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Development of synapses in macaque monkey striate cortex

Published online by Cambridge University Press:  02 June 2009

B. S. Zielinski
Affiliation:
Department of Biological Sciences, University of Windsor, Windsor, Ontario, CanadaN9B 3P4
A. E. Hendrickson
Affiliation:
Departments of Biological Structure and Ophthalmology, University of Washington, Seattle

Abstract

A quantitative electron-microscopic (EM) analysis of the development of synaptic density (number of synapses/100 μm neuropil) has been done in primary visual cortex (striate, area 17) of the Old World monkey Macaca nemesthna. A comparative EM morphological study of developing synaptic contacts also was done in the same tissue. We find that a few immature synaptic contacts are present at fetal (F) 75 days either in the marginal zone, which becomes layer 1, or in the deepest portion of the cortical plate, the future layer 6. At F90–140 days synaptic contacts are found throughout the cortical plate, but their density remains higher in lower cortical layers. By F140 days synaptic density averaged for all layers (10.9) is three times higher than at F90 days. Just before and after birth, synaptic density rises very rapidly to peak at postnatal (P)12 weeks (63) and then declines slowly to reach adult values (37.7) between 2–6 years. This pattern was further tested by comparing synaptic density in layer 2 which contains the last cells generated in the striate cortex to that in layer 6 which contains the first cells generated in the striate cortex. Layer 6 contained the first synapses, and had a higher density up to F140 days (an “inside-to-outside” distribution). Synaptic density was equal in the two layers at F152 days and P2 days, but by P12 weeks synaptic density in layer 2 was 27% higher than that in layer 6 (an “outside-to-inside” distribution). After P12 weeks, the synaptic density declined 51% in layer 2 and 21% in layer 6 so that both layers achieved similar densities by P6 years.

A light and EM comparison of neuropil and synaptic contact morphology finds that, at each age up to birth, synapses in layer 2 are generally less mature than those in layer 6, but these differences disappear shortly after birth. Between P6–24 weeks, synaptic contacts throughout the cortex acquire a mature morphology that clearly differentiates between asymmetric and symmetric types, although asymmetric contacts continue to acquire more postsynaptic density until adulthood.

This complex developmental pattern suggests a sequence for synaptic developments which is more related to neuron birthdate than to the arrival of extrinsic pathways or developmental events occurring in specific laminae.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1992

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References

Allman, J. & McGuiness, E. (1988). Visual cortex in primates. In Comparative Primate Biology; Neurosciences, Vol. 4, ed. Steklis, H.D. & Erwin, J., pp. 279326. New York: A. Liss, Inc.Google Scholar
Berry, M. & Rogers, A.W. (1965). The migration of neuroblasts in the developing cerebral cortex. Journal of Anatomy 99, 691709.Google ScholarPubMed
Blue, M.E. & Parnavelas, J.G. (1983a). The formation and maturation of synapses in the visual cortex of the rat. I. Qualitative analysis. Journal of Neurocytology 12, 599616.CrossRefGoogle ScholarPubMed
Blue, M.E. & Parnavelas, J.G. (1983b). The formation and maturation of synapses in the visual cortex of the rat. II. Quantitative analysis. Journal of Neurocytology 12, 697712.CrossRefGoogle ScholarPubMed
Boothe, R.G., Greenouoh, W.T., Lund, J.S. & Wrege, K. (1979). A quantitative investigation of spine and dendrite development of neurons in visual cortex (area 17) of Macaca nemestrina monkeys. Journal of Comparative Neurology 186, 473490.CrossRefGoogle ScholarPubMed
Boothe, R.G., Dobson, V. & Teller, D.Y. (1985). Postnatal development of vision in human and nonhuman primates. Annual Review of Neuroscience 8, 495545.CrossRefGoogle ScholarPubMed
Bourgeois, J.-P., Jastreboff, P.J. & Rakic, P. (1989). Synaptogenesis in visual cortex of normal and preterm monkeys: Evidence for intrinsic regulation of synaptic overproduction. Proceedings of the National Academy of Sciences of the U.S.A. 86, 42974301.CrossRefGoogle ScholarPubMed
Cragg, B.G. (1972). The development of synapses in cat visual cortex. Investigative Ophthalmology 11, 377385.Google Scholar
Cragg, B.G. (1975). The development of synapses in the visual system of the cat. Journal of Comparative Neurology 160, 147166.CrossRefGoogle ScholarPubMed
Dehay, C., Horseburgh, G., Berland, M., Killckey, H. & Kennedy, H. (1989). Maturation and connectivity of the visual cortex in monkey is altered by prenatal removal of retinal input. Nature 337, 265267.CrossRefGoogle ScholarPubMed
Edmunds, S.M. & Parnavelas, J.G. (1982). Retzius-Cajal cells: An ultrastructural study in the developing visual cortex of the rat. Journal of Neurocytology 11, 427446.CrossRefGoogle ScholarPubMed
Hendrickson, A. (1985). Dots, stripes and columns in monkey visual cortex. Trends in Neuroscience 8, 404410.CrossRefGoogle Scholar
Hicks, S.P. & D'amato, C.J. (1968). Cell migrations to the isocortex in the rat. Anatomical Record 160, 619634.CrossRefGoogle Scholar
Huntley, G.W. & Jones, E.G. (1990). Cajal-retzius neurons in developing monkey neocortex show immunoreactivity for calcium binding proteins. Journal of Neurocytology 19, 200212.CrossRefGoogle ScholarPubMed
Huttenlocher, P.R., Decourten, C., Garey, L.J. & Van Der Loos, H. (1982). Synaptogenesis in human visual cortex —evidence for synapse elimination during normal development. Neuroscience Letters 33, 247252.CrossRefGoogle ScholarPubMed
Juraska, J.M. & Fifkova, E. (1979). An electron microscope study of the early postnatal development of the visual cortex of the hooded rat. Journal of Comparative Neurology 183, 257268.CrossRefGoogle ScholarPubMed
Kostovic, I. & Rakic, P. (1990). Developmental history of the transient subplate zone in the visual and somatosensory cortex of the macaque monkey and human brain. Journal of Comparative Neurology 297, 441470.CrossRefGoogle ScholarPubMed
Kostovic, I. & Rakic, P. (1980). Cytology and time of origin of interstitial neurons in the white matter in infant and adult human and monkey telencephalon. Journal of Neurocytology 9, 219242.CrossRefGoogle ScholarPubMed
Kristt, D.A. & Molliver, M.E. (1976). Synapses in newborn rat cerebral cortex: A quantitative ultrastructural study. Brain Research 108, 180186.CrossRefGoogle ScholarPubMed
Kuijis, R.O. & Rakic, P. (1990). Hypercolumns in primate visual cortex can develop in the absence of cues from photoreceptors. Proceedings of the National Academy of Sciences of the U.S.A. 87, 53035306.Google Scholar
Levay, S., Wiesel, T.N. & Hubel, D.H. (1980). The development of ocular dominance columns in normal and visually deprived monkeys. Journal of Comparative Neurology 191, 151.CrossRefGoogle ScholarPubMed
Levay, S., Connolly, M., Houde, J. & Van Essen, D.C. (1985). The complete pattern of ocular dominance stripes in the striate cortex and visual field of the macaque monkey. Neuroscience 5, 486501.CrossRefGoogle ScholarPubMed
Livingston, M. & Hubel, D.H. (1985). Segregation of form, color, movement and depth: anatomy, physiology and perception. Science 240, 740749.CrossRefGoogle Scholar
Lund, J.S. (1988). Anatomical organization of macaque monkey striate visual cortex. Annual Review of Neuroscience 11, 253288.CrossRefGoogle ScholarPubMed
Luskin, M.B. & Shatz, C.J. (1985a). Studies of the earliest generated cells of the cat's visual cortex: cogeneration of subplate and marginal zone. Journal of Neuroscience 5, 10621075.CrossRefGoogle Scholar
Luskin, M.B. & Shatz, C.J. (1985b). Neurogenesis in the cat's primary visual cortex. Journal of Comparative Neurology 242, 611631.CrossRefGoogle ScholarPubMed
Marin-Padilla, M. (1971). Early prenatal ontogenesis of the cerebral cortex (neocortex) of the cat (Felis domestica): a Golgi study. I. The primordial neocortical organization. Zeitschrift fiir Anatomie und Entwicklungs Geschichte 134, 117145.CrossRefGoogle Scholar
Mates, S.L. & Lund, J.S. (1983a). Neuronal composition and development in lamina 4C of monkey striate cortex. Journal of Comparative Neurology 221, 6090.CrossRefGoogle ScholarPubMed
Mates, S.L. & Lund, J.S. (1983b). Spine formation and maturation of type I synapses on spiny stellate neurons in primate visual cortex. Journal of Comparative Neurology 221, 9197.CrossRefGoogle ScholarPubMed
Mates, S.L. & Lund, J.S. (1983c). Developmental changes in the relationship between type 2 synapses and spiny neurons in the monkey visual cortex. Journal of Comparative Neurology 221, 98105.CrossRefGoogle ScholarPubMed
McConnell, S.K. (1988). Development and decision-making in the mammalian cerebral cortex. Brain Research Review 13, 123.CrossRefGoogle Scholar
Miller, M. & Peters, A. (1981). Maturation of rat visual cortex. II. A combined Golgi-electron microscope study of pyramidal neurons. Journal of Comparative Neurology 203, 555573.CrossRefGoogle Scholar
Molliver, M.E., Kostovic, I. & Van Der Loos, H. (1973). The development of synapses in cerebral cortex of the human fetus. Brain Research 50, 403407.CrossRefGoogle ScholarPubMed
O'kusky, J. & Colonnier, M. (1982a). A laminar analysis of the number of neurons, glia, and synapses in the visual cortex (area 17) of adult macaque monkeys. Journal of Comparative Neurology 210, 278290.CrossRefGoogle ScholarPubMed
O'kusky, J. & Colonnier, M. (1982b). 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. Journal of Comparative Neurology 210, 291306.CrossRefGoogle ScholarPubMed
Powell, T.P.S. & Hendrickson, A.E. (1981). Similarity in number of neurons through the depth of the cortex in the binocular and monocular parts of area 17 of the monkey. Brain Research 216, 409413.CrossRefGoogle ScholarPubMed
Rakic, P. (1974). Neurons in the rhesus monkey visual cortex: systematic relation between time of origin and eventual disposition. Science 183, 425427.CrossRefGoogle ScholarPubMed
Rakic, P. (1977). Prenatal development of the visual system in the rhesus monkey. Philosophical Transactions of the Royal Society B (London) 278, 245260.Google ScholarPubMed
Rakic, P. (1981). Developmental events leading to laminar and areal organization of the neocortex. In The Organization of the Cerebral Cortex, ed. Schmtt, F.O., Worden, E.G., Adelman, G. & Dennis, S.G., pp. 728. Cambridge, Massachusetts: MIT Press.Google Scholar
Rakic, P. (1988). Specification of cerebral cortical areas. Science 241, 170241.CrossRefGoogle ScholarPubMed
Rakic, P., Bourgeois, J.-P., Eckenhoff, M.P., Zecevic, N. & Goldman-Rakic, P.S. (1986). Concurrent overproduction of synapses in diverse regions of the primate cerebral cortex. Science 232, 232355.CrossRefGoogle ScholarPubMed
Swindale, N.V., Vital-Durand, F. & Blakemore, C. (1981). Recovery from monocular deprivation in the monkey. III. Reversal of anatomical effects in the visual cortex. Proceedings of the Royal Society B (London) 213, 435450.Google ScholarPubMed
Winfield, D.A. (1981). The postnatal development of synapses in the visual cortex of the cat and the effects of eyelid suture. Brain Research 206, 166171.CrossRefGoogle Scholar
Winfield, D.A. (1983). The postnatal development of synapses in the different laminae of the visual cortex in the normal kitten and in kittens with eyelid suture. Developmental Brain Research 9, 155169.CrossRefGoogle Scholar
Wolff, J.R. (1977). Quantitative analysis of topography and development of synapses in the visual cortex. Experimental Brain Research (Suppl.) 1, 259263.Google Scholar
Zecevic, N., Bourgeois, J.-P. & Rakic, P. (1989). Changes in synaptic density in motor cortex of rhesus monkey during fetal and postnatal life. Developmental Brain Research 50, 1132.CrossRefGoogle ScholarPubMed