Skip to main content
Log in

Effect of nerve length and temperature on the induction of action potentials in denervated slow muscle fibres of the frog

  • Excitable Tissues and Central Nervous Physiology
  • Published:
Pflügers Archiv Aims and scope Submit manuscript

Summary

  1. A.

    Pyriformis and extensor longus digiti IV muscles of Rana temporaria were denervated by cutting the sciatic or peroneal nerve at various distances from the muscles. Slow fibres were identified by their membrane time constants, and examined for their ability to produce action potentials in response to intracellularly applied current pulses.

  2. B.

    The slow muscle fibres acquired the ability to generate action potentials several days after denervation. The duration of this latent period depended on the length of the peripheral nerve stump, and on the temperature at which the frogs were kept after the operation.

  3. C.

    At 18°C the latent period increased by 0.36 days per mm of sciatic nerve stump. At 11.5° C the corresponding value was 0.7 days/mm. The effect of length of the peroneal nerve was smaller than that of the sciatic nerve.

  4. D.

    It is suggested that the peripheral nerve stump serves as a reservoir of ‘trophic’ material which is transported towards the slow fibres at a rate of 2.8 mm/day (at 18° C) and seems to block the formation of Na channels. TheQ 10 value of this transport system would be 2.7.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Albuquerque, E. X., Schuh, F. T., Kauffman, F. C.: Early membrane depolarisation of the fast mammalian muscle after denervation. Pflügers Arch.328, 36–50 (1971)

    Google Scholar 

  • 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)

    Google Scholar 

  • Burke, W., Ginsborg, B. L.: The electrical properties of the slow muscle fibre membrane. J. Physiol. (Lond.)132, 586–598 (1956)

    Google Scholar 

  • Cangiano, A., Lutzemberger, L.: Partial denervation affects both denervated and innervated fibers in the mammalian skeletal muscle. Science196, 542–545 (1977)

    Google Scholar 

  • Edström, A., Hanson, M.: Temperature effects on fast axonal transport of proteins in vitro in frog sciatic nerves. Brain Res.58, 345–354 (1973)

    Google Scholar 

  • Emmelin, N., Malm, L.: Development of supersensitivity as dependent on the length of degenerating nerve fibres. Quart. J. Exp. Physiol.50, 142–145 (1965)

    Google Scholar 

  • Epstein, R., Bekerman, A. J.: Development of denervatory action potentials in slow muscle fibres of the toad and its trophic dependence. In: Electrobiology of nerve, synapse and muscle (J. P. Reuben, D. P. Pupura, M. V. L. Bennet, and E. R. Kandel, eds.). New York: Raven Press 1976

    Google Scholar 

  • Fernandez, H. L., Davison, P. F.: Axoplasmic transport in the crayfish nerve cord. Proc. Natl. Acad. Sci. U.S.A.64, 512–519 (1969)

    Google Scholar 

  • Grafstein, B., Forman, D. S., McEwen, B. S.: Effects of temperature on axonal transport and turnover of protein in goldfish optic system. Exp. Neurol.34, 158–170 (1972)

    Google Scholar 

  • Gross, G. W.: The effect of temperature on the rapid axoplasmic transport in C-fibres. Brain Res.56, 359–363 (1973)

    Google Scholar 

  • Guth, L.: ‘Trophic’ influences of nerve on muscle. Physiol. Rev.48, 645–687 (1969)

    Google Scholar 

  • Gutmann, E., Vodička, Z., Zelená, J.: Changes in cross striated muscle after nerve interruption depending on the length of the nerve stump. Physiol. Bohemoslov4, 200–204 (1955)

    Google Scholar 

  • Häggendal, C. J., Dahlström, A. B., Saunders, N. R.: Axonal transport and acetylcholine in rat preganglionic neurones. Brain Res.58, 494–499 (1973)

    Google Scholar 

  • Harris, J. B., Thesleff, S.: Relation of nerve stump length to membrane changes in skeletal muscle. Nature236, 60–61 (1972)

    Google Scholar 

  • Heslop, J. P., Howes, E. A.: Temperature and inhibitor effects on fast axonal transport in a molluscan nerve. J. Neurochem.19, 1709–1716 (1972)

    Google Scholar 

  • Jones, R., Vrbová, G.: Effect of muscle activity on denervation hypersensitivity. J. Physiol. (Lond.)210, 144–145 (1970)

    Google Scholar 

  • Jones, R., Vrbová, G.: Two factors responsible for the development of denervation hypersensitivity. J. Physiol. (Lond.)236, 517–538 (1974)

    Google Scholar 

  • Kuffler, S. W., Vaughan-Williams, E. M.: Small-nerve junctional potentials. The distribution of small motor nerves to frog skeletal muscle, and the membrane characteristics of the fibres they innervate. J. Physiol. (Lond.)121, 289–317 (1953

    Google Scholar 

  • Lømo, T., Rosenthal, J.: Control of ACh sensitivity by muscle activity in the rat. J. Physiol. (Lond.)221 493–513 (1972)

    Google Scholar 

  • Lømo, T., Westgaard, R. H.: Further studies on the control of ACh sensitivity by muscle activity in the rat. J. Physiol. (Lond.)252, 603–626 (1975)

    Google Scholar 

  • Lubínska, L., Niemierko, S., Oderfeld-Novak, B., Swarć, L.: Behaviour of acetylcholineesterase in isolated nerve segments. J. Neurochem.11, 493–504 (1964)

    Google Scholar 

  • Luco, J. V., Eyzaguirre, C.: Fibrillation and hypersensitivity to ACh in denervated muscle: Effect of length of degenerating nerve fibres. J. Neurophysiol.18, 65–73 (1955)

    Google Scholar 

  • Miledi, R., Slater, C. R.: On the degeneration of rat neuromuscular junctions after nerve section. J. Physiol. (Lond.)207, 507–528 (1970)

    Google Scholar 

  • Miledi, R., Stefani, E., Steinbach, A. B.: Induction of the action potential mechanism in slow muscle fibres of the frog. J. Physiol. (Lond.)217, 737–754 (1971)

    Google Scholar 

  • Naslcdov, G. A., Thesleff, S.: Denervation changes in frog skeletal muscle. Acta Physiol. Scand.90, 370–380 (1974)

    Google Scholar 

  • Ochs, S., Ranish, N.: Characteristics of the fast transport system in mammalian nerve fibres. J. Neurobiol.1, 247–261 (1969)

    Google Scholar 

  • Ochs, S., Hollingsworth, D.: Dependence of fast axoplasmic transport in nerve on oxidative metabolism. J. Neurochem.18, 107–114 (1971)

    Google Scholar 

  • Ochs, S., Smith, C.: Effect of temperature and rate of stimulation on fast axoplasmic transport in mammalian nerve fibres. Fed. Proc.30, 665 (1971)

    Google Scholar 

  • Partlow, L. M., Ross, C. D., Motwani, R., McDougal, D. B., Jr.: Transport of axonal enzymes in surviving segments of frog sciatic nerve. J. Gen. Physiol.60, 388–405 (1972)

    Google Scholar 

  • Schalow, G., Schmidt, H.: Action potentials induced in slow muscle fibres by partial denervation. Nature253, 122–123 (1975a)

    Google Scholar 

  • Schalow, G., Schmidt, H.: Effect of temperature and length of nerve stump on development of action potentials in denervated frog slow muscle fibres. Pflügers Arch.355, R51 (1975b)

    Google Scholar 

  • Schmidt, H., Tong, E. Y.: Inhibition by actinomycin D of the denervation induced action potential in frog slow muscle fibres. Proc. R. Soc. Lond. [Biol.]184, 91–95 (1973)

    Google Scholar 

  • Schmidt, H., Schalow, G.: Local development of action potentials in denervated slow muscle fibres. Pflügers Arch.359, R131 (1975)

    Google Scholar 

  • Schmidt, H., Stefani, E.: Re-innervation of twitch and slow muscle fibres of the frog after crushing the motor nerves. J. Physiol. (Lond.)258, 99–123 (1976)

    Google Scholar 

  • Schmidt, H., Stefani, E.: Action potentials in slow muscle fibres of the frog during regeneration of motor nerves. J. Physiol. (Lond.)270, 507–517 (1977)

    Google Scholar 

  • Slater, C. R.: Time course of failure of neuromuscular transmission after motor nerve section. Nature209, 305–306 (1966)

    Google Scholar 

  • Stefani, E., Steinbach, A. B.: Resting potential and electrical properties of frog slow muscle fibres. Effect of different external solutions. J. Physiol. (Lond.)203, 383–401 (1969)

    Google Scholar 

  • Stefani, E., Schmidt, H.: Early stage of re-innervation of frog slow muscle fibres. Pflügers Arch.336, 271–275 (1972a)

    Google Scholar 

  • Stefani, E., Schmidt, H.: A convenient method for repeated intracellular recording of action potentials from the same muscle fibre without membrane damage. Pflügers Arch.334, 276–278 (1972b)

    Google Scholar 

  • Stefani, E., Schmidt, H.: A ‘trophic’ nerve influence independent of neuromuscular transmission: inhibition of action potential in denervated frog slow fibres. Pflügers Arch.335, R64 (1972c)

    Google Scholar 

  • Uchitel, O.: Development of supersensitivity in denervated slow muscle of the frog. Its dependence on the nerve stump length. Acta Physiol. Lat.-Am.25, 462–466 (1975)

    Google Scholar 

  • Weiss, P.: The concept of perpetual growth and proximo-distal substance convection. In: Regional neurochemistry (Katz, S. S., Elkes, J., ed.), pp. 220–242. Oxford: Pergamon Press 1961

    Google Scholar 

  • Weiss, P.: Self-renewal and proximo-distal convection in nerve fibres. In: The effect of use and disuse on neuromuscular functions (Gutmann, E., Hník, P., eds.) pp. 171–183. Amsterdam: Elsevier 1963)

    Google Scholar 

  • Weiss, P., Holland, Y.: Neuronal dynamics and axonal flow. II. The olfactory nerve as model test object. Proc. Natl. Acad. Sci. U.S.A.57, 258–264 (1967)

    Google Scholar 

  • Wooten, G. F., Saavedra, J. M.: Axonal transport of phenylethanolamine-N-methyltransferase in toad sciatic nerve. J. Neurochem.22, 1059–1064 (1974)

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Supported by Deutsche Forschungsgemeinschaft, SFB 38-’Membranforschung’, Bonn-Bad Godesberg

Rights and permissions

Reprints and permissions

About this article

Cite this article

Schalow, G., Schmidt, H. Effect of nerve length and temperature on the induction of action potentials in denervated slow muscle fibres of the frog. Pflugers Arch. 372, 17–22 (1977). https://doi.org/10.1007/BF00582201

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00582201

Key words

Navigation