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Quantitative aspects of synaptic ribbon formation in the outer plexiform layer of the developing cat retina

Published online by Cambridge University Press:  02 June 2009

David H. Rapaport
David H. Rapaport
Affiliation:
School of Anatomy, University of New South Wales, Sydney, Australia
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Abstract

The development of synaptic ribbons in rod and cone photoreceptor terminals of the cat retina was studied using quantitative electron microscopy. At the region of the area centralis, synaptic ribbon profiles are initially recognized at PCD (postconception day) 59. Synaptic ribbon density increases rapidly, reaching a peak of 0.55 ribbons/μm3 at PCD 68 (postnatal day 3) and maintains approximately that value for an additional 8 d. Following PCD 76, ribbon density begins to decrease, to 0.37 ribbons/μm3 at PCD 82 and 0.25 ribbons/μm3 at PCD 102. Although ribbon density drops by approximately 50% during this 39-d period, the outer plexiform layer (OPL) volume at the area centralis increases by about 20%. Ribbon density continues to decrease gradually over a protracted period to reach a final adult value of 0.11–0.14 ribbons/μm3. During the period of high ribbon density, rod spherules with two, or even three ribbon profiles, were routinely observed. In contrast, in the adult, spherules with more than one ribbon profile are only rarely encountered. During development, the length of synaptic ribbon profiles increases from a mean of 0.22 μm at PCD 62 to the 0.47 μm mean length found in the adult.

Keywords

RetinaSynaptic ribbonSynaptic lamellaSynaptogenesisSynapse elimination

Information

Type
Research Articles
Information
Visual Neuroscience , Volume 3 , Issue 1 , July 1989, pp. 21 - 32
Copyright
Copyright © Cambridge University Press 1989

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References

Abercrombie, M. (1946). Estimation of nuclear population from microtome sections. Anatomical Record 94, 239–247.CrossRefGoogle ScholarPubMed
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
Cragg, B.G. (1975 a). The development of synapses in the visual system of the cat. Journal of Comparative Neurology 160, 147–166.CrossRefGoogle ScholarPubMed
Cragg, B.G. (1975 b). The development of synapses in kitten visual cortex during visual deprivation. Experimental Neurology 46, 445–451.CrossRefGoogle ScholarPubMed
Dubin, M.W. (1970). The inner plexiform layer of the vertebrate retina: a quantitative and comparative electron microscopic analysis. Journal of Comparative Neurology 140, 479–506.CrossRefGoogle ScholarPubMed
Fisher, L.J. (1979 a). Development of synaptic arrays in the inner plexiform layer of neonatal mouse retina. Journal of Comparative Neurology 187, 359–372.CrossRefGoogle ScholarPubMed
Fisher, L.J. (1979 b). Development of retinal synaptic arrays in the inner plexiform layer of dark-reared mice. Journal of Embryology and Experimental Morphology 54, 219–227.Google ScholarPubMed
Gray, E.G. & Pease, H.L. (1971). On understanding the organization of the retinal receptor synapse. Brain Research 35, 1–15.CrossRefGoogle Scholar
Greiner, J.V. & Weidman, T.A. (1980). Histogenesis of the cat retina. Experimental Eye Research 30, 439–453.CrossRefGoogle ScholarPubMed
Grun, G. (1982). Development dynamics of synapses in the vertebrate retina. Progress in Neurobiology 18, 257–274.CrossRefGoogle ScholarPubMed
Holländer, H. & Stone, J. (1972). Receptor pedicle density in the cat's retina. Brain Research 42, 497–502.CrossRefGoogle ScholarPubMed
Karasek, M. (1983). Ultrastructure of the mammalian pineal gland: its comparative and functional aspects. In Pineal Research Reviews, ed. Reiter, R.J., pp. 1–48. New York: Alan R. Liss.Google Scholar
King, T.S. & Dougherty, W.J. (1980). Neonatal development of circadian rhythm in “synaptic” ribbon numbers in the rat pinealocyte. American Journal of Anatomy 157, 335–343.CrossRefGoogle ScholarPubMed
Mariani, J. (1983). Elimination of synapses during the development of the central nervous system. In Molecular and Cellular Interactions Underlying Higher Brain Functions, ed. Changeux, J.-P., Glowinski, J., Imbert, M. & Bloom, F.E., pp. 383–392. Amsterdam: Elsevier Science Publishers.Google Scholar
Maslim, J. & Stone, J. (1986). Synaptogenesis in the retina of the cat. Brain Research 373, 35–48.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
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, 253–274.CrossRefGoogle ScholarPubMed
McCartney, M.D. & Dickson, D.H. (1985). Photoreceptor synaptic ribbons: three-dimensional shape, orientation, and diurnal (non) variation. Experimental Eye Reseach 41, 313–321.CrossRefGoogle ScholarPubMed
McNulty, J.A., Fox, L., Taylor, D., Miller, M. & Takaoka, Y. (1986). Synaptic ribbon populations in the pineal gland of the rhesus monkey (Macaca mulatta). Cell and Tissue Research 243, 353–357.CrossRefGoogle ScholarPubMed
Morrison, J.D. (1982). Postnatal development of the area centralis of the kitten retina: an electron microscopic study. Journal of Anatomy 135, 255–271.Google 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 and Visual Science 7, 250–268.Google ScholarPubMed
Pevet, P. (1983). Anatomy of the pineal gland of mammals. In The Pineal Gland, ed. Relkin, R., pp. 1–75. New York, Amsterdam, Oxford: Elsevier.Google Scholar
Purves, D. & Lichtman, J.W. (1980). Elimination of synapses in the developing nervous system. Science 210, 153–157.CrossRefGoogle ScholarPubMed
Purves, D. & Lichtman, J.W. (1985). Principles of Neural Development, Sunderland, Massachusetts: Sinauer Associates Inc.Google Scholar
Rapaport, D.H. & Stone, J. (1982). The site of commencement of maturation in mammalian retina: observations in the cat. Developmental Brain Research 5, 273–279.CrossRefGoogle Scholar
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, 289–301.CrossRefGoogle 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. (1988). Cell death in the inner and outer nuclear layers of the developing cat retina. Journal of Comparative Neurology 267, 507–515.CrossRefGoogle ScholarPubMed
Robinson, S.R., Horsburgh, G.M., Dreher, B. & McCall, M.J. (1987). Changes in the numbers of retinal ganglion cells and optic nerve axons in the developing albino rabbit. Developmental Brain Research 35, 161–174.CrossRefGoogle Scholar
Smelser, G.K., Ozanics, V., Rayborn, M. & Sagun, D. (1974). Retinal synaptogenesis in the primate. Investigative Ophthalmology and Visual Science 13, 340–361.Google ScholarPubMed
Sobkowicz, H.M., Rose, J.E., Scott, G.L. & Levenick, C.V. (1986). Distribution of synaptic ribbons in the developing organ of Corti. Journal of Neurocytology 15, 693–714.CrossRefGoogle ScholarPubMed
Spadaro, A., DeSimone, I. & Puzzolo, D. (1978). Ultrastructural data and chronobiological patterns of the synaptic ribbons in the outer plexiform layer in the retina of albino rats. Acta Anatomica 102, 365–373.CrossRefGoogle ScholarPubMed
Steinberg, R.H., Reid, M. & Lacy, P.L. (1973). The distribution of rods and cones in the retina of the cat (Felis domesticus). Journal of Comparative Neurology 148, 229–248.CrossRefGoogle ScholarPubMed
Sterling, P. (1983). Microcircuitry of the cat retina. Annual Review of Neuroscience 6, 149–185.CrossRefGoogle ScholarPubMed
Stone, J. (1981). The Wholemount Handbook, Sydney: Maitland Publications Pty. Ltd.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, 231–242.CrossRefGoogle Scholar
Tieman, S.B. (1984). Effects of monocular deprivation on geniculocortical synapses in the cat. Journal of Comparative Neurology 222, 166–176.CrossRefGoogle ScholarPubMed
Vogel, M. (1978). Postnatal development of the cat's retina. Advances in Anatomy, Embryology, and Cell Biology 54, 1–66.Google ScholarPubMed
Vollrath, L. (1981). The pineal organ. In Handbuch der Mikroskopischen Anatomie des Menschen, ed. Oksche, A. & Vollrath, L., pp. 589–665. Berlin, Heidelberg, New York: Springer.Google Scholar
Williams, R.W. & Herrup, K. (1988). The control of neuron number. Annual Review of Neuroscience 11, 423–453.CrossRefGoogle ScholarPubMed
Zimmerman, R.P., Polley, E.H. & Fortney, R.L. (1988). Cell birthdays and rate of differentiation of ganglion and horizontal cells of the developing cat retina. Journal of Comparative Neurology 274, 77–90.CrossRefGoogle Scholar