Summary
Astrocytes are implicated in the function of nodes of Ranvier because their perinodal processes form contacts with the axonal membrane at nodes. We have filled astrocytes iontophoretically with horseradish peroxidase in the intact mouse optic nerve to resolve the precise relationship between perinodal processes and astrocyte three dimensional structure. We confirm that nodal contacts were formed either by single processes which almost completely enveloped nodes, or by delicate, finger-like projections from larger processes which made discrete nodal contacts. A single perinodal process can form multiple contacts with a node and nodes were contacted by processes from more than one astrocyte. Perinodal processes emanated from larger processes, which terminated as end-feet on blood vessels and at the pia, as well as collateral branches which subsequently ended at nodes; these latter may specifically subserve nodes. Perinodal contacts were also formed directly by the soma and cytoplasmic expansions of the cell body. Both primary processes and collateral branches formed multiple associations with nodes which often appeared in clusters. Thus, all astrocytes formed multiple contacts with nodes, blood vessels and the subpial glia limitans. We conclude that perinodal processes are not formed by a specialized astrocyte in the mouse optic nerve.
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References
Black, J. A. &Waxman, S. G. (1988) The perinodal astrocyte.Glia 1, 169–83.
Black, J. A., Foster, R. E. &Waxman, S. G. (1982) Rat optic nerve: freeze-fracture studies during development of myelinated axons.Brain Research 250, 1–20.
Black, J. A., Felts, P., Smith, K. J., Kocsis, J. D. &Waxman, S. G. (1991) Distribution of sodium channels in chronically demyelinated spinal cord axons: immunoultrastructural localization and electrophysiological observations.Brain Research 544, 59–70.
Black, J. A., Friedman, B., Waxman, S. G., Elmer, L. W. &Angelides, K. J. (1989a) Immuno-ultrastructural localization of sodium channels at nodes of Ranvier and perinodal astrocyte processes in rat optic nerve.Proceedings of the Royal Society of London, Series B 238, 39–51.
Black, J. A., Waxman, S. G., Friedman, B., Elmer, L. W. &Angelides, K. J. (1989b) Sodium channels in astrocytes of rat optic nervein situ: immuno-electron microscopic studies.Glia 2, 353–69.
Blakemore, W. F. &Smith, K. J. (1983) Node-like axonal specialisations along demyelinated central nerve fibres: ultrastructural observations.Acta Neuropathologica (Berlin) 60, 291–6.
Butt, A. M. (1991) Macroglial cell types, lineage, and morphology in the CNS.Annals of the New York Academy of Sciences 633, 90–5.
Butt, A. M. &Ransom, B. R. (1989) Visualization of oligodendrocytes and astrocytes in the intact rat optic nerve by intracellular injection of Lucifer yellow and horseradish peroxidase.Glia 2, 470–5.
Butt, A. M. &Ransom, B. R. (1993) Morphology of astrocytes and oligodendrocytes during development in the intact rat optic nerve.Journal of Comparative Neurology 338, 141–58.
Butt, A. M., Colquhoun, K., Tutton, M. G. &Berry, M. (1994a) Three-dimensional morphology of astrocytes and oligodendrocytes in the intact mouse optic nerve.Journal of Neurocytology 23, 469–485.
Butt, A. M., Colquhoun, K. &Berry, M. (1994b) Confocal imaging of glial cells in the intact rat optic nerve.Glia 10, 315–22.
Ffrench-Constant, C. &Raff, M. C. (1986) The oligo-dendrocyte-type-2 astrocyte cell lineage is specialized for myelination.Nature 323, 335–8.
Ffrench-Constant, C., Miller, M. H., Kruse, J., Schachner, M. &Raff, M. C. (1986) Molecular specialization of astrocyte processes at nodes of Ranvier in rat optic nerve.Journal of Cell Biology 102, 844–52.
Fulton, B. P., Burne, J. F. &Raff, M. C. (1991) Glial cells in the rat optic nerve. The search for the type-2 astrocyte.Annals of the New York Academy of Sciences 633, 27–34.
Fulton, B. P., Burne, J. F. &Raff, M. C. (1992) Visualization of 0–2A progenitor cells in developing and adult rat optic nerve by quisqualate-stimulated cobalt uptake.Journal of Neuroscience 12, 4816–33.
Hatten, M. E. (1985) Neuronal regulation of astroglial morphology and proliferationin vitro.Journal of Cell Biology 100, 384–96.
Hildebrand, C. (1971a) Ultrastructural and light microscopic studies of the nodal region in large myelinated fibres of the adult feline spinal cord white matter.Acta Physiologica Scandinavica, Supplement 364, 43–71.
Hildebrand, C. (1971b) Ultrastructural and light microscopic studies of developing feline spinal cord white matter. I. The nodes of Ranvier.Acta Physiologica Scandinavica, Supplement 364, 81–101.
Hildebrand, C. &Waxman, S. G. (1984) Postnatal differentiation of rat optic nerve fibres: electron microscopic observations on the development of nodes of Ranvier and axoglial relations.Journal of Comparative Neurology 224, 25–37.
Hildebrand, C., Remahl, S., Persson, H. &Bjartmar, C. (1993) Myelinated fibres in the CNS.Progress in Neurobiology 40, 319–84.
Maggs, A. &Scholes, J. (1990) Reticular astrocytes in the fish optic nerve: macroglia with epithelial characteristics form an axially repeated lacework pattern, to which nodes of Ranvier are apposed.Journal of Neuroscience 10, 1600–14.
Miller, R. H., Fulton, B. P. &Raff, M. C. (1989) A novel type of glial cell associated with nodes of Ranvier in rat optic nerve.European Journal of Neuroscience 1, 172–80.
Miller, R. H., David, S., Patel, R., Abney, E. R. &Raff, M. C. (1985) A quantitative immunohistochemical study of macroglial cell development in the rat optic nerve:in vivo evidence for two distinct astrocyte lineages.Developmental Biology 111, 35–41.
Mugnaini, E. (1986) Cell junctions of astrocytes, ependyma, and related central nervous system, with emphasis on the hypothesis of a generalized functional syncytium of supporting cells. In:Astrocytes, Vol. 1. (edited byFederoff, S. &Vernadakis, A.) pp. 329–71. New York: Academic Press.
Oldfield, B. J. &Bray, G. M. (1982) Differentiation of the nodal and internodal axolemma in the optic nerves of neonatal rats.Journal of Neurocytology 11, 627–40.
Penfield, W. (1932)Cytology and Cellular Pathology of the Nervous System. Vol. 2. Neuroglia: Normal and Pathological. New York: Hoeber.
Peters, A. (1966) The node of Ranvier in the central nervous system.Quarterly Journal of Experimental Physiology 51, 229–36.
Raff, M. C., Miller, R. H. &Noble, M. (1983) A glial precursor cell that developsin vitro into an astrocyte or an oligodendrocyte depending on culture medium.Nature 303, 390–6.
Raff, M. C., Abney, E. R. &Miller, R. H. (1984) Two glial cell lineages diverge prenatally in rat optic nerve.Developmental Biology 106, 53–60.
Raine, C. (1984) On the association between perinodal astrocytic processes and the node of Ranvier in the CNS.Journal of Neurocytology 13, 21–7.
Ramón Y Cajal, S. (1909–11)Histologie du Système Nerveux de l'homme et des Vertébrés. Paris, vol. 1, Reprinted 1952, Cons. Sup. Invest. Cientificas, Institute Ramon y Cajal, Madrid.
Ransom, B. R., Butt, A. M. &Black, J. (1991) Ultrastructural identification of HRP-injected oligodendrocytes in the intact rat optic nerve.Glia 4, 37–45.
Rosenbluth, J. (1976) Intramembranous particle distribution at the node of Ranvier and adjacent axolemma in myelinated axons of the frog brain.Journal of Neurocytology 5, 731–45.
Rosenbluth, J. (1988) Role of glial cells in the differentiation and function of myelinated axons.International Journal of Developmental Neuroscience 6, 3–24.
Rosenbluth, J., Tao-Cheng, J.-H. &Blakemore, W. F. (1985) Dependence of axolemmal differentiation on contact with glial cells in chronically demyelinated lesions of cat spinal cord.Brain Research 358, 287–302.
Sims, T. J., Waxman, S. G., Black, J. A. &Gilmore, S. A. (1985) Perinodal astrocytic processes at nodes of Ranvier in developing normal and glial cell deficient rat spinal cord.Brain Research 337, 321–31.
Skoff, R. P. (1990) Gliogenesis in rat optic nerve: astrocytes are generated in a single wave before oligodendrocytes.Developmental Biology 139, 149–68.
Sobue, G. &Pleasure, D. (1984) Astroglial proliferation and phenotype are modulated by neuronal plasma membrane.Brain Research 324, 175–9.
Soffer, D. &Raine, C. S. (1980) Morphologic analysis of axo-glial membrane specializations in the demyelinated central nervous system.Brain Research 186, 301–13.
Suarez, I. &Raff, M. C. (1989) Subpial and perivascular astrocytes associated with nodes of Ranvier in the rat optic nerve.Journal of Neurocytology 18, 577–82.
Suzuki, M. &Raisman, G. (1992) The glial framework of central white matter tracts: segmented rows of contiguous interfascicular oligodendrocytes and solitary astrocytes give rise to a continuous meshwork of transverse and longitudinal processes in the adult rat fimbria.Glia 6, 222–35.
Tao-Cheng, J.-H. &Rosenbluth, J. (1984) Extranodal particle accumulations in the axolemma of myelinated frog optic axons.Brain Research 308, 289–300.
Waxman, S. G. &Black, J. A. (1984) Freeze-fracture ultrastructure of the perinodal astrocyte and associated glial junctions.Brain Research 308, 77–87.
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Butt, A.M., Duncan, A. & Berry, M. Astrocyte associations with nodes of Ranvier: ultrastructural analysis of HRP-filled astrocytes in the mouse optic nerve. J Neurocytol 23, 486–499 (1994). https://doi.org/10.1007/BF01184072
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DOI: https://doi.org/10.1007/BF01184072