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Development of the rabbit retina

I. Size of eye and retina, and postnatal cell proliferation

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Measures of rabbit eyes and retinal whole-mounts were used to evaluate the development of retinal area and shape. The retina is shown to have a horizontal axis about a third longer than the vertical axis just before birth, and to adopt an almost symmetrical shape during postnatal development to adulthood. In general, retinal thickness is shown to decrease after birth, but differently in particular retinal regions: the reduction is marked in the periphery, and less pronounced in the visual streak. As an exception, the myelinated region — after it becomes really myelinated, from 9 days p.p. — even increases in thickness. In all regions of the retina, the absolute and relative thickness of the nuclear layers decreases, whereas the relative thickness of plexiform and fibrous layers increases. Proliferation of cells within the rabbit retina was studied during the first three postnatal weeks. 3H-thymidine incorporation was used to demonstrate DNA synthesis autoradiographically in histological sections as well as in enzymatically isolated retinal cells. A first proliferation phase occurs in the neuroblastic cell layer and ceases shortly after birth in the retinal center, but lasts for about one week in the retinal periphery. We found, however, a few 3H-thymidine-labeled cells as late as in the third postnatal week.

These late-labeled cells were found within the nerve fiber layer and in the inner plexiform layer. The latter cells were shown to express antigens detected by antibodies directed to the intermediate-sized filament protein vimentin, which are known to label Müller cells and neuroepithelial stem cells. This was confirmed in our preparation of enzymatically isolated cells; all cells with autoradiographically labeled nuclei revealed a characteristic elongated morphology typical for Müller radial glia (and also for early neuroepithelial stem cells). 3H-thymidine-labeled cells in the nerve fiber layer were most probably astrocytic. In analogy to the brain, we conclude that the mammalian retina undergoes a series of proliferation phases: first an early phase producing both neurons and glial cells, and then a late phase producing glial cells, e.g., in the nerve fiber layer. Most probably, the late phase within the inner nuclear layer is glial as well, i.e., consists of dividing Müller cells; it cannot be excluded, however, that there may remain some mitotically active stem cells.

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References

  • Anderson DH, Stern WH, Fisher SK, Erickson PA, Borgula GA (1983) Retinal detachment in the cat: the pigment epithelial- photoreceptor interface. Invest Ophthalmol Vis Sci 24:906–926

    Google Scholar 

  • Anderson DH, Guérin CJ, Erickson PA, Stern WH, Fisher SK (1986) Morphological recovery in the reattached retina. Invest Ophthalmol Vis Sci 27:168–183

    Google Scholar 

  • Beach DA, Jacobson M (1979) Patterns of cell proliferation in the retina of the clawed frog during development. J Comp Neurol 183:603–614

    Google Scholar 

  • Bennett GS (1987) Changes in intermediate filament composition during neurogenesis. In: Current Topics in Developmental Biology, Vol 21, Academic Press, New York, pp 151–183

    Google Scholar 

  • Blanks JC, Bok D (1977) An autoradiographic analysis of postnatal cell proliferation in the normal and degenerative mouse retina. J Comp Neurol 174:317–328

    Google Scholar 

  • Bulliman BT, Kuchel PW (1988) A series expression for the surface area of an ellipsoid and its application to the computation of the surface area of avian erythrocytes. J Theor Biol 134:113–123

    Google Scholar 

  • Erickson PA, Fisher SK, Anderson DH, Stern WH, Borgula GA (1983) Retinal detachment in the cat: the outer nuclear and outer plexiform layers. Invest Ophthalmol Vis Sci 24:927–942

    Google Scholar 

  • Fernald RD (1989) Retinal rod neurogenesis. In: Finlay BL, Sengelaub DR (eds) Development of the vertebrate retina, Plenum Press, New York London, pp 31–42

    Google Scholar 

  • Fernald RD, Johns P (1980) Retinal specialization and growth in the cichlid fish, H. burtoni. Am Zool 20:943

    Google Scholar 

  • Foresman GE, Cohen RJ, Das ND (1985) Ornithine decarboxylase in developing neonatal rabbit ocular tissue. Ophthalmic Res 17:262–265

    Google Scholar 

  • Greiner JV, Weidman TA (1982) Embryogenesis of the rabbit retina. Exp Eye Res 34:739–765

    Google Scholar 

  • Hollyfield JG (1972) Histogenesis of the retina in the killifish Fundulus heteroclitus. J Comp Neurol 144:373–380

    Google Scholar 

  • Holt CE, Bertsch TW, Ellis HM, Harris WA (1988) Cellular determination in the Xenopus retina is independent of lineage and birth date. Neuron 1:15–26

    Google Scholar 

  • Hughes A (1975) A quantitative analysis of the cat retinal ganglion cell topography. J Comp Neurol 163:107–128

    Google Scholar 

  • Johns PR (1977) Growth of the adult goldfish eye. III. Source of the new retinal cells. J Comp Neurol 176:343–358

    Google Scholar 

  • Kelling ST, Sengelaub DR, Wikler KC, Finlay BL (1989) Differential elasticity of the immature retina: a contribution to the development of the area centralis? Vis Neurosci 2:117–120

    Google Scholar 

  • Korr H (1982) Proliferation of different cell types in the brain of senile mice. Autoradiographic studies with 3H- and 14C-thymidine. Exp Brain Res [Suppl] 5:51–57

    Google Scholar 

  • Lemmon V, Rieser G (1983) The developmental distribution of vimentin in the chick retina. Dev Brain Res 11:191–197

    Google Scholar 

  • Mares V (1980) The time and space pattern of gliogensis, its morphogenetic significance and some regulatory aspects. In: Di-Bonadetta C et al. (eds) Multidisciplinary Approach to Brain Development, Elsevier, Amsterdam, pp 79–90

    Google Scholar 

  • Mastronarde DN, Thibeault MA, Dublin MW (1984) Non-uniform postnatal growth of the cat retina. J Comp Neurol 228:598–608

    Google Scholar 

  • McArdle CB, Dowling JE, Masland RH (1977) Development of outer segments and synapses in the rabbit retina. J Comp Neurol 175:253–278

    Google Scholar 

  • Mott JC (1965) Haemorrhage as a test of the function of the cardiovascular system in rabbits of different ages. J Physiol (Lond) 181:728–752

    Google Scholar 

  • Narang HK, Wisniewski HM (1977) The sequence of myelination in the epiretinal portion of the optic nerve in the rabbit. Neuropathol Appl Neurobiol 3:15–27

    Google Scholar 

  • Noell WK (1958) Differentiation, metabolic organization, and viability of the visual cells. Arch Opthalmol 60:702–733

    Google Scholar 

  • Rapaport DH, Robinson SR, Stone J (1984) Cell movement and birth in the developing cat retina. In: Development of Visual Pathways in Mammals, Alan R Liss, New York, pp 23–38

    Google Scholar 

  • Rapaport DH, Robinson SR, Stone J (1985) Cytogenesis in the developing retina of the cat. Austr New Zealand J Ophthalmol 13:113–124

    Google Scholar 

  • Reichenbach A (1987) Quantitative and qualitative morphology of rabbit retinal glia. A light microscopical study on cells both in situ and isolated by papaine. J Hirnforsch 28:213–220

    Google Scholar 

  • Reichenbach A (1989) Glia: neuron index: review and hypothesis to account for different values in various mammals. Glia 2:71–77

    Google Scholar 

  • Reichenbach A, Birkenmeyer G (1984) Preparation of isolated Müller cells of the mammalian (rabbit) retina. Z Mikrosk Anat Forsch 98:789–792

    Google Scholar 

  • Reichenbach A, Wohlrab F (1986) Morphometric parameters of Müller (glial) cells dependent on their topographic localization in the nonmyelinated part of the rabbit retina. A consideration of functional aspects of radial glia. J Neurocytol 15:451–459

    Google Scholar 

  • Reichenbach A, Reichelt W, Schumann R (1987) Use of Pappenheim's panoptic staining method on enzymatically isolated cells for demonstration of postnatal development of the rabbit retina. Z Mikrosk Anat Forsch 101:597–608

    Google Scholar 

  • Reichenbach A, Hagen E, Schippel K, Eberhardt W (1988) Quantitative electron microscopy of rabbit Müller (glial) cells in dependence of retinal topography. Z Mikrosk Anat Forsch 102:721–755

    Google Scholar 

  • Reichenbach A, Schnitzer J, Friedrich A, Knothe A-K, Henke A (1991a) Development of the rabbit retina. II. Müller cells. Submitted

  • Reichenbach A, Schnitzer J, Reichelt E, Fritzsche B, Friedrich A, Knothe A-K, Schober W, Timmermann A (1991b) Development of the rabbit retina. III. Differential growth and ganglion cell density. In preparation

  • Reichenbach A, Eberhardt W, Scheibe R, Deich C, Seidel B, Reichelt W, Dähnert K, Rödenbeck M (1991c) Development of the rabbit retina. IV. Tissue tensility and elasticity in dependence on topographic specializations. Exp Eye Res (in press)

  • Rentsch F (1973) Preretinal proliferation of glial cells after mechanical injury of the rabbit retina. Albr v Graefe's Arch Clin Exp Ophthalmol 188:79–90

    Google Scholar 

  • Robinson SR, Dreher B, McCall M (1989) Non-uniform retinal expansion during the formation of the rabbit's visual streak: implications for the ontogeny of mammalian retinal topography. Vis Neurosci 2:201–219

    Google Scholar 

  • Schimke RT (1959) Effects of prolonged light deprivation on the development of retinal enzymes in the rabbit. J Biol Chem 234:700–703

    Google Scholar 

  • Schnitzer J (1985) Distribution and immunoreactivity of glia in the retina of the rabbit. J Comp Neurol 240:128–142

    Google Scholar 

  • Schnitzer J (1988a) The development of astrocytes and blood vessels in the postnatal rabbit retina. J Neurocytol 17:433–449

    Google Scholar 

  • Schnitzer J (1988b) Astrocytes in the mammalian retina. In: Osborne N, Chader J (eds) Progress in retinal research, Pergamon Press, Oxford, pp 210–231

    Google Scholar 

  • Schnitzer J (1988c) Immunocytochemical studies on the development of astrocytes, Müller (glial) cells, and oligodendrocytes in the rabbit retina. Dev Brain Res 44:59–72

    Google Scholar 

  • Schnitzer J (1990) Postnatal gliogenesis in the nerve fiber layer of the rabbit retina: an autoradiographic study. J Comp Neurol 292:551–562

    Google Scholar 

  • Schnitzer J, Karschin A (1986) The shape and distribution of astrocytes in the retina of the adult rabbit. Cell Tissue Res 246:91–102

    Google Scholar 

  • Sidman RL (1961) Histogenesis of mouse retina studied with thymidine-H3. In: Smelser (ed) The Structure of the Eye, Academic Press, New York, pp 487–506

    Google Scholar 

  • Sternberger LA (1979) Immunocytochemistry, 2nd edn, John Wiley and Sons, New York

    Google Scholar 

  • Stone J (1981) The Whole Mount Handbook, Maitland, Sydney

  • Stone J, Egan M, Rapaport DH (1985) The site of commencement of retinal maturation in the rabbit. Vision Res 25:309–317

    Google Scholar 

  • Straznicky K, Gaze RM (1971) The growth of the retina in Xenopus laevis: an autoradiographic study. J Embryol Exp Morphol 26:67–79

    Google Scholar 

  • Tout S, Ashwell K, Stone J (1988) The development of astrocytes in the albino rabbit retina and their relationship to retinal vasculature. Neurosci Lett 90:241–247

    Google Scholar 

  • Turner DL, Cepko CL (1987) A common progenitor for neurons and glia persists in rat retina late in development. Nature (Lond) 328:131–136

    Google Scholar 

  • Uga S, Smelser GK (1973) Electron microscopic study of the development of retinal Müllerian cells. Invest Opthhalmol 12:295–307

    Google Scholar 

  • Wässle H, Levick WR, Cleland BG (1975) The distribution of the alpha type ganglion cells in the cat's retina. J Comp Neurol 159:419–437

    Google Scholar 

  • Wetts R, Fraser SE (1988) Multipotent precursors can give rise to all major cell types of the frog retina. Science 239:1142–1145

    Google Scholar 

  • Young RW (1983) The life history of retinal cells. Trans Am Ophthalmol Soc 81:193–228

    Google Scholar 

  • Young RW (1985) Cell differentiation in the retina of the mouse. Anat Rec 212:199–205

    CAS  PubMed  Google Scholar 

Download references

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Reichenbach, A., Schnitzer, J., Friedrich, A. et al. Development of the rabbit retina. Anat Embryol 183, 287–297 (1991). https://doi.org/10.1007/BF00192216

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