Hostname: page-component-586b7cd67f-rdxmf Total loading time: 0 Render date: 2024-11-23T19:40:32.289Z Has data issue: false hasContentIssue false
  • English
  • Français

The relative time course of axonal loss from the optic nerve of the developing guinea pig is consistent with that of other mammals

Published online by Cambridge University Press:  02 June 2009

Clair Langford  and
Ann Jervie Sefton
Clair Langford
Affiliation:
Department of Physiology, University of Sydney, NSW 2006, Australia
Ann Jervie Sefton
Affiliation:
Reprint requests to: Ann Sefton, Department of Physiology, University of Sydney, NSW 2006, Australia.
Get access Rights & Permissions [Opens in a new window]

Abstract

The relative timing of a number of events during the development of the visual system has recently been suggested to be consistent across a number of mammalian species (Dreher & Robinson, 1988). Some conflicting reports, however, had suggested that the precocial guinea pig might represent an exception to the generalized scheme. A quantitative study was thus carried out on the development of the optic nerve and retina of the guinea pig. Consistent with the prediction of a stable relative time course of mammalian visual development, axons and growth cones were found in the optic stalk from the 24th postconceptional day (40% of the period from conception to eye opening —the cecal period), the peak number of axons was observed on the 32nd postconceptional day (56% of the cecal period), and the phase of rapid axonal loss extended to the 39th and 42nd postconceptional days (68–74% of the cecal period). The number of axons in the adult optic nerve (117,000) represented about 37% of the peak number of axons. Additional observations indicated that during development of the optic nerve the mean axonal diameter increased approximately threefold from 0.31 μm to 1.06 μm. As in other mammals studied so far, myelination was first noted after the period of rapid axonal loss and continued until in the adult 97% of axons were found to be myelinated. In the retina, the presence of pyknotic profiles in the ganglion cell layers extends throughout the periods of loss of the optic nerve axons. Finally, the presence of pyknotic profiles in the amacrine sublayer suggest that in the guinea pig, as in other mammalian species, there is a loss of displaced amacrine cells as well as ganglion cells from the ganglion cell layer.

Keywords

Guinea pigOptic nerveCell deathRetinal ganglion cellsTiming
Type
Research Article
Information
Visual Neuroscience , Volume 9 , Issue 6 , December 1992 , pp. 555 - 564
Copyright
Copyright © Cambridge University Press 1992

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Beazley, L.D., Perry, V.H., Baker, B. & Darby, J.E. (1987). An investigation into the role of ganglion cells in the regulation of division and death of other retinal cells. Developmental Brain Research 33, 169–184.CrossRefGoogle Scholar
Bennett, M.R. (1983). Development of neuromuscular synapses. Physiological Reviews 63, 915–1048.CrossRefGoogle ScholarPubMed
Caley, D.W., Johnson, C. & Liebelt, R.A. (1972). The postnatal development of the retina in the normal and rodless CBS mouse: A light and electron microscope study. American Journal of Anatomy 133, 179–212.CrossRefGoogle Scholar
Carmichael, L. (1934). An experimental study in the prenatal guinea pig of the origin and development of reflexes and patterns of behaviour in relation to the stimulation of specific receptor areas during the period of active fetal life. Genetic Psychological Monographs 16, 337–491.Google Scholar
Clarke, P.G.H. (1985). Neuronal death in the development of the vertebrate nervous system. Trends in Neurosciences 8, 345–349.CrossRefGoogle Scholar
Cowan, W.M., Fawcett, J.W., O'leary, D.D.M. & Stanfield, B.B. (1984). Regressive events in neurogenesis. Science 225, 1258–1265.CrossRefGoogle ScholarPubMed
Crespo, D., O'leary, D.M. & Cowan, W.M. (1985). Changes in the numbers of optic nerve fibers during late prenatal and postnatal development in the albino rat. Developmental Brain Research 19, 129–134.CrossRefGoogle Scholar
Do-Nascimento, J.L.M., Do-Nascimento, R.S.V., Damascenco, B.A. & Silveira, L.C.L. (1991). The neurons of the retinal ganglion cell layer of the guinea-pig: Quantitative analysis of their distribution and size. Brazilian Journal of Medical and Biological Research 24, 199–214.Google ScholarPubMed
Dreher, B., Potts, R.A. & Bennett, M.R. (1983). Evidence that the early postnatal reduction in the number of rat retinal cells is due to a wave of ganglion cell death. Neuroscience Letters 36, 255–260.CrossRefGoogle ScholarPubMed
Dreher, B. & Robinson, S.R. (1988). Development of the retinofugal pathway in birds and mammals: Evidence for a common ‘timetable’. Brain Behaviour and Evolution 31, 369–390.CrossRefGoogle ScholarPubMed
Dreher, B. & Robinson, S.R. (1989). The development of the mammalian visual pathway: Similarities between species in the sequence and relative timing of events. In Seeing Contour and Colour, ed. Kulikowski, J., Dlckenson, C.M. & Murray, I.J., pp. 131–139. Oxford, England: Pergamon Press.Google Scholar
Finlay, B.L., Wikler, K.C. & Sengelaub, D.R. (1987). Regressive events in brain development and scenarios for vertebrate brain evolution. Brain, Behavior and Evolution 30, 102–117.CrossRefGoogle ScholarPubMed
Gaze, R.M. & Keating, M.J. (1972). The visual system and “neuronal specificity.” 237, 375–378.Google ScholarPubMed
Gould, S.J. (1977). Ontogeny and Phytogeny. Cambridge: Harvard University Press.Google Scholar
Graur, D., Hide, W.A. & Li, W.-H. (1991). Is the guinea pig a rodent? Nature 351, 649–652.CrossRefGoogle ScholarPubMed
Gunderson, H.J.G. (1977). Notes on the elimination of the numerical density of arbitrary profiles: The edge effect. Journal of Microscopy 111, 219–223.CrossRefGoogle Scholar
Guy, J., Ellis, E.A., Kelley, K. & Hope, G.M. (1989). Spectra of G ratio, myelin sheath thickness, and axon and fiber diameter in the guinea-pig optic nerve. Journal of Comparative Neurology 287, 446–454.CrossRefGoogle ScholarPubMed
Guy, J., Hope, G.M. & Rao, N.A. (1985). Ultrastructural and morphometric analysis of acute experimental allergic optic neuritis. Investigative Ophthalmology and Visual Science (Suppl.) 26, 30.Google Scholar
Hamburger, V. & Oppenheim, R.W. (1982). Naturally occurring neuronal death in vertebrates. Neuroscience Commentaries 1, 39–55.Google Scholar
Horsburgh, G.M. (1987). Cellular degeneration in the developing nervous system. Ph.D. Thesis, University of Sydney, Australia.Google Scholar
Horsburgh, G.M. & Sefton, A.J. (1987). Cellular degeneration and synaptogenesis in the developing retina of the rat. Journal of Comparative Neurology 263, 553–566.CrossRefGoogle ScholarPubMed
Klassen, H. & Lund, R.D. (1987). Retinal transplants can drive a pupillary reflex in host rat brains. Proceedings of the National Academy of Sciences of the U.S.A. 84, 6958–6960.CrossRefGoogle ScholarPubMed
Lam, K., Sefton, A.J. & Bennett, M.R. (1982). Loss of axons from the optic nerve of the rat during early postnatal development. Developmental Brain Research 3, 487–491.CrossRefGoogle Scholar
Langford, C. & Sefton, A.J. (1990). The time course of development and loss of optic nerve axons in the guinea-pig optic nerve follow the common mammalian pattern. Proceedings of the Australian Neuroscience Society 1, 98.Google Scholar
Ng, A.Y.K. & Stone, J. (1982). The optic nerve of the cat: Appearance and loss of axons during normal development. Developmental Brain Research 5, 263–271.CrossRefGoogle Scholar
Olney, J.W. (1968). An electron microscopic study of synapse formation, receptor outer segment development, and other aspects of developing mouse retina. Investigative Ophthalmology 1, 250–268.Google Scholar
Oppenheim, R.W. (1991). Cell death during development of the nervous system. Annual Review of Neuroscience 14, 453–501.CrossRefGoogle ScholarPubMed
Perry, V.H. (1981). Evidence for an amacrine cell system in the ganglion cell layer of the rat retina. Neuroscience 6, 931–944.CrossRefGoogle ScholarPubMed
Perry, V.H. (1989). Dendritic interactions between cell populations in the developing retina. In Development of the Vertebrate Retina, ed. Finlay, B.L. & Sengelaub, D.R., pp. 149–172. New York: Plenum Press.CrossRefGoogle Scholar
Perry, V.H., Henderson, Z. & Linden, R. (1983). Postnatal changes in retinal ganglion cell and optic axon populations in the pigmented rat. Journal of Comparative Neurology 219, 356–368.CrossRefGoogle ScholarPubMed
Peters, A., Palay, S.L. & Webster, H. De F. (1991). The Fine Structure of the Nervous System. New York: Oxford University Press.Google Scholar
Potts, R.A., Dreher, B. & Bennett, M.R. (1982). The loss of ganglion cells in the developing retina of the rat. Developmental Brain Research 3, 481–486.CrossRefGoogle Scholar
Provis, J.M. (1987). Patterns of cell death in the ganglion cell layer of the human fetal retina. Journal of Comparative Neurology 259, 237–246.CrossRefGoogle ScholarPubMed
Rager, G.H. (1980). Development of the retinotectal projection in the chicken. Advances in Anatomy, Embryology, and Cell Biology 63, 1–91.CrossRefGoogle ScholarPubMed
Rager, G.H. & Rager, U. (1978). Systems-matching by degeneration I. A quantitative electron microscopic study of the generation and degeneration of retinal ganglion cells in the chicken. Experimental Brain Research 33, 65–78.CrossRefGoogle Scholar
Rakic, P. & Riley, K.P. (1983). Overproduction and elimination of retinal axons in the fetal rhesus monkey. Science 219, 1441–1444.CrossRefGoogle ScholarPubMed
Rapaport, D.H., Robinson, S.R. & Stone, J. (1984). Cell movement and birth in the developing cat retina. In Development of Visual Pathways in Mammals, ed. Stone, J., Dreher, B. & Rapaport, D.H., pp. 23–38. New York: A. Liss.Google Scholar
Reynolds, D.G. & Rapaport, D.H. (1987). Organisation of the retinal ganglion cell layer of the adult guinea pig. Neuroscience Letters 27, S114.Google Scholar
Robinson, S. R. (1985). Cytogenesis and cell death during cat retinal development. Ph.D. Thesis, University of New South Wales, Sydney, Australia.Google Scholar
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. (1991). Development of the mammalian retina. In Neuroanatomy of the Visual Pathways and their Development, ed. Dreher, B. & Robinson, S.R., pp. 69–128. London: Macmillan Press.Google Scholar
Robinson, S.R. & Dreher, B. (1990). The visual pathways of eutherian mammals and marsupials develop according to a common timetable. Brain, Behavior and Evolution 36, 177–195.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
Rosen, M.G. & McLaughlin, A. (1966). Fetal and maternal electroencephalography in the guinea pig. Experimental Neurology 16, 181–190.CrossRefGoogle ScholarPubMed
Sedlacek, J. (1974). The significance of the perinatal period in the neural and behavioural development of precocial mammals. Studies on the development of behaviour and the nervous system. In Aspects of Neurogenesis: Vol. 2, ed. Gottlieb, H., pp. 245–273. New York: Academic Press.CrossRefGoogle Scholar
Sefton, A.J. & Lam, K. (1984). Quantitative and morphological studies on developing optic axons in normal and enucleated albino rats. Experimental Brain Research 57, 107–117.CrossRefGoogle ScholarPubMed
Sefton, A.J. & Lund, R.D. (1988). Cotransplantation of embryonic mouse retina with tectum, diencephalon, or cortex to neonatal rat cortex. Journal of Comparative Neurology 269, 548–564.CrossRefGoogle ScholarPubMed
Sengelaub, D.R. & Finlay, B.L. (1982). Cell death in the mammalian visual system during normal development: I. Retinal ganglion cells. Journal of Comparative Neurology 204, 311–317.CrossRefGoogle 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
Thoenen, H., Barde, Y.-A., Davies, A.M. & Johnson, J.E. (1987). Neurotrophic factors and neuronal death. In Selective Neuronal Death., ed. Bock, G. & O'conner, M., pp. 82–95. Chichester: Wiley.Google Scholar
Vietri, A.J. (1988). Developmental events leading to the cessation of cytogenesis in the mammalian retina. B.Sc. (Honours) Thesis, University of New South Wales, Sydney, Australia.Google Scholar
Weidman, T.A. & Kuwabara, T. (1968). Postnatal development of the rat retina: An electron microscopic study. Archives of Ophthalmology 79, 470–484.CrossRefGoogle ScholarPubMed
Weidman, T.A. & Kuwabara, T. (1969). Development of the rat retina. Investigative Ophthalmology 8, 60–69.Google ScholarPubMed
Williams, R.W., Bastiani, M.J., Lia, B. & Chalupa, L.M. (1986). Growth cones, dying axons, and developmental fluctuations in the fiber population of the cat's optic nerve. Journal of Comparative Neurology 246, 32–69.CrossRefGoogle ScholarPubMed
Wong, R.O.L. & Hughes, A. (1987a). The role of cell death in the topogenesis of neuronal distributions in the developing cat retinal ganglion cell layer. Journal of Comparative Neurology 262, 496–511.CrossRefGoogle ScholarPubMed
Wong, R.O.L. & Hughes, A. (1987b). Developing neuronal populations of the cat retinal ganglion cell layer. Journal of Comparative Neurology 262, 473–495.CrossRefGoogle ScholarPubMed
Young, R.W. (1984). Cell death during differentiation of the retina in the mouse. Journal of Comparative Neurology 229, 362–373.CrossRefGoogle ScholarPubMed