Skip to main content
SpringerLink
Log in

A fine structural study of degenerative-regenerative pathology in the surgically deafferentated lateral vestibular nucleus of the rat

  • Original Investigations
  • Published:
Acta Neuropathologica Aims and scope Submit manuscript

Summary

An experiment was designed to examine the course of degeneration, phagocytosis, and regeneration in the central nervous system following surgical deafferentation. The anterior cerebellar vermis was ablated in young male rats. The animals were sacrificed by perfusion at postoperative times ranging from 24 hrs to 6 months. The lateral vestibular nuclei, to which the anterior cerebellar vermis projects, were processed for electron microscopy. Degenerating synaptic terminals, of the dark variety, were seen from 24 hrs to five days postoperatively. Phagocytosis of degenerating terminals occurred during this time. Degenerating axons persisted through 6 months survival, and phagocytosis of these degenerating axons was observed. Astrocyte scar formation began at 1 month postoperatively. The relative number of axosomatic synaptic terminals containing flattened vesicles (“F” terminals; presumed inhibitory in function) increased in operated animals. The highest F scores were found from 24 hrs to two weeks postoperatively, and then the F scores declined through six months. The significance of these sprouting activities is discussed in relation to the abortive sprouting phenomenon described by Ramón y Cajal.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Andersen, P., Eccles, J. C., Voorhoeve, P. E.: Post-synaptic inhibition of cerebellar Purkinje cells. J. Neurophysiol.27, 1138–1153 (1964)

    Google Scholar 

  • Barron, K. D., Means, E. D., Feng, T., Harris, H.: Ultrastructure of retrograde degeneration in thalamus of rat. 2. Changes in vascular elements and transvascular migration of leukocytes. Exp. molec. pathol.20, 344–362 (1974)

    Google Scholar 

  • Bernstein, J. J., Gelderd, J. B., Bernstein, Mary E.: Alteration of neuronal synaptic complement during regeneration and axonal sprouting of rat spinal cord. Exp. Neurol.44, 470–482 (1974)

    Google Scholar 

  • Bignami, A., Ralston, H. J.: The cellular reaction to Wallerian degeneration in the central nervous system of the cat. Brain Res.13, 444–461 (1969)

    Google Scholar 

  • Birks, R., Katz, B., Miledi, R.: Physiological and structural changes at the amphibian myoneural junction, in the course of nerve degeneration. J. Physiol. (Lond.)150, 145–168 (1960)

    Google Scholar 

  • Blakemore, W. F.: Microglial reactions following thermal necrosis of the rat cortex. Acta neuropath. (Berl.)21, 11–22 (1972)

    Google Scholar 

  • Bodian, D.: An electron microscopic characterization of classes of synaptic vesicles by means of controlled aldehyde fixation. J. Cell Biol.44, 115–124 (1970)

    Google Scholar 

  • Bodian, D.: Origin of specific synaptic types in the motoneuron neuropil of the monkey. J. comp. Neurol.159, 225–244 (1975)

    Google Scholar 

  • Brodal, A., Pompeiano, O., Walberg, F.: The vestibular nuclei and their connections. Henderson Trust Series No. 20 (1962)

  • Brown, J. O., McCouch, G. P.: Abortive regeneration of the transected spinal cord. J. comp. Neurol.87, 131 (1947)

    Google Scholar 

  • Clemente, C. D., Windle, W. F.: Regeneration of severed nerve fibers in the spinal cord of the adult cat. J. comp. Neurol.101, 691–731 (1954)

    Google Scholar 

  • Cramon, D. von: Licht- und elektronenmikroskopische Untersuchung der gliös-mesenchymalen Narbenstruktur in der experimentell traumatisierten Großhirnrinde des Goldhamsters nach Anwendung des bakterienpolysacchariden Piromen. Acta neuropath. (Berl.)31, 219–227 (1975)

    Google Scholar 

  • De Robertis, E.: Submicroscopic changes of the synapse after nerve section in the acoustic ganglion of the guinea pig: An electron microscopic study. J. biophys. biochem. Cytol.2, 503–512 (1957)

    Google Scholar 

  • Eager, R. P., Eager, P. R.: Glia responses to degenerating cerebellar cortico-nuclear pathways in the cat. Science153, 553–554 (1966)

    Google Scholar 

  • Eccles, J. C.: The physiology of synapses. Berlin-Göttingen-Heidelberg: Springer 1964

    Google Scholar 

  • Gentschev, T., Sotelo, C.: Degenerative patterns in the ventral cochlear nucleus of the rat after primary deafferentation. An ultrastructural study. Brain Res.62, 37–60 (1973)

    Google Scholar 

  • Goodman, D. C., Horel, J. A.: Sprouting of optic tract projections in the brain stem of the rat. J. comp. Neurol.127, 71–88 (1966)

    Google Scholar 

  • Gray, E. G., Hamlyn, L. H.: Electron microscopy of experimental degeneration in the avian optic tectum. J. Anat. (Lond.)96,309–316 (1962)

    Google Scholar 

  • Hager, H., Blinzinger, K.: Über eigenartige Astrozytenfortsätze und intrazytoplasmatische Vesikelreihen (Elektronenmikroskopische Untersuchungen an Gliosen des Säugetiergehirns). Z. Zellforsch.65, 57–73 (1965)

    Google Scholar 

  • Johnson, J. E., Jr., Miquel, J.: Fine structural changes in the lateral vestibular nucleus of aging rats. Mech. Age. Develop.3, 203–224 (1974)

    Google Scholar 

  • Johnson, J. E., Jr.: The occurrence of dark neurons in the normal and deafferentated lateral vestibular nucleus in the rat. Observations by light and electron microscopy. Acta neuropath. (Berl.)31, 117–127 (1975)

    Google Scholar 

  • Klaue, R.: Regenerationsversuche bei Rückenmarksschädigungen des Menschen, ausgehend von den hinteren Wurzeln. Wien. 2 Schr. Nervenb.2, 488–497 (1948)

    Google Scholar 

  • Konigsmark, B. W., Sidman, R. L.: Origin of brain macrophages in the mouse. J. Neuropath. exp. Neurol.22, 643–676 (1963)

    Google Scholar 

  • Lhermitte, J., Hécaen, de Ajuriaguerra: Section complete de la moelle dorsale, verifree chirurgicalment et anatomiquement. Rev. neurol.77, 308–310 (1945)

    Google Scholar 

  • Liu, Chan-Nao, Chambers, W. W.: Intraspinal sprouting of dorsal root axons. Arch. Neurol. Psychiatr (Chic.)79, 46–61 (1958)

    Google Scholar 

  • Lorente de No, R.: La regeneration de las medula espinal en los larvas de bactricio. Trabajos. Inst. Cajal Invest. Biol. Madrid19, 147–183 (1921)

    Google Scholar 

  • Lund, R. D., Lund, J. S.: Modification of synaptic pattern in the superior colliculus of the rat during development and following deafferentation. Vision Res., Suppl. No. 3, 281–198 (1971)

    Google Scholar 

  • Matus, A. I., Dennison, M. E.: Autoradiographic localisation of tritiated glycine at “flat vesicle” synapses in the spinal cord. Brain. Res.32, 195–197 (1971)

    Google Scholar 

  • Maxwell, D. S., Kruger, L.: Small blood vessels and the origin of phagocytes in the rat cerebral cortex following heavy particle irradiation. Exp. Neurol.12, 33–54 (1965)

    Google Scholar 

  • Migliavacca, A.: Richerche sperimentali sulla rigenerazione del midollo spinale nei feti e nei neonati. Arch. Ist biochim. ital.2, 201–236 (1930)

    Google Scholar 

  • Mori, Schiro, Leblond, C. P.: Identification of microglia in light and electron microscopy. J. comp. Neurol.135, 57–79 (1969)

    Google Scholar 

  • Murray, Marion, Goldberger, M. E.: Restitution of function and collateral sprouting in the cat spinal cord: The partially hemisected animal. J. comp. Neurol.158, 19–36 (1974)

    Google Scholar 

  • Otsuka, M., Obata, K., Miyata, Y., Tanaka, Yuriko.: Measurements of γ aminobutyric acid in isolated nerve cells of cat central nervous system. J. Neurochem.18, 287–295 (1971)

    Google Scholar 

  • Peters, G.: Multiple sclerosis. In: Pathology of the Nervous System (ed. J. Minckler). London: McGraw-Hill 1968

    Google Scholar 

  • Piatt, J., Piatt, M.: Transection of the spinal cord in the frog. Anat. Rec.131, 81–95 (1958)

    Google Scholar 

  • Raisman, G.: Neuronal plasticity in the septal nuclei of the adult rat. Brain Res.14, 25–48 (1969)

    Google Scholar 

  • Ralston, H. J., Chow, K. L.: Synaptic reorganization in the degenerating lateral geniculate nucleus of the rabbit. J. comp. Neurol.147, 321–350 (1973)

    Google Scholar 

  • Ramón y Cajal, S.: Degeneration and regeneration of the nervous system. London-New York: Oxford University Press 1928

    Google Scholar 

  • Scott, D., Jr., Clemente, C. D.: Regeneration of spinal cord fibers in the cat. J. comp. Neurol.102, 633–669 (1955)

    Google Scholar 

  • Spatz, H., Morphologische Grundlagen der Restitiution im Zentralnervensystem. Deutsch. Z. Nervenheilk.115, 197–231 (1930)

    Google Scholar 

  • Sugar, O., Gerard, R. W.: Spinal cord regeneration. J. Neurophysiol.3, 1–19 (1940)

    Google Scholar 

  • Uchizono, K.: Characteristics of excitatory and inhibitory synapses in the central nervous system of the cat. Nature (Lond.)207, 642–643 (1965)

    Google Scholar 

  • Uchizono, K.: Synaptic organization of the Purkinje cells in the cerebellum of the cat. Exp. Brain Res.4, 97–113 (1967)

    Google Scholar 

  • Valdivia, O.: Methods of fixation and the morphology of synaptic vesicles. J. comp. Neurol.142, 257–274 (1971)

    Google Scholar 

  • Vaughan, Deborah W., Peters, A.: Neuroglial cells in the cerebral cortex of rats from young adulthood to old age: an electron microscopic study. J. Neurocytol.3, 405–429 (1974)

    Google Scholar 

  • Vaughn, J. E., Peters, A.: A third neuroglial cell type: An electron microscopic study. J. comp. Neurol.133, 269–288 (1968)

    Google Scholar 

  • Vaughn, J. E., Hinds, Patricia, L., Skoff, R. P.: Electron microscopic studies of Wallerian degeneration in rat optic nerves. I. The multipotential glia. J. comp. Neurol.140, 175–206 (1970)

    Google Scholar 

  • Vaughn, J. E., Pease, D. C.: Electron microscopic studies of Wallerian degeneration in rat optic nerves. II. Astrocytes, oligodendrocytes and adventitial cells. J. comp. Neurol.140, 207–226 (1970)

    Google Scholar 

  • Walberg, F., Mugnaini, E.: Distinction of degenerating fibers and boutons of cerebellar and peripheral origin in the Deiters' nucleus of the same animal. Brain Res.14, 67–75 (1969)

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Neurosciences Branch, Ames Research Center, NASA, Neurosciences Branch 239-19, 94035, Moffett Field, California, U.S.A

    John E. Johnson Jr.

Authors
  1. John E. Johnson Jr.
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

This research was supported by NASA Task No. 970-21-11-11 at Ames Research Center and NIH Training Grant No. 5T01 GM00793-11 at Tulane University.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Johnson, J.E. A fine structural study of degenerative-regenerative pathology in the surgically deafferentated lateral vestibular nucleus of the rat. Acta Neuropathol 33, 227–243 (1975). https://doi.org/10.1007/BF00688396

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00688396

Key words

Search

Navigation