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A qualitative and quantitative analysis of the response of the retinal ganglion cell soma after stretch injury to the adult guinea-pig optic nerve

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Journal of Neurocytology

Summary

The development of a model for focal axonal injury in the optic nerve of the adult guinea-pig has allowed a qualitative and quantitative analysis of the response of the retinal ganglion cell soma to this type of injury. Large and medium sized retinal ganglion cells show classic ‘central chromatolysis’ in about 30% of ganglion cells between three and seven days after injury, a high proportion of which undergo degeneration between seven and 14 days. Small ganglion cells and small neurons do not demonstrate any morphological response to stretch injury of the optic nerve. However, a small number of larger ganglion cells demonstrate enlargement of the cell soma and nucleolus together with reconstitution of the rough endoplasmic reticulum between seven and 14 days after stretch injury. We suggest that these cells are either recovering from or regenerating after a non-disruptive lesion to their axons. We suggest that some of these morphological changes parallel documented regenerative responses in peripheral/extrinsic neurons after injury to their axons. We conclude that the time course of the ‘axon reaction’ after stretch injury to axons is longer than that obtained after crush or transection. We provide good morphological evidence that the level of injury after application of non-disruptive mechanical strain to axons is less severe than in the former two models of axonal injury and that a proportion of damaged neurons do not die but rather demonstrate either/or recovery or a regenerative response.

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References

  • Aldskogius, H., Barron, K. D. &Regal, R. (1980) Axon reaction in dorsal motor, vagal and hypoglossal neurons of the adult rat.Journal of Comparative Neurology 193, 165–78.

    PubMed  Google Scholar 

  • Allcutt, D. &Sievers, J. (1984) A qualitative comparison of the reactions of retinal ganglion cells to optic nerve crush in neonatal and adult mice.Developmental Brain Research 16, 231–40.

    Google Scholar 

  • Allcutt, D., Berry, M. &Sievers, J. (1984) A quantitative comparison of the reactions of retinal ganglion cells to optic nerve crush in neonatal and adult mice.Developmental Brain Research 16, 219–30.

    Google Scholar 

  • Barr, M. L. &Hamilton, J. D. (1948) A quantitative study of certain morphological changes in spinal motor neurons during axon reaction.Journal of Comparative Neurology 89, 93–122.

    Google Scholar 

  • Barron, K. D. (1983) Comparative observations on the cytologic reactions of central and peripheral nerve cells to axotomy. In:Spinal Cord Reconstruction (edited byKao, C. C., Bunge, R. P. &Reier, P. J.), pp. 7–40. New York: Raven Press.

    Google Scholar 

  • Barron, K. D., Dentinger, M. P., Krohel, G., Easton, S. K. &Mankes, R. (1986) Qualitative and quantitative ultrastructural observations on retinal ganglion cell layer of rat after intraorbital optic nerve crush.Journal of Neurocytology 15, 345–62.

    PubMed  Google Scholar 

  • Benfey, M., Bunger, U., Vidal-Sanz, M., Bray, G. M. &Aguayo, A. J. (1985) Axonal regeneration from GABAergic neurons in the adult rat thalamus.Journal of Neurocytology 14, 276–96.

    Google Scholar 

  • Boycott, B. B. &Wassle, H. (1974) The morphological types of ganglion cells of the domestic cat's retina.Journal of Physiology 240, 397–419.

    PubMed  Google Scholar 

  • Cajal, S. R. Y. (1928)Degeneration and Regeneration of the Nervous System, pp. 583–96. London: Oxford Press.

    Google Scholar 

  • Campbell, G., Lieberman, A. R., Anderson, P. N. &Turmaine, M. (1992) Regeneration of adult rat CNS axons into peripheral nerve autografts: ultrastructural studies of the early stages of axonal sprouting and regenerative axonal growth.Journal of Neurocytology 21, 755–87.

    PubMed  Google Scholar 

  • Cheng, C. L. Y. &Povlishock, J. T. (1988) The effect of traumatic brain injury on the visual system: a morphologic characterization of reactive axonal change.Journal of Neurotrauma 5, 47–60.

    PubMed  Google Scholar 

  • Choudhury, B. P. (1978) Retinotopic organization of the guinea pig visual system.Brain Research 144, 19–29.

    PubMed  Google Scholar 

  • David, S. &Aguayo, A. J. (1985) Axonal regeneration after crush injury of rat central nervous system fibres innervating peripheral nerve grafts.Journal of Neurocytology 14, 1–12.

    PubMed  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 

  • Erb, D. E. &Povlishock, J. T. (1988) Axonal damage in severe traumatic brain injury: an experimental study in the cat.Acta Neuropathologica 76, 347–58.

    PubMed  Google Scholar 

  • Gennarelli, T. A., Thibault, L. E., Adams, J. H., Graham, D. I., Thompson, C. &Marcincin, R. (1982) Diffuse axonal injury and traumatic coma in the primate.Annals of Neurology 12, 564–74.

    PubMed  Google Scholar 

  • Gennarelli, T. A., Thibault, L. E., Tipperman, R., Tomei, G., Sergot, R., Brown, M., Maxwell, W. L., Graham, D. I., Adams, J. H., Irvine, A., Gennarelli, L. M., Duhaime, A. C., Boock, R. &Greenberg, J. (1989) Axonal injury in the optic nerve: a model of diffuse axonal injury in the brain.Journal of Neurosurgery 17, 244–53.

    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. (1975) The nerve cell body response to axotomy.Experimental Neurology 48, 32–51.

    PubMed  Google Scholar 

  • Grafstein, B. &McQuarrie, I. G. (1978) Role of the nerve cell body in axonal regeneration. In:Neuronal Plasticity (edited byCotman, C. W.), pp. 155–95. New York: Raven Press.

    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 

  • Hall, L. L. &Borke, R. C. (1988) A morphometric analysis of the somata and organelles of regenerating hypoglossal motoneurons from the rat.Journal of Neurocytology 17, 835–44.

    PubMed  Google Scholar 

  • Hayes, R. L., Pechura, C. M., Katayama, Y., Povlishock, J. T., Yeatts, M. L. &Becker, D. P. (1984) Activation of midbrain cholinergic sites implicated in unconsciousness following cerebral concussion in the cat.Science 223, 301–3.

    PubMed  Google Scholar 

  • James, G. R. (1933) Degeneration of ganglion cell following axonal injury.Archives of Ophthalmology 9, 338–43.

    Google Scholar 

  • Johnson, J. E., Barde, Y.-A., Schwab, M. &Thoenen, H. (1986) Brain-derived neuronotrophic factor supports the survival of cultured rat retinal ganglion cells.Journal of Neuroscience 6, 3031–8.

    PubMed  Google Scholar 

  • Jones, K. J. &Lavelle, A. (1986) Differential effects of axotomy on immature and mature hamster facial neurons: a time course study of initial nucleolar and nuclear changes.Journal of Neurocytology 15, 197–206.

    PubMed  Google Scholar 

  • Leinfelder, P. J. (1938) Retrograde degeneration in the optic nerves and retinal ganglion cells.Transactions of the American Ophthalmologic Society 36, 307–15.

    Google Scholar 

  • Lieberman, A. R. (1971) The axon reaction: a review of the principal features of perikaryal responses to axon injury.International Review of Neurobiology 14, 49–141.

    PubMed  Google Scholar 

  • Lighthall, J. W., Goshgarian, H. G. &Pinderski, C. R. (1990) Characterization of axonal injury produced by controlled cortical impact.Journal of Neurotrauma 7, 65–76.

    PubMed  Google Scholar 

  • Mccloon, L. K. &Lavelle, A. (1981) Tritiated leucine incorporation in the developing hamster facial nucleus with injury: an autoradiographic study.Experimental Neurology 74, 573–86.

    PubMed  Google Scholar 

  • Maffei, L. &Fiorentini, A. (1981) Electroretinographic responses to alternating gratings before and after section of the optic nerve.Science 211, 953–5.

    PubMed  Google Scholar 

  • Maxwell, W. L., Kansagra, A. M., Graham, D. I., Adams, J. H. &Gennarelli, T. A. (1988) Freeze-fracture studies of reactive myelinated nerve fibres after diffuse axonal injury.Acta Neuropathologica 76, 395–406.

    PubMed  Google Scholar 

  • Maxwell, W. L., Irvine, A., Graham, D. I., Adams, J. H., Gennarelli, T. A., Tipperman, R. &Sturatis, M. (1991a) Focal axonal injury: the early axonal response to stretch.Journal of Neurocytology 20, 157–64.

    PubMed  Google Scholar 

  • Maxwell, W. L., Irvine, A., Watt, C., Graham, D. I., Adams, J. H. &Gennarelli, T. A. (1991b) The microvascular response to stretch injury in the adult guinea pig visual system.Journal of Neurotrauma 8, 271–9.

    PubMed  Google Scholar 

  • Maxwell, W. L., Watt, C., Graham, D. I. &Gennarelli, T. A. (1993) Ultrastructural evidence of axonal shearing as a result of lateral acceleration of the head in non-human primates.Acta Neuropathologica 86, 136–44.

    PubMed  Google Scholar 

  • Miller, N. M. &Oberdorfer, M. (1981) Neuronal and neuroglial responses following retinal lesions in the neonatal rats.Journal of Comparative Neurology 202, 493–504.

    PubMed  Google Scholar 

  • Misantone, L. J., Gershenbaum, M. &Murray, M. (1984) Viability of retinal ganglion cells after optic nerve crush in adult rats.Journal of Neurocytology 13, 449–65.

    PubMed  Google Scholar 

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

    PubMed  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 

  • Perry, V. H. &Cowey, A. (1979) The effects of unilateral cortical and tectal lesions on retinal ganglion cells in rats.Experimental Brain Research 35, 85–95.

    Google Scholar 

  • Pesheva, P., Spiess, E. &Schachner, M. (1989) J-160 and J-180 are oligodendrocyte-secreted nonpermissive substrates for cell adhesion.Journal of Cell Biology 109, 1765–78.

    PubMed  Google Scholar 

  • Politis, M. J. &Miller, J. E. (1985) Induction of CNS regeneration by localized exogenous tropic factor and systemic mitotic inhibitor administration.Journal of Neuropathology and Experimental Neurology 44, 354 (Abstract).

    Google Scholar 

  • Povlishock, J. T. (1986) Traumatically induced axonal damage without concomitant change in focally related neuronal somata and dendrites.Acta Neuropathologica 70, 53–9.

    PubMed  Google Scholar 

  • Povlishock, J. T. (1992) Traumatically induced axonal injury: pathogenesis and pathobiological implications.Brain Pathology 2, 1–12.

    PubMed  Google Scholar 

  • Povlishock, J. T. &Becker, D. P. (1985) Fate of reactive axonal swellings induced by head injury.Laboratory Investigation 52, 540–52.

    PubMed  Google Scholar 

  • Povlishock, J. T. &Kontos, H. A. (1985) Continuing axonal and vascular change following experimental brain trauma.Central Nervous System Trauma 2, 285–97.

    PubMed  Google Scholar 

  • Povlishock, J. T., Becker, D. P., Cheng, C. &Vaughan, G. (1983) Axonal change in minor head injury.Journal of Neuropathology and Experimental Neurology 42, 225–42.

    PubMed  Google Scholar 

  • Povlishock, J. T., Becker, D. P., Miller, J. D., Jenkins, L. W. &Dietrich, W. D. (1979) The morphopathologic substrates of concussion?Acta Neuropathologica 47, 1–11.

    PubMed  Google Scholar 

  • Quigley, H. A., Davis, E. B. &Anderson, D. R. (1977) Descending optic nerve degeneration in primates.Investigative Ophthamology and Visual Science 16, 841–9.

    Google Scholar 

  • Reichardt, L. F. &Tomaselli, K. J. (1991) Extracellular matrix molecules and their receptors: functions in neural development.Annual Review of Neuroscience 14, 531–70.

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Richardson, P. M., Issa, V. M. K. &Aguayo, A. J. (1984) Regeneration of long spinal axons in the rat.Journal of Neurocytology 13, 165–82.

    PubMed  Google Scholar 

  • Risling, M., Linda, H., Cullheim, S. &Franson, P. (1989) A persistent defect in the blood-brain barrier after ventral funiculus lesion in adult cats — implications for CNS regeneration.Brain Research 494, 13–21.

    PubMed  Google Scholar 

  • Risling, M., Fried, K., Lind, H., Cullheim, S. &Meier, M. (1992) Changes in nerve growth factor receptor-like immunoreactivity in the spinal cord after ventral funiculus lesion in adult cats.Journal of Neurocytology 21, 79–93.

    PubMed  Google Scholar 

  • Sievers, J., Hausmann, B. &Berry, M. (1989) Fetal brain grafts rescue adult retinal ganglion cells from axotomy-induced cell death.Journal of Comparative Neurology 281, 467–78.

    PubMed  Google Scholar 

  • Stevenson, J. A. (1985) Growth of optic tract axons in nerve grafts in hamsters.Experimental Neurology 87, 446–57.

    PubMed  Google Scholar 

  • Takahashi, J. B., Hoshimaru, M., Kikuchi, H. &Hatanaka, M. (1993) Extension of optic nerve fibres on genetically modified cells producing brain-derived neuronotrophic factor.Neuroscience Letters 149, 83–6.

    PubMed  Google Scholar 

  • Van Buren, J. M. (1963)The Retinal Ganglion Cell Layer Springfield, Illinois: Charles C. Thomas.

    Google Scholar 

  • Watson, W. E. (1965) An autoradiographic study of the incorporation of nucleic acid precursors by neurones and glia during nerve regeneration.Journal of Physiology 180, 41–53.

    Google Scholar 

  • Watson, W. E. (1968) Observations on the nucleolar and total cell body nucleic acid of injured nerve cells.Journal of Physiology 196, 655–76.

    PubMed  Google Scholar 

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Maxwell, W.L., Islam, M.N., Graham, D.I. et al. A qualitative and quantitative analysis of the response of the retinal ganglion cell soma after stretch injury to the adult guinea-pig optic nerve. J Neurocytol 23, 379–392 (1994). https://doi.org/10.1007/BF01666527

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  • DOI: https://doi.org/10.1007/BF01666527

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