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Perisomatic changes in the maturing hypoglossal nucleus after axon injury

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Journal of Neurocytology

Summary

The perisomatic retrograde reactions to peripheral nerve injury during postnatal maturation were investigated by quantitative light and electron microscopy. The hypoglossal nerve was crushed, ligated or transected in 10 and 21 day postnatal (dpn) rats. Only crush injury was made in 7 dpn rats. Survival periods ranged from 3 to 40 days postoperative (dpo). Normal and sham operated animals of corresponding ages served as controls. A remarkable, transient response of neuronal somata in the young (7–10 dpn) rats, following all three types of axon injury, was the formation of excrescences which engulfed neuronal processes: boutons, dendrites, small neurites and a few myelinated axons in adjacent neuropil. The somal engulfment was rarely evident after nerve injury to 21 dpn rats. Bouton displacement from the somal surface, accompanied by glial incursion, followed each type of nerve injury but was less extensive and occurred later in the young rats. There seemed to be no association in the amount of boutons displaced from neuronal somata with the type of nerve injury for any of the three experimental age groups. However, the rate and intensity of the perineuronal glial reaction were related to the severity of the nerve injury in the older (21 dpn) but not in the younger (7–10 dpn) rats. Substantial loss of neurons occurred in the affected nucleus after each type of trauma to the young neurons. The degree of neuronal loss was related to the age and the volume of axoplasm disrupted. Only nerve transection in 21 dpn rats resulted in appreciable neuronal loss. The responses of axotomized neurons, their afferent axon terminals and the surrounding glia are quantitatively and qualitatively different in the hypoglossal nucleus of rats of increasing postnatal ages.

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References

  • Banks, B. E. C. &Walter, S. J. (1977) The effects of postganglionic axotomy and nerve growth factor on the superior cervical ganglia of developing mice.Journal of Neurocytology 6, 287–97.

    Google Scholar 

  • Barron, K. D., Chiang, T. Y., Daniels, A. C. &Doolin, P. F. (1971) Subcellular accompaniments of axon reaction in cervical motoneurons of the cat. InProgress in Neuropathology (edited byZimmerman, H. M.), pp. 255–80. New York: Grune and Stratton.

    Google Scholar 

  • Berthold, C. H., Kellerth, J. O. &Conradi, S. (1979) Electron microscopic studies of serially sectioned cat spinal α-motoneurons. 1. Effects of microelectrode impalement and intracellular staining with the fluorescent dye ‘Procion Yellow’.Journal of Comparative Neurology 184, 709–40.

    PubMed  Google Scholar 

  • Black, I. B., Coughlin, M. D. &Cochard, P. (1979) Factors regulating neuronal differentiation. InAspects of Developmental Neurobiology, Society for Neuroscience Symposia, Vol. IV, (edited byFerrendelli, J. A.), pp. 184–207. Bethesda, Maryland: Society for Neuroscience.

    Google Scholar 

  • Blinzinger, K. &Kreutzberg, G. (1968) Displacement of synaptic terminals from regenerating motoneurons by microglial cells.Zeitschrift für Zellforschung und mikroskopische Anatomie 85, 145–57.

    Google Scholar 

  • Borke, R. C. &Brightman, M. W. (1979) Morphological response of the maturing neuronal soma and surrounding neuropil to axonal injury.Anatomical Record 193, 488 (abstract).

    Google Scholar 

  • Brodal, A. (1952) Experimental demonstration of cerebellar connections from the peri-hypoglossal nuclei (nucleus intercalatus, nucleus praepositus hypoglossi and nucleus of Roller) in the cat.Journal of Anatomy 86, 110–28.

    PubMed  Google Scholar 

  • Conradi, S. (1969a) Ultrastructure and distribution of neuronal and glial elements on the motoneuron surface in the lumbosacral spinal cord of the adult cat.Acta physiologica scandinavica Suppl.332, 5–48.

    Google Scholar 

  • Conradi, S. (1969b) Ultrastructure of dorsal root boutons on lumbosacral motoneurons of the adult cat, as revealed by dorsal root section.Acta physiologica scandinavica Suppl.332, 85–115.

    Google Scholar 

  • Eckenhoff, M. F. &Pysh, J. J. (1979) Double-walled coated vesicle formation: evidence for massive and transient internalization of plasma membranes during cerebellar development.Journal of Neurocytology 8, 623–38.

    PubMed  Google Scholar 

  • Gentschev, T. &Sotelo, C. (1973) Degenerative patterns in the ventral cochlear nucleus of the rat after primary deafferentiation. An ultrastractural study.Brain Research 62, 37–60.

    PubMed  Google Scholar 

  • Gray, E. G. &Guillery, R. W. (1966) Synaptic morphology in the normal and degenerating nervous system.International Review of Cytology 19, 111–82.

    PubMed  Google Scholar 

  • Gudden, B. (1870) Experimental Untersuchungen über das periperische und central nervensystem.Archiv für Psychiatrie und Nervenkrankheiten 2, 693–723.

    Google Scholar 

  • Hamberger, A., Hansson, H. A. &Sjostrand, J. (1970) Surface structure of isolated neurons: Detachment of nerve terminals during axon regeneration.Journal of Cell Biology 47, 319–31.

    Google Scholar 

  • Hendry, I. A. &Campbell, J. (1976) Morphometric analysis of rat superior cervical ganglion after axotomy and NGF treatment.Journal of Neurocytology 5, 351–60.

    PubMed  Google Scholar 

  • Hinds, J. W. &Hinds, P. L. (1976) Synapse formation in the mouse olfactory bulb. II. Morphogenesis.Journal of Comparative Neurology 169, 41–62.

    PubMed  Google Scholar 

  • Imamoto, K. &Leblond, C. P. (1978) Radioautographic investigation of gliogenesis in the corpus callosum of young rats. II. Origin of microglial cells.Journal of Comparative Neurology 180, 139–64.

    PubMed  Google Scholar 

  • Kirkpatrick, J. B. (1968) Chromatolysis in the hypoglossal nucleus of the rat: An electron microscopic analysis.Journal of Comparative Neurology 132, 189–212.

    PubMed  Google Scholar 

  • Konigsmark, B. W. (1970) Methods for counting neurons. InContemporary Research Methods in Neuroanatomy (edited byNauta, W. J. H. &Ebbeson, S. O. E.), pp. 315–40. Berlin: Springer-Verlag.

    Google Scholar 

  • Landmesser, L. &Pilar, G. (1976) Fate of ganglionic synapses and ganglion cell axons during normal and induced cell death.Journal of Cell Biology 68, 357–74.

    PubMed  Google Scholar 

  • Larramendi, L. M. H. (1969) Analysis of synaptogenesis in the cerebellum of the mouse. InNeurobiology of Cerebellar Evolution and Development (edited byLlinas, R.), pp. 803–43. Chicago: American Medical Association.

    Google Scholar 

  • Lavelle, A. (1973) Levels of maturation and reactions to injury during neuronal development.Progress in Brain Research 40, 161–6.

    PubMed  Google Scholar 

  • Lavelle, A. &Lavelle, F. W. (1970) Cytodifferentiation in the neuron. InDevelopmental Neurobiology (edited byHimwich, W. H.), pp. 117–64. Springfield, IL: Charles C. Thomas.

    Google Scholar 

  • Lieberman, A. R. (1974) Some factors affecting retrograde neuronal responses to axonal lesions. InEssays on theNervous System (edited byBellairs, R. &Gray, E. G.), pp. 71–105. Oxford: Clarendon Press.

    Google Scholar 

  • Ling, E. A., Peterson, J. A., Privat, A., Mori, S. &Leblond, C. P. (1973) Investigation of glial cells in semithin sections. 1. Identification of glial cells in the brain of young rats.Journal of Comparative Neurology 149, 43–72.

    PubMed  Google Scholar 

  • Matthews, M. A., Narayanan, C. H., Narayanan, Y. &St. Onge, M. F. (1977) Neuronal maturation and synaptogenesis in the rat ventrobasal complex: Alignment with developmental changes in rate and severity of axon reaction.Journal of Comparative Neurology 173, 745–72.

    PubMed  Google Scholar 

  • Matthews, M. R. &Nelson, V. H. (1975) Detachment of structurally intact nerve endings from chromatolytic neurons of rat superior cervical ganglion during the depression of synaptic transmission induced by postganglionic axotomy.Journal of Physiology 245, 91–135.

    PubMed  Google Scholar 

  • May, M. R. &Biscoe, T. J. (1975) An investigation of the foetal rat spinal cord. I. Ultra structural observations on the onset of synaptogenesis.Cell and Tissue Research 158, 241–9.

    PubMed  Google Scholar 

  • Rees, R. P., Bunge, M. B. &Bunge, R. P. (1976) Morphological changes in the neuritic growth cone and target neuron during synaptic junction development in culture.Journal of Cell Biology 68, 240–63.

    PubMed  Google Scholar 

  • Reese, T. S. &Karnovsky, M. J. (1967) Fine structural localization of a blood-brain barrier to exogenous peroxidase.Journal of Cell Biology 34, 207–17.

    PubMed  Google Scholar 

  • Ronnevi, L. (1979) Spontaneous phagocytosis of C-type synaptic terminals by spinal motoneurons in newborn kittens. An electron microscopic study.Brain Research 162, 189–99.

    PubMed  Google Scholar 

  • Sakla, F. B. (1965) Post-natal growth of neuroglial cells and blood vessels of the cervical spinal cord of the albino mouse.Journal of Comparative Neurology 124, 189–202.

    PubMed  Google Scholar 

  • Simionescu, N. &Simionescu, M. (1976) Galloylglucoses of low molecular weight as mordant in electron microscopy. I. Procedure and evidence for mordanting effect.Journal of Cell Biology 70, 608–21.

    Google Scholar 

  • Sumner, B. E. H. (1975a) A quantitative study of subsurface cisterns and their relationships in normal and axotomized hypoglossal neurons.Experimental Brain Research 22, 175–83.

    Google Scholar 

  • Sumner, B. E. H. (1975b) A quantitative analysis of the response of presynaptic boutons to postsynaptic motor neuron axotomy.Experimental Neurology 46, 605–15.

    PubMed  Google Scholar 

  • Sumner, B. E. H. (1975c) A quantitative analysis of boutons with different types of synapse in normal and injured hypoglossal nuclei.Experimental Neurology 49, 406–17.

    PubMed  Google Scholar 

  • Sumner, B. E. H. &Sutherland, F. I. (1973) Quantitative electron microscopy on the injured hypoglossal nucleus in the rat.Journal of Neurocytology 2, 315–28.

    PubMed  Google Scholar 

  • Torvik, A. (1972) Phagocytosis of nerve cells during retrograde degeneration. An E.M. study.Journal of Neuropathology and Experimental Neurology 31, 132–46.

    PubMed  Google Scholar 

  • Vaughn, J. E. (1969) An electron microscopic analysis of gliogenesis in rat optic nerves.Zeitschrift für Zellforschung und mikroskopische Anatomie 94, 293–324.

    Google Scholar 

  • Watson, W. E. (1974) Cellular responses to axotomy and to related procedures.British Medical Bulletin 30, 112–5.

    PubMed  Google Scholar 

  • Watson, W. E. (1976)Cell Biology of Brain, p. 527. New York: John Wiley and Sons.

    Google Scholar 

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  1. Department of Anatomy, Uniformed Services University of the Health Sciences, 4301 Jones Bridge Road, 20814, Bethesda, Maryland, USA

    Rosemary C. Borke

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  1. Rosemary C. Borke
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Borke, R.C. Perisomatic changes in the maturing hypoglossal nucleus after axon injury. J Neurocytol 11, 463–485 (1982). https://doi.org/10.1007/BF01257989

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  • DOI: https://doi.org/10.1007/BF01257989

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