Summary
Neuromuscular junctions, muscle fibers, and intramuscular nerve branches in crayfish opener muscles denervated for periods up to 368 days were examined with the electron microscope. The majority of the denervated muscles responded to stimulation of the isolated distal part of the motor axon with electrical activity and contractions. The neuromuscular junctions and muscle fibers appeared normal in such preparations: synapses and synaptic vesicles were present in the nerve terminals, and the organization of filaments and tubules in the muscle fibers was not distinguishable from that in normal muscles.
In some preparations denervated for a long time, and in others denervated by tying the motor axon close to the muscle, the motor axons showed physiological and morphological evidence of degeneration. Synapses, when present in such preparations, showed few synaptic vesicles, which were often clumped. Muscle fibers showed signs of degeneration. These observations suggest that isolated distal motor axon segments can remain alive for at least a year, retaining normal structure. As long as the motor axon is viable, the muscle remains normal in appearance, but if the axon degenerates, the muscle becomes abnormal. A trophic interdependence between nerve and muscle is probably involved.
Similar content being viewed by others
References
Albuquerque, E. X., Warnick, J. E., Tasse, J. R., Sansome, F. M.: Effects of vinblastine and colchicine on neural regulation of the fast and slow skeletal muscles of the rat. Exp. Neurol. 37, 607–634 (1972)
Atwood, H. L.: Z and T tubules in stomach muscles of the spiny lobster. J. Cell Biol. 50, 264–268 (1971)
Atwood, H. L.: Crustacean muscle, p. 421–489. In: The structure and function of muscle, vol. 1, 2nd ed. (ed. G. H. Bourne). New York: Academic Press 1972
Atwood, H. L., Lang, F., Morin, W. A.: Synaptic vesicles: Selective depletion in crayfish excitatory and inhibitory axons. Science 176, 1353–1355 (1972)
Atwood, H. L., Morin, W. A.: Neuromuscular and axo-axonalsynapses of the crayfish opener muscle. J. Ultrastruct. Res. 32, 351–369 (1970)
Birks, R., Katz, B., Miledi, R.: Physiological and structural changes at the amphibian myoneural junction in the course of nerve degeneration. J. Physiol. (Lond.) 150, 145–168 (1960)
Bittner, G. D.: Degeneration and regeneration in crustacean neuromuscular systems. Amer. Zool. 13, 379–408 (1973a)
Bittner, G. D., Kennedy, D.: Quantitative aspects of transmitter release. J. Cell Biol. 47, 585–592 (1970)
Ceccarelli, B., Hurlbut, W. P., Mauro, A.: Turnover of transmitter and synaptic vesicles at the frog neuromuscular junction. J. Cell Biol. 57, 499–524 (1973)
Guth, L.: “Trophic” influence of nerve on muscle. Physiol. Rev. 48, 645–687 (1968)
Heuser, J. E., Reese, T. S.: Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J. Cell Biol. 57, 315–344 (1973)
Hoy, R. R.: Degeneration and regeneration in abdominal flexor motor neurons in the crayfish. J. exp. Zool. 172, 219–232 (1970)
Hoy, R. R., Bittner, G. D., Kennedy, D.: Regeneration in crustacean motor neurons: Evidence for axonal fusion. Science 156, 1640–1643 (1967)
Lang, F., Atwood, H. L., Morin, W. A.: Innervation and vascular supply of the crayfish opener muscle: Scanning and transmission electron microscopy. Z. Zellforsch. 127, 189–200 (1972)
Miledi, R., Slater, C. R.: Electrophysiology and electron microscopy of rat neuromuscular junctions after nerve degeneration. Proc. roy. Soc. B. 159, 289–306 (1968)
Miledi, R., Slater, C. R.: On the degeneration of rat neuromuscular junctions after nerve section. J. Physiol. (Lond.) 207, 507–528 (1970)
Nordlander, R. H., Singer, M.: Electron microscopy of severed motor fibers in the crayfish. Z. Zellforsch. 126, 157–181 (1972)
Nordlander, R. H., Singer, M.: Effects of temperature on the ultrastructure of severed crayfish motor axons. J. exp. Zool. 184, 289–301 (1973)
Peachey, L. D.: Membrane systems of crab fibers. Amer. Zool. 7, 505–513 (1967)
Peracchia, C., Mittler, B. S.: Fixation by means of glutaraldehyde-hydrogen peroxide reaction products. J. Cell Biol. 53, 234–238 (1972)
Rees, D., Usherwood, P.N.R.: Fine structure of normal and degenerating motor axons and nerve muscle synapses in the locust, Schistocerca gregaria. Comp. Biochem. Physiol. 43A, 83–101 (1972)
Reynolds, E. S.: The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 17, 208–212 (1963)
Author information
Authors and Affiliations
Additional information
This study was supported by grants from the National Research Council of Canada, the Muscular Dystrophy Association of Canada, NIH grant No 5-R01- N508609 and NSF grant No 6B-30199. Ms. Frances Eggleston, Mr. Martis Ballinger, and Ms. Irene Kwan provided technical assistance. We thank Dr. Thomas Hamilton for his critical reading of the manuscript.
Rights and permissions
About this article
Cite this article
Atwood, H.L., Govind, C.K. & Bittner, G.D. Ultrastructure of nerve terminals and muscle fibers in denervated crayfish muscle. Z.Zellforsch 146, 155–165 (1973). https://doi.org/10.1007/BF00307344
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00307344