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Evidence of photoreceptor migration during early foveal development: A quantitative analysis of human fetal retinae

Published online by Cambridge University Press:  02 June 2009

Claudia Diaz Araya
Affiliation:
Department of Anatomy and Clinical Ophthalmology, University of Sydney, Australia
Jan M. Provis
Affiliation:
Department of Anatomy and Clinical Ophthalmology, University of Sydney, Australia

Abstract

We have analyzed aspects of photoreceptor topography in wholemounts of human fetal retinae in the age range 13–24 weeks of gestation. Fetal retinae were stained with cresyl violet and the sizes and packing densities of rods and cones analyzed in the conventional manner.

Cones and rods were present within a differentiating region, free of mitotic figures and approximately centered on the putative fovea, represented by the foveal cone mosaic. At 13 weeks of gestation the foveal cone mosaic was clearly differentiated, cone nuclei reaching a packing density of 14,200 per mm; a small number of rods were present in the immediately adjacent region. The packing densities of both rods and cones in these regions gradually increased and the area of the foveal cone mosaic gradually decreased throughout the age range sampled, although individual variations were evident. By 24 weeks of gestation, cone density was approximately 38,000 per mm in the foveal cone mosaic. The maximum rod density observed was 59,200 per mm in the region surrounding the foveal cone mosaic in a specimen of 20–21 weeks of gestation. In all specimens, maximum cone density occurred within the foveal cone mosaic and gradually declined towards the periphery of the differentiating region; a pronounced inverse relationship between cone soma diameter and packing density was also observed. The evidence strongly suggests that both rods and cones migrate centripetally, that is towards the center of the developing fovea, from early in development, possibly from the time that they first differentiate. The implications of these findings for fovealdevelopment are discussed.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1992

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References

Bach, L. & Seefelder, R. (1911, 1912, 1914). Arias zur Entwicklungs geschichte des menschlichen Auges. Parts 1–. Leipzig: W. Englemann.Google Scholar
Beazley, L.D. & Dunlop, S.A. (1983). The evolution of an area centralis and visual streak in the marsupial Setonix brachyurus. Journal of Comparative Neurology 216, 211231.CrossRefGoogle ScholarPubMed
Curcio, C.A.SloanK.R., Jr. K.R., Jr., Packer, O., Hendrickson, A.E. & Kalina, R.E. (1987). Distribution of cones in human and monkey retina: Individual variability and radial asymmetry. Science 236, 579582.CrossRefGoogle ScholarPubMed
Curcio, C.A., Sloan, K.R., Kalina, R.E. & Hendrickson, A.E. (1990). Human photoreceptor topography. Journal of Comparative Neurology 292, 497523.CrossRefGoogle ScholarPubMed
Dreher, B., Potts, R.A., Ni, S.Y.K. & Bennett, M.R. (1984). The development of heterogeneities in distribution and soma size of rat retinal ganglion cells. In Development of Visual Pathways in Mammals, ed. Stone, J., Dreher, B. & Rapaport, D.H., pp. 7588. New York: Alan R. Liss, Inc.Google Scholar
Hendrickson, A. & Kupfer, C. (1976). The histogenesis of the fovea in the macaque monkey. Investigative Ophthalmology 15, 746–756.Google ScholarPubMed
Hendrickson, A.E. & Yuodelis, C. (1984). The morphological development of the human fovea. Ophthalmology 91, 603612.CrossRefGoogle ScholarPubMed
Hollenberg, M.J. & Spira, A.W. (1972). Early development of the human retina. Canadian Journal of Ophthalmology 7, 472491.Google ScholarPubMed
Hollenberg, M.J. & Spira, A.W. (1973). Human retinal development: Ultrastructure of the outer retina. American Journal of Anatomy 137, 357386.CrossRefGoogle ScholarPubMed
Kitchen, W.H. (1968). The relationship between birth weight and gestational age in an Australian hospital population. Australian Paediatric Journal 4, 2937.Google Scholar
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. London: British Medical Association.Google Scholar
Østerberg, G.A. (1935). Topography of the layer of rods and cones in the human retina. Ada Ophthalmologica (Suppl. 6) 13, 197.Google Scholar
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
Polyak, S.L. (1941). The Retina. Chicago, Illinois. The University of Chicago Press.Google Scholar
Provis, J.M., Van Driel, D., Billson, F.A. & Russell, 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
Rapaport, D.H. & Stone, J. (1982). The site of commencement of maturation in mammalian retina: Observations in the cat. Developmental Brain Research 5, 273279.CrossRefGoogle Scholar
Rapaport, D.H. & Stone, J. (1983). Time course of morphological differentiation of cat retinal ganglion cells: Influences on soma size. Journal of Comparative Neurology 221, 4252.CrossRefGoogle ScholarPubMed
Rapaport, D.H. & Stone, J. (1984). The area centralis of the retina in the cat and other mammals: Focal point for function and development of the visual system. Neuroscience 11, 289301.CrossRefGoogle Scholar
Robinson, S.R. (1987). Ontogeny of the area centralis in the cat. Journal of Comparative Neurology 255, 5067.CrossRefGoogle ScholarPubMed
Robinson, S.R. (1991). Development of the mammalian retina. In Vision and Visual Dysfunction (series ed. Cronly-Dillon, J.R.), Vol. 3, Neuroanatomy of the Visual Pathways and Their Development, ed. Dreher, B. & Robinson, S.R., pp. 69128. London: MacMillan Press.Google Scholar
Spira, A.W. & Hollenberg, M.J. (1973). Human retinal development: Ultrastructure of the inner retinal layers. Developmental Biology 31, 121.CrossRefGoogle ScholarPubMed
Stone, J. (1981). The Wholemount Handbook. A Guide to the Preparation and Analysis of Retinal Wholemounts. Sydney, Australia: Maitland Publications.Google Scholar
Stone, J., Rapaport, D.H., Williams, R.W. & Chalupa, L. (1982). Uniformity of cell distribution in the ganglion cell layer of prenatal cat retina: Implications for mechanisms of retinal development. Developmental Brain Research 2, 231242.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 human retina. Journal of Comparative Neurology 291, 203219.CrossRefGoogle Scholar
Wässle, H., Levick, W.R. & Cleland, B.G. (1975). The distribution of the alpha type of ganglion cells in the cat's retina. Journal of Comparative Neurology 159, 419438.CrossRefGoogle ScholarPubMed
Yamada, E. & Ishikawa, T. (1965). Some observations on the submicroscopic morphogenesis of the human retina. In The Structure of the Eye: II. Symposium, ed. Rohen, J.W., pp. 516. Stuttgart: Schattauer-Verlag.Google Scholar
Yuodelis, C. & Hendrickson, A. (1986). A qualitative and quantitative analysis of the human fovea during development. Vision Research 26, 847855.CrossRefGoogle ScholarPubMed