Hostname: page-component-78c5997874-mlc7c Total loading time: 0 Render date: 2024-11-05T05:51:25.624Z Has data issue: false hasContentIssue false
  • English
  • Français

What is myelin?

Published online by Cambridge University Press:  08 September 2009

Daniel K. Hartline
Daniel K. Hartline*
Affiliation:
Békésy Laboratory of Neurobiology, Pacific Biosciences Research Center, University of Hawaii at Manoa, Honolulu, HI USA
*
Correspondence should be addressed to: Daniel K. Hartline, Békésy Laboratory of Neurobiology, Pacific Biosciences Research Center, University of Hawaii at Manoa, Honolulu, HI 96822, USA phone: 808-956-8003 fax: 808-956-6984 email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The evolution of a character is better appreciated if examples of convergent emergence of the same character are available for comparison. Three instances are known among invertebrates of the evolution of axonal sheaths possessing the functional properties and many of the structural properties of vertebrate myelin. Comparison of these invertebrate myelins raises the question of what structural features must a sheath possess in order to produce the two principal functional characteristics of impulse speed enhancement and energy savings. This essay reviews the features recognized by early workers as pertaining to myelin in vertebrate and invertebrate alike: osmiophilia, negative birefringence and saltatory conduction. It then examines common features revealed by the advent of electron microscopy: multiplicity of lipid membranes, condensation of those membranes, specialized marginal seals, and nodes. Next it examines the robustness of these features as essential components of a speed-enhancing sheath. Features that are not entirely essential for speed enhancement include membrane compaction, spiral wrapping of layers, glial cell involvement, non-active axonal membrane, and even nodes and perinodal sealing. This permissiveness is discussed in relation to the possible evolutionary origin of myelin.

Keywords

Evolutioninvertebratessaltatory conductioncrustaceansoligochaetes
Type
Research Article
Information
Neuron Glia Biology , Volume 4 , Issue 2 , May 2008 , pp. 153 - 163
Copyright
Copyright © Cambridge University Press 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Bear, R.S. and Schmitt, F.O. (1937) Optical properties of the axon sheaths of crustacean nerves. Journal of Cellular and Comparative Physiology 9, 275–287.CrossRefGoogle Scholar
Bekkers, J.M., Greeff, N.G. and Keynes, R.D. (1986) The conductance and density of sodium channels in the cut-open squid giant axon. Journal of Physiology 377, 463–486.CrossRefGoogle ScholarPubMed
Bullock, T.H. (2004) The natural history of neuroglia: an agenda for comparative studies. Neuron and Glia Biology 1, 97–100.CrossRefGoogle ScholarPubMed
Bullock, T.H. and Horridge, G.A. (1965) Structure and Function in the Nervous System of Invertebrates, Vol. I. San Francisco: W.H. Freeman, 798 pp.Google Scholar
Bunge, M.B., Bunge, R.P. and Pappas, G.D. (1962) Electron microscopic demonstration of connections between glia and myelin sheaths in the developing mammalian central nervous system. Journal of Cellular Biology 12, 448–453.CrossRefGoogle ScholarPubMed
Bunge, R.P. (1968) Glial cells and the central myelin sheath. Physiological Reviews 48, 197–251.CrossRefGoogle ScholarPubMed
Cole, K.S. and Hodgkin, A.L. (1939) Membrane and protoplasm resistance in the squid giant axon. Journal of General Physiology 22, 671–687.CrossRefGoogle ScholarPubMed
Davis, A.D., Weatherby, T.M., Hartline, D.K. and Lenz, P.H. (1999) Myelin-like sheaths in copepod axons. Nature 398, 571.CrossRefGoogle ScholarPubMed
Eccles, J.C., Granit, R. and Young, J.Z. (1932) Impulses in the giant nerve fibres of earthworms. Journal of Physiology 77, 23P.Google Scholar
Ehrenberg, C.G. (1849) Verhaltungen Preußischen Akademie der Wissenschaften zu Berlin (cited in Schmitt, 1936).Google Scholar
Fan, S.F., Hsu, K., Chen, F.S. and Hao, B. (1961) On the high conduction velocity of the giant nerve fiber of shrimp Penaeus orientalis. Kexue Tongbao 12, 51–52.Google Scholar
Fernández, I., Pardos, F., Benito, J. and Roldán, C. (1996) Ultrastructural observations on the phoronid nervous system. Journal of Morphology 230, 265–281.3.0.CO;2-D>CrossRefGoogle ScholarPubMed
Fernández-Morán, H. (1950) Electron microscope observations on the structure of the myelinated nerve sheath. Experimental Cell Research 1, 143–149.CrossRefGoogle Scholar
Friedländer, B. (1889) Über die markhaltigen Nervenfasern und Neurochorde der Crustaceen und Anneliden. Mittheilungen aus der Zoologischen Station zu Neapel 9, 205–265.Google Scholar
Gasser, H.S. and Grundfest, H. (1939) Axon diameters in relation to spike dimensions and conduction velocity in mammalian A fibers. American Journal of Physiology 127, 393–414.CrossRefGoogle Scholar
Gerard, R.W. (1927) Studies on nerve metabolism. II. Respiration in oxygen and nitrogen. American Journal of Physiology 82, 381–404.CrossRefGoogle Scholar
Gerard, R.W. (1932) Nerve metabolism. Physiological Reviews 12, 469–592.CrossRefGoogle Scholar
Govind, C.K. and Lang, F. (1976) Growth of lobster giant axons: correlation between conduction velocity and axon diameter. Journal of Comparative Neurology 170, 421–433.CrossRefGoogle ScholarPubMed
Greef, N.G. and Yasargil, G.M. (1980) Experimental evidence for saltatory propagation of the Mauthner axon impulse in the tench spinal cord. Brain Research 193, 47–57.CrossRefGoogle Scholar
Günther, J. (1976) Impulse conduction in the myelinated giant fibers of the earthworm. Structure and function of the dorsal nodes in the median giant fiber. Journal of Comparative Neurology 168, 505–532.CrossRefGoogle ScholarPubMed
Hall, S.M. and Williams, P.L. (1970) Studies of the ‘incisures’ of Schmidt and Lanterman. Journal of Cell Science 6, 767–791.CrossRefGoogle Scholar
Hama, K. (1959) Some observations on the fine structure of the giant nerve fibers of the earth worm Eisenia foetida. Journal of Biophysical and Biochemical Cytology 6, 61–66.CrossRefGoogle Scholar
Hao, B. and Hsu, K. (1965) The birefringence properties of the myelin sheath of shrimp nerve fibre. Sheng Li Xue Bao 28, 373–377 (in Chinese; citation from Medline).Google ScholarPubMed
Hartline, D.K. and Colman, D.R. (2007) Rapid conduction and the evolution of giant axons and myelinated fibers. Current Biology 17, R29–R35.CrossRefGoogle ScholarPubMed
Heuser, J.E. and Doggenweiler, C.F. (1966) The fine structural organization of nerve fibers, sheaths and glial cells in the prawn, Palaemonetes vulgaris. Journal of Cell Biology 30, 381–403.CrossRefGoogle ScholarPubMed
Hild, W. (1957) Myelogenesis in cultures of mammalian central nervous tissue. Zeitschrift für Zellforschung und Mikroskopische Anatomie 46, 71–95.CrossRefGoogle ScholarPubMed
Hines, M.L. and Carnevale, N.T. (1997) The NEURON simulation environment. Neural Computation 9, 1179–1209.CrossRefGoogle ScholarPubMed
Hodgkin, A.L. (1964) The Conduction of the Nervous Impulse. Liverpool: Liverpool University Press, 108 pp.Google Scholar
Hodgkin, A.L. and Rushton, W.A.H. (1946) The electrical constants of a crustacean nerve fibre. Proceedings of the Royal Society of London, Series B, Biological Science 133, 444–479.Google Scholar
Holmes, W., Pumphrey, R.J. and Young, J.Z. (1941) The structure and conduction velocity of the medullated nerve fibers of prawns. Journal of Experimental Biology 18, 50–54.CrossRefGoogle Scholar
Hsu, K., Tan, T.P. and Chen, F.S. (1964) On the excitation and saltatory conduction in the giant fiber of shrimp (Penaeus orientalis). In Proceedings of the 14th National Congress of the Chinese Association for Physiological Science. Dalian, August 7–15, p. 17 (cited in Xu and Terakawa 1999).Google Scholar
Hsu, K. and Terakawa, S. (1984) Localization of the excitable membrane in the myelinated giant fiber of shrimp Penaeus japonicus. Japanese Journal of Physiology 34, 181–185.Google ScholarPubMed
Hsu, K. and Terakawa, S. (1996) Fenestration in the myelin sheath of nerve fibers of the shrimp: a novel node of excitation for saltatory conduction. Journal of Neurobiology 30, 397–409.3.0.CO;2-#>CrossRefGoogle ScholarPubMed
Huxley, A.F. and Stämpfli, R. (1949) Evidence for saltatory conduction in peripheral myelinated nerve fibres. Journal of Physiology (London) 108, 315–339.CrossRefGoogle ScholarPubMed
Kusano, K. (1966) Electrical activity and structural correlates of giant nerve fibers in Kuruma shrimp (Penaeus japonicus). Journal of Cellular Physiology 68, 361–384.CrossRefGoogle Scholar
Kusano, K. and LaVail, M.M. (1971) Impulse conduction in the shrimp medullated giant fiber with special reference to the structure of functionally excitable areas. Journal of Comparative Neurology 142, 481–494.CrossRefGoogle Scholar
Lenz, P.H., Hartline, D.K. and Davis, A.D. (2000) The need for speed. I. Myelinated axons and fast reaction times in copepods. Journal of Comparative Physiology A 186, 337–345.CrossRefGoogle Scholar
Lillie, R.S. (1925) Factors affecting transmission and recovery in the passive iron nerve model. Journal of General Physiology 7, 473–507.CrossRefGoogle ScholarPubMed
Nageotte, J. (1916) Notes sur les fibres à myeline et sur les étranglements de Ranvier chez certains crustacés. Comptes Rendus des Séances de la Societé de Biologie et de ses Filiales 79, 259–263.Google Scholar
Poliak, S. and Peles, E. (2003) The local differentiation of myelinated axons at nodes of Ranvier. Nature Reviews, Neuroscience 4, 968–980.CrossRefGoogle ScholarPubMed
Pumphrey, R.J. and Young, J.Z. (1938) The rates of conduction of nerve fibres of various diameters in cephalopods. Journal of Experimental Biology 15, 453–466.CrossRefGoogle Scholar
Raine, C.S. (1984) Morphology of myelin and myelination. In Morell, P. (ed). Myelin. London: Plenum Press, second edition, pp. 1–50.Google Scholar
Ranvier, L.-A. (1871) Contributions a l'histologie et a la physiologie des nerf peripheriques. Comptes Rendus de l'Academie des Sciences (Paris) 73, 1168–1171.Google Scholar
Ranvier, L.-A. (1878) Leçons sur l'Histologie du Système Nerveux. Paris: Librairie F. Savy.Google Scholar
Ritchie, J.M. (1967) The oxygen consumption of mammalian non-myelinated nerve fibres at rest and during activity. Journal of Physiology 188, 309–329.CrossRefGoogle ScholarPubMed
Ritchie, J.M. (1984) Physiological basis of conduction in myelinated nerve fibers. In Morell, P. (ed), Myelin. New York: Plenum Press, pp. 117–145.CrossRefGoogle Scholar
Robertson, J.D. (1958) Structural alterations in nerve fibers produced by hypotonic and hypertonic solutions. Journal of Biophysical and Biochemical Cytology 4, 349–364.CrossRefGoogle ScholarPubMed
Roots, B.I. (1984) Evolutional aspects of the structure and function of the nodes of Ranvier. In: Zagoren, J.C. & Fedoroff, S. (eds) The Node of Ranvier. Orlando: Academic Press, pp. 1–29.Google Scholar
Roots, B. (2009) The phylogeny of invertebrates and the evolution of myelin. Neuron Glia Biology (this volume).Google Scholar
Rosenbluth, J. (1962) The fine structure of acoustic ganglia in the rat. Journal of Cell Biology 12, 329–359.CrossRefGoogle ScholarPubMed
Rosenbluth, J. (1984) Membrane specializations at the nodes of Ranvier and paranodal and juxtaparanodal regions of myelinated central and peripheral nerve fibers. In: Zagoren, J.C. & Fedoroff, S. (eds) The Node of Ranvier. Orlando: Academic Press, pp. 31–67.CrossRefGoogle Scholar
Rosenbluth, J. (1999) A brief history of myelinated nerve fibers: one hundred and fifty years of controversy. Journal of Neurocytology 28, 251–262.CrossRefGoogle ScholarPubMed
Rosenbluth, J. (2009) Multiple functions of the paranodal junction of myelinated nerve fibers. Journal of Neuroscience Research February 17, 2009 (Epub ahead of print).CrossRefGoogle ScholarPubMed
Scharf, J.-H. (1951) Die markhaltigen Ganglienzellen und ihre Beziehungen zu dem myelogenetischen Theorien. Morphologische Jahrbuch 91, 187–252.Google Scholar
Schmitt, F.O. (1936) Nerve ultrastructure as revealed by x-ray diffraction and polarized light studies. Cold Spring Harbor Symposia on Quantitative Biology 4, 7–12.CrossRefGoogle Scholar
Schmitt, F.O. and Bear, R.S. (1939) The ultrastructure of the nerve axon sheath. Biological Reviews 14, 27–50.CrossRefGoogle Scholar
Sjöstrand, F.S. (1953) The lamellated structure of the nerve myelin sheath as revealed by high-resolution electron microscopy. Experientia 9, 68–69.CrossRefGoogle ScholarPubMed
Susuki, K. and Rasband, M.N. (2008) Molecular mechanisms of node of Ranvier formation. Current Opinion in Cell Biology 20, 616–623.CrossRefGoogle ScholarPubMed
Tasaki, I. (1939) The electro-saltatory transmission of the nerve impulse and the effect of narcosis upon the nerve fiber. American Journal of Physiology 127, 211–227.CrossRefGoogle Scholar
Taylor, G.W. (1940) The optical properties of the earthworm giant fiber sheath as related to fiber size. Journal of Cellular and Comparative Physiology 15, 363–371.CrossRefGoogle Scholar
Terakawa, S. and Hsu, K. (1991) Ionic currents of the nodal membrane underlying the fastest saltatory conduction in myelinated giant nerve fibers of the shrimp Penaeus japonicus. Journal of Neurobiology 22, 342–352.CrossRefGoogle ScholarPubMed
Virchow, R. (1858) Cellular Pathology. Berlin: Hirschwald. Translated by Chance, F. 1860. London: Churchill. as cited by Rosenbluth 1999.Google Scholar
Weatherby, T.M., Davis, A.D., Hartline, D.K. and Lenz, P.H. (2000) The need for speed. II. Myelin in calanoid copepods. Journal of Comparative Physiology A 186, 347–357.CrossRefGoogle ScholarPubMed
Wilson, C. and Hartline, D.K. (2007) The development of calanoid copepod myelin. Program No. 674.8. 2007 Neuroscience Meeting Planner. Washington, DC: Society for Neuroscience, 2007 (online).Google Scholar
Wilson, C. and Hartline, D.K. (2008) A non-glial source of myelin in copepods? Program No. 79.23. 2008 Neuroscience Meeting Planner. Washington, DC: Society for Neuroscience, 2008 (online).Google Scholar
Xu, K., Sun, H. and Sung, Y. (1994) Electron microscopic observation on ontogenesis of the myelinated nerve fiber in the shrimp (Penaeus orientalis). Chinese Journal of Neuroanatomy 10, 239–242.Google Scholar
Xu, K. and Terakawa, S. (1993) Saltatory conduction and a novel type of excitable fenestra in shrimp myelinated nerve fibers. Japanese Journal of Physiology 43 (Suppl. 1), S285–S293.Google Scholar
Xu, K. and Terakawa, S. (1999) Fenestration nodes and the wide submyelinic space form the basis for the unusually fast impulse conduction of shrimp myelinated axons. Journal of Experimental Biology 202, 1979–1989.Google ScholarPubMed
Yamada, S. (1923) Über die Leitungsgeschwindigkeit des Nervenimpulses in den sympathischen Hautnerven des Frosches. Plfügers Archiv für die Gesamte Physiologie des Menschen und der Tiere 200, 221–227.CrossRefGoogle Scholar
Yeh, Y., Huang, S.-K. and Hsu, K. (1962) Microscopic and electron microscopic observations on a fibre-like structure in the axoplasm of the nerve fibre of Penaeus orientalis. Acta Physiologica Sinica 26, 4–52.Google Scholar
Zalc, B. (2006) The acquisition of myelin: a success story. In Chadwick, D.J. & Goode, J. (eds) Purinergic Signalling in Neuron-Glia Interactions, No. 276 Chichester: Wiley, pp. 15–25.CrossRefGoogle Scholar
Zalc, B. and Colman, D.R. (2000) Origins of vertebrate success. Science 288, 271–272.CrossRefGoogle ScholarPubMed
Zalc, B., Goujet, D. and Colman, D.R. (2008) The origin of the myelination program in vertebrates. Current Biology 18, R511–R512.CrossRefGoogle ScholarPubMed