Hostname: page-component-78c5997874-fbnjt Total loading time: 0 Render date: 2024-11-10T21:19:49.168Z Has data issue: false hasContentIssue false

Early dendritic outgrowth of primate retinal ganglion cells

Published online by Cambridge University Press:  02 June 2009

Michael A. Kirby
Affiliation:
Departments of Pediatrics and Anatomy, and the Division of Perinatal Biology, School of Medicine, Loma Linda University, Loma Linda
Thomas C. Steineke
Affiliation:
Departments of Pediatrics and Anatomy, and the Division of Perinatal Biology, School of Medicine, Loma Linda University, Loma Linda

Abstract

The pattern of dendritic stratification of retinal ganglion cells in the fetal monkey (Macaca mulatta) was examined using horseradish peroxidase and retinal explants. Ganglion cells in the rhesus monkey are born between embryonic day (E) 30–70 (La Vail et al., 1983). At E60, E67, and E68, approximately 50% of all ganglion cells within the central 3.0 mm of the retina had dendritic arbors that were unistratified within the inner plexiform layer (IPL), while the remaining 50% had bistratified arbors. Unistratified cells had relatively flat arbors that ramified within a restricted portion of the IPL. In contrast, bistratified cells had one portion of the arbor that branched in the inner half of the IPL and a second portion that branched in the outer half of the IPL. Relatively few bistratified cells were encountered in the central 1.0 mm of the retina but were more numerous with increasing eccentricity. At E81, E90, and E110, the dendritic arbors of ganglion cells increased in both area and complexity, but occupied a relatively small percentage of the total depth of the IPL. The bistratified cells encountered at these fetal ages were typically located in the far retinal periphery. Between E125-E140, the dendritic arbors of individual ganglion cells increased in area and depth to occupy a greater proportion of the total IPL than at earlier fetal ages.

These observations suggest that ganglion cells in the macaque undergo at least three stages of dendritic stratification: (1) an initial period of dendritic growth during which the cells have either unistratified or bistratified dendritic arbors; (2) a loss of the majority of bistratified cells through cell death or remodeling of the arbor; and (3) growth or expansion of the arbor to occupy a greater percentage of the total depth of the IPL. The first two stages are similar to recent observations in the fetal cat (Maslim & Stone, 1988) with the exception that dendritic development in the primate lacks an initial diffuse ingrowth to the IPL. Additionally, primate ganglion cells undergo a third stage of dendritic growth in late fetal development during which the arbor occupies a greater proportion of the depth of the IPL.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1991

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adams, J.C. (1981). Heavy metal intensification of DAB-based HRP reaction product. Journal of Histochemistry and Cytochemistry 29, 775.CrossRefGoogle ScholarPubMed
Ault, S.J., Schall, J.D. & Leventhal, A.G. (1985). Experimental alteration of cat retinal ganglion cell dendritic field structures. Society for Neuroscience Abstracts 11, 15.Google Scholar
Bloomfield, S.A. & Miller, R.F. (1986). A functional organization of ON and OFF pathways in the rabbit retina. Journal of Neuroscience 6, 113.CrossRefGoogle Scholar
Bourgeosis, J.-P. & Rakic, P. (1983). Synaptogenesis in the primary visual cortex: quantitative analysis in prenatal and postnatal rhesus monkeys. Society for Neuroscience Abstracts 9, 692.Google Scholar
Boycott, B.B. & Dowling, J.E. (1969). Organization of the primate retina: light microscopy. Philosophical Transactions of the Royal Society (London) 255, 109184.Google Scholar
Boycott, B.B. & Wässle, H. (1974). The morphological types of cells of the domestic cat's retina. Journal of Physiology (London) 240, 397419.Google Scholar
Brecha, N. (1983). Retinal neurotransmitters: histochemical and biochemical studies. In Chemical Neuroanatomy, ed. Emson, P.C., pp. 85129. New York: Raven Press.Google Scholar
Brecha, N. & Karten, H.J. (1983). Identification and localization of neuropeptides in the vertebrate retina. In Brain Peptides, ed. Krieger, D., Brownstein, M. & Martin, J., pp. 437462. New York: John Wiley.Google Scholar
Brecha, N., Hendrickson, A., Floren, I. & Karten, H.J. (1982). Localization of substance P-like immunoreactivity within the monkey retina. Investigative Ophthalmology and Visual Science 23, 147153.Google ScholarPubMed
Cajal, S.R. (1893). La retine des vertebres. Cellule 9, 17257.Google Scholar
Cleland, B.G. & Levick, W.R. (1974). Properties of rarely encountered types of ganglion cells in the cat's retina and on overall classification. Journal of Physiology (London) 240, 457492.Google Scholar
Cooper, M.L. & Rakic, P. (1983). Gradients of cellular maturation and synaptogenesis in the superior colliculus of the fetal rhesus monkey. Journal of Comparative Neurology 215, 165186.CrossRefGoogle ScholarPubMed
Cragg, B.G. (1975). The development of synapses in the visual system of the cat. Journal of Comparative Neurology 160, 147166.CrossRefGoogle ScholarPubMed
Dann, J.F., Buhl, E.H. & Peichl, L. (1987). Dendritic maturation in cat retinal ganglion cells: a lucifer yellow study. Neuroscience Letters 80, 2126.CrossRefGoogle ScholarPubMed
Dann, J.F., Buhl, E.H. & Peichl, L. (1988). Postnatal maturation of alpha- and beta-ganglion cells in the cat retina. Journal of Neuroscience 8, 14851499.CrossRefGoogle ScholarPubMed
DeJager, D. & Kirby, M.A. (1988). Morphological development of primate retinal ganglion cell dendrites. Society for Neuroscience Abstracts 14, 458.Google Scholar
Dogiel, A.S. (1891). Ueber die nervosen elemente in der retina des menschen. Archiv Fur Mikroskopische Anatomie und Entwicklungsmechanik 38, 317344.CrossRefGoogle Scholar
Dowling, J.E. & Boycott, B.B. (1966). Organization of the primate retina: electron microscopy. Proceedings of the Royal Society B 166, 80111.Google ScholarPubMed
Dunlop, S.A. (1990). Early development of retinal ganglion cell dendrites in the marsupial (Setonix brachyurus) quokka. Journal of Comparative Neurology 293, 425447.CrossRefGoogle ScholarPubMed
Eysel, U., Peichl, L. & Wässle, H. (1985). Dendritic plasticity in the early postnatal feline retina: quantitative characteristics and sensitive period. Journal of Comparative Neurology 242, 134145.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. (1983). “Starburst” amacrine cells and cholinergic neurons: symmetric ON and OFF amacrine cells of rabbit retina. Brain Research 261, 138144.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. & Kolb, H. (1975). A bistratified amacrine cell and synaptic circuitry of the inner plexiform layer of the retina. Brain Research 84, 293300.CrossRefGoogle Scholar
Famiglietti, E.V. & Kolb, H. (1976). Structural basis for ON- and OFF-center responses in retinal ganglion cells. Science 194, 193195.CrossRefGoogle ScholarPubMed
Fischer, Q.S. & Kirby, M.A. (1991). The number and distribution of ganglion cells in adult baboons (Papio anubis). Brain, Behavior, and Evolution 37, 189203.CrossRefGoogle Scholar
Gottlieb, M.D., Pasik, P. & Pasik, T. (1985). Early postnatal development of the monkey visual system. Developmental Brain Research 17, 5362.CrossRefGoogle Scholar
Hendrickson, A.E. & Kupfer, C. (1976). The histogenesis of the fovea in the macaque monkey. Investigative Ophthalmology 15, 746756.Google ScholarPubMed
Hendrickson, A.E. & Rakic, P. (1977). Histogenesis and synaptogenesis in the dorsal lateral geniculate nucleus (LGd) of the fetal monkey brain. Anatomical Record 187, 602.Google Scholar
Hollenberg, M.J. & Spira, A.W. (1973). Human retinal development: ultrastructure of the outer retina. American Journal of Anatomy 137, 357386.CrossRefGoogle ScholarPubMed
Holstein, G.R., Pasik, T., Pasik, P. & Hamori, J. (1985). Early postnatal development of the monkey visual system, II: Elimination of retinogeniculate synapses. Developmental Brain Research 20, 1531.CrossRefGoogle Scholar
Hughes, A. (1985). New perspectives in retinal organization. In Progress in Retinal Research, ed. Osborne, N.N. & Chader, G.J., Vol. 4, pp. 243313. Oxford: Pergamon Press.Google Scholar
Kalil, R.E. & Scott, G. (1979). Development of retinogeniculate synapses in the dorsal lateral geniculate nucleus of the cat. Society for Neuroscience Abstracts 5, 791.Google Scholar
Kirby, M.A. & Chalupa, L.M. (1986). Retinal crowding alters the morphology of alpha ganglion cells. Journal of Comparative Neurology 251, 532541.CrossRefGoogle ScholarPubMed
Kliot, M. & Shatz, C.J. (1982). Genesis of different retinal ganglion cell types in the cat. Society for Neuroscience Abstracts 8, 815.Google Scholar
Kolb, H. (1980). The inner plexiform layer in the retina of the cat; electron microscopic observations. Journal of Neurocytology 8, 295329.CrossRefGoogle Scholar
Kolb, H., Nelson, R. & Mariani, A. (1981). Amacrine cells, bipolar cells, and ganglion cells of the cat retina. A Golgi study. Vision Research 21, 10811114.CrossRefGoogle ScholarPubMed
la Vail, M.M., Yasumura, D. & Rakic, P. (1983). Cell genesis in the rhesus monkey retina. Investigative Ophthalmology and Visual Science (Suppl.) 24, 7.Google Scholar
Lennie, P. (1980). Parallel visual pathways. Vision Research 20, 561594.CrossRefGoogle ScholarPubMed
Leventhal, A.G. & Schall, J.D. (1983). Structural basis of orientation selectivity of cat retinal ganglion cells. Journal of Comparative Neurology 220, 465475.CrossRefGoogle Scholar
Leventhal, A.G., Schall, J.D. & Ault, S.J. (1988). Extrinsic determinants of retinal ganglion cell structure in the cat. Journal of Neuroscience 8, 20282036.CrossRefGoogle ScholarPubMed
Lia, B. & Chalupa, L.M. (1988). Prenatal development of regional specialization in the primate retina. Investigative Ophthalmology and Visual Science (Suppl.) 29, 378.Google Scholar
Linden, R. & Perry, V.H. (1982). Ganglion cell death within the developing retina: a regulatory role for retinal dendrites? Neuroscience 7, 28132837.CrossRefGoogle ScholarPubMed
Maffei, L. & Perry, V.H. (1988). The axon initial segment as a possible determinant of retinal ganglion cell dendritic geometry. Developmental Brain Research 41, 185194.CrossRefGoogle Scholar
Marc, R.E. (1986). Neurochemical stratification in the IPL of the vertebrate retina. Vision Research 26, 223228.CrossRefGoogle Scholar
Mariani, A. (1982). Biplexiform cells: ganglion cells of the primate retina that contact photoreceptors. Science 216, 11341136.CrossRefGoogle ScholarPubMed
Mariani, A.P. (1990). Amacrine cells of the rhesus monkey retina. Journal of Comparative Neurology 301, 382400.CrossRefGoogle ScholarPubMed
Masland, R.H., Mills, J.W. & Hayden, S.A. (1984). Acetylcholinesynthesising amacrine cells: identification and selective staining by using autoradiography and fluorescent markers. Proceedings of the Royal Society B (London) 223, 79100.Google Scholar
Maslim, J. & Stone, J. (1986). Synaptogenesis in the retina of the cat. Brain Research 373, 3548.CrossRefGoogle ScholarPubMed
Maslim, J. & Stone, J. (1988). Time course of stratification of the dendritic fields of ganglion cells in the retina of the cat. Developmental Brain Research 44, 8793.CrossRefGoogle ScholarPubMed
Maslim, J., Webster, M. & Stone, J. (1986). Stages in the structural differentiation of retinal ganglion cells. Journal of Comparative Neurology 254, 382402.CrossRefGoogle ScholarPubMed
Mason, C.A. (1982a). Development of terminal arbors of retinogeniculate axons in the kitten, I: Light-microscopical observations. Neuroscience 7, 541559.CrossRefGoogle ScholarPubMed
Mason, C.A. (1982b). Development of terminal arbors of retinogeniculate axons in the kitten, II: Electron-microscopical observations. Neuroscience 7, 561582.CrossRefGoogle ScholarPubMed
Mastronarde, D.N., Thibeault, M.A. & Dubin, M.W. (1984). Nonuniform postnatal growth of the cat retina. Journal of Comparative Neurology 288, 598608.CrossRefGoogle Scholar
Nelson, R. & Kolb, H. (1985). A17: a broad-field amacrine cell in the rod system of the cat retina. Journal of Neurophysiology 54, 592614.CrossRefGoogle ScholarPubMed
Nelson, R., Famiglietti, E.V. Jr & Kolb, H. (1978). Intracellular staining reveals different levels of stratification for ON- and OFF-center ganglion cells in the cat retina. Journal of Neurophysiology 41, 472483.CrossRefGoogle ScholarPubMed
Nishimura, Y. & Rakic, P. (1985). Development of the rhesus monkey retina, I: Emergence of the inner plexiform layer and its synapses. Journal of Comparative Neurology 241, 420434.CrossRefGoogle ScholarPubMed
Nishimura, Y. & Rakic, P. (1987). Development of the rhesus monkey retina, II: A three-dimensional analysis of the sequences of synaptic combinations in the inner plexiform layer. Journal of Comparative Neurology 262, 290313.CrossRefGoogle Scholar
Peichl, L. & Wässle, H. (1981). Morphological identification of ON- and OFF-center brisk transient (Y) cells in the cat retina. Proceedings of the Royal Society B (London) 212, 139156.Google Scholar
Perry, V.H. (1984). The development of ganglion cell mosaics. In Development of Visual Pathways in Mammals, ed. Stone, J., Dreher, B. & Rapaport, D.H., pp. 5974. New York: Alan R. Liss.Google Scholar
Perry, V.H. & Cowey, A. (1984). Retinal ganglion cells that project to the superior colliculus and pretectum in the macaque monkey. Neuroscience 12, 11251137.CrossRefGoogle Scholar
Perry, V.H. & Linden, R. (1982). Evidence for dendritic competition in the developing retina. Nature 297, 683.CrossRefGoogle ScholarPubMed
Perry, V.H., Oehler, R. & Cowey, A. (1984). Retinal ganglion cells that project to the dorsal lateral geniculate nucleus in the macaque monkey. Neuroscience 12, 11011123.CrossRefGoogle Scholar
Polyak, S.L. (1941). The Retina. Chicago, Illinois: The University of Chicago Press.Google Scholar
Polyak, S.L. (1957). The Vertebrate Visual System. Chicago, Illinois: University of Chicago Press.Google Scholar
Provis, J.M., Van Driel, D., Billson, F.A. & Russel, P. (1985). Development of the human retina: patterns of cell distribution and redistribution in the ganglion cell layer. Journal of Comparative Neurology 233, 429451.CrossRefGoogle ScholarPubMed
Rakic, P. & Riley, K.P. (1983). Overproduction and elimination of retinal axons in the fetal rhesus monkey. Science 219, 14411444.CrossRefGoogle ScholarPubMed
Ramoa, A.S.Campbell, G. & Shatz, C.J. (1987). Transient morphological features of identified ganglion cells in living fetal and neonatal retina. Science 237, 522525.CrossRefGoogle ScholarPubMed
Ramoa, A.S., Campbell, G. & Shatz, C.J. (1988). Dendritic growth and remodeling of cat retinal ganglion cells during fetal and postnatal development. Journal of Neuroscience 8, 42394261.CrossRefGoogle ScholarPubMed
Rapaport, D.H., Fletcher, J.T., la Vail, M.M. & Rakic, P. (1990). Genesis of retinal ganglion cell subtypes in the monkey. Society for Neuroscience Abstracts 16, 334.Google Scholar
Rapaport, D.H. & Stone, J. (1984). The site of commencement of maturation in mammalian retina: observations in the cat. Developmental Brain Research 5, 273279.CrossRefGoogle Scholar
Rapaport, D.H., Yasumura, D., la Vail, M.M. & Rakic, P. (1987). Cytogenesis of the monkey retina: comparison of the generation of retinal pigment epithelium and neural retina. Society for Neuroscience Abstracts 13, 238.Google Scholar
Robinson, S.R. (1987). Ontogeny of the area centralis in the cat. Journal of Comparative Neurology 255, 5067.CrossRefGoogle ScholarPubMed
Robinson, S.R., Dreher, B. & McCall, M.J. (1989). Nonuniform retinal expansion during the formation of the rabbit visual streak: implications for the ontogeny of mammalian retinal topography. Visual Neuroscience 2, 201220.CrossRefGoogle ScholarPubMed
Rodieck, R.W. (1973). The Vertebrate Retina: Principles of Structure and Function. San Francisco, California: Freeman Press.Google Scholar
Rodieck, R.W. (1979). Visual pathways. Annual Review of Neuroscience 2, 193225.CrossRefGoogle ScholarPubMed
Rodieck, R.W. (1988). The primate retina. Comparative Primate Biology (Neurosciences) 4, 203278.Google Scholar
Rodieck, R.W., Binmoeller, K.F. & Dineen, J. (1985). Parasol and midget ganglion cells of the human retina. Journal of Comparative Neurology 233, 115132.CrossRefGoogle ScholarPubMed
Rusoff, A.C. & Dubin, M.W. (1978). Kitten ganglion cells: dendritic field size at 3 weeks of age and correlation with receptive-field size. Investigative Ophthalmology and Visual Science 17, 819821.Google ScholarPubMed
Sherman, S.M. & Spear, P.D. (1982). Organization of visual pathways in normal and deprived cats. Physiological Reviews 62, 740855.CrossRefGoogle ScholarPubMed
Smelser, G.K., Ozanics, V., Rayborn, M. & Sagun, D. (1974). Retinal synaptogenesis in the primate. Investigative Ophthalmology 13, 340361.Google ScholarPubMed
Stanford, L.R. (1987). W cells in the cat retina: correlated morphological and physiological evidence for two distinct classes. Journal of Neurophysiology 57, 218244.CrossRefGoogle ScholarPubMed
Sterling, P., Freed, M. & Smith, R.G. (1986). Microcircuitry and functional architecture of the cat retina. Trends in Neuroscience 9, 186192.CrossRefGoogle Scholar
Stone, J. (1981). The Wholemount Handbook. A Guide to the Preparation and Analysis of Retinal Wholemounts. Sydney, Australia: Maitland.Google Scholar
Stone, J. (1983). Parallel Processing In the Visual System. New York: Plenum Press.CrossRefGoogle Scholar
Stone, J. & Fabian, M. (1966). Specialized receptive fields of the cat's retina. Science 152, 12771279.CrossRefGoogle ScholarPubMed
Stone, J. & Fukuda, Y. (1974). Properties of cat retinal ganglion cells: a comparison of W cells with X and Y cells. Journal of Neurophysiology 37, 722748.CrossRefGoogle ScholarPubMed
Walsh, C. & Polley, E.H. (1985). The topography of ganglion cell production in the cat's retina. Journal of Neuroscience 5, 741750.CrossRefGoogle ScholarPubMed
Walsh, C., Polley, E.H., Hickey, T.L. & Guillery, R.W. (1983). Generation of cat retinal ganglion cells in relation to central pathways. Nature 302, 611614.CrossRefGoogle ScholarPubMed
Wässle, H. (1982). Morphological types and central projections of ganglion cells in the cat retina. In Progress in Retinal Research, ed. Osborne, N. & Chandler, G., pp. 125152. Oxford: Pergamon Press.Google Scholar
Wässle, H. & Reiman, H.J. (1978). The mosaic of nerve cells in the mammalian retina. Proceedings of the Royal Society B (London) 200, 441461.Google Scholar
Wässle, H., Boycott, B.B. & Illing, R.-B. (1981a). Morphology and mosaic of ON- and OFF-beta cells in the cat retina and some functional considerations. Proceedings of the Royal Society B (London) 212, 177195.Google Scholar
Wässle, H., Peichl, L. & Boycott, B.B. (1981b). Dendritic territories of cat retinal ganglion cells. Nature 292, 344345.CrossRefGoogle ScholarPubMed
Wässle, H., Peichl, L. & Boycott, B.B. (1981c). Morphology and topography of ON- and OFF-cells in the cat retina. Proceedings of the Royal Society B (London) 212, 157175.Google Scholar
Wässle, H., Peichl, L. & Boycott, B.B. (1983). A spatial analysis of ON- and OFF-ganglion cells in the cat retina. Vision Research 23, 11511160.CrossRefGoogle Scholar
Watanabe, M. & Rodieck, R.W. (1989). Parasol and midget ganglion cells of the primate retina. Journal of Comparative Neurology 289, 434454.CrossRefGoogle ScholarPubMed
Wong, R.O.L. & Collin, S.P. (1989). Dendritic maturation of displaced putative cholinergic amacrine cells in the rabbit retina. Journal of Comparative Neurology 287, 164178.CrossRefGoogle ScholarPubMed
Zrenner, E., Nelson, R. & Mariani, A. (1983). Intracellular recordings from a biplexiform ganglion cell in the macaque retina, stained with horseradish peroxidase. Brain Research 262, 181185.CrossRefGoogle ScholarPubMed