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Three-dimensional morphology of astrocytes and oligodendrocytes in the intact mouse optic nerve

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Journal of Neurocytology

Summary

The three-dimensional morphology of astrocytes and oligodendrocytes was analysed in the isolated intact mature mouse optic nerve, by correlating laser scanning confocal microscopy and camera lucida drawings of single cells, dye-filled with lysinated rhodamine dextran or horseradish peroxidase, respectively. These techniques enabled the entire process field of single dye-filled cells to be visualized in all planes and resolved the fine details of glial morphology. Morphometric analysis showed that the processes of all astrocytes had branches ending at the pial surface, on blood vessels, and freely in the nerve; branches ending in the nerve were described to end at nodes of Ranvier in the accompanying paper. Astrocytes were classified into a single morphological population in which each cell subserved multiple functions. The results of this study do not support the contention that astrocytes can be subdivided into two morphological and functional subtypes, namely type-1 and type-2, which have processes ending either at the glia limitans or at nodes, respectively. Three-dimensional analysis of oligodendrocyte units, defined as the oligodendrocyte, its processes and the axons it ensheaths, showed the provision of single myelin segments for an average of 19 nearby axons (range 12–35) with a mean internodal length of 138 μm (range 50–350 μm). Mouse optic nerve oligodendrocytes were a homogeneous population and were markedly similar to those in the rat optic nerve. The results of our analysis of oligodendrocyte morphology are consistent with the view that the number and internodal length of myelin sheaths supported by a single oligodendrocyte are related to the diameter of the ensheathed axons.

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References

  • Abbott, N. J., Revest, P. A. &Romero, I. A. (1992) Astrocyte-endothelial interaction: physiology and pathology.Neuropathology and Applied Neurobiology 18, 424–33.

    Google Scholar 

  • Berger, T. &Frotscher, M. (1993) Distribution and morphological characteristics of oligodendrocytesin situ andin vitro — an immunocytochemical study with the monoclonal Rip antibody.Journal of Neurocytology 23, 61–74.

    Google Scholar 

  • Berger, T., Schnitzer, J. &Kettenmann, H. (1991) Developmental changes in the membrane current pattern, K+ buffer capacity, and morphology of glial cells in the corpus callosum slice.Journal of Neuroscience 11, 3008–24.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Blakemore, W. F. &Murray, J. A. (1981) Quantitative examination of internodal length of remyelinated nerve fibres in the central nervous system.Journal of the Neurological Sciences 49, 273–84.

    Google Scholar 

  • Blakemore, W. F. &Smith, K. J. (1983) Node-like axonal specialisations along demyelinated central nerve fibres: ultrastructural observations.Acta Neuropathologica 60, 291–6.

    Google Scholar 

  • Brightman, M. W. &Reese, T. S. (1969) Junctions between intimately apposed cell membranes in the vertebrate brain.Journal of Cell Biology 40, 648–77.

    Google Scholar 

  • Bunge, R. P. (1968) Glial cells and the central myelin sheath.Physiological Reviews 48, 197–251.

    Google Scholar 

  • Bunge, M. B., Bunge, R. P. &Pappas, G. D. (1967) Electron microscopic demonstration of connections between glia and myelin sheaths in the developing mammalian nervous system.Journal of Cell Biology 12, 448–53.

    Google Scholar 

  • Butt, A. M. (1991) Macroglial cell types, lineage, and morphology in the CNS.Annals of the New York Academy of Sciences 633, 90–5.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Butt, A. M., Duncan, A. &Berry, M. (1994a) Astrocyte association with nodes of Ranvier: ultrastructural analysis of HRP-filled astrocytes in the mouse optic nerve.Journal of Neurocytology,23, 486–499.

    Google Scholar 

  • Butt, A. M., Colquhoun, K. &Berry, M. (1994b) Confocal imaging of glial cells in the intact rat optic nerve.Glia 10, 315–22.

    Google Scholar 

  • Chan-Ling, T. &Stone, J. (1991) Factors determining the morphology and distribution of astrocytes in the cat retina: a ‘contact-spacing’ model of astrocyte interaction.Journal of Comparative Neurology 303, 387–99.

    Google Scholar 

  • Del Rio-Hortega, P. (1928) Tercera aportación al conocimiento morfologica e interpretación funcional de la oligodendroglia.Memorias de la Real Sociedad Espanola de Historia Natural 14, 5–122.

    Google Scholar 

  • Dennis, M. J. &Gerschenfeld, H. M. (1969) Some physiological properties of identified mammalian neuroglial cells.Journal of Physiology 203, 211–22.

    Google Scholar 

  • Dermietzel, R. (1974) Junctions in the central nervous system of the cat. III. Gap junctions and membrane associated orthogonal particle complexes (MOPC) in astrocyte membranes.Cell and Tissue Research 149, 121–35.

    Google Scholar 

  • Eberhardt, W. &Reichenbach, A. (1987) Spatial buffering of potassium by retinal Müller (glial) cells of various morphologies calculated by a model.Neuroscience 22, 687–96.

    Google Scholar 

  • Ffrench-Constant, C. &Raff, M. C. (1986a) Proliferating bipotential glial progenitor cells in adult rat optic nerve.Nature 319, 499–502.

    Google Scholar 

  • Ffrench-Constant, C. &Raff, M. C. (1986b) The oligo-dendrocyte-type-2 astrocyte cell lineage is specialized for myelination.Nature 323, 335–8.

    Google Scholar 

  • 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.

    Google Scholar 

  • Foster, R. E., Connors, B. W. &Waxman, S. G. (1982) Rat optic nerve: electrophysiological, pharmacological and anatomical studies during development.Developmental Brain Research 3, 371–86.

    Google Scholar 

  • Friedman, B., Hockfield, S., Black, J. A., Woodruff, K. A. &Waxman, S. G. (1989)In situ demonstration of mature oligodendrocytes and their processes: an immunocytochemical study with a new monoclonal antibody, Rip.Glia 2, 380–90.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Gledhill, R. F. &Mcdonald, W. I. (1977) Morphological characteristics of central demyelination and remyelination: a single fibre study.Annals of Neurology 1, 552–60.

    Google Scholar 

  • Godement, P., Vanselow, J., Thanos, S. &Bonhoeffer, F. (1987) A study in developing visual systems with a new method of staining neurones and their processes in fixed tissue.Development 101, 697–713.

    Google Scholar 

  • Gotow, T. (1984) Cytochemical characteristics of astrocytic plasma membranes specialized with numerous orthogonal arrays.Journal of Neurocytology 13, 431–48.

    Google Scholar 

  • Gotow, T. &Hashimoto, P. H. (1989) Developmental alterations in membrane organization of rat subpial astrocytes.Journal of Neurocytology 18, 731–47.

    Google Scholar 

  • Hatten, M. E. (1985) Neuronal regulation of astroglial morphology and proliferationin vitro.Journal of Cell Biology 100, 384–96.

    Google Scholar 

  • Hess, A. &Young, J. Z. (1949) Correlation of internodal length and fibre diameter in the central nervous system.Nature 164, 490–1.

    Google Scholar 

  • Hess, A. &Young, J. Z. (1952) The nodes of Ranvier.Proceedings of the Royal Society of London, Series B 140, 301–20.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Hildebrand, C. &Waxman, S. G. (1984) Postnatal differentiation of rat optic nerve fibers: electron microscopic observation on the development of nodes of Ranvier and axoglial relations.Journal of Comparative Neurology 224, 25–37.

    Google Scholar 

  • Hildebrand, C., Remahl, S., Persson, H. &Bjartmar, C. (1993) Myelinated fibres in the CNS.Progress in Neurobiology 40, 319–84.

    Google Scholar 

  • Hirano, A. (1968) A confirmation of oligodendroglial origin of myelin in the adult rat.Journal of Cell Biology 38, 637–40.

    Google Scholar 

  • Hirano, A. &Dembitzer, H. M. (1967) A structural analysis of the myelin sheath in the central nervous system.Journal of Cell Biology 34, 555–67.

    Google Scholar 

  • Jaeger, C. B. (1988) Plasticity of astroglia: evidence supporting process elongation by ‘stretch’.Glia 1, 31–8.

    Google Scholar 

  • Jhaveri, S., Erzurumlu, R. S., Friedman, B. &Schneider, G. E. (1992) Oligodendrocytes and myelin formation along the optic tract of the developing hamster: an immunohistochemical study using the Rip antibody.Glia 6, 138–48.

    Google Scholar 

  • Klatzo, I. (1952) A study of glia by the Golgi method.Laboratory Investigation 1, 345–50.

    Google Scholar 

  • Landis, D. M. D. (1981) Membrane structure in mammalian astrocytes: a review of freeze-fracture studies on adult, developing, reactive and cultured astrocytes.Journal of Experimental Biology 95, 35–48.

    Google Scholar 

  • Landis, D. M. D. &Reese, T. S. (1974) Arrays of particles in freeze-fractured astrocytic membranes.Journal of Cell Biology 60, 316–20.

    Google Scholar 

  • Landis, D. M. D. &Reese, T. S. (1982) Regional organization of astrocytic membranes in cerebellar cortex.Neuroscience 7, 937–50.

    Google Scholar 

  • Lassman, H., Zimprich, F., Vass, K. &Hickey, W. F. (1991) Microglial cells are a component of the perivascular glia limitans.Journal of Neuroscience Research 28, 236–43.

    Google Scholar 

  • Lent, R. &Jhaveri, S. (1991) Myelination of the cerebral commissures of the hamster, as revealed by a monoclonal antibody specific or oligodendrocytes.Developmental Brain Research 66, 193–201.

    Google Scholar 

  • Levison, S. W. &Goldman, J. E. (1993) Both oligodendrocytes and astrocytes develop from progenitors in the subventricular zone of postnatal rat forebrain.Neuron 10, 201–12.

    Google Scholar 

  • Ling, T., Mitrofanis, J. &Stone, J. (1989) Origin of retinal astrocytes in the rat: evidence of migration from the optic nerve.Journal of Comparative Neurology 286, 345–52.

    Google Scholar 

  • Marrero, H., Orkand, P. M., Kettenmann, H. &Orkand, R. K. (1991) Single channel recording from glial cells on the untreated surface of the frog optic nerve.European Journal of Neuroscience 3, 813–19.

    Google Scholar 

  • Marriott, D. R. &Wilkin, G. P. (1993) Substance P receptors on 0–2A progenitor cells and type-2 astrocytesin vitro.Journal of Neurochemistry 61, 826–34.

    Google Scholar 

  • Matthews, M. A. &Duncan, D. (1971) A quantitative study of morphological changes accompanying the initiation and progress of myelin production in the dorsal funiculus of the rat spinal cord.Journal of Comparative Neurology 142, 1–22.

    Google Scholar 

  • Mcdonald, W. I. &Ohlrich, G. D. (1971) Quantitative anatomical measurements on single isolated fibres from the cat spinal cord.Journal of Anatomy 110, 191–202.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Murray, J. A. &Blakemore, W. F. (1980) The relationship between internodal length and fibre diameter in the spinal cord of the cat.Journal of the Neurological Sciences 45, 29–41.

    Google Scholar 

  • Newman, E. A. (1986) High potassium conductance in astrocyte endfeet.Science 233, 453–4.

    Google Scholar 

  • Newman, E. A., Frambach, D. A. &Odette, L. L. (1984) Control of extracellular potassium levels by retinal glial cell K+ siphoning.Science 225, 1174–5.

    Google Scholar 

  • Ogawa, Y., Eins, S. &Wolff, J. R. (1985) Oligodendrocytes in the pons and middle cerebellar peduncle of the cat.Cell and Tissue Research 240, 541–52.

    Google Scholar 

  • Orkand, R. K. (1986) Introductory remarks: glial-interstitial fluid exchange.Annals of the New York Academy of Sciences 481, 269–72.

    Google Scholar 

  • Penfield, W. (1924) Oligodendroglia and its relation to classical neuroglia.Brain 47, 430–52.

    Google Scholar 

  • Penfield, W. (1932)Cytology and Cellular Pathology of the Nervous System. Vol. 2. Neuroglia: Normal and Pathological. New York: Hoeber.

    Google Scholar 

  • Peters, A. (1964) Observations on the connexions between myelin sheaths and glial cells in the optic nerves of young rats.Journal of Anatomy 98, 125–34.

    Google Scholar 

  • Peters, A. (1966) The node of Ranvier in the central nervous system.Quarterly Journal of Experimental Physiology 51, 229–36.

    Google Scholar 

  • Peters, A. &Proskauer, C. C. (1969) The ratio between segments and oligodendrocytes in the optic nerve of the adult rat.Anatomical Record 163, 243 (Abstract).

    Google Scholar 

  • Raff, M. C. (1989) Glial cell diversification in the rat optic nerve.Science 243, 1450–5.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Raine, C. (1984) On the association between perinodal astrocytic processes and the node of Ranvier in the CNS.Journal ofNeurocytology 13, 21–7.

    Google Scholar 

  • 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 Ramón y Cajal, Madrid.

    Google Scholar 

  • 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.

    Google Scholar 

  • Reichenbach, A. (1989) Attempt to classify glial cells by means of their process specialization using the rabbit retinal Müller cell as an example of cytotopographic specialization of glial cells.Glia 2, 250–9.

    Google Scholar 

  • Remahl, S. &Hildebrand, C. (1990a) Relation between axons and oligodendroglial cells during initial myelination. I. The glial unit.Journal of Neurocytology 19, 313–28.

    Google Scholar 

  • Remahl, S. &Hildebrand, C. (1990b) Relations between axons and oligodendroglial cells during initial myelination. II. The individual axon.Journal of Neurocytology 19, 883–98.

    Google Scholar 

  • Robinson, S. R. &Dreher, Z. (1989) Evidence for three morphological classes of astrocyte in the adult rabbit retina: functional and developmental implications.Neuroscience Letters 106, 261–8.

    Google Scholar 

  • Schmechel, D. E. &Rakic, P. (1979) A Golgi study of radial glial cells in developing monkey telencephalon: morphogenesis and transformation into astrocytes.Anatomy and Embryology 156, 115–52.

    Google Scholar 

  • 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.

    Google Scholar 

  • Skoff, R. P. (1990) Gliogenesis in rat optic nerve: astrocytes are generated in a single wave before oligodendrocytes.Developmental Biology 139, 149–68.

    Google Scholar 

  • Skoff, R. P. &Knapp, P. E. (1991) Division of astroblasts and oligodendroblasts in postnatal rodent brain: evidence for separate astrocyte and oligodendrocyte lineages.Glia 4, 165–74.

    Google Scholar 

  • Skoff, R. P., Price, D. L. &Stocks, A. (1976a) Electron microscopic autoradiographic studies of gliogenesis in the rat optic nerve. I. Cell proliferation.Journal of Comparative Neurology 169, 291–312.

    Google Scholar 

  • Skoff, R. P., Price, D. L. &Stocks, A. (1976b) Electron microscopic autoradiographic studies of gliogenesis in the rat optic nerve. II. Time of origin.Journal of Comparative Neurology 169, 313–34.

    Google Scholar 

  • Sobue, G. &Pleasure, D. (1984) Astroglial proliferation and phenotype are modulated by neuronal plasma membrane.Brain Research 324, 175–9.

    Google Scholar 

  • Soffer, D. &Raine, C. S. (1980) Morphologic analysis of axo-glial membrane specializations in the demyelinated central nervous system.Brain Research 186, 301–13.

    Google Scholar 

  • Stensaas, L. J. &Stensaas, S. S. (1968) Astrocytic neuroglial cells, oligodendrocytes and microgliacytes in the spinal cord of the toad. I. Light microscopy.Zeitschrift für Zellforschung und mikroskopische Anatomie 84, 473–89.

    Google Scholar 

  • Sternberger, N. H., Itoyama, Y., Kies, M. W. &Webster, H. De F. (1978) Immunocytochemical method to identify basic protein in myelin-forming oligodendrocytes of newborn rat CNS.Journal of Neurocytology 7, 251–63.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    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 

  • Vaughn, J. E. &Peters, A. (1967) Electron microscopy of the early postnatal development of fibrous astrocytes.American Journal of Anatomy 121, 131–52.

    Google Scholar 

  • Voigt, T. (1989) Development of glial cells in the cerebral wall of ferrets: direct tracing of their transformation from radial glia into astrocytes.Journal of Comparative Neurology 289, 74–88.

    Google Scholar 

  • Waxman, S. G. &Black, J. A. (1984) Freeze-fracture ultrastructure of the perinodal astrocyte and associated glial junctions.Brain Research 308, 77–87.

    Google Scholar 

  • Wolswijk, G. &Noble, M. (1989) Identification of an adult-specific glial progenitor cell.Development 105, 387–400.

    Google Scholar 

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Butt, A.M., Colquhoun, K., Tutton, M. et al. Three-dimensional morphology of astrocytes and oligodendrocytes in the intact mouse optic nerve. J Neurocytol 23, 469–485 (1994). https://doi.org/10.1007/BF01184071

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