Skip to main content
Log in

Intramembrane particles and responses of sensory axon terminals during reinnervation of the frog muscle spindle

  • Published:
Journal of Neurocytology

Summary

Changes in the density of intramembrane particles (IMPs) of sensory nerve terminals in the bullfrog muscle spindle were correlated with recovery in the response of the spindle to stretch during postcrush reinnervation. A few IMPs on the protoplasmic (P) face in summer experiments (June to October) reappeared by the 3rd week after the nerve crush, then rapidly increased to 110% and 120% of control values 2 and 2.5 months after the crush. Afferent responses to stretch could be recorded after the mean IMP density on the P-face in terminal branches had recovered to more than 25% of the control value. The discharge rate showed a plateau pattern during the period of the excessive IMPs. This was supplanted by a normal pattern after a myelinated branch of the sensory axon was cut. The IMPs in winter experiments (November to April) reappeared by day 90 after nerve crush, and then slowly increased. The sustained responses to stretch reappeared after 5 months, when the mean IMP density on the P-face was restored to 25% or more of the control. Neither excessive density of the IMPs nor plateau pattern of the discharge rate were observed in winter experiments. The relation between the regenerated IMP densities and the functional recovery is discussed.

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

  • Banks, R. W. &Barker, D. (1989) Specificities of afferents reinnerva ting cat muscle spindles after nerve section.Journal of Physiology 408, 345–72.

    PubMed  Google Scholar 

  • Barker, D. &Boddy, A. (1980) Reinnervation of stretch receptors in cat muscle after nerve crush. InOntogenesis and Functional Mechanisms of Peripheral Synapses (edited byTaxi, J.) pp. 251–63. Amsterdam: Elsevier.

    Google Scholar 

  • Barker, D., Scott, J. J. A. &Stagey, M. J. (1985) Sensory reinnervation of cat peroneus brevis muscle spindles after nerve crush.Brain Research 333, 131–8.

    PubMed  Google Scholar 

  • Black, J. A., Foster,- R. E. &Waxman, S. G. (1981) Freeze-fracture ultrastructure of rate CNS and PNS non-myelinated axolemma.Journal of Neurocytology 10, 981–93.

    PubMed  Google Scholar 

  • Boyd, I. A., Murphy, P. R. &Mann, C. (1985) The effect of chain fibre ‘driving’ on the length sensitivity of primary sensory endings in the tenuissimus, peroneus tertius and soleus muscles. InThe Muscle Spindle (edited byBoyd, I. A. &Gladden, M. H.) pp. 195–9. London: Macmillan.

    Google Scholar 

  • Brown, M. C. &Butler, R. G. (1976) Regeneration of afferent and efferent fibres to muscle spindles after nerve crush injury in adult cats.Journal of Physiology 260, 253–66.

    PubMed  Google Scholar 

  • Diwan, F. H. &Ito, F. (1989) Intrafusal muscle fibre types in frog spindles.Journal of Anatomy 163, 191–200.

    PubMed  Google Scholar 

  • Fuiitsuka, N., Kama, K., Ito, F. &Sokabe, M. (1987) Intramembrane particles and terminal responses following denervation of frog muscle spindles.Journal of Neurocytology 16, 185–94.

    PubMed  Google Scholar 

  • Gabriel, G., Thomas, P. K., King, R. H. M., Stolinski, C. &Breathnach, A. S. (1986) Freeze-fracture observations on human peripheral nerve.Journal of Anatomy 146, 153–66.

    PubMed  Google Scholar 

  • Gregory, J. E., Luff, A. R. &Proske, U. (1982) Muscle receptors in the cross-reinnervated soleus muscle of the cat.Journal of Physiology 331, 367–83.

    PubMed  Google Scholar 

  • Hyde, D. &Scott, J. J. A. (1983) Responses of cat peroneus brevis muscle spindle afferents during recovery from nerve-crush injury.Journal of Neurophysiology 50, 344–57.

    PubMed  Google Scholar 

  • Ip, M. C., Vrbová, G. &Westbury, D. R. (1977) The sensory reinnervation of hindlimb muscles of the cat following denervation and de-efferentation.Neuroscience 2, 423–34.

    PubMed  Google Scholar 

  • Ito, F. (1968a) Functional properties of tendon receptors in the frog.Japanese Journal of Physiology 18, 576–89.

    PubMed  Google Scholar 

  • Ito, F. (1968b) Functional properties of leaf-like receptors in the frog sartorius muscle.Japanese Journal of Physiology 18, 590–600.

    PubMed  Google Scholar 

  • Ito, F., Fujitsuka, N., Funahashi, A. &Hama, K. (1985a) Ionic channels in the sensory terminal of the frog muscle spindle. InThe Muscle Spindle (edited byBoyd, I. A. &Gladden, M. H.) pp. 353–8. London: Macmillan.

    Google Scholar 

  • Ito, F., Fujitsuka, N. &Fan, X. L. (1985b) Reversal of the static component of spindle potential by imposed depolarizing current in the frog muscle spindle.Brain Research 326, 107–16.

    PubMed  Google Scholar 

  • Ito, F. &Komatsu, Y. (1977) Frog muscle spindles with unbranched myelinated afferent axons: the response to stretch and the length of the first myelinated segment.Journal of Physiology 264, 881–91.

    PubMed  Google Scholar 

  • Katz, B. (1961) The terminations of the afferent nerve fibre in the muscle spindle of the frog.Philosophical Transactions of the Royal Society of London B 243, 221–40.

    Google Scholar 

  • Kim, N., Fujitsuka, N. &Ito, F. (1985) Ultrastructural changes of the sensory nerve terminals in frog muscle spindle during dynamic stretch.Journal of Neurocytology 14, 105–12.

    PubMed  Google Scholar 

  • Miledi, R., Stefani, E. &Steinback, A. B. (1971) Induction of the action potential mechanism in slow muscle fibres of the frog.Journal of Physiology 217, 737–54.

    PubMed  Google Scholar 

  • Morgan, D. L. &Proske, U. (1984) Vertebrate slow muscle: its structure, pattern of innervation and mechanical properties.Physiological Reviews 64, 103–69.

    PubMed  Google Scholar 

  • Schalow, G. &Schmidt, H. (1975) Action potential induced in slow muscle fibres by partial denervation.Nature 253, 122–3.

    PubMed  Google Scholar 

  • Schmidt, H. &Stefani, E. (1977) Action potentials in slow muscle fibres of the frog during regeneration of motor nerves.Journal of Physiology 270, 507–17.

    PubMed  Google Scholar 

  • Schnapp, B. &Mugnaini, E. (1978) Membrane architecture of myelinated fibres as seen by freeze-fracture. InPhysiology and Pathobiology of Axons (edited byWaxman, S. G.) pp. 83–123. New York: Raven Press.

    Google Scholar 

  • Schröder, J. M. (1974) The fine structure of de- and reinnervated muscle spindles. II. Regenerated sensory and motor nerve terminals.Acta Neuropathologica 30, 129–44.

    PubMed  Google Scholar 

  • Scott, J. J. A. (1983) Some properties of cat peroneus brevis muscle spindles reinnervated after short periods of denervation.Journal of Physiology 345, 55.

    Google Scholar 

  • Scott, J. J. A. (1985) Regeneration of gamma-fusimolor axons after nerve freeze injury in the cat.Brain Research 348, 159–62.

    PubMed  Google Scholar 

  • Small, R. K. &Pfenninger, K. H. (1984) Components of the plasma membrane of growing axons. I. Size and distribution of intra-membrane particles.Journal of Cell Biology 98, 1422–33.

    PubMed  Google Scholar 

  • Stefani, E. &Schmidt, H. (1972) Early stage of reinnervation of frog slow muscle fibres.Pflügers Archivs 336, 271–5.

    Google Scholar 

  • Stolinski, C., Breathnack, A. S., Martin, B., Thomas, P. K., King, R. H. M. &Gabriel, G. (1981) Associated particle aggregates in juxtaparanodal axolemma and axonal Schwann cell membrane of rat peripheral nerve.Journal of Neurocytology 10, 679–91.

    PubMed  Google Scholar 

  • Tao-Cheng, J.-H., Hirosawa, K., Nakajima, Y. &Peng, J. B. (1981) Freeze-fracture study of the crayfish stretch receptor.Journal of Comparative Neurology 200, 23–38.

    PubMed  Google Scholar 

  • Zelenä, J. &Hnik, P. (1963) Effect of innervation on the development of muscle receptors. InThe Effect of Use and Disuse on Neuromuscular Functions (edited byGutmann, E. &Hnik, P.) pp. 95–109. Amsterdam: Elsevier.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fujitsuka, C., Fujitsuka, N., Diwan, F.H. et al. Intramembrane particles and responses of sensory axon terminals during reinnervation of the frog muscle spindle. J Neurocytol 19, 175–186 (1990). https://doi.org/10.1007/BF01217296

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01217296

Keywords

Navigation