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Shifting relationships between photoreceptors and pigment epithelial cells in monkey retina: Implications for the development of retinal topography

Published online by Cambridge University Press:  02 June 2009

S.R. Robinson
Affiliation:
Vision, Touch and Hearing Research Centre, University of Queensland, Brisbane, Australia
A. Hendrickson
Affiliation:
Departments of Biological Structure and Ophthalmology, University of Washington, Seattle

Abstract

This study examines the spatiotemporal relationships between retinal pigment epithelium (RPE) and photoreceptors (PR) during development of Macaca nemestrina retina. Our aim was to learn more about the developmental dynamics of these two important cell populations, particularly whether developmental changes in RPE cell densities mimic those of PR at selected retinal points. Twelve eyes ranging in age from 100 fetal days (Fd) to adulthood were flatmounted; the retinal perimeters were traced; and then sample punches were taken of the RPE and neural retina at the fovea, optic disc, mid- and far-nasal periphery, and far temporal, inferior and superior periphery. The two tissues were gently separated and the RPE cells and photoreceptors from the same region of the punch were counted using Nomarski contrast interference optics. We found that the total number of cones remains stable around 4 million between Fd100 and adulthood, but RPE number increases from 1.6 million at Fd100 to 2.56 million in adulthood. At the fovea, the core:RPE ratio increases from 5.4:1 at Fd100 to 28:1 by adulthood. In the temporal periphery by contrast, the cone:RPE ratio declines from 2.2:1 at Fd100–110 to less than 1:1 in the adult. In the vicinity of the optic disc, the ratio of (cones + rods): RPE remains around 35:1 throughout development, but in the retinal periphery it decreases to the adult value of 22:1. These changing ratios indicate that photoreceptors and RPE cells are redistributed independently during development, and that these two cellular sheets slide over one another to achieve their final distribution. This situation suggests that the forces or factors causing foveation are intrinsic to the neural retina.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1995

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References

Berson, E.L. (1994). Retinitis pigmentosa and allied diseases. In Principles and Practice of Ophthalmology, Vol. 2, ed. Albert, D.M. & Jakobiec, F.A., pp. 12141237. Philadelphia, Pennsylvania: W.B. Saunders.Google Scholar
Besharse, J. (1982). The daily light-dark cycle and rhythmic metabolism in the photoreceptor-pigment epithelial complex. In Progress in Retinal Research, Vol. 1, ed. Osborne, N. & Chader, G., pp. 81124. Oxford, England: Pergamon Press.Google Scholar
Bok, D. (1985). Retinal photoreceptor-pigment epithelium interactions. Investigative Ophthalmology and Visual Science 26, 16591694.Google 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
Bressler, S.B., Bressler, N.M. & Gragoudas, E.S. (1994). Age-related macular degeneration: Drusen and geographic atrophy. In Principles and Practice of Ophthalmology, Vol. 2, ed. Albert, D.M. & Jakobiec, F.A., pp. 826833. Philadelphia, Pennsylvania: W.B. Saunders.Google Scholar
Curcio, C.A., Sloan, K.R., Kalina, R.E. & Hendrickson, A.E. (1990). Human photoreceptor topography. Journal of Comparative Neurology 191, 497523.CrossRefGoogle Scholar
Curcio, C.A. & Hendrickson, A. (1991). Organization and development of the primate photoreceptor mosaic. In Progress in Retinal Research, Vol. 10, ed. Osborne, N.N. & Chader, G.J., pp. 89120. Oxford: Pergamon Press.Google Scholar
Curcio, C.A., Millican, C.L., Allen, K.A. & Kalina, R.E. (1993). Aging of the human photoreceptor mosaic: Evidence for selective vulnerability of rods in central retina. Investigative Ophthalmology and Visual Science 34, 32783296.Google ScholarPubMed
Diaz-Araya, C. & Provis, J.M. (1992). Evidence of photoreceptor migration during early foveal development: A quantitative analysis of fetal and adult human retinae. Visual Neuroscience 8, 505514.CrossRefGoogle Scholar
Dorey, C.K., Wu, G., Ebenstein, D., Garsd, A. & Weiter, J.J. (1989). Cell loss in the aging retina: Relationship to lipofuscin accumulation and macular degeneration. Investigative Ophthalmology and Visual Science 30, 16911699.Google ScholarPubMed
Dreher, B. & Robinson, S.R. (1988). Development of the retinofugal pathway in birds and mammals: Evidence for a common ‘timetable’. Brain, Behavior, and Evolution 31, 369390.Google ScholarPubMed
Gao, H. & Hollyfield, J.G. (1992). Aging of the human retina. Investigative Ophthalmology and Visual Science 33, 117.Google ScholarPubMed
Hendrickson, A. & Kupfer, C. (1976). The histogenesis of the fovea in the macaque monkey. Investigative Ophthalmology 15, 746756.Google ScholarPubMed
Hendrickson, A. (1992). A morphological comparison of foveal development in man and monkey. Eye 6, 136144.CrossRefGoogle ScholarPubMed
Hendrickson, A. (1994). The morphologic development of human and monkey retina. In Principles and Practice of Ophthalmology, Basic Sciences, ed. Albert, D.M. & Jakobiec, F.A., pp. 561577. Philadelphia, Pennsylvania: W.B. Saunders.Google Scholar
Hollenberg, M.J. & Spira, A.W. (1972). Human retina development: Ultrastructure of the outer retina. American Journal of Anatomy 137, 357386.CrossRefGoogle Scholar
Kiely, P.M., Crewther, S.G., Nathan, J., Brennan, N.A., Efron, N. & Madigan, M.A. (1987). Comparison of ocular development of cynomolgus monkey and man. Clinical Vision Science 1, 269280.Google Scholar
La Vail, M.M., Rapaport, D.H. & Rakic, P. (1991). Cytogenesis in the monkey retina. Journal of Comparative Neurology 309, 86114.CrossRefGoogle ScholarPubMed
Lia, B. & Chalupa, L.M. (1988). Prenatal development of regional specialization in the infant primate retina. Investigative Ophthalmology and Visual Science (Suppl.) 29, 378.Google Scholar
Lin, T., Grimes, P.A. & Stone, R.A. (1993). Expansion of the retinal pigment epithelium in experimental myopia. Vision Research 33, 18811885.CrossRefGoogle ScholarPubMed
Linberg, K.A. & Fisher, S.K. (1990). A burst of differentiation in the outer posterior retina of the eleven-week human fetus: An ultrastructural study. Visual Neuroscience 5, 4360.CrossRefGoogle ScholarPubMed
Mann, I. (1964). The Development of the Human Eye. 3rd ed.New York: Grune and Stratton.Google Scholar
Mastronarde, D.N., Thibeault, M.A. & Dubin, M.W. (1984). Nonuniform postnatal growth of the cat retina. Journal of Comparative Neurology 228, 598608.CrossRefGoogle ScholarPubMed
Newsome, D.A., Miceli, M.A., Liles, M.R., Tate, D.J. & Oliver, P.D. (1994). Antioxidants in the retinal pigment epithelium. Progress in Retinal Research 13, 101123.CrossRefGoogle Scholar
Okada, M., Erickson, A. & Hendrickson, A. (1994). Light and electron microscopy analysis of synaptic development in Macaca monkey retina as detected by immunocytochemical labeling for the synaptic vesicle protein, SV2. Journal of Comparative Neurology 339, 535558.CrossRefGoogle ScholarPubMed
Østerberg, G.A. (1935). Topography of the layer of rods and cones in the human retina. Acta Ophthalmology (Copenhagen) (Suppl. 6) 13, 1103.Google Scholar
Packer, O., Hendrickson, A.E. & Curcio, C.A. (1989). Photoreceptor topography of the adult pigtail macaque (Macaca nemestrina) retina. Journal of Comparative Neurology 288, 165183.CrossRefGoogle ScholarPubMed
Packer, O., Hendrickson, A.E. & Curcio, C.A. (1990). Developmental redistribution of photoreceptors across the Macaca nemestrina (pigtail macaque) retina. Journal of Comparative Neurology 298, 472493.CrossRefGoogle Scholar
Rapaport, D.H., Yasumura, D., LaVail, M.M. & Rakic, P. (1987). Cytogenesis of monkey retina: Comparison of the generation of retinal pigment epithelium and neural retina. Society of Neuroscience Abstracts 13, 238.Google Scholar
Robb, R.M. (1983). Increase in retinal surface area during infancy and childhood. Journal of Pediatric Ophthalmology and Strabismus 19, 1620.CrossRefGoogle Scholar
Robb, R.M. (1985). Regional changes in retinal pigment epithelial cell density during ocular development. Investigative Ophthalmology and Visual Science 26, 614620.Google ScholarPubMed
Robinson, S.R. (1988). Cell death in the inner and outer nuclear layers of the developing cat retina. Journal of Comparative Neurology 267, 507515.CrossRefGoogle ScholarPubMed
Robinson, S.R. (1991). Development of the mammalian retina. In Vision and Visual Dysfunction, ed. Dreher, B. & Robinson, S.R., Neuro-anatomyofthe Visual Pathways and Their Development, series ed. Cronly-Dillon, J.R., Vol. 3, pp. 69128. London: Macmillan.Google Scholar
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, 201219.CrossRefGoogle ScholarPubMed
Robinson, S.R. & Hendrickson, A. (1994 a). Photoreceptors slide against the pigment epithelium during retinal development in monkeys. Proceedings of the Australian Neuroscience Society 5, 119.Google Scholar
Robinson, S.R. & Hendrickson, A. (1994 b). Shearing between photo-receptors and the retinal pigment epithelium in retinae of developing monkeys. Investigative Ophthalmology and Visual Science (Suppl.) 35, 1728.Google Scholar
Rodieck, R.W. (1988). The primate retina. In Comparative Primate Biology, Vol. 4, ed. Steklis, H.D. & Erwin, J., pp. 203278. New York: Alan R Liss.Google Scholar
Samorajski, T., Keefe, J.R. & Ordy, J.M. (1965). Morphogenesis of photoreceptor and retinal ultrastructure in a subhuman primate. Vision Research 5, 639648.CrossRefGoogle Scholar
Steinberg, R.H. (1985). Interactions between the retinal pigment epithelium and the neural retina. Documenta Ophthatmologica 60, 327336.CrossRefGoogle ScholarPubMed
Steineke, T.C. & Kirby, M.A. (1993). Early axon outgrowth of retinal ganglion cells in the retina of the rhesus macaque. Developmental Brain Research 74, 151162.CrossRefGoogle ScholarPubMed
Streeten, B.W. (1969). Development of the human retinal pigment epithelium and the posterior segment. Archives of Ophthalmology 81, 383394.CrossRefGoogle ScholarPubMed
Stroeva, O.G. & Panova, I.G. (1983). Retinal pigment epithelium: Pattern of proliferative activity and its regulation by intraocular pressure in postnatal rats. Journal of Embryology and Experimental Morphology 75, 271291.Google ScholarPubMed
Ts'o, M.O.M. & Friedman, E. (1968). The retinal pigment epithelium. III. Growth and development. Archives of Ophthalmology 80, 214216.CrossRefGoogle Scholar
Van Alphen, G.W.H.M. (1990). Emmetropization in the primate eye. In Myopia and the Control of Eye Growth, ed. Bock, G. & Widdows, K., Ciba Foundation Symposium #155, pp. 115125. Chichester, England: Wiley & Sons.Google Scholar
Wallman, J. (1990). Retinal influences on sclera underlie visual deprivation myopia. In Myopia and the Control of Eye Growth, ed. Bock, G. & Widdows, K., Ciba Foundation Symposium #155, pp. 126141. Chichester, England: John Wiley & Sons.Google ScholarPubMed
Wallman, J. (1993). Retinal control of eye growth and refraction. In Progress in Retinal Research, Vol. 12, ed. Osborne, N.N. & Chader, G.J., pp. 134153. Oxford: Pergamon Press.Google Scholar
Watzke, R.C., Soldevilla, J.D. & Trune, D.R. (1993). Morphometric analysis of human retinal pigment epithelium: Correlation with age and location. Current Eye Research 12, 133142.CrossRefGoogle ScholarPubMed
Yuodelis, C. & Hendrickson, A. (1986). A qualitative and quantitative analysis of the human fovea during development. Vision Research 26, 847856.CrossRefGoogle ScholarPubMed
Young, R.W. (1971). The renewal of rod and cone outer segments in the rhesus monkey. Journal of Cell Biology 49, 303318.CrossRefGoogle ScholarPubMed