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Retrograde degeneration of myelinated axons and re-organization in the optic nerves of adult frogs (Xenopus laevis) following nerve injury or tectal ablation

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Journal of Neurocytology

Summary

The optic nerve proximal to the lesion (toward the retina) was examined by light and electron microscopy in adultXenopus laevis after various types of injury to optic nerve fibres. Intraorbital resection, transection or crush of the optic nerve or ablation of the contralateral optic tectum all resulted in marked alterations in the myelinated axon population and in the overall appearance of the nerve proximal to the site of injury. Examination of the nerves from 3 days to 6 months postoperatively indicated that a progressive, retrograde degeneration of myelin and loss of large-diameter axons occurred throughout the retinal nerve stump regardless of the type of injury or distance of the injury from the retina. The retinal stump of nerves receiving resection or transection showed a nearly complete loss of myelin and large-diameter axons while the degree of degeneration was subtotal in nerves receiving crush injury or after lesions farther from the retina (i.e. tectal ablation). In addition, the entire retinal nerve stump after all types of injury was characterized by the appearance of an actively growing axon population situated circumferentially under the glia limitans. The latter fibres are believed to represent regrowing axons which are being added onto the nerve, external to the original axon population and are suspected to modify actively the glial terrain and glia limitans.

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References

  • Aguayo, A. J., Bray, G. M., Perkins, C. S. &Duncan, I. D. (1979) Axon-sheath cell interactions in peripheral and central nervous system transplants. InSociety for Neuroscience Symposium, Vol. 4 (edited byFerrendelli, J. A.), pp. 361–83. Bethesda, USA.

  • Aguayo, A. J., Dickson, R., Trecarten, J., Attiwell, M., Bray, G. &Richardson, P. (1978) Ensheathment and myelination of regenerating PNS fibers by transplanted optic nerve glia.Neuroscience Letters 9, 97–104.

    Google Scholar 

  • Aitken, J. T. &Thomas, P. K. (1962) Retrograde changes in fiber size following nerve section.Journal of Anatomy 96, 121–29.

    PubMed  Google Scholar 

  • Attardi, D. G. &Sperry, R. W. (1963) Preferential selection of central pathways by regenerating optic fibers.Experimental Neurology 7, 46–64.

    PubMed  Google Scholar 

  • Beazley, L. D. (1981) Retinal ganglion cell death and regeneration of abnormal retinotectal projections after removal of a segment of optic nerve inXenopus tadpoles.Developmental Biology 85, 164–70.

    PubMed  Google Scholar 

  • Bohn, R. C. &Palumbo, J. M. (1983) Retrograde myelin and axonal degeneration in the optic nerve after tectal ablation in adult frogs.Anatomical Record 205, 20A.

    Google Scholar 

  • Bohn, R. C. &Reier, P. J. (1981) Retrograde myelin and axonal degeneration after optic nerve transection in adult frogs.Anatomical Record 199, 30A.

    Google Scholar 

  • Bohn, R. C. &Reier, P. J. (1982) Anomalous axonal outgrowth at the retina caused by injury to the optic nerve or tectal ablation in adultXenopus.Journal of Neurocytology 11, 211–34.

    PubMed  Google Scholar 

  • Bohn, R. C., Reier, P. J. &Sourbeer, E. B. (1982) Axonal interactions with connective tissue and glial substrata during optic nerve regeneration inXenopus larvae and adults.American Journal of Anatomy 165, 397–419.

    PubMed  Google Scholar 

  • Cole, M. (1968) Retrograde degeneration of axon and soma in the nervous system. InThe Structure and Function of Nervous Tissue, Vol. 1 (edited byBourne, G. H.), pp. 269–300. New York: Academic Press.

    Google Scholar 

  • Constantine-Paton, M. &Capranica, R. R. (1976) Axonal guidance of developing optic nerve in the frog. I. Anatomy of the projection from transplanted eye primordia.Journal of Comparative Neurology 170, 17–32.

    PubMed  Google Scholar 

  • Cowey, A. &Perry, V. H. (1979) The projection of the temporal retina in rats studied by retrograde transport of horseradish peroxidase.Experimental Brain Research 35, 457–64.

    Google Scholar 

  • Cragg, B. G. &Thomas, P. K. (1961) Changes in conduction velocity and fibre size proximal to peripheral nerve lesions.Journal of Physiology (London)157, 315.

    Google Scholar 

  • Eayrs, J. T. (1952) Relationship between the ganglion cell layer of the retina and the optic nerve in the rat.British Journal of Ophthalmology 36, 453–9.

    PubMed  Google Scholar 

  • Egar, M. &Singer, M. (1972) The role of ependyma in spinal cord regeneration in the Urodele,Triturus.Experimental Neurology 37, 422–30.

    PubMed  Google Scholar 

  • Gaze, R. M. (1970)The Formation of Nerve Connections. New York: Academic Press.

    Google Scholar 

  • Gaze, R. M. &Grant, P. (1978) The diencephalic course of regenerating retino-tectal fibers inXenopus tadpoles.Journal of Embryology and Experimental Morphology 44, 201–16.

    PubMed  Google Scholar 

  • Goldberg, S. &Frank, B. (1980) Will central nervous system axons in the adult mammal regenerate after bypassing a lesion? A study in the mouse and chick visual systems.Experimental Neurology 70, 675–89.

    PubMed  Google Scholar 

  • Grafstein, B. (1971) The role of slow axonal transport in nerve regeneration.Acta Neuropathologica (Berlin), Suppl. V, 144–52.

    Google Scholar 

  • Grafstein, B. &Ingoglia, N. A. (1982) Intracranial transection of the optic nerve in adult mice: preliminary observations.Experimental Neurology 76, 318–30.

    PubMed  Google Scholar 

  • Grafstein, B. &Mcquarrie, I. (1978) Role of the nerve cell body in axonal regeneration. InNeuronal Plasticity (edited byCotman, C. W.), pp. 155–96. New York: Raven Press.

    Google Scholar 

  • Horder, T. J. &Martin, K. A. C. (1978) Morphogenetics as an alternative to chemospecificity in the formation of nerve connections. InCell-Cell Recognition (edited byCurtis, A. S. G.), pp. 275–358, Society for Experimental Biology Symposium, Vol. 32. Cambridge: Cambridge Univ. Press.

    Google Scholar 

  • Jacobson, M. (1978)Developmental Neurobiology, Second Edition. New York: Plenum Press.

    Google Scholar 

  • Lanners, H. N. &Grafstein, B. (1980) Early stages of axonal regeneration in the goldfish optic tract: an electron microscopic study.Journal of Neurocytology 9, 733–51.

    PubMed  Google Scholar 

  • Mantz, J. &Klein, M. (1951) Recherches experimentales sur la section et la ligature du nerf optique chez le rat.Comptes Rendus des Seances de la Societe' de Biologie 145, 920–4.

    Google Scholar 

  • Maturana, H. R. (1958) Efferent fibres in the optic nerve of the toad (Bufo bufo).Journal of Anatomy 92, 21–7.

    PubMed  Google Scholar 

  • Misantone, L., Barron, K., Gershenbaum, M., Cipolla, V., Zanakis, M. &Murray, M. (1981) Effect of optic nerve crush on retinal ganglion cells in hooded rats.Neuroscience Abstracts 7, 681.

    Google Scholar 

  • Muchnick, N. &Hibbard, E. (1980) Avian retinal ganglion cells resistant to degeneration after optic nerve lesion.Experimental Neurology 68, 205–16.

    PubMed  Google Scholar 

  • Murray, M. (1976) Regeneration of retinal axons into the goldfish optic tectum.Journal of Comparative Neurology 168, 175–96.

    PubMed  Google Scholar 

  • Murray, M. (1982) A quantitative study of regenerative sprouting by optic axons in goldfish.Journal of Comparative Neurology 209, 352–62.

    PubMed  Google Scholar 

  • Murray, M. &Edwards, M. A. (1982) A quantitative study of the reinnervation of the goldfish optic tectum following optic nerve crush.Journal of Comparative Neurology 209, 363–73.

    Google Scholar 

  • Murray, M. &Forman, D. S. (1971) Fine structural changes in goldfish retinal ganglion cells during axonal regeneration.Brain Research 32, 287–98.

    PubMed  Google Scholar 

  • Murray, M. &Grafstein, B. (1969) Changes in the morphology and amino acid incorporation of regenerating goldfish optic neurons.Experimental Neurology 23, 544–60.

    PubMed  Google Scholar 

  • Nordlander, R. H. &Singer, M. (1978) The role of ependyma in regeneration of the spinal cord in the urodele amphibian tail.Journal of Comparative Neurology 180, 349–74.

    PubMed  Google Scholar 

  • Nordlander, R. H. &Singer, M. (1982) Spaces precede axons inXenopus embryonic spinal cord.Experimental Neurology 75, 221–8.

    PubMed  Google Scholar 

  • Polyak, S. (1957)The Vertebrate Visual System, pp. 288–385. Chicago: Univ. of Chicago Press.

    Google Scholar 

  • Ramon y Cajal, S. (1928)Degeneration and Regeneration of the Nervous System (Trans, byMAY, R. M.), pp. 396. London: Oxford University Press.

    Google Scholar 

  • Richardson, P. J., Issa, V. J. K. &Shemie, S. (1981) Axonal changes in the retinal stump of the transected optic nerve.Neuroscience Abstracts 7, 680.

    Google Scholar 

  • Richardson, P. M., Issa, V. M. &Shemie, S. (1982) Regeneration and retrograde degeneration of axons in the rat optic nerve.Journal of Neurocytology 11, 949–66.

    PubMed  Google Scholar 

  • Reier, P. J. (1979) Penetration of grafted astrocytic scars by regenerating optic nerve axons inXenopus tadpoles.Brain Research 164, 61–8.

    PubMed  Google Scholar 

  • Reier, P. J., Stensaas, L. J. &Guth, L. (1983) The astrocytic scar as an impediment to regeneration in the central nervous system. InSpinal Cord Reconstruction (edited byKao, C. C., Bunge, R. P. andReier, P. J.), pp. 163–95. New York: Raven Press.

    Google Scholar 

  • Reier, P. J. &Webster, H. de F. (1974) Regeneration and remyelination ofXenopus tadpole optic nerve fibres following transection or crush.Journal of Neurocytology 3, 591–618.

    PubMed  Google Scholar 

  • Scott, T. M. &Foote, J. (1981) A study of degeneration, scar formation and regeneration after section of the optic nerve in the frog,Rana pipiens.Journal of Anatomy 133, 213–26.

    PubMed  Google Scholar 

  • Stone, J. (1965) A quantitative analysis of the distribution of ganglion cells in the cat's retina.Journal of Comparative Neurology 124, 337–52.

    PubMed  Google Scholar 

  • Turner, J. E., Delaney, R. K. &Powell, R. E. (1978) Retinal ganglion cell response to axotomy in the regenerating visual system of the newt (Triturus viridescens): an ultrastructural morphometric analysis.Experimental Neurology 62, 444–62.

    PubMed  Google Scholar 

  • Turner, J. E. &Singer, M. (1974) The ultrastructure of regeneration in the severed newt optic nerve.Journal of Experimental Zoology 190, 249–68.

    PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Anatomy, The George Washington University Medical Center, 20037, Washington, DC, USA

    Ronald C. Bohn & Paul J. Reier

  2. Department of Anatomy, University of Maryland School of Medicine, 21201, Baltimore, MD, USA

    Ronald C. Bohn & Paul J. Reier

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  1. Ronald C. Bohn
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  2. Paul J. Reier
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Bohn, R.C., Reier, P.J. Retrograde degeneration of myelinated axons and re-organization in the optic nerves of adult frogs (Xenopus laevis) following nerve injury or tectal ablation. J Neurocytol 14, 221–244 (1985). https://doi.org/10.1007/BF01258449

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  • DOI: https://doi.org/10.1007/BF01258449

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