Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-24T03:25:27.031Z Has data issue: false hasContentIssue false
  • English
  • Français

Morphogenesis of retinal ganglion cells during formation of the fovea in the Rhesus macaque

Published online by Cambridge University Press:  02 June 2009

Michael A. Kirby  and
Thomas C. Steineke
Michael A. Kirby
Affiliation:
Departments of Pediatrics and Anatomy, and the Division of Perinatal Biology, School of Medicine, Loma Linda University, Loma Linda Reprint requests to: Michael A. Kirby, Department of Pediatrics, School of Medicine, Loma Linda University, Loma Linda, CA 92350, USA.
Thomas C. Steineke
Affiliation:
Departments of Pediatrics and Anatomy, and the Division of Perinatal Biology, School of Medicine, Loma Linda University, Loma Linda
Get access Rights & Permissions [Opens in a new window]

Abstract

The morphology of retinal ganglion cells within the central retina during formation of the fovea was examined in retinal explants with horseradish-peroxidase histochemistry. A foveal depression was first apparent in retinal wholemounts at embryonic day 112 (El 12; gestational term is approximately 165 days). At earlier fetal ages, the site of the future fovea was identified by several criteria that included peak density of ganglion cells, lack of blood vessels in the inner retinal layers, arcuate fiber bundles, and the absence of rod outer segments in the photoreceptor layer. Prior to E112, the terminal dendritic arbor of retinal ganglion cells within the central retina extended into the inner plexiform layer and were located directly beneath their somas of origin or at most were slightly displaced from it. For example, at E90 the mean horizontal displacement of the geometric center of the dendritic arbor from the somas of cells within 600 μm of the estimated center of the future fovea was 4.1 μm (S.D. 2.7, range 1.0-10.0, n = 97). Following formation of the foveal depression the dendritic arbors of cells were significantly displaced from their somas. For example, at E138 the mean displacement was 41.2 μm (S.D. 12.2, range 12.0-56.0, n = 97). The displacement of the dendritic arbor which occurred during this period was not accounted for by areal growth of the dendritic arbor, the somas, or the retina, but was produced by the lengthening of the primary dendritic trunk. Moreover, no significant displacement was observed within the remaining 1.5–6.5 mm of the central retina. These observations provide evidence supporting early speculations that the formation of the foveal pit occurs, in part, by the radial migration of ganglion cells from the center of the fovea during its formation. Our analyses suggest that this migration occurs by the lengthening of the primary dendrite presumably by the addition of membrane. This migration is in a direction opposite to the inward movement of photoreceptors that occurs during late fetal and early postnatal periods (Packer et al., 1990, Journal of Comparative Neurology 298, 472–493).

Keywords

FoveaPrimateGanglion cellsMigrationDendrite
Type
Research Article
Information
Visual Neuroscience , Volume 9 , Issue 6 , December 1992 , pp. 603 - 616
Copyright
Copyright © Cambridge University Press 1992

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

Abramov, I., Gordon, J., Hendrickson, A., Hainline, L., Dobson, V. & Labossiere, E. (1982). The retina of the newborn human infant. Science 217, 265–267.CrossRefGoogle ScholarPubMed
Adams, J.C. (1981). Heavy metal intensification of DAB-based HRP reaction product. Journal of Histochemistry and Cytochemistry 29, 775.CrossRefGoogle ScholarPubMed
Bunt, A.H. & Minckler, D.S. (1977). Foveal Sparing: New anatomical evidence for bilateral representation of the central retina. Archives of Ophthalmology 95, 1445–1447.CrossRefGoogle ScholarPubMed
Bunt, A.H., Minckler, D.S. & Johanson, G.W. (1977). Demonstration of bilateral projection of the central retina of the monkey with horseradish peroxidase neuronography. Journal of Comparative Neurology 171, 619–630.CrossRefGoogle ScholarPubMed
Chalupa, L.M. & Lia, B. (1991). The nasotemporal division of retinal ganglion cells with crossed and uncrossed projections in the fetal Rhesus monkey. Journal of Neuroscience 11, 191–202.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, 21–26.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, 1485–1499.CrossRefGoogle ScholarPubMed
Dejager, D. & Kirby, M.A. (1988). Morphological development of primate retinal ganglion cell dendrites. Society of Neuroscience Abstracts 14, 458.Google Scholar
Duke-Elder, S. & Cook, C. (1963). System of Ophthalmology. St. Louis, Missouri: CV Mosby & Co.Google Scholar
Dunlop, S.A. (1990). Early development of retinal ganglion cell dendrites in the marsupial Setonix brachyurus, quokka. Journal of Comparative Neurology 293, 425–447.CrossRefGoogle ScholarPubMed
Hendrickson, A.E. & Kupfer, C. (1976). The histogenesis of the fovea in the macaque monkey. Investigative Ophthalmology 15, 746–756.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
Hendrickson, A.E. & Yuodelis, C. (1984). The morphological development of the human fovea. Ophthalmology 91, 603–612.CrossRefGoogle ScholarPubMed
Hooan, M.J., Alvarado, J.A. & Weddell, J.E. (1971). Histology of the Human Eye: An Atlas and Textbook. Philadelphia, Pennsylvania: WB Saunders.Google Scholar
Hollenberg, M.J. & Spria, A.W. (1973). Human retinal development: ultrastructure of the outer retina. American Journal of Anatomy 137, 357–386.CrossRefGoogle ScholarPubMed
Huber, A. (1962). Homonymous-hemianopia after occipital lobectomy. American Journal of Ophthalmology 54, 623–629.CrossRefGoogle ScholarPubMed
Jacobson, M. (1978). Development Neurobiology. New York: Plenum.Google Scholar
Kirby, M.A. & Steineke, T.C. (1991). Early dendritic outgrowth of primate retinal ganglion cells. Visual Neuroscience 7, 1–18.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
La Vail, M.M., Rapaport, D.H. & Rakic, P. (1991). Cytogenesis in the monkey retina. Journal of Comparative Neurology 309, 86–114.CrossRefGoogle ScholarPubMed
Leventhal, A.G., Schall, J.D. & Ault, S.J. (1988). Extrinsic determinants of retinal ganglion cell structure in the cat. Journal of Neuroscience 8, 2028–2036.Google Scholar
Leventhal, A.G., Ault, S.J., Vitek, D.J. & Shou, T. (1989). Extrinsic determinants of retinal ganglion cell development in primates. Journal of Comparative Neurology 286, 190–207.Google Scholar
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
Lia, B., Williams, R.W. & Chalupa, L.M. (1987). Formation of retinal ganglion cell topography during prenatal development. Science 236, 848–851.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, 185–194.CrossRefGoogle Scholar
Mann, I. (1964). The Development of the Human Eye. New York: Grune and Stratton.Google Scholar
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, 87–93.CrossRefGoogle ScholarPubMed
Maslim, J., Webster, M. & Stone, J. (1986). Stages in the structural differentiation of retinal ganglion cells. Journal of Comparative Neurology 254, 382–402.CrossRefGoogle ScholarPubMed
Mastronarde, D.N., Thibeault, M.A. & Dubin, M.W. (1984). Nonuniform postnatal growth of the cat retina. Journal of Comparative Neurology 228, 598–608.CrossRefGoogle ScholarPubMed
Morest, D.K. (1970). A study of neurogenesis in the forebrain of opossum pouch young. Zeitschrift Anatomie Entwicklungsgesch 130, 265–305.CrossRefGoogle ScholarPubMed
Nishimura, Y. & Rakic, P. (1985). Development of the Rhesus monkey retina: I. Emergence of the inner plexiform layer and its synapsis. Journal of Comparative Neurology 241, 420–434.Google Scholar
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, 290–313.CrossRefGoogle Scholar
Packer, O., Hendrickson, A.E. & Curcio, C.A. (1990). Development redistribution of photoreceptors across the Macaca nemestrina (Pigtail Macaque) retina. Journal of Comparative Neurology 298, 472–493.CrossRefGoogle ScholarPubMed
Perry, V.H. & Linden, R. (1982). Evidence for dendritic competition in the developing retina. Nature 297, 683.Google Scholar
Polyak, S.L. (1941). The Retina. Chicago, Illinois: 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, 429–451.CrossRefGoogle ScholarPubMed
Rakic, P. (1971). Guidance of neurons migrating to fetal monkey neocortex. Brain Research 33, 471–476.CrossRefGoogle ScholarPubMed
Rakic, P. (1972). Mode of cell migration to the superficial layers of the fetal monkey neocortex. Journal of Comparative Neurology 145, 61–84.CrossRefGoogle Scholar
Rakic, P. (1976). Prenatal genesis of connections subserving ocular dominance in the Rhesus monkey. Nature 261, 467–471.CrossRefGoogle ScholarPubMed
Rakic, P. & Riley, K.P. (1983). Overproduction and elimination of retinal axons in the fetal Rhesus monkey. Science 219, 1441–1444.Google Scholar
Ramoa, A.S., Campbell, G. & Shatz, C.J. (1987). Transient morphological features of identified ganglion cells in living fetal and neonatal retina. Science 237, 522–525.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, 4239–4261.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, 273–279.CrossRefGoogle Scholar
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
Robinson, S.R. (1987). Ontogeny of the area centralis in the cat. Journal of Comparative Neurology 255, 50–67.CrossRefGoogle ScholarPubMed
Robinson, S.R., Dreher, B. & McCall, M.J. (1989). Nonuniform retinal expansion during the formation of the rabbit's visual streak: Implications for the ontogeny of mammalian retinal topography. Visual Neuroscience 2, 201–219.Google Scholar
Rodieck, R.W. (1973). The Vertebate Retina: Principles of Structure and Function. San Francisco, California: Freeman Press.Google Scholar
Rodieck, R.W. (1979). Visual pathways. Annual Review of Neuroscience 2, 193–225.CrossRefGoogle ScholarPubMed
Rodieck, R.W. (1988). The primate retina. Comparative Primate Biology (Neurosciences) 4, 203–278.Google Scholar
Smelser, G.K., Ozanics, V., Rayborn, M. & Sagun, D. (1974). Retinal synaptogenesis in primate. Investigative Ophthalmology 13, 340–361.Google ScholarPubMed
Spira, A.W. & Hollenberg, M.J. (1973). Human retinal development: Ultrastructure of the inner retinal layers. Developmental Biology 31, 1–21.CrossRefGoogle ScholarPubMed
Steineke, T.C. & Kirby, M.A. (1989). Early axon outgrowth of ganglion cells in the retina of the Rhesus macaque. Investigative Ophthalmology and Visual Science (Suppl.) 30, 226.Google 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., Hollander, H. & Dreher, Z. (1991). “Sunbursts” in the inner plexiform layer: a spectacular feature of Miiller cells in the retina of the cat. Journal of Comparative Neurology 303, 400–411.CrossRefGoogle Scholar
Van Driel, D., Provis, J.M. & Billson, F.A. (1990). Early differentiation of ganglion, amacrine, bipolar, and Miiller cells in the developing fovea of the human retina. Journal of Comparative Neurology 291, 203–219.Google Scholar
Walls, G.L. (1942). The Vertebrate Eye and Its Adaptive Radiation. New York: Hafner.Google Scholar
Weale, R.A. (1966). Why does the human retina possess a fovea? Nature 212, 255–256.CrossRefGoogle ScholarPubMed
Wong, R.O.L. & Dunlop, S.A. (1988). Dendritic development of retinal ganglion cells in the marsupial Setonix brachyurus, quokka. Neuroscience Letters 30, S141.Google Scholar
Yuodelis, C. & Hendrickson, A.E. (1986). A qualitative and quantitative analysis of the human fovea during development. Vision Research 26, 847–855.Google Scholar