Summary
Axon plasma membranes (axolemma) were studied by freeze-fracture electron microscopy at stages prior to and during myelination in the optic nerves of neonatal rats. In unensheathed axons, intramembranous particles associated with the internal (P) and external (E) leaflets of the axolemma increased in number before reaching a plateau (approximately 600/μm2 in both leaflets) at about 9 days postnatally. In newly myelinated fibres, by contrast, the distribution of particles was asymmetrical; fewer particles (approximately 200/μm2) were found on the E-face and greater numbers (approximately 1400/μm2) were present on the P-face, distributions similar to those observed in mature myelinated fibres. Node-like aggregations of particles were not found in unensheathed pre-myelinated axons nor were they present in axons presumed to be ensheathed by glial cytoplasm but not yet myelinated, although nodal specializations could be easily identified in fibres with only a few turns of compact myelin. These observations show first that there is a redistribution of particles in the P- and E-faces of the internodal axolemma coincident with the onset of myelination and secondly, that nodal specializations (represented by the increased densities of E-face particles) appear after ensheathment but before the formation of compact myelin in fibres of the rat optic nerve.
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References
Aguayo, A. J., Bray, G. M. &Perkins, C. S. (1979) Axon-Schwann cell relationships in neuropathies of mutant mice.Annals of the New York Academy of Sciences 317, 512–31.
Aguayo, A. J., Charron, L. &Bray, G. M. (1976) Potential of Schwann cells from unmyelinated nerves to produce myelin: A quantitative ultrastructural and autoradiographic study.Journal of Neurocytology 5, 565–73.
Bernstein, J. J. (1966) Relationship of corticospinal tract growth to age and body weight in the rat.Journal of Comparative Neurology 127, 207–18.
Berthold, C-H. (1968) Ultrastructure of the node-paranode region of mature feline ventral lumbar spinal root fibres.Acta Societatis medicorum upsaliensis 73, Suppl. 9, 37–70.
Black, J. A., Foster, R. E. &Waxman, S. G. (1981) Freeze-fracture ultrastructure of adult and developing optic nerves.Anatomical Record 199, 27A Abs.
Bostock, H., Hall, S. M. &Smith, K. J. (1980) Demyelinated axons can form nodes prior to remyelination.Journal of Physiology 308, 21P.
Bray, G. M., Cullen, M. J., Aguayo, A. J. &Rasminsky, M. (1979) Node-like areas of intramembranous particles in the unensheathed axons of dystrophic mice.Neuroscience Letters 13, 203–8.
Bullivant, S. (1977) Evaluation of membrane structure facts and artefacts produced during freeze-fracturing.Journal of Microscopy 111, 101–16.
Conti, F., Hille, B., Neumcke, B., Nonner, W. &Stampfli, R. (1976) Measurement of the conductance of the sodium channel from current fluctuations at the node of Ranvier.Journal of Physiology 262, 699–727.
Dempsey, G. P., Bullivant, S. &Watkins, W. B. (1973) Endothelial cell membranes: Polarity of particles as seen by freeze-fracture.Science 179, 190–2.
Dermietzel, R. (1974) Junctions in the central nervous system of the cat. III. Gap junctions and membrane associated orthogonal particle complexes (MOPC) in astrocytic membranes.Cell and Tissue Research 149, 129–35.
Dermietzel, R. &Kroczek, H. (1980) Interlamellar tight junctions of central myelins. I. Developmental mechanisms during myelinogenesis.Cell and Tissue Research 213, 81–94.
Ellisman, M. H. (1976) The distribution of membrane molecular specializations characteristic of the node of Ranvier is not dependent upon myelination.Neuroscience Abstracts 2, 410.
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.
Feasby, T. E., Bostock, H. &Sears, T. A. (1981) Conduction in regenerating dorsal root fibres.Journal of the Neurological Sciences 49, 439–54.
Foster, R. E., Whalen, C. C. &Waxman, S. G. (1980) Reorganization of the axon membrane in demyelinated peripheral nerve fibres: Morphological evidence.Science 210, 661–3.
Fraher, J. P. (1972) A quantitative study of anterior root fibres during early myelination.Journal of Anatomy 112, 99–124.
Friede, R. L. &Samorajski, T. (1967) Relation between the number of myelin lamellae and axon circumference in fibres of vagus and sciatic nerves of mice.Journal of Comparative Neurology 130, 223–31.
Garcia-Segura, L. M. &Perrelet, A. (1981) Freeze-fracture of developing neuronal plasma membrane in postnatal cerebellum.Brain Research 208, 19–33.
Gross, H., Kuebler, O., Bas, E. &Moor, H. (1978) Decoration of specific sites on freeze-fractured membranes.Journal of Cell Biology 79, 646–56.
Heuser, J. E., Reese, T. S., Dennis, M. J., Jan, Y., Jan, L. &Evans, L. (1979) Synaptic vesicle exocytosis captured by quick freezing and correlated with quantal transmitter release.Journal of Cell Biology 81, 275–300.
Huxley, A. F. &Stampfli, R. (1949) Evidence for saltatory conduction in peripheral myelinated nerve fibres.Journal of Physiology 108, 315–9.
Kristol, C., Sandri, C. &Akert, K. (1978) Intramembranous particles at the node of Ranvier of the cat spinal cord: A morphometric study.Brain Research 142, 391–400.
Landis, D. M. D. &Reese, T. S. (1974) Arrays of particles in freeze-fractured astrocytic membranes.Journal of Cell Biology 60, 316–20.
Livingston, R. B., Pfenninger, K., Moor, H. &Akert, K. (1973) Specialised paranodal and interparanodal glial axonal junctions in the peripheral and central nervous system: A freeze-etching study.Brain Research 58, 1–24.
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.
Omlin, F. X., Bischoff, A. &Moor, H. (1980) Myelin and glial membrane structures in the optic nerve of normal and Jimpy mouse. A freeze-etching study.Journal of Neuropathology and Experimental Neurology 39, 215–31.
Pauli, B. V., Weinstein, R. S., Soble, L. W. &Alroy, J. (1977) Freeze-fracture of monolayer cultures.Journal of Cell Biology 72, 763–9.
Peters, A. (1966) The node of Ranvier in the central nervous system.Quarterly Journal of Experimental Physiology 51, 229–36.
Pfenninger, K. H. &Bunge, R. P. (1974) Freeze-fracturing of nerve growth cones and young fibres. A study of developing plasma membrane.Journal of Cell Biology 63, 180–96.
Pricam, C., Fisher, K. A. &Friend, D. S. (1977) Intramembranous particle distribution in human erythrocytes: Effects of lysis, glutaraldehyde and poly-1-lysine.Anatomical Record 189, 595–608.
Quick, D. C. &Waxman, S. G. (1977) Specific staining of the axon membrane at nodes of Ranvier with ferric ion and ferrocyanide.Journal of Neurological Sciences 31, 1–11.
Raine, C. S., Wisniewski, H. &Prineas, J. (1969) An ultrastructural study of experimental demyelination and remyelination. II. Chronic experimental allergic encephalomyelitis in the peripheral nervous system.Laboratory Investigation 21, 316–27.
Rash, J. E., Graham, W. F. &Hudson, C. S. (1979) Controlled contamination of freeze-fractured specimens. InFreeze Fracture: Methods, Artefacts and Interpretations (edited byRash, J. E. &Hudson, C. S.), pp. 111–22. New York: Raven Press.
Ritchie, J. M. &Rogart, R. B. (1977) The density of sodium channels in mammalian myelinated nerve fibers and nature of the axonal membrane under the myelin sheath.Proceedings of the National Academy of Sciences USA 74, 211–15.
Robertson, J. D. &Vergara, J. (1980) Analysis of the structure of intramembrane particles of the mammalian urinary bladder.Journal of Cell Biology 86, 514–28.
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.
Schnapp, B., Perracchia, C. &Mugnaini, E. (1975) The paranodal axoglial junction in the central nervous system studied with thin sections and freeze-fracture.Neuroscience 1, 181–90.
Skoff, R. P., Price, D. L. &Stocks, A. (1976a) Electron microscopic autoradiographic studies of gliogenesis in rat optic nerve. I. Cell proliferation.Journal of Comparative Neurology 169, 291–312.
Skoff, R. P., Price, D. L. &Stock, A. (1976b) Electron microscopic autoradiographic studies of gliogenesis in rat optic nerve. II. Time of origin.Journal of Comparative Neurology 169, 313–34.
Speidel, C. C. (1964)In vitro studies of myelinated nerve fibers.International Review of Cytology 16, 173–231.
Steere, R. L., Erbe, E. F. &Mosley, J. M. (1979) Sources and rates of contamination in a conventional Balzers freeze-etch device. InFreeze-Fracture: Methods, Artefacts and Interpretation (edited byRash, J. E. &Hudson, C. S.), pp. 99–109. New York: Raven Press.
Tao-Cheng, J-H. &Rosenbluth, J. (1980a) Nodal and paranodal membrane structure in complementary freeze-fracture replicas of amphibian peripheral nerves.Brain Research 199, 249–65.
Tao-Cheng, J-H. &Rosenbluth, J. (1980b) Developing nodes of Ranvier in frog and rat peripheral and central axons.Neuroscience Abstracts 6, 732.
Tasaki, I. (1959) Conduction of the nerve impulse. InHandbook of Physiology, (edited byField, J., Magoun, H. W. &Hall, N. E.), pp. 75–121. Washington DC: American Physiological Society.
Tennekoon, G. I., Cohen, S. R., Price, D. L. &Mckhann, G. M. (1977) Myelinogenesis in optic nerve. A morphological, autoradiographic and biochemical analysis.Journal of Cell Biology 72, 604–15.
Vaughn, J. E. (1969) An electron microscopic analysis of gliogenesis in rat optic nerves.Zeitschrift für Zellforschüng und mikroskopische Anatomie 94, 293–324.
Vizoso, A. D. &Young, J. Z. (1948) Internode length and fibre diameter in developing and regenerating nerves.Journal of Anatomy 82, 110–34.
Waxman, S. G. &Foster, R. E. (1980a) Development of the axon membrane during differentiation of myelinated fibres in spinal nerve roots.Proceedings of the Royal Society (B) 209, 441–6.
Waxman, S. G. &Foster, R. E. (1980b) Ionic channel distribution and heterogeneity of the axon membrane in myelinated fibres.Brain Research Reviews 2, 205–34.
Webster, H. de F. (1971) The geometry of peripheral myelin sheaths during their formation and growth in rat sciatic nerves.Journal of Cell Biology 48, 348–67.
Weinstein, R. S., McNutt, N. S., Nielson, G. L. &Pinn, V. W. (1970) Intramembranous fibrils at tight junctions. InProceedings of the Electron Microscopy Society of America (edited byFavard, P.), pp. 108–9. Baton Rouge: Claitors.
Wiley, C. A. &Ellisman, M. H. (1980) Rows of dimeric-particles within the axolemma and juxtaposed particles within glia, incorporated into a new model for the paranodal glial-axonal junction at the node of Ranvier.Journal of Cell Biology 84, 261–80.
Wiley-Livingston, C. A. &Ellisman, M. H. (1980a) Development of axonal membrane specializations defines nodes of Ranvier and precedes Schwann cell myelin elaboration.Developmental Biology 79, 334–55.
Wiley-Livingston, C. A. &Ellisman, M. H. (1980b) Myelination-dependent and independent membrane specializations at the node of Ranvier, demonstrated in insufficiently myelinated nerves of the dystrophic mouse.Neuroscience Abstracts 6, 22.
Wood, P. M. &Bunge, R. P. (1975) Evidence that sensory axons are mitogenic for Schwann cells.Nature 256, 662–4.
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Oldfield, B.J., Bray, G.M. Differentiation of the nodal and internodal axolemma in the optic nerves of neonatal rats. J Neurocytol 11, 627–640 (1982). https://doi.org/10.1007/BF01262428
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DOI: https://doi.org/10.1007/BF01262428