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A burst of differentiation in the outer posterior retina of the eleven-week human fetus: An ultrastructural study

Published online by Cambridge University Press:  02 June 2009

Kenneth A. Linberg  and
Steven K. Fisher
Kenneth A. Linberg
Affiliation:
Neuroscience Research Institute, University of California, Santa Barbara
Steven K. Fisher
Affiliation:
Neuroscience Research Institute and Department of Biological Sciences, University of California, Santa Barbara
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Abstract

Many studies on human retinal development have cited the third gestational month as a period when the posterior retina undergoes rapid differentiation and maturation, including a lining up of cone precursors. Ultrastructural data on the posterior retina during the third month are very limited, and totally lacking for the cone monolayer. We have examined two human fetal retinas between ten and 11 gestational weeks. Before the appearance of the cone monolayer, the outer neural retina consists of a homogeneous population of undifferentiated neuroblasts. Mitotic figures are still evident, even posteriorally. There is no outer plexiform layer (OPL). The interface of neural retina to retinal pigment epithelium (RPE) is largely featureless. By 11 weeks, the posterior retina has a thin OPL that separates the many rows of cells in the developing inner nuclear layer from the single tier of macular cone precursors. The RPE monolayer consists of cuboidal cells whose apical surface elaborates ridges of cytoplasm and branched processes that project into the subretinal space. The large, cuboidal cones are linked to each other and Müller cells at the outer limiting membrane. They show definitive signs of the structural polarity typical of vertebrate photoreceptors. Their apical cytoplasm contains many organelles common to the inner segment, while the basal cytoplasm has synaptic ribbons and vesicles, and receives invaginating contacts from processes in the OPL neuropil arising from differentiating second-order neurons. Lateral cone surfaces are mutually underlain by large subsurface cisterns.

Keywords

PhotoreceptorElectron microscopyDevelopmentMacular conesOuter nuclear layer
Type
Research Article
Information
Visual Neuroscience , Volume 5 , Issue 1 , July 1990 , pp. 43 - 60
Copyright
Copyright © Cambridge University Press 1990

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References

Anderson, D.H. & Fisher, S.K. (1979). The relationship of primate foveal cones to the pigment epithelium. Journal of Ultrastructure Research 67, 23–32.CrossRefGoogle Scholar
Barber, A.N. (1955). Embryology of the Human Eye. St. Louis, Missouri: Mosby.Google Scholar
Blanks, J.C., Adinolfi, A.M. & Lolley, R.N. (1974). Synaptogenesis in the photoreceptor terminal of the mouse retina. Journal of Comparative Neurology 156, 81–94.CrossRefGoogle ScholarPubMed
Burnside, B. & Laties, A.M. (1976). Actin filaments in apical projections of the primate pigmented epithelial cell. Investigative Ophthalmology 15, 570–575.Google ScholarPubMed
Cohen, A.I. (1963). The fine structure of the visual receptors of the pigeon. Experimental Eye Research 2, 88–97.CrossRefGoogle ScholarPubMed
Dowling, J.E. & Boycott, B.B. (1966). Organization of the primate retina: electron microscopy. Proceedings of the Royal Society B (London) 166, 80–111.Google ScholarPubMed
Duke-Elder, S. & Cook, C. (1963). In Systems of Ophthalmology. Vol. 3: Normal and Abnormal Development, Part I–Embryology, ed. Duke-Elder, S., London: Kimpton.Google Scholar
Fisher, S.K. & Goldman, K. (1975). Subsurface cisterns in the vertebrate retina. Cell and Tissue Research 164, 473–480.CrossRefGoogle ScholarPubMed
Fisher, S.K. & Linberg, K.A. (1975). Intercellular junctions in the early human embryonic retina. Journal of Ultrastructure Research 51, 69–78.CrossRefGoogle ScholarPubMed
Fisher, S.K. & Steinberg, R.H. (1982). Origin and organization of pigment epithelial apical projections to cones in cat retina. Journal of Comparative Neurology 206, 131–145.CrossRefGoogle ScholarPubMed
Greiner, J.V. & Weidman, T.A. (1980). Histogenesis of the cat retina. Experimental Eye Research 30, 439–453.CrossRefGoogle ScholarPubMed
Hendrickson, A. & Kupfer, C. (1976). The histogenesis of the fovea in the macaque monkey. Investigative Ophthalmology 15, 746–756.Google ScholarPubMed
Hendrickson, A.E. & Youdelis, C. (1984). The morphological development of the human fovea. Ophthalmology 91, 603–612.CrossRefGoogle ScholarPubMed
Hervouët, F. (1958).Développement normal de l'oeil et de ses annexes, I: Embryologie de la rétine. In L'Embryologie de L'Oeil et sa Tératologie, Chapter 3, ed. Dejean, C., Hervouët, F. & Leplat, G., pp. 53–170. Paris, France: Masson & Cie.Google Scholar
Hollenberg, M.J. & Spira, A.W. (1972). Early development of the human retina. Canadian Journal of Ophthalmology 7, 421–491.Google ScholarPubMed
Hollenberg, M.J. & Spira, A.W. (1973). Human retinal development: ultrastructure of the outer retina. American Journal of Anatomy 137, 357–386.CrossRefGoogle ScholarPubMed
Johnson, A.T., Kretzer, F.L., Hittner, H.M., Glazebrook, P.A., Bridges, C.D.B. & Lam, D.M.K. (1985). Development of the subretinal space in the preterm human eye: ultrastructural and immunocytochemical studies. Journal of Comparative Neurology 233, 497–505.CrossRefGoogle ScholarPubMed
Linberg, K.A. & Fisher, S.K. (1986). An ultrastructural study of interplexiform cell synapses in the human retina. Journal of Comparative Neurology 243, 561–576.CrossRefGoogle ScholarPubMed
Mann, I. (1969). The Development of the Human Eye, 3rd edition, New York: Grune and Stratton.Google Scholar
McArdle, C.B., Dowling, J.E. & Masland, R.H. (1977). Development of outer segments and synapses in the rabbit retina. Journal of Comparative Neurology 175, 253–273.CrossRefGoogle ScholarPubMed
Missotten, L. (1965). The Ultrastructure of the Human Retina. Bruxelles: Editions Arscia S.A.Google Scholar
Mund, M.L. & Rodrigues, M.M. (1979). Embryology of the human retinal pigment epithelium. In The Retinal Pigment Epithelium, ed. Zinn, K.M. & Marmor, M.F., pp. 45–54. Cambridge, Massachusetts: Harvard University Press.Google Scholar
Murray, R.L. & Dubin, M.W. (1975). The occurrence of actin-like filaments in association with migrating pigment granules in frog retinal pigment epithelium. Journal of Cell Biology 64, 705–710CrossRefGoogle Scholar
Nir, I., Cohen, D. & Papermaster, D.S. (1984). Immunocytochemical localization of opsin in the cell membrane of developing rat retinal photoreceptors. Journal of Cell Biology 98, 1788–1795.CrossRefGoogle ScholarPubMed
Olney, J.W. (1968). An electron-microscopic study of synapse formation, receptor outer segment development, and other aspects of developing mouse retina. Investigative Ophthalmology 7, 250–268.Google ScholarPubMed
O'Rahilly, R. (1966). The early development of the eye in staged human embryos. Contributions to Embryology (Carnegie Institution) 38, 1–42.Google Scholar
O'Rahilly, R. (1975). The prenatal development of the human eye. Experimental Eye Research 21, 93–112.CrossRefGoogle ScholarPubMed
Patten, B.M. (1953). Human Embryology. New York: McGraw-Hill.Google Scholar
Pfeffer, B.A. & Fisher, S.K. (1981). Development of retinal pigment epithelial surface structures ensheathing cone outer segments in the cat. Journal of Ultrastructure Research 76, 158–172.CrossRefGoogle ScholarPubMed
Polyak, S.L. (1941). The Retina. Chicago: 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, 429–451.CrossRefGoogle ScholarPubMed
Purves, D. & Lichtman, J.W. (1985). Principles of Neural Development. Sunderland, Massachusetts: Sinauer Associates, p. 149.Google Scholar
Rhodes, R.H. (1979). A light-microscopic study of the developing human neural retina. American Journal of Anatomy 154, 196–210.CrossRefGoogle ScholarPubMed
Rhodes, R.H. (1984). Ultrastructure of Müller cells in the developing human retina. Graefe's Archive for Clinical and Experimental Ophthalmology 221, 171–178.CrossRefGoogle ScholarPubMed
Smelser, G.K., Ozanics, V., Rayborn, M. & Sagun, D. (1974). Retinal synaptogenesis in the primate. Investigative Ophthalmology 13, 340–361.Google ScholarPubMed
Spira, A.W. (1975). In utero development and maturation of the retina of a non-primate mammal: a light- and electron-microscopic study of the guinea pig. Anatomy and Embryology 146, 279–300.CrossRefGoogle ScholarPubMed
Spira, A.W. & Hollenberg, M.J. (1973). Human retinal development: ultrastructure of the inner retinal layers. Developmental Biology 31, 1–21.CrossRefGoogle ScholarPubMed
Steinberg, R.H. (1986). Research update: report from a workshop on cell biology of retinal detachment. Experimental Eye Research 43, 695–706.CrossRefGoogle ScholarPubMed
Townes-Anderson, E. & Raviola, G. (1981). The formation and distribution of intercellular junctions in the rhesus monkey optic cup: the early development of the cilio-iridic and sensory retinas. Developmental Biology 85, 209–232.CrossRefGoogle ScholarPubMed
Vogel, M. (1978). Postnatal development of the cat's retina. Advances in Anatomy Embryology and Cell Biology 54, 1–66.Google ScholarPubMed
Vrabec, F. (1983). Early differentiation of the human retina. A neurohistological study. Graefe's Archive for Clinical and Experimental Ophthalmology 220, 47–52.CrossRefGoogle ScholarPubMed
Weidman, T.A. & Kuwabara, T. (1968). Postnatal development of the rat retina. An electron-microscopic study. Archives of Ophthalmology 79, 470–484.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. 5–16, Stuttgart: F.K. Schattauer-Verlag.Google Scholar
Youdelis, C. & Hendrickson, A. (1986). A qualitative and quantitative analysis of the human fovea during development. Vision Research 26, 847–855.CrossRefGoogle Scholar
Zinn, K.M. & Benjamin-Henkind, J.V. (1979). Anatomy of the human retinal pigment epitheium. In The Retinal Pigment Epithelium. ed. Zinn, K.M. & Marmor, M.F., pp. 3–31. Cambridge, Massachusetts: Harvard University Press.Google Scholar