Summary
The features of unlesioned and lesioned trochlear nerves of goldfish have been examined electron microscopically. Lesioned nerves were studied between 1 and 107 days after cutting or crushing the nerve.
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1.
Unlesioned nerves contained, on average, 77 myelinated axons and 19 unmyelinated axons. The latter were found in 1–2 fascicles per nerve. A basal lamina surrounded each myelinated axon and fascicle of unmyelinated axons. The numbers of myelinated axons, fascicles of unmyelinated axons and basal laminae varied by less than 5% over the intraorbital extramuscular segment of the nerve.
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2.
Following interruption of the nerve, by either cutting or crushing, all of the axons and their myelin sheaths began to degenerate by 4 days in the distal nerve-stump. Both abnormally electron-dense and electron-lucent axons were observed. Both Schwann cells and macrophages appeared to phagocytose the myelin sheaths.
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3.
Following a lesion, the Schwann cells and their basal laminae persisted in the distal nerve-stump. In crushed nerves, the basal laminae surrounding myelinated axons formed 97%, on average, of the Schwann tubes in the distal stump. The perimeters of the basal laminae were of similar size to those in the proximal stump, at least for the first 8 days after crush.
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4.
In crushed nerves, single myelinated axons in the proximal nerve-stump gave rise to multiple sprouts, some of which reached the site of crush by 2 days, the distal stump by 4 days and the superior oblique muscle by 8 days. The regeneration of the unmyelinated axons was not examined.
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5.
In both crushed and transected nerves, nearly all of the sprouts in the proximal and distal stumps were found within the basal laminae of Schwann cells, even though the sprouts were disorganized in the transected region where there were no basal laminae. The growth cones of the regenerating axons were always found apposed to the inner surface of the basal laminae, which may have provided an adhesive substrate that directed their growth.
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6.
Terminal sprouts from the ends of myelinated axons in the proximal stump accounted for the majority of the regenerating axons in the distal stump, as only a few collateral sprouts were found in the proximal stump, and only a small amount of axonal branching was found within the distal stump itself.
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7.
The largest axons in the distal stump were remyelinated first, and the number of remyelinated axons increased progressively between 8 and 31 days after crush, at which time there were about twice as many as in unlesioned nerves. The number of remyelinated axons remained constant at least until 107 days, the longest time considered, and none was observed to degenerate, whereas some axons that were not remyelinated appeared to degenerate.
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8.
Although each basal lamina in the distal stump often surrounded several regenerating axons during the first 2 weeks post-lesion, each remyelinated axon became individually surrounded by a basal lamina, collagen fibres and extracellular space between 13 and 107 days, thereby increasing the number of basal laminae in the distal stump.
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9.
Regenerated axonal terminals in the superior oblique were first observed 8 days after crush. The number of synapses increased progressively between 8 and 107 days, at which time they were as numerous as in unlesioned animals.
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References
Aguayo, A. J., David, S. &Bray, G. M. (1981) Influence of the glial environment on the elongation of axons after injury: transplantation studies in adult rodents,Journal of Experimental Biology 95, 231–40.
Aguayo, A. J., Epps, J., Charron, L. &Bray, G. M. (1976) Multipotentiality of Schwann cells in cross-anastomosed and grafted myelinated nerves: quantitative microscopy and radioautography.Brain Research 104, 1–20.
Aitken, J. T. (1949) The effect of peripheral connections on the maturation of regenerating nerve fibres.Journal of Anatomy 83, 32–43.
Aitken, J. T., Sharman, M. &Young, J. Z. (1947) Maturation of regenerating nerve fibres with various terminal connexions.Journal of Anatomy 81, 1–22.
Akers, R. M., Mosher, D. F. &Lilien, J. E. (1981) Promotion of retinal neurite outgrowth by substratum-bound fibronectin.Developmental Biology 86, 179–88.
Akert, K., Sandri, C., Weibel, E. R., Peper, K. &Moor, H. (1976) The fine structure of the perineural endothelium.Cell and Tissue Research 165, 281–95.
Al-Ghaith, L. K. &Lewis, J. H. (1982) Pioneer growth cones in virgin mesenchyme: an electron-microscope study in the developing chick wing.Journal of Embryology and Experimental Morphology 68, 149–60.
Autilio-Gambetti, L., Sipple, J., Sudilovsky, O. &Gambetti, P. (1982) Intermediate filaments of Schwann cells.Journal of Neurochemistry 38, 774–80.
Ballin, R. H. M. &Thomas, P. K. (1969) Electron microscope observations on demyelination and remyelination in experimental allergic neuritis. II. Remyelination.Journal of the Neurological Sciences 8, 225–37.
Barber, D. L., Westerman, J. E. M. &White, M. G. (1981) The blood cells of the Antarctic icefishChaenocephalus acemtus Lonnberg: light and electron microscopic observations.Journal of Fish Biology 19, 11–28.
Barton, A. A. (1962) An electron microscopic study of degeneration and regeneration of nerve.Brain 85, 799–808.
Berger, B. (1971) Etude ultrastructurale de la dégénerescence Wallérienne experimentale d'un nerf entierement amyelinique: le nerf olfactif. I. Modications axonales.Journal of Ultrastructure Research 37, 105–18.
Berner, A., Torvik, A. &Stenwig, A. E. (1973) Origin of macrophages in traumatic lesions and Wallerian degeneration in peripheral nerves.Acta neuropathologica 25, 228–36.
Bittner, G. D. &Johnson, A. L. (1974) Degeneration and regeneration in crustacean peripheral nerves.Journal of Comparative Physiology 89, 1–21.
Bloom, W.&Fawcett, D. W. (1975)A Textbook of Histology. Philadelphia: Saunders.
Blümcke, S., Niedorf, H. R. &Rode, J. (1966) Axoplasmic alterations in the proximal and distal stumps of transected nerves.Acta neuropathologica 7, 44–61.
Bohn, R. C., Reier, P. J. &Sourbeer, E. B. (1982) Axonal interactions with connective tissue and glial substrata during optic nerve regeneration inXenopus larvae and adults.American Journal of Anatomy 165, 397–419.
Bohn, R. C. &Stelzner, D. J. (1981) The aberrant retino-retinal projection during optic nerve regeneration in the frog. I. Time course of formation and cells of origin.Journal of Comparative Neurology 196, 605–20.
Boydston, W. R. &Sohal, G. S. (1980) Intact peripheral target essential for branching of developing nerve fibers.Experimental Neurology 70, 173–8.
Bray, G. M. &Aguayo, A. J. (1974) Regeneration of peripheral unmyelinated nerves. Fate of axonal sprouts which develop after injury.Journal of Anatomy 117, 517–29.
Brushart, T. M. &Mesulam, M-M. (1980) Alternation in connections between muscle and anterior horn motoneurons after peripheral nerve repair.Science 208, 603–5.
Bunge, M. B. (1973) Fine structure of nerve fibers and growth cones of isolated sympathetic neurons in culture.Journal of Cell Biology 56, 713–35.
Bunge, M. B., Williams, A. K. &Wood, P. M. (1982) Neuron-Schwann cell interaction in basal lamina formation.Developmental Biology 92, 449–60.
Calabretta, A. M., Munger, B. L. &Graham, W. P. (1973) The ultrastructure of degenerating rat sciatic nerves.Journal of Surgical Research 14, 465–71.
Cannon, M. S., Mollenhauer, H. H., Eurell, T. E., Lewis, D. H., Cannon, A. M. &Tompkins, C. (1980) An ultrastructural study of the leukocytes of the channel catfish.Ictalurus punctatus.Journal of Morphology 164, 1–23.
Causey, G. &Huffman, H. (1955) Axon sprouting in partially deneurotized nerves.Brain 78, 661–8.
Chu-Wang, I.-W. &Oppenheim, R. W. (1978) Cell death of motoneurons in the chick embryo spinal cord. II. A quantitative and qualitative analysis of degeneration in the ventral root, including evidence for axon outgrowth and limb reinnervation prior to cell death.Journal of Comparative Neurology 177, 59–86.
Coggeshall, R. E. (1980) Law of separation of function of spinal roots.Physiological Reviews 60, 716–55.
Collins, F. &G Arrett, J. E. (1980) Elongating nerve fibers are guided by a pathway of material released from embryonic nonneuronal cells.Proceedings of the National Academy of Sciences USA 77, 6626–8.
Conover, W. J. (1971)Practical Nonparametric Statistics. New York: Wiley.
Cook, R. D., Ghetti, B. &Wisniewski, H. M. (1974) The pattern of Wallerian degeneration in the optic nerve of newborn kittens: an ultrastructural study.Brain Research 75, 261–75.
Cornbrooks, C. (1983) Expression and distribution of entactin in extracellular matrix of adult rat peripheral nerve and peripheral nerve cells in culture.Society for Neuroscience Abstracts 9, 346.
Cravioto, H. (1969) Wallerian degeneration: ultrastructural and histochemical studies.Bulletin of the Los Angeles Neurological Society 34, 233–53.
Davey, D. F., Mark, R. F., Marotte, L. R. &Proske, U. (1975) Structure and innervation of extraocular muscles ofCarassius.Journal of Anatomy 120, 131–47.
Dyck, P. J. &Hopkins, A. P. (1972) Electron microscopic observations on degeneration and regeneration of unmyelinated fibers.Brain 95, 123–34.
Easter Jr, S. S. (1979) The growth and development of the superior oblique muscle and trochlear nerve in juvenile and adult goldfish.Anatomical Record 195, 683–98.
Easter Jr, S. S., Rusoff, A. C. &Kish, P. E. (1981) The growth and organization of the optic nerve and tract in juvenile and adult goldfish.Journal of Neuroscience 1, 799–811.
Edgington, D. R., Kuffler, D. P. &McMahon, U. J. (1980) Extracellular structures at the neuromuscular junction direct the growth of regenerating axons.Society for Neuroscience Abstracts 6, 92.
Ehrlich, D. &Mark, R. F. (1977) Fiber counts of regenerating peripheral nerves in axolotls and the effect of metamorphosis.Journal of Comparative Neurology 174, 306–16.
Elliot, E. J. &Muller, K. J. (1981) Long term survival of glial segments during nerve regeneration in the leech.Brain Research 218, 99–113.
Ellis, A. E. (1977) The leukocytes of fish: a review.Journal of Fish Biology 11, 453–91.
Estable, C., Acosta-Ferreira, W. &Sotelo, J. R. (1957) An electron microscope study of regenerating nerve fibers.Zeitschrift für Zellforschung und mikroskopische Anatomie 46, 387–99.
Evans, D. H. L. &Murray, J. G. (1956) A study of regeneration in a motor nerve with a unimodal fiber diameter distribution.Anatomical Record 126, 311–33.
Fawcett, J. W. &Gaze, R. M. (1981) The organization of regenerating axons in theXenopus optic nerve.Brain Research 229, 487–90.
Ferguson, H. W. (1976) The ultrastructure of plaice (Pleuronectes platessa) leucocytes.Journal of Fish Biology 8, 139–42.
Fisher, E. R. &Turano, A. (1963) Schwann cells in Wallerian degeneration.Archives of Pathology 75, 517–27.
Friede, R. L. &Bischhausen, R. (1980) The fine structure of transected nerve fibers in subserial sections.Journal of Neurological Sdences 44, 181–203.
Fujisawa, H., Tani, M., Watanabe, K. &Ibata, Y. (1982) Branching of regenerating retinal axons and preferential selection of appropriate branches for specific neuronal connection in the newt.Developmental Biology 90, 43–57.
Gasser, H. S. (1955) Properties of dorsal root unmyelinated fibers on the two sides of the ganglion.Journal of General Physiology 38, 709–28.
Gaze, R. M. (1970)The Formation of Nerve Connections, pp. 8–75. London: Academic Press.
Gibson, J. D. (1979) The origin of the neural macrophage: a quantitative ultrastructural study of cell population changes during Wallerian degeneration.Journal of Anatomy 129, 1–19.
Glees, P. (1943) Observations on the structure of the connective tissue sheaths of cutaneous nerves.Journal of Anatomy 77, 153–9.
Grafstein, B. &McQuarrie, I. G. (1978) Role of the nerve cell body in axonal regeneration. InNeuronal Plastidty (edited byCotman, C. W.), pp. 155–95. New York: Raven Press.
Grimm, L. (1971) An evaluation of myotypic respecification in axolotls.Journal of Experimental Zoology 178, 479–96.
Guth, L. (1956) Regeneration in the mammalial peripheral nervous system.Physiological Reviews 36, 441–78.
Gutmann, E. &Sanders, F. K. (1943) Recovery of fibre numbers and diameters in the regeneration of peripheral nerves.Journal of Physiology 101, 489–518.
Gutmann, E. &Young, J. Z. (1944) The reinnervation of muscle after various periods of atrophy.Journal of Anatomy 78, 15–43.
Haftek, J. &Thomas, P. K. (1968) Electron-microscope observations on the effects of localized crush injuries on the connective tissues of the peripheral nerve.Journal of Anatomy 103, 233–43.
Hall, S. M. (1973) Some aspects of remyelination after demyelination produced by intraneural injection of lysophosphatidyl choline.Journal of Cell Science 13, 461–77.
Herrick, C. J. (1899) The cranial nerves and first spinal nerves ofMenidia; a contribution upon the nerve components of bony fishes.Journal of Comparative Neurology 9, 153–455.
Holmes, W. &Young, J. Z. (1942) Nerve regeneration after immediate and delayed suture.Journal of Anatomy 77, 63–97.
Holtzman, E. &Novikoff, A. B. (1965) Lysosomes in the rat sciatic nerve following crush.Journal of Cell Biology 27, 651–69.
Horch, K. W. (1979) Guidance of regrowing sensory axons after cutaneous nerve lesions in the cat.Journal of Neurophysiology 42, 1437–49.
Hughes, A. F. (1965) A quantitative study on the development of the nerves in the hindlimb ofElentherodactylus martinensis.Journal of Embryology and Experimental Morphology 13, 9–34.
Hughes, A. &Egar, M. (1972) The innervation of the hindlimb ofElentherodactylus martinicensis: further comparison of cell and fiber numbers during development.Journal of Embryology and Experimental Morphology 27, 389–412.
Ide, C. (1983) Nerve regeneration and Schwann cell basal lamina: observations of long-term regeneration.Archivum Histologicum Japonicum 46, 243–57.
Inberg, K. R. (1949) Regeneration of motor and sensory fibres in the sciatic nerve and in the suralis nerve of the cat.Acta physiologica scandinavica 18, 308–23.
Joseph, B. S. (1973) Somatofugal events in Wallerian degeneration: a conceptual overview.Brain Research 59, 1–18.
Kapeller, K. &Mayor, D. (1969) An electron microscopic study of early changes proximal to a constriction in sympathetic nerves.Proceedings of the Royal Society of London B 172, 39–51.
Karnovsky, M. J. (1967) The ultrastructural basis of capillary permeability studied with peroxidase as a tracer.Journal of Cell Biology 35, 213–36.
Kilarski, W. &Bigaj, J. (1969) Organization and fine structure of extraocular muscle inCarassius andRana.Zeitschrift für Zellforschung und mikroskopische Anatomie 94, 194–204.
King, R. H. M. &Thomas, P. K. (1971) Electron microscopic observations on aberrant regeneration of unmyelinated axons in the vagus nerve of the rabbit.Acta neuropathologica 18, 150–9.
Kruger, L. &Maxwell, D. S. (1969) Wallerian degeneration in the optic nerve of a reptile: an electron microscopic study.American Journal of Anatomy 125, 247–70.
Lance-Jones, C. (1982) Motoneuron cell death in the developing lumbar spinal cord of the mouse.Developmental Brain Research 4, 473–9.
Lander, A. J., Fujii, D. K., Gospodarowicz, D. &Reichard, L. F. (1982) Characterization of a factor that promotes neunte outgrowth—evidence linking activity to a heparan sulfate proteoglycan.Journal of Cell Biology 94, 574–85.
Lanners, N. N. &Grafstein, B. (1980) Early stages of axonal regeneration in the goldfish optic nerve: an electron microscopic study.Journal of Neurocytology 9, 733–51.
Lee, J. C-Y. (1963) Electron microscopy of Wallerian degeneration.Journal of Comparative Neurology 120, 65–80.
Letinsky, M. S., Fischbeck, K. H. &McMahan, U. J. (1976) Precision of reinnervation of original postsynaptic sites in frog muscle after nerve crush.Journal of Neurocytology 5, 691–718.
Letourneau, P. C. (1975a) Possible roles for cell-to-substratum adhesion in neuronal morphogenesis.Developmental Biology 44, 77–91.
Letourneau, P. C. (1975b) Cell-to-substratum adhesion and guidance of axonal elongation.Developmental Biology 44, 92–101.
Letourneau, P. C. (1982) Nerve fiber growth and extrinsic factors. InNeuronal Development (edited bySpitzer, N. C.), pp. 213–54. New York: Plenum.
Lubińska, L. (1959) Region of transition between preserved and regenerated parts of myelinated fibers.Journal of Comparative Neurology 113, 315–25.
Luiten, P. J. M. (1979) Proprioceptive reflex connections of head musculature and the mesencephalon trigeminal nucleus in the carp.Journal of Comparative Neurology 183, 903–12.
Luiten, P. J. M. &Dijkstra-De Vlieger, H. P. (1978) Extraocular muscle representation in the brainstem of the carp.Journal of Comparative Neurology 179, 669–76.
Mark, R. F. (1965) Fin movements after regeneration of neuromuscular connections: an investigation of myotypic respecification.Experimental Neurology 12, 292–302.
Mark, R. F. &Marotte, L. R. (1972) The mechanism of selective reinnervation of fish eye muscles. III. Functional, electrophysiological, and anatomical analysis of recovery from section of the IIIrd and IVth nerves.Brain Research 46, 131–48.
Marotte, L. R. &Mark, R. F. (1970) The mechanism of selective reinnervation of fish eye muscle. II. Evidence from electron microscopy of nerve endings.Brain Research 19, 53–62.
Matsumoto, D. E. &Scalia, F. (1981) Long-term survival of centrally projecting axons in the optic nerve of the frog following destruction of the retina.Journal of Comparative Neurology 202, 135–55.
Matthews, M. A. (1968) An electron microscopic study of the relationship between axon diameter and the initiation of myelin production in the peripheral nervous system.Anatomical Record 161, 337–52.
Matthews, M. R. (1973) An ultrastructural study of axonal changes following constriction of the postganglionic branches of the superior cervical ganglion in the rat.Philosophical Transactions of the Royal Society of London B 264, 479–508.
Meyer, R. L. (1980) Mapping the normal and regenerating retinotectal projection of goldfish with autoradiographic methods.Journal of Comparative Neurology 189, 273–89.
Miledi, R. &Slater, C. R. (1970) On the degeneration of rat neuromuscular Junctions after nerve section.Journal of Physiology 207, 507–28.
Mira, J-C. (1976) Etudes quantitatives sur la régénération des fibres nerveuses myélinisées. II. Variations du nombre et du calibre des fibres régénérées après un écrasement ou une section du nerf.Archives d'Anatomie Microscopique et de Morphologie Experimentale 65, 255–84.
Mira, J-C. (1977) Etudes quantitatives sur la régénération des fibres nerveuses myélinisées. III. Variations du numbre et du calibre des fibres régénérées après une congélation localisée.Archives d'Anatomie Microscopique et de Morphologie Experimentale 66, 1–15.
Mire, J. J., Hendelman, W. J. &Bunge, R. P. (1970) Observations on a transient phase of focal swelling in degenerating unmyelinated nerve fibres.Journal of Cell Biology 45, 9–22.
Mizuno, N., Uamura, M., Matsuda, K., Takenchi, Y., Kume, M. &Matsushima, R. (1980) Non-selective distribution of hypoglossal nerve fibers of hypoglossal section and resuture.Neuroscience Letters 19, 33–7.
Montgomery, J. C. &MacDonald, J. A. (1980) Stretch receptors in the eye muscles of teleost fish.Experientia 36, 1176–7.
Morris, J. H., Hudson, A. R. &Weddell, A. G. M. (1972) A study of degeneration and regeneration in the divided rat sciatic nerve. I–IV.Zeitschrift für Zellforschung und mikroskopische Anatomie 124, 76–203.
Murray, M. (1976) Regeneration of retinal axons in the goldfish optic tectum.Journal of Comparative Neurology 168, 175–96.
Murray, M. (1982) A quantitative study of regenerative sprouting by optic axons in goldfish.Journal of Comparative Neurology 209, 352–62.
Nathaniel, E. J. H. &Pease, D. C. (1963a) Degenerative changes in rat dorsal roots during Wallerian degeneration.Journal of Ultrastructure Research 9, 511–32.
Nathaniel, E. J. H. &Pease, D. C. (1963b) Regenerative changes in rat dorsal roots following Wallerian degeneration.Journal of Ultrastructure Research 9, 533–49.
Nathaniel, E. J. H. &Pease, D. C. (1963c) Collagen and basement membrane formation by Schwarm cells during nerve regeneration.Journal of Ultrastructure Research 9, 550–60.
O'Daly, J. A. &Imaeda, T. (1967) Electron microscopic study of Wallerian degeneration in cutaneous nerves caused by mechanical injury.Laboratory Investigation 170, 744–66.
Oehmichen, M. &Torvik, A. (1976) The origin of reactive cells in retrograde and Wallerian degeneration.Cell and Tissue Research 173, 343–8.
Ohmi, S. (1961) Electron microscopic study on Wallerian degeneration of the peripheral nerve.Zeitschrift für Zellforschung und mikroskopische Anatomie 54, 39–67.
Oldfors, A. (1980) Macrophages in peripheral nerves.Acta neuropathologica 49, 43–9.
Olsson, Y. &Sjöstrand, J. (1969) Origin of macrophages in Wallerian degeneration demonstrated autoradiographically.Experimental Neurology 23, 102–12.
Payer, A. (1979) An ultrastructural study of Schwarm cell response to axonal degeneration.Journal of Comparative Neurology 183, 365–84.
Politis, M. J., Ederle, K. &Spencer, P. S. (1982) Tropism in nerve regenerationin vivo. Attraction of regenerating axons by diffusible factors derived from cells in distal nerve stumps of transected peripheral nerves.Brain Research 253, 1–12.
Politis, M. J. &Spencer, P. S. (1981) A method to separate spatially the temporal sequence of axon-Schwann cell interaction during nerve regeneration.Journal of Neurocytology 10, 221–32.
Pollard, J. D. &Fitzpatrick, L. (1973a) An ultrastructural comparison of peripheral nerve allografts and autografts.Acta neuropathologica 23, 152–65.
Pollard, J. D. &Fitzpatrick, L. (1973b) A comparison of the effects of irradiation and immunosuppressive agents on the regeneration through peripheral nerve allografts: an ultrastructural study.Acta neuropathologica 23, 166–80.
Prestige, M. C. &Wilson, M. A. (1974) A quantitative study of the growth and development of the ventral root in normal and experimental conditions.Journal of Embryology and Experimental Morphology 32, 819–33.
Prestige, M. C. &Wilson, M. A. (1980) Growth of a limb spinal nerve: an ultrastructural study.Journal of Comparative Neurology 194, 235–66.
Quilliam, T. A. (1958) Growth changes in sensory fibre aggregates undergoing remyelinarion.Journal of Anatomy 72, 383–98.
Ramón Y Cajal, S. (1928)Degeneration and Regeneration of the Nervous System (translated byMay, R. M.). Oxford: Oxford University Press.
Rawlins, F. A., Villegas, G. M., Hedley-White, E. T. &Uzman, B. G. (1972) Fine Structural localization of cholesterol-1,2-3H in degenerating and regenerating mouse sciatic nerve.Journal of Cell Biology 52, 615–25.
Reier, P. J. &Hughes, H. (1972) Evidence for spontaneous axon degeneration during peripheral nerve maturation.American Journal of Anatomy 135, 147–52.
Reier, P. J. &Webster, H. De F. (1974) Regeneration and remyelination ofXenopus tadpole optic nerve fibres following transection or crush.Journal of Neurocytology 3, 591–618.
Reynolds, E. S. (1963) The use of lead citrate at high pH as an electron opaque stain in electron microscopy.Journal of Cell Biology 17, 208–12.
Richardson, P. M., Issa, V. M. K. &Shemie, S. (1982) Regeneration and retrograde degeneration of axons in the rat optic nerve.Journal of Neurocytology 11, 949–66.
Roberts, A. &Taylor, J. S. H. (1982) A scanning electron microscopic study of the development of a peripheral sensory neunte network.Journal of Embryology and Experimental Morphology 69, 237–50.
Rogers, S. L., Letourneau, P. C., Palm, S. L., McCarthy, J. &Furcht, L. (1983) Neunte extension by peripheral and central nervous system neurons in response to substratum-bound fibronectin and laminin.Developmental Biology 98, 211–20.
Romer, A. S. &Parsons, T. S. (1977)The Vertebrate Body, Philadelphia: Saunders.
Rotshenker, S. &McMahan, U. J. (1976) Altered pattern of innervation in frog muscle after denervation.Journal of Neurocytology 5, 719–30.
Sanes, J. R. &Cheney, J. S. H. (1982) Laminin, fibronectin, and collagen in synaptic, and extrasynaptic portions of muscle fiber basement membrane.Journal of Cell Biology 93, 442–51.
Satinsky, D., Pepe, F. A. &Liu, C. N. (1964) The neurilemma cell in peripheral nerve degeneration and regeneration.Experimental Neurology 9, 441–51.
Scadding, J. W. &Thomas, P. K. (1983) Retrograde growth of myelinated fibres in experimental neuromas.Journal of Anatomy 136, 793–9.
Scherer, S. S. (1983) Non-selectivity of axonal regeneration in the oculomotor nerve of goldfish.Society for Neuroscience Abstracts 9, 47.
Schlaepfer, W. W. &Haster, M. B. (1979) The persistence and possible externalization of axonal debris during Wallerian degeneration.Journal of Neuropathology and Experimental Neurology 38, 242–52.
Scott, S. A. (1977) Maintained function of foreign and appropriate junctions on reinnervated goldfish extraocular muscles.Journal of Physiology 268, 87–109.
Scott, T. M.&Foote, J. (1981) A study of degeneration, scar formation, and regeneration after section of the optic nerve in the frog,Rana pipiens.Journal of Anatomy 133, 213–25.
Shawe, G. D. H. (1954) On the number of branches formed by regenerating nerve-fibres.British Journal of Surgery 42, 474–88.
Simionescu, N. &Simionescu, M. (1976) Galloylglucoses of low molecular weight as mordant for electron microscopy.Journal of Cell Biology 70, 608–21.
Singer, M. &Steinberg, M. C. (1972) Wallerian degeneration, a reevaluation based on transected and colchicine-poisoned nerves in amphibianTriturus.American Journal of Anatomy 133, 51–83.
Sohal, G. S. &Weidman, T. A. (1978) Development of the trochlear nerve: Loss of axons during normal ontogeny.Brain Research 142, 455–465.
Sokal, R. R. &Rohlf, F. J. (1981)Biometry. San Francisco: Freeman.
Speidel, C. C. (1935) Studies of living nerves. III. Phenomena of nerve irration, recovery, degeneration and repair.Journal of Comparative Neurology 61, 1–82.
Spencer, P. S. &Thomas, P. K. (1974) Ultrastructural studies of the dying-back process II. The sequestration and removal by Schwärm cells and oligodendrocytes of organelles from normal and diseased axons.Journal of Neurocytology 3, 763–83.
Sperry, R. W. (1945) The problem of central nervous reorganization after nerve regeneration and muscle transposition.Quarterly Review of Biology 20, 311–69.
Sperry, R. W. &Arora, H. L. (1965) Selectivity in the regeneration of the oculomotor nerve in the cichlid fish,Astronotus ocellatus.Journal of Embryology and Experimental Morphology 14, 307–17.
Springer, A. D. (1981) Normal and abnormal retinal projections following the crush of one optic nerve in goldfish (Carassius auratus).Journal of Comparative Neurology 199, 87–95.
Stelzner, D. J. (1982) Regenerating frog optic and mammalian PNS axons. Are they really so different?Trends in Neurosciences 5, 167–9.
Stensaas, L. J. &Feringa, E. R. (1977) Axon regeneration across the site of injury in the optic nerve of the newtTriturus pyrrhogaster.Cell and Tissue Research 179, 501–16.
Stephenson, R. S. (1979) Axon reflexes in axolotl limbs: evidence that branched motor axons reinnervate muscles selectively.Experimental Neurology 64, 174–84.
Sterling, P. (1977) Anatomy and physiology of the goldfish oculomotor system. I. Structure of the abducens nucleus.Journal of Neurophysiology 40, 557–72.
Stuermer, C. A. O. &Easter, jr, S. S. (1984) A comparison of the normal and regenerated retinotectal pathways of goldfish.Journal of Comparative Neurology 223, 57–76.
Sunderland, S. &Bradley, K. C. (1950) Endoneurial tube shrinkage in the distal segment of a severed nerve.Journal of Comparative Neurology 93, 411–20.
Thomas, P. K. (1963) The connective tissue of peripheral nerve: an electron microscope study.Journal of Anatomy 97, 35–44.
Thomas, P. K. (1964) Changes in the endoneurial sheaths of peripheral myelinated nerve fibers during Wallerian degeneration.Journal of Anatomy 98, 175–82.
Thomas, P. K. &King, R. H. M. (1974) The degeneration of unmyelinated axons following nerve section: an ultrastructural study.Journal of Neurocytology 3, 497–512.
Thomas, P. K. &Olsson, Y. (1975) Microscopic anatomy and function of the connective tissue components of peripheral nerve. InPeripheral Neuropathy (edited byDyck, P. J., Thomas, P. K.&Lambers, E. H.), pp. 168–89. Philadelphia: Saunders.
Thomas, P. K. &Young, J. Z. (1949) Internode lengths in the nerve of fishes.Journal of Anatomy 83, 336–50.
Tohyama, K., Ide, C., Nitatori, T. &Yokata, R. (1983) Nearest neighbor distance of intermediate filaments in axons and Schwann cells.Acta neuropathologica 60, 194–8.
Turner, J. E. &Singer, M. (1974) Ultrastructure of regeneration in the severed newt optic nerve.Journal of Experimental Zoology 190, 249–68.
Varon, S. S. &Bunge, R. P. (1978) Trophic mechanisms in the peripheral nervous system.Annual Review of Neuroscience 1, 327–61.
Vlodavsky, I., Levi, A., Lax, I., Fuks, Z. &Schlessinger, J. (1982) Induction of cell attachment and morphological differentiation of a pheochromocytoma cell line and embryonal sensory cells by the extracellular matrix.Developmental Biology 93, 285–300.
Watrous, W. G. (1940) Axon branching after nerve regeneration.Proceedings of the Society for Experimental Biology and Medicine 44, 541–2.
Webster, H. De F. (1962) Transient, focal accumulation of axonal mitochondria during the early stages of Wallerian degeneration.Journal of Cell Biology 12, 361–83.
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.
Webster, H. De F., Martin, J. R. &O'Connell, M. F. (1973) The relationships between interphase Schwann cells and axons before myelination: a quantitative electron microscope study.Developmental Biology 32, 401–16.
Weddell, G. (1942) Axonal regeneration in cutaneous nerve plexuses.Journal of Anatomy 77, 49–62.
Weddell, G. &Glees, P. (1941) The early stages in the degeneration of cutaneous nerve fibres.Journal of Anatomy 76, 65–93.
Weinberg, H. J. &Spencer, P. S. (1976) Studies on the control of myelinogenesis. II. Evidence for neuronal regulation of myelin production.Brain Research 113, 363–78.
Weinberg, H. J. &Spencer, P. S. (1978) The fate of Schwann cells isolated from axonal contact.Journal of Neurocytology 7, 555–69.
Weiss, P. (1934)In vitro experiments on the factors determining the course of the outgrowing nerve fiber.Journal of Experimental Zoology 68, 393–448.
Weiss, P. (1941) Nerve patterns: the mechanics of nerve growth.Growth Supplement 5, 163–203.
Weiss, P. &Campbell, C. J. (1944) Nerve fiber counts and muscle tension after nerve regeneration in the rat.American Journal of Physiology 140, 616–26.
Weiss, P., Hdds, M. V. &Cavanaugh, M. (1945) The effect of terminal connections on the caliber of nerve fibers.Anatomical Record 92, 215–33.
Weiss, P.&Taylor, A. C. (1944) Further experimental evidence against ‘neurotropism’ in nerve regeneration.Journal of Experimental Zoology 95, 233–57.
Weiss, P. &Wang, H. (1945) Transformation of adult Schwann cells into macrophages.Proceedings of the Society for Experimental Biology and Medicine 58, 273–5.
Westerfield, M. &Powell, S. (1983) Selective reinnervation of limb muscles by regenerating from motor axons.Developmental Brain Research 10, 301–4.
Wettstein, R. &Sotelo, J. R. (1963) Electron-microscope study on the regenerative process of peripheral nerves in mice.Zeitschrift für Zellforschung und mikroskopische Anatomie 59, 708–30.
Williams, P. L. &Hall, S. M. (1972) Chronic Wallerian degeneration: anin vivo and ultrasrructural study.Journal of Anatomy 109, 487–503.
Williams, S. W. (1930) Regeneration of peripheral nerves in Amphibia studied with the aid of a vital stain.Journal of Experimental Zoology 57, 145–81.
Yamada, K. M., Spooner, B. S. &Wessells, N. K. (1971) Ultrastructure and function of growth cones and axons of cultured nerve cells.Journal of Cell Biology 49, 614–35.
Yu, W-H. A. &Yu, M. C. (1983) Acceleration of regeneration of the crushed hypoglossal nerve by testosterone.Experimenatal Neurology 80, 349–60.
Zelena, J., Lubinska, L. &Gutmann, E. (1968) Accumulation of organelles at the ends of interrupted axons.Zeitschrift für Zellforschung und mikroskopishe Anatomie 91, 200–19.
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Scherer, S.S., Easter, S.S. Degenerative and regenerative changes in the trochlear nerve of goldfish. J Neurocytol 13, 519–565 (1984). https://doi.org/10.1007/BF01148079
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DOI: https://doi.org/10.1007/BF01148079