Skip to main content
SpringerLink
Log in

Reactive alterations in non-neuronal elements of the degenerating ventrobasal complex of immature and mature rats

An electron microscopic study

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Summary

Sprague-Dawley albino rats ranging in age from neonate to 60 days postnatal (dpn) were subjected to cortical extirpations encompassing the SmI somato-sensory projection fields of neurons in the ventrobasal (VB) complex. Electron microscopy of this region reveals degenerative changes in VB neurons, the rate and severity of which is inversely proportional to the age of the animal (Matthews et al., 1977). Numerous, distinctive non-neuronal elements, similar to those infiltrating the perivascular space of some vessels in the area, rapidly accumulate within the zone of degeneration in animals lesioned between 0 and 9 dpn. These display dense, heterochromatin nuclei, concentrations of free ribosomes and rosettes, and pleomorphic dense bodies which become more evident as further reactive transformations accompany the phagocytic incorporation of degenerating neuronal remnants. Other non-neuronal elements exhibit a euchromatin nucleus, bundles of microtubules, and fewer free ribosomes. Such cells are also capable of phagocytosis and production of dense bodies. Both variants are comparable in appearance to the “M” cells of previous reports (Matthews and Kruger, 1973 b). Cortical lesions of older animals result in the appearance of “M” cells in VB; however, the population densities observed in the immature VB are not achieved. Conversely, astrocytic hypertrophy, associated with the increased incidence of degenerating boutons in the more mature animal, represents a prominent response to injury which does not occur to a significant extent in younger animals.

Morphological criteria for determining the nature of some “M” cells are given for a discussion of their presumptive derivation from various mesodermal progenitors and a brief consideration of other hypothesized origins.

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

  • Anderson, C.A., Westrum, L.E.: An electron microscopic study of the normal synaptic relationships and early degenerative changes in the rat olfactory tubercle. Z. Zellforsch. 127, 462–482 (1972)

    Google Scholar 

  • Baron, M., Gallego, A.: The relation of the microglia with the pericytes in the cat cerebral cortex. Z. Zellforsch. 128, 42–57 (1972)

    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. Path. 20, 344–362 (1974)

    Google Scholar 

  • Blakemore, W.F.: The ultrastructure of the subependymal plate in the rat. J. Anat. (Lond.) 104, 423–433 (1969)

    Google Scholar 

  • Blinzinger, K., Kreutzberg, G.: Displacement of synaptic terminals from regenerating motoneurons by microglial cells. Z. Zellforsch. 85, 145–156 (1968)

    Google Scholar 

  • Brizzee, K.R., Jacobs, L.A.: Glia neuron index in the submolecular layers of motor cortex in the cat. Anat. Rec. 134, 97–105 (1959)

    Google Scholar 

  • Cammermeyer, J.: Juxtavascular karyokinesis and microglia cell proliferation during retrograde reaction in the mouse facial nucleus. Ergebn. Anat. Entwickl.-Gesch. 38, 1–22 (1965)

    Google Scholar 

  • Cammermeyer, J.: The life history of the microglial cell: A light microscopic study. In: Neurosciences research, Vol. 3 (S. Ehrenpreis and O.C. Solnitzky, eds.), pp. 43–129. New York: Academic Press 1970

    Google Scholar 

  • Dobbing, J.: Effects of experimental undernutrition on development of the nervous system. In: Malnutrition, learning and behavior (N.S. Scrimshaw and J.E. Gordon, eds.), pp. 181–202. Cambridge, Mass.: M.I.T. 1968

    Google Scholar 

  • Eager, R.P., Eager, P.R.: Glial responses to degenerating cerebellar corticonuclear pathways in the cat. Science 153, 553–554 (1966)

    Google Scholar 

  • Emmers, R.: Organization of the first and the second somesthetic regions (S1 and S11) in the rat thalamus. J. comp. Neurol. 124, 215–228 (1965)

    Google Scholar 

  • Feigin, I.: Mesenchymal tissue of the nervous system. J. Neuropath. exp. Neurol. 28, 6–23 (1969)

    Google Scholar 

  • Frederickson, R.G., Low, F.N.: Blood vessels and tissue space associated with the brain of the rat. Amer. J. Anat. 125, 123–146 (1969)

    Google Scholar 

  • Gray, E.G., Guillery, R.W.: Synaptic morphology in the normal and degenerating nervous system. Int. Rev. Cytol. 19, 111–182 (1966)

    Google Scholar 

  • Gurdjian, E.S.: The diencephalon of the albino rat. J. comp. Neurol. 43, 1–114 (1927)

    Google Scholar 

  • Hall, R.D., Lindholm, E.P.: Organization of motor and somatosensory neocortex in the albino rat. Brain Res. 66, 23–38 (1974)

    Google Scholar 

  • Juba, A.: Untersuchungen über die Entwicklung der Hortegaschen Microglia des Menschen. Arch. Psychiat. Nervenkrankr. 10, 577–592 (1934a)

    Google Scholar 

  • Juba, A.: Das erste Erscheinen und die Urformen der Hortegaschen Mikroglia im Zentralnerven-system. Arch. Psychiat. Nervenkr. 102, 225–232 (1934b)

    Google Scholar 

  • King, J.S.: A light and electron microscopic study of perineuronal glial cells and processes in the rabbit neocortex. Anat. Rec. 161, 111–124 (1968)

    Google Scholar 

  • Kruger, L., Hamori, J.: An electron microscopic study of dendritic degeneration in the cerebral cortex resulting from laminar lesions. Exp. Brain Res. 10, 1–16 (1970)

    Google Scholar 

  • Lashley, K.S.: Thalamo-cortical connections of the rat's brain. J. comp. Neurol. 75, 67–121 (1941)

    Google Scholar 

  • Ling, E.A., Paterson, J.A., Privat, A., Mori, S., Leblond, C.P.: Investigation of glial cells in semithin sections. I. Identification of glial cells in the brain of young rats. J. comp. Neurol. 149, 43–72 (1973)

    Google Scholar 

  • Matthews, M.A.: Death of the central neuron: an electron microscopic study of thalamic retrograde degeneration following cortical ablation. J. Neurocytol. 20, 265–288 (1973)

    Google Scholar 

  • Matthews, M.A.: Microglia and reactive “M” cells of degenerating central nervous system: Does similar morphology and function imply a common origin? Cell Tiss. Res. 148, 477–491 (1974)

    Google Scholar 

  • Matthews, M.A.: Reactive events in cerebral microvasculature associated with neural degeneration in thalamic relay nuclei. In: The cerebral vessel wall (J. Cervos-Navarro et al., eds.). New York: Raven Press 1976

    Google Scholar 

  • Matthews, M.A., Kruger, L.: Electron microscopy of non-neuronal cellular changes accompanying neural degeneration in thalamic nuclei of the rabbit. I. Reactive hematogenous and perivascular elements within the basal lamina. J. comp. Neurol. 148, 285–312 (1973a)

    Google Scholar 

  • Matthews, M.A., Kruger, L.: Electron microscopy of non-neuronal cellular changes accompanying neural degeneration in thalamic nuclei of the rabbit. II. Reactive elements within the neuropil. J. comp. Neurol. 148, 313–346 (1973b)

    Google Scholar 

  • Matthews, M.A., Narayanan, C.H., Narayanan, Y., St. Onge, M.F.: Neuronal maturation and synaptogenesis in the rat ventrobasal complex: Alignment with developmental changes in rate and severity of axon reaction. J. comp. Neurol. (in press) 1977

  • Maxwell, D.S., Kruger, L.: Small blood vessels and the origin of phagocytes in the rat cerebral cortex following heavy particle irradiation. Exp. Neurol. 120, 33–54 (1965)

    Google Scholar 

  • Maxwell, D.S., Kruger, L.: The reactive oligodendrocyte, an electron microscopic study of cerebral cortex following alpha particle irradiation. Amer. J. Anat. 118, 437–460 (1966)

    Google Scholar 

  • Metz, A., Spatz, H.: Die Hortega'schen Zellen, das sogenannte ‘dritte Element’ und über ihre funktionelle Bedeutung. Z. Nervenheilk. 89, 138–170 (1924)

    Google Scholar 

  • Mori, S., Leblond, C.P.: Identification of microglia in light and electron microscopy. J. comp. Neurol. 135, 57–80 (1969)

    Google Scholar 

  • Mori, S., Leblond, C.P.: Electron microscopic identification of three classes of oligodendrocytes and a preliminary study of their proliferative activity in the corpus callosum of young rats. J. comp. Neurol. 139, 1–30 (1970)

    Google Scholar 

  • Morse, D.E., Low, F.N.: The fine structure of subarachnoid macrophages in the rat. Anat. Rec. 174, 469–476 (1972)

    Google Scholar 

  • Mugnaini, E., Walberg, F.: Ultrastructure of neuroglia. Ergebn. Anat. Entwickl.-Ges. 37, 194–236 (1964)

    Google Scholar 

  • Nissl, F.: Kritische Bemerkungen zu Schmaus. Vorlesungen über die pathologischen Anatomie des Rückenmarks. Zbl. Nervenheilk. Psych. 157 (1903)

  • Nissl, F.: Zur Histopathologie der paralytischen Rindenerkrankungen. Histol. hist. Arb. Großhirnrinde 10, 315–494 (1904)

    Google Scholar 

  • Oehmichen, M.: Monocytic origin of microglia cells. In: Mononuclear phagocytes in immunity, infection and pathology (R. van Furth, ed.). Oxford-London-Edinburgh-Melbourne: Blackwell Scientific Publications 1975

    Google Scholar 

  • Oehmichen, M., Saebisch, R.: Zur Problematik histochemischer Färbungen und autoradiographischer Technik. Acta histochem. (Jena) 41, 353–364 (1971)

    Google Scholar 

  • Paterson, J.A., Privat, A., Ling, E.A., Leblond, C.P.: Investigation of glial cells in semithin sections. III. Transformation of subependymal cells into glial cells, as shown by radioautography after 3H-thymidine injection into the lateral ventricle of the brain of young rats. J. comp. Neurol. 149, 83–102 (1973)

    Google Scholar 

  • Privat, A., Leblond, C.P.: The subependymal layer and neighboring region in the brain of the young rat. J. comp. Neurol. 146, 277–302 (1972)

    Google Scholar 

  • Ramón y Cajal, S.: Algunas consideraciones sobre la mesoglia de Robertson y Rio-Hortega. Trab. Lab. invest. Biol. 18, 109–127 (1920)

    Google Scholar 

  • Rio-Hortega, P. Del: Microglia. In: Cytology and cellular pathology of the nervous system, Vol. II (W. Penfield, ed.), pp. 482–543. New York: Paul B. Hoeber, Inc. 1932

    Google Scholar 

  • Santha, K. von, Juba, A.: Weitere Untersuchungen über die Entwicklung der Hortegaschen Mikroglia. Arch. Psychiat. Nervenkr. 98, 598–613 (1932)

    Google Scholar 

  • Schultz, R.L., Maynard, E.A., Pease, D.C.: Electron microscopy of neurons and neuroglia of cerebral cortex and corpus callosum. Amer. J. Anat. 100, 369–408 (1957)

    Google Scholar 

  • Stensaas, L.J.: Pericytes and perivascular microglial cells in the basal forebrain of the neonatal rabbit. Cell Tiss. Res. 158, 517–541 (1975)

    Google Scholar 

  • Stensaas, L.J., Gilson, B.C.: Ependymal and subependymal cells of the caudato-pallial junction in the lateral ventricle of the neonatal rabbit. Z. Zellforsch. 132, 297–322 (1972)

    Google Scholar 

  • Stensaas, L.J., Reichert, W.H.: Round and amoeboid microglial cells in the neonatal rabbit brain. Z. Zellforsch. 119, 147–163 (1971)

    Google Scholar 

  • Sumi, S.M., Hager, H.: Electron microscopic study of the reaction of the newborn rat brain to injury. Acta neuropath. (Berl.) 10, 324–335 (1968)

    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., Skoff, R.P.: Neuroglia in experimentally altered central nervous system. In: The structure and function of the nervous system, Vol. 5 (G.W. Bourne, ed.), pp. 39–72. New York: Academic Press 1972

    Google Scholar 

  • Waller, W.H.: Topographical relations of cortical lesions to thalamic nuclei in the albino rat. J. comp. Neurol. 60, 237–269 (1934)

    Google Scholar 

  • Welker, C.: Microelectrode delineation of fine grain somatotopic organization of SmI cerebral neocortex in albino rat. Brain Res. 26, 259–275 (1971)

    Google Scholar 

  • Westrum, L.E.: Electron microscopy of degeneration in the lateral olfactory tract and plexiform layer of the pre-pyriform cortex of the rat. Z. Zellforsch. 98, 157–187 (1969)

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Anatomy, Louisiana State University Medical Center, New Orleans, Louisiana, USA

    M. A. Matthews

Authors
  1. M. A. Matthews
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

A special note of thanks is given to Mrs. Merrill Frost, for aid with surgical procedures, to Ms. Christal Faciane and Mrs. Michelle St. Onge for technical assistance, to Mr. Garbis Kerimian, for preparing the micrographs and to Mrs. Susan Orazio and Mrs. Jo Ann Richard for typing the manuscript. This work was supported by a grant from the Edward G. Schlieder Foundation and N.I.H. Grant RR 05376-11

Rights and permissions

Reprints and permissions

About this article

Cite this article

Matthews, M.A. Reactive alterations in non-neuronal elements of the degenerating ventrobasal complex of immature and mature rats. Cell Tissue Res. 179, 413–427 (1977). https://doi.org/10.1007/BF00221111

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00221111

Key words

Search

Navigation