]  P. Rakić,et al.  Genesis of the dorsal lateral geniculate nucleus in the rhesus monkey: Site and time of origin, kinetics of proliferation, routes of migration and pattern of distribution of neurons , 1977, The Journal of comparative neurology.

[19]  P. Rakić Prenatal development of the visual system in rhesus monkey. , 1977, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[20]  T. Wiesel,et al.  Functional architecture of macaque monkey visual cortex , 1977 .

[21]  P. Rakic,et al.  Neuronal migration and contact guidance in the primate telencephalon. , 1978, Postgraduate medical journal.

[22]  C. Blakemore,et al.  The physiological effects of monocular deprivation and their reversal in the monkey's visual cortex. , 1978, The Journal of physiology.

[23]  J. Lund,et al.  A quantitative investigation of spine and dendrite development of neurons in visual cortex (area 17) of Macaca nemestrina monkeys , 1979, The Journal of comparative neurology.

[24]  T M Mayhew,et al.  Stereological approach to the study of synapse morphometry with particular regard to estimating number in a volume and on a surface , 1979, Journal of neurocytology.

[25]  P. Huttenlocher Synaptic density in human frontal cortex - developmental changes and effects of aging. , 1979, Brain research.

[26]  D. Hubel,et al.  The development of ocular dominance columns in normal and visually deprived monkeys , 1980, The Journal of comparative neurology.

[27]  C. Blakemore,et al.  Recovery from monocular deprivation in the monkey. I. Reversal of physiological effects in the visual cortex , 1981, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[28]  P. Rakić,et al.  Neurogenetic gradients in the superior and inferior colliculi of the rhesus monkey , 1981, The Journal of comparative neurology.

[29]  H. Loos,et al.  Synaptogenesis in human visual cortex — evidence for synapse elimination during normal development , 1982, Neuroscience Letters.

[30]  P S Goldman-Rakic,et al.  Postnatal development of monoamine content and synthesis in the cerebral cortex of rhesus monkeys. , 1982, Brain research.

[31]  M. Colonnier,et al.  Postnatal changes in the number of neurons and synapses in the visual cortex (area 17) of the macaque monkey: A stereological analysis in normal and monocularly deprived animals , 1982, The Journal of comparative neurology.

[32]  The first few weeks in monkey's visual cortex , 1983, Behavioural Brain Research.

[33]  J. Lund,et al.  Developmental changes in the relationship between type 2 synapses and spiny neurons in the monkey visual cortex , 1983, The Journal of comparative neurology.

[34]  P. Rakić,et al.  Gradients of cellular maturation and synaptogenesis in the superior colliculus of the fetal rhesus monkey , 1983, The Journal of comparative neurology.

[35]  D. Winfield The postnatal development of synapses in the different laminae of the visual cortex in the normal kitten and in kittens with eyelid suture. , 1983, Brain research.

[36]  John H. R. Maunsell,et al.  The visual field representation in striate cortex of the macaque monkey: Asymmetries, anisotropies, and individual variability , 1984, Vision Research.

[37]  C. Toran-Allerand On the genesis of sexual differentiation of the general nervous system: morphogenetic consequences of steroidal exposure and possible role of alpha-fetoprotein. , 1984, Progress in brain research.

[38]  S. Foote,et al.  Postnatal development of laminar innervation patterns by monoaminergic fibers in monkey (Macaca fascicularis) primary visual cortex , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[39]  Toran-Allerand Cd On the genesis of sexual differentiation of the general nervous system: morphogenetic consequences of steroidal exposure and possible role of alpha-fetoprotein. , 1984 .

[40]  G. Blasdel,et al.  Intrinsic connections of macaque striate cortex: afferent and efferent connections of lamina 4C , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[41]  M. Colonnier,et al.  An empirical assessment of stereological formulae applied to the counting of synaptic disks in the cerebral cortex , 1985, The Journal of comparative neurology.

[42]  R G Boothe,et al.  Postnatal development of vision in human and nonhuman primates. , 1985, Annual review of neuroscience.

[43]  P. Rakić,et al.  Development of the rhesus monkey retina. I. Emergence of the inner plexiform layer and its synapses , 1985, The Journal of comparative neurology.

[44]  E. Jones,et al.  Neurotransmitters in the cerebral cortex. , 1986, Journal of neurosurgery.

[45]  E. Smith,et al.  Multiple sensitive periods in the development of the primate visual system. , 1986, Science.

[46]  J. Gouzé,et al.  Effect of activity on the selective stabilization of the motor innervation of fast muscle posterior latissimus dorsi from chick embryo , 1986, International Journal of Developmental Neuroscience.

[47]  P. Goldman-Rakic,et al.  Concurrent overproduction of synapses in diverse regions of the primate cerebral cortex. , 1986, Science.

[48]  P. Rakić,et al.  Development of the rhesus monkey retina: II. A three‐dimensional analysis of the sequences o synaptic combinations in the inner plexiform layer , 1987, The Journal of comparative neurology.

[49]  A. Matsumoto,et al.  Gonadal Steroid Control of Synaptogenesis in the Neuroendocrine Brain , 1987 .

[50]  P. Huttenlocher,et al.  The development of synapses in striate cortex of man. , 1987, Human neurobiology.

[51]  A. Peters Number of Neurons and Synapses in Primary Visual Cortex , 1987 .

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

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

[54]  D. Purves Body and Brain: A Trophic Theory of Neural Connections , 1988 .

[55]  P. Rakić,et al.  Multiple types of neuropeptide Y‐containing neurons in primate neocortex , 1989, The Journal of comparative neurology.

[56]  J. Tigges,et al.  Effects of aging on the neurons within area 17 of rhesus monkey cerebral cortex , 1989, The Anatomical record.

[57]  D. Price,et al.  Age-related changes in multiple neurotransmitter systems in the monkey brain , 1989, Neurobiology of Aging.

[58]  P. Rakić,et al.  Synaptogenesis in visual cortex of normal and preterm monkeys: evidence for intrinsic regulation of synaptic overproduction. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[59]  P. Rakić,et al.  Axon overproduction and elimination in the corpus callosum of the developing rhesus monkey , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[60]  E. Callaway,et al.  Emergence and refinement of clustered horizontal connections in cat striate cortex , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[62]  G. Rager,et al.  Synaptogenesis in the primary visual cortex of the tree shrew (Tupaia belangeri) , 1991, The Journal of comparative neurology.

[63]  J. Lund,et al.  Postnatal development of thalamic recipient neurons in the monkey striate cortex: Comparison of spine acquisition and dendritic growth of layer 4C alpha and beta spiny stellate neurons , 1991, The Journal of comparative neurology.

[64]  J. Lund,et al.  Postnatal development of thalamic recipient neurons in the monkey striate cortex: Somatic inhibitory synapse acquisition by spiny stellate neurons of layer 4C , 1991, The Journal of comparative neurology.

[65]  J. Lund,et al.  Postnatal development of thalamic recipient neurons in the monkey striate cortex: Influence of afferent driving on spine acquisition and dendritic growth of layer 4c spiny stellate neurons , 1991, The Journal of comparative neurology.

[66]  W. Singer,et al.  Selection of intrinsic horizontal connections in the visual cortex by correlated neuronal activity. , 1992, Science.

[67]  N. Daw,et al.  Critical period for monocular deprivation in the cat visual cortex. , 1992, Journal of neurophysiology.