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Axo-glial relations in the retina-optic nerve junction of the adult rat: freeze-fracture observations on axon membrane structure

  • Published:
Journal of Neurocytology

Summary

The axolemmal ultrastructure of nerve fibres within the retina-optic nerve junction (ROJ) from adult rats was examined by freeze-fracture electron microscopy. In the juxtaocular (proximal) region of the ROJ, all fibres are unmyelinated. The axons generally have a membrane ultrastructure similar to that of retinal nerve fibre layer axons, with a high density of intramembranous particles (IMPs) on the P-fracture face and a low density of IMPs on the E-face. However, along some axons in this region of the ROJ, localized aggregations of E-face IMPs are observed. At levels of the ROJ closer to the optic nerve proper, the unmyelinated fibres enter a transition zone in which the axons acquire myelin sheaths. By the distal boundary of the transitional zone (optic nerve proper), virtually all fibres are myelinated. Within the transitional zone, conventional axo-glial associations and axolemmal ultrastructure is present at nodes of Ranvier. In addition, atypical axo-glial relationships and atypical nodal segments are observed in this region. At some nodes, an isolated oligodendroglial process traverses obliquely across the nodal membrane. Beneath the oligodendroglial process, the axolemma usually displays a paranodal-like ultrastructure. Finger-like oligodendroglial processes were also observed in association with non-nodal unmyelinated axon membrane. At these sites of association, the axon membrane tends to be indented and may have a paranodal-like morphology. Nodal axolemma may exhibit several atypical forms in the transition zone. At some nodes, the nodal axolemma has a low density of E-face particles. Also, nodes of extended linear length (∼2μm) exhibit a lower-than-normal density of P-face IMPs. At heminodes, the axolemma immediately adjacent to the terminal loops lacks the usual nodal characteristics of high IMP density and high percentage of large particles. The results show that aberrant axo-glial associations accompanied by unusual ultrastructural characteristics of the axolemma are present in the ROJ of normal adult rats.

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References

  • Aguayo, A. J. &Bray, G. M. (1982) Developmental disorders of myelination in mouse mutants. InNeuronal-glial Cell Interrelationships (edited bySears, T. A.), pp. 57–76. Berlin, Heidelberg, New York: Springer-Verlag.

    Google Scholar 

  • Black, J. A., Foster, R. E. &Waxman, S. G. (1981) Freeze-fracture ultrastructure of rat C.N.S. and P.N.S. nonmyelinated axolemma.Journal of Neurocytology 10, 981–93.

    PubMed  Google Scholar 

  • Black, J. A., Foster, R. E. &Waxman, S. G. (1982a) Rat optic nerve: freeze-fracture studies during development of myelinated axons.Brain Research 250, 1–20.

    PubMed  Google Scholar 

  • Black, J. A., Foster, R. E. &Waxman, S. G. (1983) Freeze-fracture ultrastructure of developing and adult non-myelinated ganglion cell axolemma in the retinal nerve fibre layer.Journal of Neurocytology 12, 201–12.

    PubMed  Google Scholar 

  • Black, J. A., Sims, T. J., Waxman, S. G. &Gilmore, S. A. (1985) Membrane ultrastructure of developing axons in glial cell deficient rat spinal cord.Journal of Neurocytology 14, 78–104.

    Google Scholar 

  • Black, J. A., Waxman, S. G. &Foster, R. E. (1982b) Spatial heterogeneity of the axolemma of non-myelinated fibers in the optic disc of the adult rat: freeze-fracture observations.Cell and Tissue Research 224, 239–246.

    PubMed  Google Scholar 

  • Black, J. A., Waxman, S. G. &Hildebrand, C. (1984) Membrane specialization and axo-glial association in the rat retinal nerve fibre layer: freeze-fracture observations.Journal of Neurocytology 13, 417–30.

    PubMed  Google Scholar 

  • Bray, G. M., Duncan, I. D. &Griffiths, I. R. (1983) ‘Shaking pups’: a disorder of central myelination in the spaniel dog. IV. Freeze-fracture electron microscopic studies of axons, oligodendrocytes and astrocytes in the spinal cord white matter.Neuropathology and Applied Neurobiology 9, 355–368.

    PubMed  Google Scholar 

  • Bray, G. M., Rasminsky, M. &Aguayo, A. J. (1981) Interactions between axons and their sheath cells.Annual Review of Neuroscience 4, 127–62.

    PubMed  Google Scholar 

  • Conti, F., Hille, B., Neumcke, B., Nonner, W. &Stämplfi, R. (1976) Conductance of the sodium channels in myelinated nerve fibres with moderate sodium inactivation.Journal of Physiology 262, 729–42.

    PubMed  Google Scholar 

  • Deerinck, T. J. &Ellisman, M. H. (1984) Transcellular filaments at the node of Ranvier.Neurosciences Abstracts 10, 163.

    Google Scholar 

  • Ellisman, M. H. (1977) High voltage electron microscopy of cortical specializations associated with membranes at nodes of ranvier.Journal of Cell Biology 75, 108a.

    Google Scholar 

  • Ellisman, M. H. (1979) Molecular specializations of the axon membrane at nodes of Ranvier are not dependent upon myelination.Journal of Neurocytology 8, 719–35.

    PubMed  Google Scholar 

  • Elfvin, L. G. (1961) The ultrastructure of the nodes of Ranvier in cat sympathetic fibers.Journal of Ultrastructure Research 5, 374–87.

    PubMed  Google Scholar 

  • Hildebrand, C. (1971) Ultrastructural and light-microscopic studies of the developing feline spinal cord white matter. I. The nodes of Ranvier.Acta physiologica scandinavica, Suppl.364, 81–109.

    Google Scholar 

  • Hildebrand, C., Remahl, S. &Waxman, S. G. (1985) Axo-glial relations in the retina-optic nerve junction of the adult rat: electron-microscopic observations.Journal of Neurocytology 14, 597–617.

    Google Scholar 

  • Hildebrand, C. &Waxman, S. G. (1983) Regional node-like membrane specializations in non-myelinated axons of rat retinal nerve fiber layer.Brain Research 258, 23–32.

    Google Scholar 

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

    PubMed  Google Scholar 

  • Kristol, C., Akert, K., Sandri, C., Wyss, U. R., Bennett, M. V. L. &Moor, H. (1977) The Ranvier nodes in the neurogenic electric organ of the knifefishSternarchus: a freeze-etching study on the distribution of membrane-associated particles.Brain Research 125, 197–212.

    PubMed  Google Scholar 

  • Kristol, C., Sandri, C. &Akert, K. (1978) Intramembranous particles at the nodes of Ranvier of the cat spinal cord: a morphometric study.Brain Research 142, 391–400.

    PubMed  Google Scholar 

  • Oaklander, A. L., Pellegrino, R. G. &Ritchie, J. M. (1984) Saxitoxin binding to central and peripheral nervous tissue of the myelin deficiency (md) mutant rat.Brain Research 307, 393–7.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Quick, D. C., Kennedy, W. R. &Donaldson, L. (1979) Dimensions of myelinated nerve fibers near the motor and sensory terminals in cat tenuissimus muscle.Neuroscience 4, 1089–96.

    PubMed  Google Scholar 

  • Revenko, S. V., Timin, Y. N. &Khodorov, B. I. (1973) Special features of the conduction of nerve impulses from the myelinated part of the axon into the non-myelinated terminal.Biofizika 18, 1074–8.

    PubMed  Google Scholar 

  • Ritchie, J. M. &Rogart, R. B. (1977) Density of sodium channels in mammalian myelinated nerve fibers and the nature of the axonal membrane under the myelin sheath.Proceedings of the National Academy of Sciences, USA 74, 211–5.

    Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Rosenbluth, J. (1979) Aberrant axon-Schwann cell junctions in dystrophic mouse nerves.Journal of Neurocytology 8, 655–72.

    PubMed  Google Scholar 

  • Rosenbluth, J. (1981a) Axoglial junctions in the mouse mutant Shiverer.Brain Research 208, 283–97.

    PubMed  Google Scholar 

  • Rosenbluth, J. (1981b) Freeze-fracture approaches to ionophore localization in normal and myelin-deficient nerves. InDemyelinating Disease: Basic and Clinical Electrophysiology (edited byWaxman, S. G. &Ritchie, J. M.), pp. 391–418. New York: Raven Press.

    Google Scholar 

  • Rosenbluth, J. (1983) Structure of the node of Ranvier. InStructure and Function in Excitable Cells (edited byChang, D. C., Tasaki, I., Adelman, W. J. &Leuchtag, R.), pp. 25–52. New York: Plenum Press.

    Google Scholar 

  • Waxman, S. G. (1977) Conduction in myelinated, unmyelinated, and demyelinated fibers.Archives of Neurology 34, 585–9.

    PubMed  Google Scholar 

  • Waxman, S. G., Bradley, W. G. &Hartwieg, E. A. (1978) Organization of the axolemma in amyelinated axons: a cytochemical study in dy/dy dystrophic mice.Proceedings of the Royal Society of London, Series B 201, 301–8.

    Google Scholar 

  • Waxman, S. G. &Brill, M. H. (1978) Conduction through demyelinated plaques in multiple sclerosis: computer simulations of facilitation by short internodes.Journal of Neurology, Neurosurgery and Psychiatry 41, 408–17.

    Google Scholar 

  • Waxman, S. G. &Foster, R. E. (1980) Development of the axon membrane during differentiation of myelinated fibres in spinal nerve roots.Proceedings of the Royal Society of London, Series B 209, 441–6.

    Google Scholar 

  • Waxman, S. G. &Quick, D. C. (1978) Intra-axonal ferric ion-ferrocyanide staining of nodes of Ranvier and initial segments in central myelinated fibers.Brain Research 144, 1–10.

    PubMed  Google Scholar 

  • Waxman, S. G. &Ritchie, J. M. (1985) Organization of ion channels in the myelinated nerve fiber.Science 228, 1502–7.

    PubMed  Google Scholar 

  • Wiley-Livingston, C. A. &Ellisman, M. H. (1981) Development of axonal membrane specializations defines nodes of Ranvier and precedes Schwann cell myelin elaboration.Developmental Biology 79, 344–55.

    Google Scholar 

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Black, J.A., Waxman, S.G. & Hildebrand, C. Axo-glial relations in the retina-optic nerve junction of the adult rat: freeze-fracture observations on axon membrane structure. J Neurocytol 14, 887–907 (1985). https://doi.org/10.1007/BF01224803

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