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Electron microscopic serial section analysis of nodes of Ranvier in lumbosacral spinal roots of the cat: ultrastructural organization of nodal compartments in fibres of different sizes

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Journal of Neurocytology

Summary

The general ultrastructural organization of nodes of Ranvier in peripheral nerve fibres from 2 to 20 μm in diameter (D) was investigated in the adult cat using serially sectioned ventral and dorsal spinal roots. The study was performed in order to collect and systematize information considered necessary for a morphometric analysis of the node of Ranvier. In all cases a node of Ranvier could be divided into a central nodal axon segment and a surrounding nodal Schwann cell compartment. The latter included a nodal gap matrix substance, more or less overlapping nodal Schwann cell collars and, as a rule, also a Schwann cell brush-border emanating from the nodal Schwann cell collars and occupying the nodal gap. The relative size and the organization level of the nodal Schwann cell compartment increased with increasing fibre size up to a fibre diameter of 8–10 μm. At this fibre size the nodal gap was of a fairly even height (1 μm) all around the nodal axon and contained a thick brush-border of densely packed, more or less radially arranged Schwann cell microvilli. In very small fibres (D < 3 μm) the nodal gap was low (<0.1 μm) and contained no or few microvilli. In fibres >10 μm in diameter the relative size and the degree of structural order of the nodal Schwann cell compartment decreased with increasing fibre size. Drastic sectorial variations in nodal gap height and local thinning-out of the brush-border became prominent features in the largest fibres. The possiblein vivo organization of the nodal Schwann cell compartment is discussed. Preliminary calculations indicate that the extracellular space directly surrounding the nodal axon might be quite small and that the area open for free communication between this extracellular space and the endoneurial space might be very much restricted, measuring as little as 2% of the area of the nodal axolemma. Algorithms for calculating various nodal structural parameters are discussed.

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References

  • Adelman, W. J., Moses, J. &Rice, R. V. (1977) An anatomical basis for the resistance and capacitance in series with the excitable membrane of the squid giant axon.Journal of Neurocytology 6, 621–46.

    PubMed  Google Scholar 

  • Arbuthnott, E. R., Boyd, I. A. &Kalu, K. U. (1980) Ultrastructural dimensions of myelinated peripheral nerve fibres in the cat and their relation to conduction velocity.Journal of Physiology 308, 125–57.

    PubMed  Google Scholar 

  • Berthold, C. -H. (1968a) A study on the fixation of large mature feline myelinated ventral lumbar spinal root fibres.Acta Societatis medicorum upsaliensis 73, suppl. 9, 1–36.

    Google Scholar 

  • Berthold, C. -H. (1968b) Ultrastructure of the node-paranode region of mature feline ventral lumbar spinal root fibres.Acta Societatis medicorum upsaliensis 73, suppl. 9, 37–70.

    PubMed  Google Scholar 

  • Berthold, C. -H. (1978) Morphology of normal peripheral axons. InPhysiology and Pathobiology of Axons (edited byWaxman, S. G.), pp. 3–64. New York: Raven Press.

    Google Scholar 

  • Berthold, C. -H. (1982) Some aspects on the ultrastructural organization of peripheral myelinated axons in the cat. InProceedings of Life Sciences. Axoplasmic Transport (edited byWeiss, D. G.), pp. 40–54. Berlin, Heidelberg, New York: Springer-Verlag.

    Google Scholar 

  • Berthold, C. -H. &Carlstedt, T. (1977) Observations on the morphology at the transition between the peripheral and the central nervous system in the cat. III. Myelinated fibres in S1 dorsal rootletsActa Physiologica scandinavica, suppl.446, 43–60.

    Google Scholar 

  • Berthold, C. -H. &Skoglund, S. (1965) Ultrastructure and histochemistry of the developing node of Ranvier in the hindlimb nerves of the cat.Acta Societatis medicorum upsaliensis 70, 287–93.

    Google Scholar 

  • Berthold, C. -H., Corneliuson, O. &Rydmark, M. (1982a) Changes in shape and size of cat spinal root myelinated nerve fibres during fixation and Vestopal-W embedding for electron microscopy.Journal of Ultrastructure Research 80, 23–41.

    PubMed  Google Scholar 

  • Berthold, C. -H., Rydmark, M. &Corneliuson, O. (1982b) Estimation of sectioning compression and thickness of ultrathin sections through Vestopal-W embedded cat spinal roots.Journal of Ultrastructure Research 80, 42–52.

    PubMed  Google Scholar 

  • Berthold, C.-H., Nilsson, I. &Rydmark, M. (1983) Axon diameter and myelin sheath thickness in nerve fibres of the ventral root L7 of the adult and the developing cat.Journal of Anatomy, in press.

  • Binah, O. &Palti, Y. (1981) Potassium channels in the nodal membrane of rat myelinated fibres.Nature 290, 598–600.

    PubMed  Google Scholar 

  • Bischoff, A. &Thomas, P. K. (1975) Microscopic anatomy of myelinated nerve fibres. InPeripheral Neuropathy (edited byDyck, P. J., Thomas, P. K. andLambert, E. H.), pp. 104–30. Philadelphia, London, Toronto: W. B. Saunders Company.

    Google Scholar 

  • Brinley, F. J. JR. (1980) Excitation and conduction in nerve fibres. InMedical Physiology (edited byMountcastle, V. B.), pp. 46–81. St Louis, Toronto, London: C. V. Mosby Company.

    Google Scholar 

  • Brismar, T. (1979) Potential clamp experiments on myelinated nerve fibres from alloxan diabetic rats.Acta physiologies scandinavica 105, 384–6.

    Google Scholar 

  • Brismar, T. (1980) Potential clamp analysis of membrane currents in rat myelinated nerve fibres.Journal of Physiology 298, 171–84.

    PubMed  Google Scholar 

  • Brismar, T. &Frankenhaeuser, B. (1981) Potential clamp analysis of mammalian myelinated fibres.Trends in Neurosciences 4, 68–70.

    Google Scholar 

  • Carlstedt, T. (1977) Observations on the morphology at the transition between the peripheral and the central nervous system in the cat. I. A preparative procedure useful for electron microscopy of the lumbosacral dorsal rootlets.Acta physiologica scandinavica, suppl.446, 5–22.

    Google Scholar 

  • Carlstedt, T. (1980) Internodal length of nerve fibres in dorsal roots of cat spinal cord.Neuroscience Letters 19, 251–6.

    PubMed  Google Scholar 

  • Chan-Palay, V. (1972) The tripartite structure of the undercoat in initial segments of Purkinje cell axons.Zeitschrift für Anatomie und Entwicklungsgeschichte 139, 1–10.

    Google Scholar 

  • Chiu, S. Y. &Ritchie, J. M. (1980) Potassium channels in the paranodal region of acutely demyelinated voltage clamped mammalian myelinated nerve.Journal of Physiology 305, 61P-62P.

    Google Scholar 

  • Chiu, S. Y., Ritchie, J. M., Rogart, R. &Stagg, D. (1979) A quantitative description of membrane currents in rabbit myelinated nerve.Journal of Physiology 292, 149–66.

    PubMed  Google Scholar 

  • Dubois, J. M. &Bergman, C. (1975) Potassium accumulation in the perinodal space of frog myelinated axons.Pflügers Archiv 358, 111–24.

    Google Scholar 

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

    PubMed  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 

  • Friede, R. L. &Bischhausen, R. (1980) The precise geometry of large internodes.Journal of the Neurological Sciences 48, 367–81.

    PubMed  Google Scholar 

  • Gasser, H. S. (1952) In Discussion to Frankenhaeuser: The hypothesis of saltatory conduction.Cold Spring Harbor Symposia on Quantitative Biology 17, 32–6.

    Google Scholar 

  • Hall, S. M. &Williams, P. L. (1971) The distribution of electron-dense tracers in peripheral nerve fibres.Journal of Cell Science 8, 541–55.

    PubMed  Google Scholar 

  • Hess, A. &Lansing, A. J. (1953) The fine structure of peripheral nerve fibres.Anatomical Record 117, 175–200.

    PubMed  Google Scholar 

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

    Google Scholar 

  • Hodgkin, A. L. (1964)The Conduction of the Nervous Impulse. Liverpool: Liverpool University Press.

    Google Scholar 

  • Hora'kova, M., Nonner, W. &Stämpfli, R. (1968) Action potentials and voltage clamp currents of single rat Ranvier nodes.Proceedings of the International Union of Physiological Sciences 7, 198.

    Google Scholar 

  • Ishikawa, H., Tsukita, S. A. &Tsukita, Sh. (1981) Ultrastructural aspects of the plasmalemmal undercoat. InNerve Membrane. Biochemistry and Function of Channel Proteins (edited byMatsumoto, G. andKotani, M.). Tokyo: University of Tokyo Press.

    Google Scholar 

  • Jack, J. J. B., Noble, D. &Tsien, R. W. (1975)Electric Current Flow in Excitable Cells Oxford: Oxford University Press.

    Google Scholar 

  • Kalu, K. U. (1973) Conduction velocity and fibre diameter in myelinated afferent nerve fibres of the cat, PhD thesis, University of Glasgow.

  • Kenny, A. J. &Booth, A. G. (1978) Microvilli: their ultrastructure, enzymology and molecular organization.Essays in Biochemistry 14, 1–44.

    PubMed  Google Scholar 

  • Koles, Z. J. &Rasminsky, M. (1972) A computer simulation of conduction in demyelinated nerve fibres.Journal of Physiology 227, 351–64.

    PubMed  Google Scholar 

  • Landon, D. N. (1981) Structure of normal peripheral myelinated nerve fibres. InAdvances in Neurology, Vol. 31,Demyelinating Diseases, Basic and Clinical Electrophysiology (edited byWaxman, S. G. andRitchie, J. M.), pp. 25–49. New York: Raven Press.

    Google Scholar 

  • Landon, D. N. &Hall, S. (1976) The myelinated nerve fibre. InThe Peripheral Nerve (edited byLandon, D. N.), pp. 1–105. London: Chapman & Hall.

    Google Scholar 

  • Landon, D. N. &Langley, O. K. (1971) The local chemical environment of the node of Ranvier. A study of cation binding,Journal of Anatomy 108, 419–32.

    PubMed  Google Scholar 

  • Landon, D. N. &Williams, P. L. (1963) Ultrastructure of the node of Ranvier.Nature 199, 575–7.

    PubMed  Google Scholar 

  • Langley, O. K. (1979) Histochemistry of polyanions in peripheral nerve.In Complex Carbohydrates of Nervous Tissue (edited byMargolis, R. U. andMargolis, R. K.), pp. 193–207. New York, London: Plenum Press.

    Google Scholar 

  • Leduc, E., Marinozzi, V. &Bernhard, W. (1963) The use of water-soluble glycol methacrylate in ultrastructural cytochemistry.Journal of the Royal Microscopical Society 81, 119–30.

    Google Scholar 

  • Livingstone, R. B., Pfenninger, K., Moor, H. &Akert, K. (1973) Specialized paranodal and interparanodal glial-axonal junctions in the peripheral and the central nervous system: a freeze-etching study.Brain Research 58, 1–24.

    PubMed  Google Scholar 

  • Lüttgau, H. C. (1977) New trends in membrane physiology of nerve and muscle fibres.Journal of Comparative Physiology 120, 51–70.

    Google Scholar 

  • Millonig, G. &Marino Zzi, V. (1968) Fixation and embedding in electron-microscopy. InAdvances in Optic and Electron Microscopy Vol. 2 (edited byBarer, R. AndCosslett, V. E.), pp. 251–341. London, New York: Academic Press.

    Google Scholar 

  • Moran, N., Palti, Y., Levitan, E. &Stämpfli, R. (1980) Potassium ion accumulation at the external surface of the nodal membrane in frog myelinated fibres.Biophysical Journal 32, 939–54.

    PubMed  Google Scholar 

  • Müller-Mohnssen, H., Tippe, A., Hillenkamp, F. &Unsöld, E. (1975) Über die bedeutung paranodaler Strukturen für die Impulsregeneration am Ranvierschen Schnurring.Zeitschrift für Naturforschung 30c, 271–7.

    Google Scholar 

  • Ochoa, J. (1976) The unmyelinated nerve fibre. InThe Peripheral Nerve (edited byLandoa, D. N.), pp. 106–58. London: Chapman and Hall.

    Google Scholar 

  • Peracchia, C. &Mittler, B. S. (1972) New glutaraldehyde fixation procedures.Journal of Ultrastructure Research 36, 57–64.

    Google Scholar 

  • Phillips, D. D., Hibbs, R. G., Ellison, J. P. &Shapiro, H. (1972) An electron microscopic study of central and peripheral nodes of Ranvier.Journal of Anatomy 111, 229–38.

    PubMed  Google Scholar 

  • Ritchie, J. M. (1979) A pharmacological approach to the structure of sodium channels in myelinated axons.Annual Review of Neuroscience 2, 341–62.

    PubMed  Google Scholar 

  • Robertson, J. D. (1959) Preliminary observations on the ultrastructure of nodes of Ranvier.Zeitschrift für Zellforschung 50, 553–60.

    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. (1978) Glial membrane specializations in extra paranodal regions.Journal of Neurocytology 7, 709–19.

    PubMed  Google Scholar 

  • Rydmark, M. (1981) Nodal axon diameter correlates linearly with internodal axon diameter in spinal roots of the cat.Neuroscience Letters 24, 247–50.

    PubMed  Google Scholar 

  • Rydmark, M. &Berthold, C. -H. (1983) Electron microscopic serial section analysis of nodes of Ranvier in lumbar spinal roots of the cat: a morphometric study of nodal compartments in fibres ot different sizes.Journal of Neurocytology 12, in press.

  • Schnapp, B. &Mugnaini, E. (1975) The myelin sheath. Electron microscopic studies with thin section and freeze-fracture. InGolgi Centennial Symposium: Proceedings (edited bySantini, M.), pp. 209–30. New York: Raven Press.

    Google Scholar 

  • Schnapp, B., Peracchia, C. &Mugnaini, E. (1976) The paranodal axo-glial junction in the central nervous system studied with thin sections and freeze-fracture.Neuroscience 1, 181–90.

    PubMed  Google Scholar 

  • Seneviratne, K. N., Peiris, O. A. &Weerasuriya, A. (1972) Effects of hyperkalaemia on the excitability of peripheral nerve.Journal of Neurology, Neurosurgery, and Psychiatry 35, 149–55.

    Google Scholar 

  • Smith, K. J. &Schauf, C. L. (1981) Size-dependent variation of nodal properties in myelinated nerve.Nature 293, 297–9.

    PubMed  Google Scholar 

  • Stämpfli, R. &Hille, B. (1976) Electrophysiology of the peripheral myelinated nerve. InFrog Neurobiology (edited byLlinas, R. andPrecht, W.), pp. 3–32. Berlin, Heidelberg, New York: Springer-Verlag.

    Google Scholar 

  • Tao-Cheng, J.-H. &Rosenbluth, J. (1980) Nodal and paranodal membrane structure in complementary freeze-fracture replicas of amphibian peripheral nerves.Brain Research 199, 249–65.

    PubMed  Google Scholar 

  • Uhrik, B. &Stämpfli, R. (1981) Ultrastructural observations on nodes of Ranvier from isolated single frog peripheral nerve fibres.Brain Research 215, 93–101.

    PubMed  Google Scholar 

  • Waxman, S. G. (1978) Variations in axonal morphology and their functional significance. InPhysiology and Pathobiology of Axons (edited byWaxman, S. G.), pp. 169–90. New York: Raven Press.

    Google Scholar 

  • Waxman, S. G. &Foster, R. E. (1980) Ionic channel distribution and heterogeneity of the axon membrane in myelinated fibres.Brain Research Review 2, 205–34.

    Google Scholar 

  • Webster, H. De F. &Collins, G. H. (1964) Comparison of osmium tetroxide and glutaraldehyde perfusion fixation for the electronmicroscopic study of the normal rat peripheral nervous system.Journal of Neuropathology and Experimental Neurology 23, 109–26.

    PubMed  Google Scholar 

  • Weller, R. O. &Nester, B. (1972) Early changes at the node of Ranvier in segmental demyelination.Brain 95, 665–74.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Williams, P. L. &Hall, S. M. (1971) Prolongedin vivo observations of normal peripheral nerve fibers and their acute reactions to crush and deliberate trauma.Journal of Anatomy 197, 397–408.

    Google Scholar 

  • Williams, P. L. &Landon, D. N. (1963) Paranodal apparatus of peripheral nerve fibres of mammals.Nature 198, 670–3.

    PubMed  Google Scholar 

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  1. Department of Anatomy, Section of Neuroanatomy, University of Gothenburg, Gothenburg, Sweden

    C. -H. Berthold

  2. Department of Anatomy, Karolinska Institute, Stockholm, Sweden

    M. Rydmark

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  1. C. -H. Berthold
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  2. M. Rydmark
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Berthold, C.H., Rydmark, M. Electron microscopic serial section analysis of nodes of Ranvier in lumbosacral spinal roots of the cat: ultrastructural organization of nodal compartments in fibres of different sizes. J Neurocytol 12, 475–505 (1983). https://doi.org/10.1007/BF01159386

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