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The design of the optic nerve in fish

Published online by Cambridge University Press:  02 June 2009

John Scholes
John Scholes
Affiliation:
Medical Research Council, Muscle and Cell Motility Unit, King's College, London, 26–29 Drury Lane, London WC2B 5RL, UK
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Abstract

Fish have large eyes, with short optic nerves that are continually flexed by compensatory eye movements during swimming. Here, I review the tissue construction of the fish optic nerve, to see how the glia and axons are adapted to withstand these mechanical stresses, which are not normally encountered by CNS tissue within the skull.

As in other lower vertebrates, the optic nerve astrocytes are highly unusual: their intermediate filaments are composed of cytokeratins (Giordano et al., 1989), not GFAP. Their processes are linked together by desmosomes, forming thin transverse lace-like partitions, placed at quasi-regular intervals longitudinally (Maggs & Scholes, 1990). This accordion-like arrangement is interpreted as providing a flexible tissue-skeleton for the optic nerve.

A new observation is that the optic axons run in coherent parallel waves. This pattern, which is complementary to that of the astroglia, reversibly accommodates limited axial stretches. The waves are equivalent to those underlying the optical banding of Fontana (1781) in peripheral nerves, but wavelength (30 μm) and amplitude (5 μm) are about an order of magnitude less, reflecting the much smaller average size of the optic axons. The pattern also occurs in mammals, and may be restricted to the visual pathway: if present elsewhere in the CNS, nerve-fiber waves are inconspicuous at best.

In fish, the astroglial partitions occur in register with the waves, suggesting that steric interactions between developing axons and glia may help to establish, or stabilize, the regular longitudinal spacing. This may have functional as well as mechanical implications, since the astrocytes form perinodal associations and their pattern is one which strongly clusters the nodes of Ranvier.

Keywords

Optic nerveReticular astrocytesFontana bandsNodes of RanvierFish
Type
Research Articles
Information
Visual Neuroscience , Volume 7 , Issue 1-2 , August 1991 , pp. 129 - 139
Copyright
Copyright © Cambridge University Press 1991

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References

Alberts, B., Bray, D., Lewis, J., Raff, M., Roberts, K. & Watson, J.D. (1989). Molecular Biology of the Cell. New York & London: Garland Publishing, Inc.Google Scholar
Baer, E., Cassidy, J.J. & Hiltner, A. (1988). Hierarchical structure of collagen and its relation to the physical properties of tendon. In Collagen. Vol. 2, ed. Nimni, M.E. pp. 177–199. Boca Raton, Florida. Chemical Rubber Company Press.Google Scholar
Barres, B.A., Chun, L.L.Y. & Corey, D.P. (1988). Ion-channel expression by white matter glia; I: Type 2 astrocytes and oligodendrocytes. Glia 1, 10–30.Google Scholar
Bertolini, B. (1964). Ultrastructure of the spinal cord of the lamprey. Journal of Ultrastructural Research 11, 1–24.Google Scholar
Birk, D.E., Southern, J.F., Zycband, E.I., Fallon, J.T. & Trelstad, R.L. (1989a). Collagen fibril bundles: a branching assembly unit in tendon morphogenesis. Development 107; 437–443.Google Scholar
Birk, D.E., Zycband, E.L., Winkelmann, D.A. & Trelstad, R.L. (1989b). Collagen fibrillogenesis in situ: fibril segments are intermediates in matrix assembly. Proceedings of the National Academy of Sciences of the U.S.A. 86, 4549–4553.CrossRefGoogle ScholarPubMed
Black, J.A. & Waxman, S.G. (1988). The perinodal astrocyte, Glia 1, 169–183.CrossRefGoogle ScholarPubMed
Black, J.A., Friedman, B., Waxman, S.G., Elmer, L.W. & Angelides, K.J. (1989). Immuno-ultrastructural localization of sodium channels at nodes of Ranvier and perinodal astrocytes in rat optic nerve. Proceedings of the Royal Society B (London) 238, 39–51.Google Scholar
Bunge, M.B., Williams, A.K., Wood, P.M., Uitto, J. & Jeffrey, J.J. (1980). Comparison of nerve cell and nerve cell plus Schwann cell cultures, with particular emphasis on basal lamina and collagen formation. Journal of Cell Biology 84, 184–202.Google Scholar
Cajal, S.R.-Y. (1955). Histologie du Système Nerveux de l'homme et des vertébrés. Madrid: Instituto Ramon y Cajal.Google Scholar
Clarke, E. & Bearn, J.G. (1972). The spiral bands of Fontana. Brain 95, 1–20.CrossRefGoogle ScholarPubMed
Dahl, D. & Bignami, E. (1973). Immunochemical and immunofluorescence studies of the glial fibrillary acidic protein in vertebrates. Brain Research 61, 279–293.Google Scholar
Dahl, D., Crosby, C.J., Sethi, J.S. & Bignami, E. (1986). Glial fibrillary acidic (GFA) protein in vertebrates: immunofluorescence and immunoblotting study with monoclonal and polyclonal antibodies. Journal of Comparative Neurology 239, 75–88.Google Scholar
Dale, W.C. & Baer, E. (1974). Fiber buckling in composite systems: a model for the ultrastructure of uncalcified collagen tissues. Journal of Material Science 9, 369–382.Google Scholar
Diamant, J., Keller, A., Baer, E., Litt, M. & Arridge, R.G.C. (1972). Collagen: ultrastructure and its relation to mechanical properties as a function of aging. Proceedings of the Royal Society B (London) 180, 293–315.Google Scholar
Dowding, A.J., Maggs, A. & Scholes, J. (1991). Diversity among the microglia in growing and regenerating fish CNS: immunohistochemical characterisation using FL. 1, an anti-macrophage monoclonal antibody. Glia (in press).Google Scholar
Fernald, R.D. (1980). Optic nerve distention in a cichlid fish. Vision Research 20, 1015–1019.Google Scholar
Ffrench-Constant, C. & Raff, M.C. (1986). The oligodendrocyte-type two-astrocyte lineage is specialized for myelination. Nature 323, 335–338.Google Scholar
Fontana, F. (1781). Traité sur le vénin de la vipère sur les poissons Americains sur le lauriercérise, tome. 2. Florence, pp. 187–221.Google Scholar
Gamble, H.J. (1964). Comparative electron-microscope observations on the connective tissues of a peripheral nerve and a spinal nerve root in the rat. Journal of Anatomy 98, 17–25.Google Scholar
Gans, C. & Northcutt, G. (1983). Neural crest and the origin of vertebrates: a new head. Science 220, 268–274.Google Scholar
Gardner-Medwin, A.R. (1983). Analysis of potassium dynamics in mammalian brain tissue. Journal of Physiology 335, 393–426.Google Scholar
Gilbert, D.S. (1972). Helical structure of Myxicola axoplasm. Nature 237, 195–198.Google Scholar
Gilbert, D.S. (1975). Axoplasm architecture and physical properties in the Myxicola giant axon. Journal of Physiology 253, 257–301.Google Scholar
Giordano, S., Glasgow, E.Tesser, P. & Schechter, N. (1989). A type-II keratin is expressed in glial cells of the goldfish visual pathway. Neuron 2, 1507–1516.Google Scholar
Hanimec, P. (1986). Undulating course of nerve fibers and bands of Fontana in peripheral nerves of the rat. Anatomy and Embryology 174, 407–411.CrossRefGoogle Scholar
Heacock, A.M. & Agranoff, B.W. (1977). Clockwise growth of neurites from retinal explants. Science 198, 64–66.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 Scandinavia (Suppl.) 364, 81–108.Google Scholar
Hollenbeck, P.J. (1989). The transport and assembly of the axonal cytoskeleton. Journal of Cell Biology 108, 223–227.CrossRefGoogle ScholarPubMed
Kastelic, J., Galeski, A. & Baer, E. (1978). The multicomposite structure of tendon. Connective Tissue Research 6, 11–23.CrossRefGoogle ScholarPubMed
Kuffler, S.W., Nicholls, J.G. & Orkand, R.K. (1966). Physiological properties of glial cells in the central nervous system. Journal of Neurophysiology 36, 768–786.Google Scholar
Lillie, J.H., Maccallum, D.K., Scaletta, L.J. & Occhino, J.C. (1977). Collagen structure: evidence for a helical organization of the collagen fibril. Journal of Ultrastructural Research 58, 134–143.CrossRefGoogle Scholar
Maggs, A. & Scholes, J. (1986). Glial domains and nerve fiber patterns in the fish retinotectal pathway. Journal of Neuroscience 6, 424–438.CrossRefGoogle ScholarPubMed
Maggs, A. & Scholes, J. (1990). Reticular astrocytes in the fish optic nerve: macroglia with epithelial characteristics form an axially repeated lacework pattern, to which nodes of Ranvier are apposed. Journal of Neuroscience 10, 1600–1614.Google Scholar
Marrero, H., Astion, M.L., Coles, J.A. & Orkand, R.K. (1989). Facilitation of voltage-gated ion channels in frog neuroglia by nerve impulses. Nature 339, 378–380.Google Scholar
Maturana, H. (1960). The fine anatomy of the optic nerve of Anurans–an electron-microscope study. Journal of Biophysical and Biochemical Cytology 7, 107–119.Google Scholar
Miller, R.H. & Raff, M.C. (1984). Fibrous and protoplasmic astrocytes are biochemically and developmentally distinct. Journal of Neuroscience 4, 585–592.Google Scholar
Miller, R.H., Ffrench-Constant, C. & Raff, M.C. (1989a). The macroglial cells of the rat optic nerve. Annual Review of Neuroscience 12, 517–534.Google Scholar
Miller, R.H., Fulton, B.P. & Raff, M.C. (1989b). A novel type of glial cell associated with nodes of Ranvier in the rat optic nerve. European Journal of Neuroscience 1, 172–180.Google Scholar
Niven, H., Baer, E. & Hiltner, A. (1982). Organization of collagen fibers in rat tail tendon at the optical microscope level. Collagen and Related Research 2, 131–137.Google Scholar
Nona, S.N., Shehab, S.A.S., Stafford, C.A. & Cronly-Dillon, J.R. (1989). Glial fibrillary acidic protein (GFAP) from goldfish: its localization in the visual pathway. Glia 2, 189–200.Google Scholar
Papasozomenas, S.Ch. & Binder, L.I. (1986). Microtubule-associated protein 2 (MAP-2) is present in astrocytes of the optic nerve, but absent from astrocytes of the optic tract. Journal of Neuroscience 6, 1748–1756.Google Scholar
Peters, A., Palay, S.L. & Webster, H.De F. (1976). The Fine Structure of the Nervous System. Philadelphia, Pennsylvania: W.B. Saunders.Google Scholar
Quitschke, W., Jones, P.S. & Schechter, N. (1985). Survey of intermediate filament proteins in the optic nerve and spinal cord. Journal of Neurochemistry 44, 1465–1476.Google Scholar
Quitschke, W. & Schechter, N. (1986). Homology and diversity between intermediate filament proteins of neuronal and non-neuronal origin in goldfish optic nerve. Journal of Neurochemistry 46, 545–555.Google Scholar
Raff, M.C. (1989). Glial cell diversification in the rat optic nerve. Science 243, 1450–1455.Google Scholar
Rigby, B.J., Hirai, N., Spikes, J.D. & Eyring, H. (1960). The mechanical properties of rat tail tendon. Journal of General Physiology 43, 265–283.Google Scholar
Rovainen, C.M. (1979). Neurobiology of lampreys. Physiological Reviews 59, 1007–1077.Google Scholar
Rungger-Brändle, E., Achtstätter, T. & Franke, W.W. (1989). An epithelial-type cytoskeleton in a glial cell: astrocytes of amphibian optic nerves contain cytokeratin filaments and are connected by desmosomes. Journal of Cell Biology 109, 705–716.Google Scholar
Scholes, J. (1979). Nerve fiber topography in the retinal projection to the tectum. Nature 278, 620–624.Google Scholar
Scholes, J. (1981a). Ribbon optic nerves and axonal growth in the retinal projection to the tectum. In Development in the Nervous System, ed. Garrod, D.R. & Feldman, J.D., pp. 181–214. Cambridge: Cambridge University Press.Google Scholar
Scholes, J. (1981b). Retinal fiber projection patterns in the primary visual pathways to the brain. In Sense Organs, ed. Laverack, M. & Cosens, J., pp. 255–275. Edinburgh, UK: Blackie.Google Scholar
Shaw, G. & Bray, D. (1977). Movement and extension of isolated growth cones. Experimental Cell Research 104, 55–62.Google Scholar
Shaw, G., Osborn, M. & Weber, K. (1981). An immunofluorescence study of the neurofilament triplet proteins, vimentin, and glial fibrillary acidic protein within the adult rat brain. European Journal of Cell Biology 26, 68–82.Google Scholar
Shehab, S.A.S., Stafford, C.A., Warren, A., Nona, S. & Cronly-Dillon, J.R. (1991). Localization of protoplasmic and fibrous-like astrocytes in the rat optic nerve and tract. Journal of Neurocytology (submitted).Google Scholar
Skoff, R.P., Knapp, P.E. & Bartlett, W.P. (1986). Astrocytic diversity in the optic nerve: a cytoarchitectural study. In Astrocytes, Vol. 1, ed. Fedorov, S. & Vernadakis, A., pp. 269–291. London: Academic Press.Google Scholar
Stensaas, L.J. & Stensaas, S.S. (1968). Astrocytic neuroglial cells, oligodendrocytes, and microgliacytes in the spinal cord of the toad, II: Electron microscopy. Zeitschrift für Zellforschung 86, 184–213.Google Scholar
Sunderland, S. (1978). Nerves and Nerve Injuries, 2nd edition. Edinburgh, UK. Churchill Livingstone.Google Scholar
Tabony, J. & Job, D. (1990). Spatial structures in microtubular solutions requiring a sustained energy source. Nature 346, 448–451.CrossRefGoogle ScholarPubMed
Tapp, R.L. (1974). Axon numbers and distribution, myelin thickness, and the reconstruction of the compound action potential in the optic nerve of the teleost Eugerres plumieri. Journal of Comparative Neurology 153, 267–274.Google Scholar
Thomas, P.K. & Olsson, Y. (1984). Microscopic anatomy and function of the connective tissue components of peripheral nerves. In Peripheral Neuropathy, ed. Dyck, P.J., Thomas, P.K., Lambert, E.H. & Bunge, R. pp. 97–120. Philadelphia, Pennsylvania: W.B. Saunders.Google Scholar
Trewavas, E. (1983). Tilapiine Fish of the Genera Sarotherodon, Oreochromis and Danakilia, British Museum, Dorchester, UK: The Dorset Press.Google Scholar
Ushiki, T. & Ide, C. (1990). Three-dimensional organizational of the collagen fibrils in the rat sciatic nerve as revealed by transmission- and scanning-electron microscopy. Cell Tissue Research 260, 175–184.Google Scholar
Usowicz, M.M., Gallo, V. & Cull-Candy, S.G. (1989). Multiple conductance channels in type-2 cerebellar astrocytes activated by excitatory amino acids. Nature 339, 380–383.Google Scholar
Wainwright, S.A., Biggs, W.D., Currey, J.D. & Gosline, J.M. (1976). Mechanical Design in Animals. London: Edward Arnold.Google Scholar
Walls, G.L. (1963). The Vertebrate Eye and Its Adaptive Radiation. New York: Hafner.Google Scholar
Walsh, F.B. & Hoyt, W.F. (1982). Walsh & Hoyt's Clinical Neuro-Ophthalmology, 4th edition. ed. Miller, N.R.Baltimore, Maryland: Williams & Wilkins.Google Scholar
Wässle, H. & Riemann, H.J. (1978). The mosaic of nerve cells in the mammalian retina. Proceedings of the Royal Society B (London) 200, 441–461.Google Scholar
Wässle, H., Peichl, L. & Boycott, B.B. (1981). Dendritic territories of cat retinal ganglion cells. Nature 292, 344–345.Google Scholar
Zvěřina, E. & Šprincl, L. (1979a). Basic facts about peripheral nerves reviewed after 200 years Časopis Lekaru Československa 118, 920–924.Google Scholar
Zvěřina, E. & Šprincl, L. (1979b). Fontanovy spirálové pruhy a vlnovitý prübéh nervoých vláken. Československa Neurologie a Neurochirurgia 42, 333–339.Google Scholar