Abstract
The retina in the developing macaque monkey is an unexcelled model system for the analysis of cellular events and the mechanisms that govern formation of the human eye. Application of the powerful methods of modern neurobiology applied to either normal embryos, or mature animals with altered visual systems, suggests that the emergence of cell classes and their segregation into primate-specific functional domains emerges as a result of multiple factors operating at each retinal layer during successive developmental stages. The available data are compatible with the hypothesis that, at early developmental stages, intrinsic mechanisms operating within the retina predominate, while at later stages reciprocal interactions with the visual centers refines the numerical cellular relationships and synaptic architecture. These studies may provide insight into the development of normal and abnormal vision in humans.
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References
Algan, O., and Rakic, P. (1997) Radiation-induced area-and lamina-specific deletion of neurons in the primate visual cortex. J. Comp. Neurol. 381: 335–352.
Antonini, A., and Stryker, M.R. (1993) Development of individual geniculocortical arbors in cat striate cortex and effects of binocular impulse blockade. J. Neurosci. 13: 3549–5373.
Bok, S.T. (1915) Stimulogenous fibrillation as the cause of the structure of the nervous system. Psychiatrishe en Neurologishe Bladen 19: 393–408.
Bolz, J., Novak, N., and Staiger, V. (1992) Formation of specific afferent connections in organotypic slice cultures from rat visual cortex cocultured with lateral geniculate nucleus. J Neurosci 12: 3054–3070.
Bourgeois, J.-P., and Rakic, P. (1993) Changing of synaptic density in the primary visual cortex of the rhesus monkey from fetal to adult stage. J. Neurosci. 13: 2801–2820.
Campbell, G., Ramoa, A.S., Striker, M.R., and Shatz, C.J. (1997) Dendritic development of retinal ganglion cells after prenatal intracranial infusion of tetradotoxin. Vis. Neurosci. 14: 779–788.
Chalupa, L.M., and Williams, R.W., and Henderson, T. (1984) Binocular interaction in the fetal cat regulates the size of the ganglion cell population. Neurosci., 12: 1139–1146.
Chalupa, L.M., and Williams, R.W. (1984) Organization of the cat’s lateral geniculate nucleus following interruption of prenatal binocular competition. Human Neurobiology 3: 103–107.
Cooper, M.L., and Rakic, P. (1983) Gradients of cellular maturation and synaptogenesis in the superior colliculus of the fetal rhesus monkey. J. Comp. Neurol. 215: 165–186.
Curcio, C.A., Allen, K.A., Sloan, D.R., Lerea, C.L., Hurley, J.B., Klock, I.B., and Milam, A.H. (1991) Distribution and morphology of human cone photoreceptors stained with antiblue opsin. J. Comp. 312: 610–624.
Dehay, C., Horsburgh, O., Berland, M., Killackey, H., and Kennedy, H. (1989) Maturation and connectivity of the visual cortex in monkey is altered by prenatal removal of retinal input. Nature 337:265–267.
DeMonasterio, F.M. (1978) Properties of concentrically organized X and Y ganglion cells of macaque retina. J. Neurophysiol. 41: 1394–1417.
Easter, S.S., Jr., Purves, D., Rakic, P., and Spitzer, N.C. (1985) The changing view of neural specificity. Science 230:507–511.
Feller, M.B., Butts, D.A., Aaron, H.L., Rokhsat, D.S., and Shatz, C.J. (1997) Dynamic processes shape spatiotemporal properties of retinal waves. Neuron, 19: 293–306.
Garraghty, P.E., and Sur, M. (1993) Competitive interactions influencing the development of retinal axonal arbors in cat lateral geniculate nucleus. Physiol Rev. 73: 529–545.
Goodman, C.S., and Shatz, C.J. (1993) Developmental mechanisms that generate precise patterns of neuronal connectivity. Cell 72: 77–98.
Hendrickson, A., and Rakic, P. (1977) Histogenesis and synaptogenesis in the dorsal lateral geniculate nucleus (LGd) of the fetal monkey brain. Anal. Rec. 187: 602.
Holt, C.E., Bertsch, T.W., Ellis, H.M., and Harris, W.A. (1988) Cellular determination in the Xenopus retina is independent of lineage and birth date. Neuron 1: 15–26.
Kaiserman-Abramof, I.R., Graybiel, A.M., and Nauta W.J.H. (1989) The thalamic projection to cortical area 17 in congenitally anophthalmic mouse strain. Neurosci. 5: 41–52.
Kennedy H., and Dehay, C. (1997) The nature and nurture of cortical development. (In: Normal and Abnormal Development of the Cortex. (Galaburda A and Christen Y eds) Springer, Berlin pp. 25–56.
Kennedy, H., and Dehay, C. (1993) Cortical specification of mice and men. Cerebral Cortex 3: 171–186.
Kuljis, R.O., and Rakic, P. (1991) Hypercolumns in primate visual cortex develop in the absence of cues from photoreceptors. Proc. Nat. Acad. Sci. USA 87: 5303–5306.
LaVail, M.M., Fletcher, J., Rapaport, D.H., and Rakic, P. (1991) Cytogenesis in the monkey retina. J. Comp. Neurol. 309:86–114.
Linden, D.C., Guillery, R.W., and Cucchiaro, J. (1981) The dorsal lateral geniculate nucleus of the normal ferret and its postnatal development. J. Comp Neurol. 203: 189–211.
Livingstone, M.S., and Hubel, D.H. (1988) Segregation of form, color, movement, and depth: Anatomy, physiology and perception. Science 240:140–149.
Maunsell, J.H.R. (1992) Functional visual streams. Current Opinion in Neurobiology 2: 502–510.
McLoon, S.C., and Barnes, R.B. (1989) Early differentiation of retinal ganglion cells: an axonal protein expressed by premigratory and migrating retinal ganglion cells. J. Neurosci. 9: 1424–1432.
Meissirel, C., Wikler, K.C., Chalupa, L.M., and Rakic, P. (1997) Early divergence of M and P visual subsystems in the embryonic primate brain. Proc. Nat. Acad. Sci.(USA), 94: 5900–5905.
Mombaerts, P., Wang, F., Dulac, C., Chao, S.K., Nemes, A., Mendelsohn, M., Edmondson, J., and Axel, R. (1996) Complete record visualizing an olfactory sensory map. Cell. 87: 675–686.
Mrzljak, L., Levey, A.I., and Rakic, P. (1996) Selective expression of m2 muscarinic receptor in parvocellular channel of the primate visual cortex. Proc. Nat. Acad. Sci. (USA), 93: 7337–7340.
Nishimura, Y., and Rakic, P. (1985) Development of the rhesus monkey retina: I. Emergence of the inner plexiform layer and its synapses. J. Comp. Neurol. 241: 420–434.
Nishimura, Y. and Rakic, P. (1987a) Development of the rhesus monkey retina: II. A three-dimensional analysis of the sequences of synaptic combinations in the inner plexiform layer. J. Comp. Neurol. 262: 290–313.
Nishimura, Y. and Rakic, P. (1987b) Synaptogenesis in the primate retina proceeds from the ganglion cells toward the photoreceptors. Neurosci. Res. Suppl. 6: 253–268.
Olavarria, J., and Van Sluyters, R.C. (1984) Callosal connections of the posterior neocortex in normal-eyed, congenitally anophthalmic and neonatally enucleated mice. J. Comp. Neurol. 230, 249–268.
Perry, V.H., Oehler, R., and Cowey, A. (1984) Retinal ganglion cells that project to the dorsal lateral geniculate nucleus in the macaque monkey. Neuroscience 12: 1101–1123.
Perry, V.H., and Cowey, A. (1984) Retinal ganglion cells that project to the superior colliculus and pretectum in the macaque monkey. Neuroscience 12: 1125–1137.
Polyak, S.L. (1957) The Vertebrate Visual System. Chicago: University of Chicago Press.
Rakic, P. (1985) Limits of neurogenesis in primates. Science 227: 154–156.
Rakic, P. (1972) Mode of cell migration to the superficial layers of fetal monkey neocortex. J. Comp. Neurol. 145: 61–84.
Rakic, P. (1973) Kinetics of proliferation and latency between final cell division and onset of differentiation of cerebellar stellate and basket neurons. J. Comp. Neurol. 147: 523–546.
Rakic, P. (1975) Timing of major ontogenetic events in the visual cortex of the rhesus monkey. In: Brain Mechanisms in Mental Retardation. (N.A. Buchwald and M. Brazier, eds.) Academic Press, New York, pp. 3–40.
Rakic, P. (1976) Prenatal genesis of connections subserving ocular dominance in the rhesus monkey. Nature 261: 467–471.
Rakic, P. (1977a) 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. J. Comp. Neurol. 176: 23–52.
Rakic, P. (1977b) Prenatal development of the visual system in the rhesus monkey. Phil. Trans. Roy. Soc. Lond. B. 278: 245–260.
Rakic, P. (1983) Geniculo-cortical connections in primates: Normal and experimentally altered development. Progress in Brain Res. 58: 393–404.
Rakic, P. (1981) Development of visual centers in the primate brain depends on binocular competition before birth. Science 214: 928–931.
Rakic, P. (1988) Specification of cerebral cortical areas. Science 241: 170–176.
Rakic, P. (1992) Development of primate visual system: From photoreceptors to cortical modules. In: Visual System from Genesis to Maturity. R. Lent, ed. Birkhauser, Boston, pp. 1–17.
Rakic, P., and Lidow, M.S. (1995) Distribution and density of neurotransmitter receptors in the visual cortex devoid of retinal input from early embryonic stages. J. Neurosci., 15: 2561–2574
Rakic, P., and Riley, K.P. (1983) Regulation of axon numbers in the primate optic nerve by prenatal binocular competition. Nature 305: 135–137.
Rakic, P., and Riley, K.P. (1983) Overproduction and elimination of retinal axons in the fetal rhesus monkey. Science 209: 1441–1444.
Rakic, P. (1974) Neurons in the monkey visual cortex: Systematic relation between time of origin and eventual disposition. Science 183: 425–427.
Rakic, P., Suner, I., and Williams, R.W. (1991) A novel cytoarchitectonic area induced experimentally within the primate visual cortex. Proc. Nat. Acad. Sci. (USA), 88: 2083–2087.
Rapaport, D.H., LaVail, M.M., and Rakic, P. (1992) Genesis of subclasses of neurons in the retinal ganglion cell layer of the monkey. J. Comp. Neurol. 322:577–588.
Rapaport, D.H., Rakic, P., and LaVail M. (1996) Spatiotemporal gradients of cell genesis in the primate retina. Perspective on Dev. Neurobiol. 3: 142–159.
Rapaport, D.H., Rakic, P., Yasamura, D., and LaVail, M.M. (1995) Genesis of the retinal pigment epithelium in the macaque monkey. J. Comp. Neurol. 363: 359–376.
Reese, F.R. (1996) Chromotopic order of optic axons. Presp. Dev. Neurobiol. 3: 233–242.
Rodieck, R.W. (1988) The Vertebrate Visual System. University of Chicago Press. Chicago.
Rowe, M.H., and Stone, J. (1980) The interpretation of variation in the classification of nerve cells. Brain Behav. Evol. 17: 123–151.
Shapley, R., and Perry, V.H. (1986) Cat and monkey retinal ganglion cells and their visual functional roles. Trends Neurosci. 9: 229–235.
Shatz, C.J. (1983) Prenatal development of cat’s retinogeniculate pathway. J. Neurosci. 3: 482–499.
Shatz, C., and Rakic, P. (1981) The genesis of efferent connections from the visual cortex of the fetal rhesus monkey. J. Comp. Neurol. 196: 287–307.
Shatz, C.J. (1996) Emergence of order in visual system development. Proc. Nat. Acad. Sci., USA 93: 602–608.
Sidman, L.R. (1970) Autoradiographic methods and principles for study of the nervous system with thymidine H3. In: Contemporary Research Methods in Neuroanatomy, W.J.H. Nauta and J.O.E. Ebbeson, eds., pp 225–274. Springer, Berlin.
Skaliora, I., Scobey, R.P., and Chalupa, L.M. (1993) Prenatal development of excitability in cat retinal ganglion cells: action potentials and sodium. J. Neurosci. 13: 313–323.
Sretavan, D.W., and C.J. Shatz (1984) Prenatal development of individual retinogeniculate axons during the period of segregation. Nature 308: 845–848.
Stone, J. (1983) Parallel processing in the visual system. New York: Plenum.
Stryker, M.P., and Harris, W.A. (1986) Binocular impulse blockade prevents the formation of ocular dominance columns in cat visual cortex. J. Neurosci. 6: 2117–2133.
Suner, I., and Rakic, P. (1996) Numerical Relationship between Neurons in the Lateral Geniculate Nucleus and Primary Visual Cortex in Adult Macaque Monkeys. Visual Neurosci., 13: 585–590.
Sur, M., Humphrey, A.L., and Sherman S.M. (1982) Monocular deprivation affects X-and Y-cell retinogeniculate terminations in cats. Nature. 300: 183–185.
Trisler, D., Rutin, J., and Pessac, B. (1996). Retinal engineering: Engrafted neural cell lines locate in appropriate layers. Proc Natl Acad Sci USA 93: 6269–6274.
Turner, D.L., and Cepko, C.L. (1987) A common progenitor for neurons and glia persists in rat retina late in development. Nature 328: 131–136.
Wetts, R., and Fraser, S.E. (1988) Multipotent precursors can give rise to all major cell types of the frog retina. Science 239: 1142–1145.
Wikler, K.C., and Rakic, P. (1990) Distribution of photoreceptor subtypes in the retina of diurnal and nocturnal primates. J. Neurosci. 10: 3390–3400.
Wikler, K.C., and Rakic, P. (1991) Emergence of the photoreceptor mosaic from a protomap of early-differentiating cones in the primate retina. Nature 351: 397–400.
Wikler, K.C., and Rakic, P. (1996) Development of photoreceptor mosaic in the primate retina. Perceptive on Developmental Neurobiology, 3: 161–175.
Wikler, K.C., Rakic, P., and Barnstable, C. (1996) Differential onset of cone opsin expression in the fetal monkey retina. Invest. Ophthal. Vis. Sci. Abstr., 35, S693.
Wikler, K.C., Rakic, P., Bhattacharyya, N., and MacLeish, P.R. (1997) A novel cone-specific monoclonal antibody, 7G6, identifies sub-populations of cones in the fetal monkey retina. J. Comp. Neurol., 377: 500–508.
Wikler, K.C., Williams, R.W., and Rakic, P. (1990) The photoreceptor mosaic: Number, distribution, and patterns of rods and cones in the rhesus monkey retina. J. Comp. Neurol. 297: 499–508.
Wikler, K.S., and Rakic, P. (1994) An array of early-differentiating cones precedes the emergence of the photoreceptor mosaic in the fetal monkey retina. Proc. Nat. Acad. Sci.USA 91: 6534–6538.
Williams, R.W., and Chalupa, L.M. (1982) Prenatal development of retinocollicular projections in the cat: An anterograde tracer transport study. J. Neurosci. 2: 604–622.
Williams, R.W., and Rakic, P. (1985) Dispersion of growing axons within the optic nerve of the embryonic monkey. Proc. Natl. Acad. Sci. USA 82: 3906–3910.
Williams, R.W., and Rakic, P. (1988) Elimination of neurons in the rhesus monkey’s lateral geniculate nucleus during development. J. Comp. Neurol. 272: 424–436.
Williams, R.W., Borodkin, M., and Rakic, P. (1991) Growth cone distribution patterns in the optic nerve of fetal monkeys: Implications for mechanisms of axonal guidance. J. Neurosci. 11: 1081–1094.
Williams, R.W., and Goldowitz, D. (1992) Structure of clonal and polyclonal arrays in chimeric mouse retina. Proc. Natl. Acad. Sci. USA 89: 1164–1188.
Wong, R.O., Chernjavsky, A., Smith, S.J., and Shatz, C.J. (1995) Early functional neural networks in the developing retina. Nature. 374: 716–718.
Xiang, M., Zhou, L., Macke, J., Yoshioka, T., Hendry, S.H.C., Eddy, R., Shows, T.B., and Nathans, J. (1995) The Brn-3 family of POU-domains factors: Primary structure, binding specificity, and expression in subsets of retinal ganglion cells and somatosensory neurons. J. Neuroci. 15: 4762–4785.
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Rakic, P. (1998). Genesis of Topographic and Cellular Diversity in the Primate Retina. In: Chalupa, L.M., Finlay, B.L. (eds) Development and Organization of the Retina. NATO ASI Series, vol 299. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-5333-5_5
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