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Survival of ganglion cells which form the retino-retinal projection during optic nerve regeneration in the frog

Published online by Cambridge University Press:  02 June 2009

M. Tennant ,
S. R. Bruce  and
L. D. Beazley
M. Tennant
Affiliation:
Department of Psychology, University of Western Australia
S. R. Bruce
Affiliation:
Department of Psychology, University of Western Australia
L. D. Beazley
Affiliation:
Department of Psychology, University of Western Australia
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Abstract

During optic nerve regeneration in the frog, axons transiently grow along the opposite optic nerve forming a retino-retinal projection. In the present study, we crushed the left optic nerve in the frog Litoria (Hyla) moorei and later applied horseradish peroxidase (HRP) or diamidino yellow (DY) to the right optic nerve. In one series, retinae were examined 3 days after application of the tracer. The retino-retinal projection was found to be maximal at 5 weeks, fell significantly by 7 weeks, and returned to close-to-normal levels by 24 weeks. In a second series, we applied DY at 5 weeks as before but did not sacrifice the frogs until 7 weeks. Numbers of labeled ganglion cells were not significantly different from those frogs in the first series labeled and examined at 5 weeks. We conclude that ganglion cells giving rise to the retino-retinal projection had not died in appreciable numbers, presumably being sustained by collateral axons in the brain.

Keywords

FrogOptic nerve regenerationRetino-retinal projection
Type
Research Articles
Information
Visual Neuroscience , Volume 10 , Issue 4 , July 1993 , pp. 681 - 686
Copyright
Copyright © Cambridge University Press 1993

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References

Beazley, L.D. (1981). Retinal ganglion cell death and regeneration of abnormal retinotectal projections after removal of a segment of optic nerve in Xenopus tadpoles. Developmental Biology 85, 164–170.CrossRefGoogle ScholarPubMed
Beazley, L.D. & Darby, J.E. (1993). A second episode of ganglion cell death takes place when an optic nerve regenerates a second time in the frog. Visual Neuroscience 10, 297–301.CrossRefGoogle ScholarPubMed
Beazley, L.D. (1984). Formation of specific nerve connections in the visual system of lower vertebrates. In Current Topics in Research in Synapses, Vol. 1, ed. Jones, D.G., pp. 55–117. New York: Liss.Google Scholar
Beazley, L.D., Darby, J.E. & Perry, V.H. (1986). Cell death in the retinal ganglion cell layer during optic nerve regeneration for the frog Rana pipiens Vision Research 26, 543–556.CrossRefGoogle ScholarPubMed
Becker, D.L. & Cook, J.E. (1988). Divergent axon collaterals in the regenerating goldfish optic tract: A fluorescence double-label study. Development 104, 317–320.CrossRefGoogle ScholarPubMed
Bhide, P.G. & Frost, D.O. (1991). Stages of growth of hamster retinofugal axons: Implications for developing axonal pathways with multiple targets. Journal of Neuroscience 11, 485–504.CrossRefGoogle ScholarPubMed
Bohn, R.C. & Stelzner, D.J. (1979). Aberrant retino-retinal pathway during early stages of regeneration in adult Rana pipiens Brain Research 160, 139–144.CrossRefGoogle ScholarPubMed
Bohn, R.C. & Stelzner, D.J. (1981 a). The aberrant retino-retinal projection during optic nerve regeneration in the frog. I. Time course of formation and cells of origin. Journal of Comparative Neurology 196, 605–620.CrossRefGoogle ScholarPubMed
Bohn, R.C. & Stelzner, D.J. (1981 b). The aberrant retino-retinal projection during optic nerve regeneration in the frog. II. Anterograde labeling with horseradish peroxidase. Journal of Comparative Neurology 196, 621–632.CrossRefGoogle ScholarPubMed
Bohn, R.C. & Stelzner, D.J. (1981 c). The aberrant retino-retinal projection during optic nerve regeneration in the frog. III. Effects of crushing both nerves. Journal of Comparative Neurology 196, 633–643.CrossRefGoogle ScholarPubMed
Braekevelt, C.R., Beazley, L.D., Dunlop, S.A. & Darby, J.E. (1985). Numbers of axons in the optic nerve and of retinal ganglion cells during development in the marsupial Setonix brachyurus Developmental Brain Research 25, 117–125.CrossRefGoogle Scholar
Bunt, S.M. & Lund, R.D. (1981). Development of a transient retinoretinal pathway in hooded and albino rats. Brain Research 211, 399–404.CrossRefGoogle ScholarPubMed
Crespo, D., O’Leary, D.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
Dunlop, S.A. & Beazley, L.D. (1986). A retino-retinal projection contributes minimally towards high axon numbers in the marsupial Setonix brachyurus Neuroscience Abstracts 12, 34·12.Google Scholar
Dunlop, S.A. & Beazley, L.D. (1987). The number and distribution of dying cells in the developing ganglion cell layer of the marsupial Setonix brachyurus. Journal of Comparative Neurology 264, 14–23.CrossRefGoogle Scholar
Dunlop, S.A., Fraley, S.M. & Beazley, L.D. (1992 a). The morphology of developing and regenerating retinal ganglion cells. In The Formation and Regeneration of Nerve Connections, ed. Sharma, S.C., Chap. 12, pp. 148–161. Boston, Massachusetts: Birkhauser.Google Scholar
Dunlop, S.A., Humphrey, M.F. & Beazley, L.D. (1992 b). Displaced ganglion cells in normal frogs and those with regenerated optic nerves. Anatomy and Embryology 185, 431–438.CrossRefGoogle ScholarPubMed
Frost, D.O. (1984). Axonal growth and target selection during development: Retinal projections to the ventrobasal complex and other “nonvisual” structures in neonatal Syrian hamsters. Journal of Comparative Neurology 230, 576–592.CrossRefGoogle Scholar
Gaze, R.M. (1970). Formation of Nerve Connections. New York: Academic Press.Google Scholar
Harvey, A.R., Robertson, D. & Cole, K.S. (1990). Direct visualization of death of neurones projecting to specific targets in the developing rat brain. Experimental Brain Research 80, 213–217.CrossRefGoogle ScholarPubMed
Humphrey, M.F. (1985). The formation of nerve connections between the eye and the brain during optic nerve regeneration in the frog Hyla moorei. Ph.D. Thesis, University of Western Australia.Google Scholar
Humphrey, M.F. & Beazley, L.D. (1985). Retinal ganglion cell death during optic nerve regeneration in the frog Hyla moorei. Journal of Comparative Neurology 236, 382–402.CrossRefGoogle ScholarPubMed
Jacobson, M. (1991). Developmental Neurobiology. New York: Plenum Press.CrossRefGoogle Scholar
Jhaveri, S. & Morest, K. (1982). Sequential alterations of neuronal architecture in nucleus magnocellularis of the developing chicken: An electron-microscopic study. Neuroscience 4, 855–870.CrossRefGoogle Scholar
Kirby, M.A., Lia, B. & Chalupa, L.M. (1988). Retino-retinal projections in the foetal cat. Investigative Ophthalmology and Visual Science 29, 206.Google Scholar
Malmgren, L. & Olsson, Y.A. (1978). A sensitive method for histochemical identification of HRP in neurons following retrograde axonal transport. Brain Research 148, 279–294.CrossRefGoogle ScholarPubMed
McLoon, S.C. & Lund, R.D. (1982). Transient retinofugal pathways in the chick. Experimental Brain Research 45, 277–284.Google ScholarPubMed
Murray, M., Sharma, S.C. & Edwards, M.E. (1982). Target regulation of synaptic number in the compressed retinotectal projection of the goldfish. Journal of Comparative Neurology 209, 374–385.CrossRefGoogle ScholarPubMed
Perry, V.H. & Cowey, A. (1984). Retinal ganglion cells that project to the superior colliculus and pretectum in the Macaque monkey. Neuroscience 12, 1101–1123.CrossRefGoogle Scholar
Rager, G. & 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, 165–176.Google Scholar
Scalia, F., Arango, V. & Singman, E.L. (1985). Loss and displacement of ganglion cells after optic nerve regeneration in adult Rana pipiens Brain Research 344, 267–280.CrossRefGoogle ScholarPubMed
Schneider, G.E., Jhaveri, S. & Davis, W.F. (1987). On the development of neuronal arbors. In Developmental Neurobiology of Mam-mals, ed. Chagas, C. & Linden, R., pp. 31–64. Vatican City: The Pontifical Academy of Sciences.Google Scholar
Schulz, M., Raju, T., Ralston, G. & Bennett, M.R. (1990). A retinal ganglion cell neurotrophic factor purified from the superior colliculus. Journal of Neurochemistry 55, 832–841.CrossRefGoogle ScholarPubMed
Sheard, P.W. & Beazley, L.D. (1988). Retinal ganglion cell death is not prevented by application of tetrodotoxin during optic nerve regeneration for the frog Hyla moorei. Vision Research 28, 461–470.CrossRefGoogle Scholar
Sperry, R.W. (1951). Mechanisms of neural maturation. In Handbook of Experimental Psychology, ed. Stevens, S.S., pp. 236–280. New York: Wiley.Google Scholar
Stelzner, D.J. & Strauss, J.A. (1986). A quantitative analysis of frog optic nerve regeneration: Is retrograde ganglion cell death or collateral axonal loss related to selective reinnervation? Journal of Comparative Neurology 245, 83–106.CrossRefGoogle ScholarPubMed
Stelzner, D.J., Bohn, R.C. & Strauss, J.A. (1986). Regeneration of the frog optic nerve. Comparisons with development. Neurochemical Pathology 5, 255–288.CrossRefGoogle ScholarPubMed
Stone, J., Rapaport, D.H., Williams, R.W. & Chalupa, L.M. (1982). Uniformity of cell distribution in the ganglion cell layer of the prenatal cat: Implications for mechanisms of retinal development. Developmental Brain Research 2, 231–242.CrossRefGoogle Scholar
Straznicky, C. & Chehade, M. (1987). The formation of the area centralis of the retinal ganglion cell layer in the chick. Development 100, 411–420.CrossRefGoogle ScholarPubMed
Straznicky, C., McCart, R. & Toth, P. (1989). Retinal ganglion cell death induced by unilateral tectal ablation in Xenopus Visual Neuroscience 2, 339–347.CrossRefGoogle ScholarPubMed
Tennant, M., Bruce, S.R. & Beazley, L.D. (1993). Evidence for the long-term survival of retinal ganglion cells which form the transient retino-retinal projection during optic nerve regeneration in the frog Litoria moorei Proceedings of the Australian Neuroscience Society 4, 38.Google Scholar
Tennant, M., Masini, L.J., Darby, J.E. & Beazley, L.D. (1992). Dimensions of the lesion site influence the extent of retinal ganglion cell death during optic nerve regeneration in the frog Litoria (Hyla) moorei Proceedings of the Australian Neuroscience Society 3, 97.Google Scholar
Toth, P. & Straznicky, C. (1989). Retino-retinal projections in three Anuran species. Neuroscience Letters 104, 43–47.CrossRefGoogle ScholarPubMed
Usai, C., Ratto, G.M. & Bisti, S. (1991). Two systems of branching axons in monkey’s retina. Journal of Comparative Neurology 308, 149–161.CrossRefGoogle ScholarPubMed
Williams, R.W., Bastiani, M.J., Lia, B. & Chalupa, L.M. (1986). Growth cones, dying axons, and developmental fluctuations in the fibre population of the cat’s optic nerve. Journal of Comparative Neurology 246, 32–69.CrossRefGoogle ScholarPubMed