Summary
Cut and crushed crayfish claw nerves were examined with the electron microscope at intervals up to 6 months after lesion. In sections 1 centimeter distal to the lesion there were no signs of degeneration among the giant motor axons even after many months. Swelling of glial wrappings was observed within 48 hours of nerve severance and was particularly notable in the innermost glial layer, the adaxonal layer. Golgi elements, rough endoplasmic reticulum, and mitochondria accumulated in the glia. These changes were perhaps indicative of a greater supportive role required by the severed axons. Regeneration from the proximal stumps of the giant axons began within one week and had proceeded across the lesion gap by 4 weeks. Axon sprouts appeared to travel toward the terminals within the glial sheaths of the distal giant axon segments. Before regeneration was complete, as determined by a simple behaviour test, the regenerating axons occupied increasing proportions of the sheath space. After regeneration was complete occasional degenerations were seen among the sprouts. These degenerations may have occurred in regenerating axons which had grown to the incorrect muscles. The original distal giant axons probably degenerated, as well, after regeneration was complete. There was no evidence of rehealing of proximal and distal segments of the axons.
Similar content being viewed by others
References
Aghajanian, G. K., Bloom, F. E., Sheard, M. H.: Electron microscopy of degeneration within the serotonin pathway of rat brain. Brain Res. 13, 266–273 (1969).
Andersson, E., Edström, A., Jarlstedt, J.: Properties of RNA from giant axons of the crayfish. Acta physiol. scand. 1969, 1–12 (1969).
Armstrong, J. A.: An experimental study of the visual pathways in a reptile (Lacerta vivipara). J. Anat. (Lond.) 84, 146–167 (1950).
Birks, R., Katz, B., Miledi, R.: Physiological and structural changes at the amphibian myoneuronal junction in the course of nerve degeneration. J. Physiol. (Lond.) 150, 145–168 (1960).
Boeckh, J., Sandri, C., Akert, K.: Sensorische Eingänge und synaptische Verbindungen im Zentralnervensystem von Insekten. Experimentelle Degeneration in der antennalen Sinnesbahn im Oberschlundganglion von Fliegen und Schaben. Z. Zellforsch. 103, 429–446 (1970).
Boulton, R. S.: Degeneration and regeneration in the insect central nervous system. I. Z. Zellforsch. 101, 98–118 (1969).
— Rowell, C. H. F.: Degeneration and regeneration in the insect central nervous system. II. Z. Zellforsch. 101, 119–134 (1969).
Cuenod, M., Sandri, C., Akert, K.: Enlarged synaptic vesicles as an early sign of secondary degeneration in the optic nerve terminals of the pigeon. J. Cell Sci. 6, 605–613 (1970).
Gamble, H. J., Goldberg, F., Smith, G. M. R.: Effect of temperature on the degeneration of nerve fibers. Nature (Lond.) 179, 527 (1957).
Grainger, F., James, D. W.: Association of glial cells with terminal parts of neurite bundles extending from chick spinal cord in vitro. Z. Zellforsch. 108, 93–105 (1970).
Guth, L.: “Trophic” influence of nerve on muscle. Physiol. Rev. 48, 645–687 (1968).
Guthrie, D. M.: The regeneration of motor axons in an insect. J. Insect Physiol. 13, 1593–1611 (1967).
Hàmori, J., Horridge, G. A.: The lobster optic lamina. III. Degeneration of retinula cell endings. J. Cell Sci. 1, 271–274 (1966).
Hess, A.: Experimental anatomical studies of pathways in the severed central nerve cord of the cockroach. J. Morph. 103, 479–501 (1958).
— The fine structure of degenerating nerve fibers, their sheaths, and their terminations in the central nerve cord of the cockroach (Periplaneta americana). J. biophys. biochem. Cytol. 7, 339–344 (1960).
Holtzman, E., Freeman, A. R., Kashner, L. A.: A cytochemical and electron microscope study of channels in the Schwann cell surrounding lobster giant axons. J. Cell Biol. 44, 438–445 (1970).
— Novikoff, A. B.: Lysosomes in the rat sciatic nerve following crush. J. Cell Biol. 27, 651–669 (1965).
Hoy, R. R.: Degeneration and regeneration in abdominal flexor motor neurones in the crayfish. J. exp. Zool. 172, 219–232 (1970).
— Bitner, G. D., Kennedy, D.: Regeneration in crustacean motor neurones; evidence for axonal fusion. Science 156, 251–252 (1967).
Jacklet, J. W., Cohen, J. J.: Nerve regeneration: Correlation of electrical, histological, and behavioral events. Science 156, 1640–1643 (1967).
James, D. W., Tresman, R. L.: Synaptic profiles in the outgrowth from chick spinal cord in vitro. Z. Zellforsch. 101, 598–606 (1969).
Karnovsky, M. J.: A formaldehyde-gluteraldehyde fixative of high osmolality for use in electron microscopy. J. Cell Biol. 27, 137 A (1965).
Kruger, T., Maxwell, D. S.: Wallerian degeneration in the optic nerve of a reptile; an electron microscopic study. Amer. J. Anat. 125, 247–270 (1969).
Laatsch, R. H., Cowan, W. M.: Electron microscopic studies of the dentate gyrus of the rat. J. comp. Neurol. 130, 241–262 (1967)
Lamparter, H. E. von, Akert, K., Sandri, C.: Wallersche Degeneration im Zentralnervensystem der Ameise. Elektronenmikroskopische Untersuchungen am Prothorakalganglion von Formica lugubris Zett. Schweiz. Arch. Neurol. Neurochir. Psychiat. 100, 337–354 (1967).
— Localization of primary sensory afferents in the prothoracic ganglion of the wood ant (Formica lugubris Zett.): a combined light and electron microscopic study of secondary degeneration. J. comp. Neurol. 137, 367–376 (1969).
Lampert, P. W.: A comparative electron microscopic study of reactive, degenerating, regenerating and dystrophic axons. J. Neuropath. exp. Neurol. 26, 345–368 (1967).
Lasek, R. J.: Protein transport in neurones. Int. Rev. Neurobiol. 13, 289–324 (1970).
Lee, J. C.: The fine structural alterations of nerve during Wallerian degeneration. J. comp. Neurol. 120, 65–80 (1963).
Lyser, K. M.: Early differentiation of motor neuroblasts in the chick embryo as studied by electron microscopy. II. Microtubules and neurofilaments. Develop. Biol. 17, 117–142 (1968).
May, R. W.: The relation of nerves to degenerating and regenerating taste buds. J. exp. Zool. 42, 371–410 (1925).
Millonig, G.: A modified procedure for lead staining of thin sections. J. biophys. biochem. Cytol. 11, 736–739 (1961).
Nathaniel, E. J. E., Pease, D. C.: Degenerative changes in rat dorsal roots during Wallerian degeneration. J. Ultrastruct. Res. 9, 511–532 (1963).
Nüesch, H.: The role of the nervous system in insect morphogenesis and regeneration. Ann. Rev. Entomol. 13, 27–44 (1968).
Ohmi, S.: Electronmicroscopic study on Wallerian degeneration of the peripheral nerve. Z. Zellforsch. 54, 39–67 (1961).
Pevzner, L. Z.: Topochemical aspects of nucleic acid and protein metabolism within the neuron-neuroglia unit of the superior cervical ganglion. J. Neurochem. 12, 993–1002 (1965).
Rowell, C. H. F., Dorey, A. W.: The number and size of axons in the thoracic connectives of the desert locust Schistocerca gregaria Forsck. Z. Zellforsch. 83, 288–294 (1967).
Singer, M., Green, M.: Autoradiographic studies of the ribonucleic acid in the peripheral nerve of the newt, Triturus. J. Morph. 124, 321–344 (1968).
-- Steinberg, M. C.: Wallerian degeneration: a reevaluation based on transected and colchicine-poisoned nerves in the amphibian, Triturus. Amer. J. Anat. In press, 1972.
Sutherland, R. G., Nunnemacher, R. F.: Microanatomy of crayfish thoracic cord and roots. J. comp. Neurol. 132, 499–518 (1968).
Tennyson, V. M.: The fine structure of the axon and growth cone of the dorsal root neuroblast of the rat embryo. J. Cell Biol. 44, 62–79 (1970).
Usherwood, P. N. R.: Response of insect muscle to denervation. I. Resting potential changes. J. Insect Physiol. 9, 247–255 (1963).
— Cochrane, D. G., Rees, D.: Changes in insect excitatory nerve-muscle synapses after motor nerve section. Nature (Lond.) 218, 589–591 (1968).
Vial, J. D.: The early changes in the axoplasm during Wallerian degeneration. J. biophys. biochem. Cytol. 4, 551–556 (1958).
Webster, H. de F.: Transient, focal accumulation of axonal mitochondria during the early stages of Wallerian degeneration. J. Cell Biol. 12, 361–383 (1962).
Weller, R. O., Herzog, I.: Schwann cell lysosomes in hypertrophy neuropathy and in normal human nerves. Brain 93, 347–356 (1970).
Wiersma, C. A. G.: Reflexes and the central nervous system, p. 191–240. In: The physiology of crustacea, vol. II. (ed. T. H. Watermann) New York: Academic Press, 1960.
Wilson, D. M.: Nervous control of movement in cephalopods. J. exp. Biol. 37, 57–72 (1960).
Zelená, J., Lubińska, L., Gutmann, E.: Accumulation of organelles at the ends of interrupted axons. Z. Zellforsch. 91, 200–219 (1968).
Author information
Authors and Affiliations
Additional information
This work was supported by NIH postdoctoral fellowship number 1F2 NB 32, 723 N RB awarded to RHN and grants in aid from the Multiple Sclerosis Society, The American Cancer Society and The National Institutes of Health.
Rights and permissions
About this article
Cite this article
Nordlander, R.H., Singer, M. Electron microscopy of severed motor fibers in the crayfish. Z. Zellforsch. 126, 157–181 (1972). https://doi.org/10.1007/BF00307214
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00307214