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Retinal ganglion cell death induced by unilateral tectal ablation in Xenopus

Published online by Cambridge University Press:  02 June 2009

Charles Straznicky
Affiliation:
Department of Anatomy and Histology, School of Medicine, Flinders University of South Australia, Australia
Roger McCart
Affiliation:
Department of Anatomy and Histology, School of Medicine, Flinders University of South Australia, Australia
Pál Tóth
Affiliation:
Department of Anatomy and Histology, School of Medicine, Flinders University of South Australia, Australia

Abstract

The survival of retinal ganglion cells (GCs) in the left eye was studied on retinal wholemounts from 2–33 weeks after the surgical removal of the right tectum in juvenile Xenopus. Two to five weeks after tectal removal, about 76% of neurons of the retinal ganglion cell (GC) layer showed signs of retrograde degeneration: swelling of their somata and chromatolysis. Neurons that were not affected by the operation were taken to be either displaced amacrine cells (DAs) or GCs not projecting to the tectum. A portion of GCs showing retrograde degeneration became pyknotic and died within the period of 2–16 weeks after operation. Counts of surviving GCs 20–33 weeks after tectal removal amounted to about 55% of the corresponding neuron number in the right intact retina of the same animal. No discernible GC loss was observed in animals where only the optic fibers were cut at their entry point to the tectum indicating that axotomy alone, followed by rapid regrowth to the target, does not adversely influence the survival of GCs. In long-surviving animals, the left optic nerve was exposed to cobaltic-lysine complex and the position of filled optic axons within the brain determined. Optic axons whose tectal target had been removed were seen to cross over to the left intact tectum via the posterior and pretectal commissures. Aberrant projections were detected to the ipsilateral tectum and the diencephalic periventricular grey in addition to an increased projection to the accessory optic nucleus. It is concluded that the removal of the tectum, the main target of optic fiber projection, induces a very substantial GC death. Since only a portion of optic fibers were able to grow to alternative targets, the surviving GCs may have also included those with main projection areas to the diencephalic visual centers.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1989

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References

Adams, J.C. (1977). Technical considerations on the use of horseradish peroxidase as a neuronal marker. Neuroscience 2, 141145.CrossRefGoogle ScholarPubMed
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, 164170.CrossRefGoogle ScholarPubMed
Beazley, L.D., Darby, J.E. & Perry, V.H. (1985). Cell death in the retinal ganglion cell layer during optic nerve regeneration for the frog (Rana pipiens). Vision Research 26, 543556.CrossRefGoogle Scholar
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, 169184.CrossRefGoogle Scholar
Bohn, R.C. & Reier, P. J. (1985). Retrograde degeneration of myelinated axons and reorganization in the optic nerves of adult frogs (Xenopus laevis) following nerve injury or tectal ablation. Journal of Neurocytochemistry 14, 221244.Google ScholarPubMed
Cantore, W.A. & Scalia, F. (1987). Ultrastructural evidence of the formation of synapses by retinal ganglion cell axons in two nonstan-dard targets. Journal of Comparative Neurology 261, 137147.CrossRefGoogle Scholar
Dreher, B., Potts, R.A. & Bennett, M.R. (1983). Evidence that the early postnatal reduction in the number of rat retinal ganglion cells is due to a wave of ganglion cell death. Neuroscience Letters 36, 255260.CrossRefGoogle ScholarPubMed
Dunlop, S.A. & Beazley, L.D. (1984). A morphometric study of the retinal ganglion cell layer and optic nerve from metamorphosis in Xenopus laevis. Vision Research 24, 417427.CrossRefGoogle ScholarPubMed
Frank, B.D. & Hollyfield, J.G. (1987). Retinal ganglion cell morphology in the frog (Rana pipiens). Journal of Comparative Neurology 266, 413434.CrossRefGoogle ScholarPubMed
Gallyas, F. (1979). Light insensitive physical developer. Stain Technology 54, 173176.Google Scholar
Gaze, R.M. (1970). The Formation of Nerve Connections. London: Academic Press.Google Scholar
Hughes, W.F. & la Velle, A. (1975). The effects of early tectal lesions on development in the retinal ganglion cell layer of chick embryos. Journal of Comparative Neurology 163, 265284.Google Scholar
Hughes, W.F. & McLoon, S.C. (1979). Ganglion cell death during normal retinal development in the chick: comparisons with cell death induced by early target-field destruction. Experimental Neurology 66, 587601.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, 382402.CrossRefGoogle ScholarPubMed
Jenkins, S. & Straznicky, C. (1986). Naturally occurring and induced ganglion cell death: a wholemount autoradiographic study in Xenopus. Anatomy and Embryology 174, 5966.Google Scholar
Lázár, G. (1971). The projection of the retinal quadrants on the optic centres in the frog. A terminal degeneration study. Acta Morphologica Hungarica 19, 325334.Google ScholarPubMed
Lázár, G., TóTH, P., Csank, Gy. & Kickliter, E. (1983). Morphology and location of tectal projection neurons in frogs: a study with HRP and cobalt filling. Journal of Comparative Neurology 215, 108120.CrossRefGoogle ScholarPubMed
Levine, R.L. (1978). An autoradiographic analysis of the retinal projection in the frog (Xenopus laevis): new observations in an anuran visual projection. Brain Research 148, 202206.CrossRefGoogle Scholar
Maturana, H.R., Lettvin, J.Y., McCulloch, W.S. & Pitts, W.H. (1960). Anatomy and physiology of vision in the frog (Rana pipiens). Journal of General Physiology 43, Suppl. 2, 129175.CrossRefGoogle Scholar
McCaffery, C.A., Bennett, M.R. & Dreher, B. (1982). The survival of neonatal rat retinal ganglion cells in vitro is enhanced in the presence of appropriate parts of the brain. Experimental Brain Research 48, 377386.Google Scholar
Montgomery, N., Fite, K.V. & Bengston, L. (1981). The accessory optic system of Rana pipiens: neuroanatomical connections and intrinsic organization. Journal of Comparative Neurology 203, 595612.CrossRefGoogle ScholarPubMed
Montgomery, N., Fite, K.V. & Grigonis, A.M. (1985). The pretectal nucleus lentiformis mesencephali of Rana pipiens. Journal of Comparative Neurology 234, 595612.Google ScholarPubMed
Nurcombe, V. & Bennett, M.R. (1981). Embryonic chick retinal ganglion cells identified in vitro. Their survival is dependent on a factor from the optic tectum. Experimental Brain Research 44, 249258.CrossRefGoogle ScholarPubMed
Perry, V.H. & Cowey, A. (1979). The effects of unilateral cortical and tectal lesions on retinal ganglion cells in rats. Experimental Brain Research 35, 8595.Google Scholar
Perry, V.H. & Linden, R. (1982). Evidence for dendritic competition in the developing retina. Nature 297, 683685.CrossRefGoogle ScholarPubMed
Sakaguchi, D.S., Murphey, R.K., Hunt, R.K. & Tompkins, R. (1984). The development of retinal ganglion cells in a tetraploid strain of Xenopus laevis: a morphological study utilizing intracel-lular dye injection. Journal of Comparative Neurology 224, 231251.CrossRefGoogle Scholar
Scalia, F. (1976). The optic pathway of the frog: nuclear organization and connections. In Frog Neurobiology, ed. Llinas, R. & Precht, W., pp. 386406. Berlin: Springer Verlag.CrossRefGoogle Scholar
Scalia, F., Arango, V. & Singman, F.L. (1985). Loss and displacement of retinal ganglion cells after optic nerve regeneration in adult Rana pipiens. Brain Research 344, 267280.CrossRefGoogle ScholarPubMed
Schneider, G.E. (1973). Early lesions of superior colliculus: factors affecting the formation of abnormal retinal projections. Brain Behavior and Evolution 8, 73109.CrossRefGoogle ScholarPubMed
Sengelaub, D.R., Dolan, R.P. & Finley, B.L. (1986). Cell generation, death, and retinal growth in the development of the hamster retinal ganglion cell layer. Journal of Comparative Neurology 246, 527543.Google Scholar
Sharma, S.C. (1973). Anomalous retinal projection after removal of contralateral optic tectum in adult goldfish. Experimental Neurology 41, 661669.Google Scholar
Stirling, R.V. & Merrill, E.G. (1987). Functional morphology of frog retinal ganglion cells and their central projections: the dimming detectors. Journal of Comparative Neurology 258, 477495.Google Scholar
Straznicky, C. (1988 a). On the dendritic arbors of retinal ganglion cells. Proceedings of the Australian Physiological and Pharmacological Society 19, 3743.Google Scholar
Straznicky, C. (1988 b). Atrophy, regeneration, and hypertrophy of the dendritic field of large ganglion cells following optic nerve section in Xenopus. Neuroscience Letters (Suppl.) 30, S 132.Google Scholar
Straznicky, K. & Gaze, R.M. (1971). The growth of the retina in Xenopus laevis: an autoradiographic study. Journal of Embryology and Experimental Morphology 26, 6779.Google Scholar
Straznicky, C. & Glastonbury, J. (1979). Anomalous ipsilateral optic fiber projection in Xenopus induced by larval tectal ablation. Journal of Embryology and Experimental Morphology 50, 111122.Google Scholar
Straznicky, C. & Straznicky, I.T. (1988). Morphological classification of retinal ganglion cells in adult Xenopus laevis. Anatomy and Embryology 178, 143153.Google Scholar