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Sprouting and regression of the nerve at the frog neuromuscular junction in normal conditions and after prolonged paralysis with curare

  • Published:
Journal of Neurocytology

Summary

A light microscopical, histochemical and electron microscopical investigation of the frog neuromuscular junction has been performed on muscles from animals in different functional states of activity.

The combined staining of axon terminals and cholinesterase (ChE) allows a precise description of the nerve terminal arborization and its synaptic contacts. Most terminal arborizations form long continuous contacts with the muscle cell. Distinguishable from these are nerve branches (usually of small diameter) or distal endings of branches with one or several small and isolated contacts. It is assumed that these are sprouts with newly-formed synaptic sites. Other sprouts end without apparent synaptic contact. At the ultrastructural level, nerve sprouts growing into empty, well-differentiated synaptic gutters or inducing the formation of new synaptic sites were observed.

In other sites, ChE is apparently located at postsynaptic gutters with no nerve present. Similarly, in the electron microscope, well-differentiated synaptic gutters lacking any nerve or Schwann cell elements were observed. In addition, synaptic gutters only partially occupied by the nerve were frequently seen. These features have been interpreted as signs of regression of the nerve terminals.

Nerve regression and sprouting were found in animals chronically paralysed with curare over several weeks as well as in untreated frogs (winter and summer frogs, laboratory frogs, fed and unfed). When quantitatively evaluating the occurrence of presumed features of nerve sprouting and nerve regression, differences were found between different experimental groups. From this it is concluded that, in addition to developmental changes, the degree of nerve sprouting and regression is controlled by external factors such as muscle activity and seasonal variations.

Signs of sprouting and nerve regression can be simultaneously present in a single synapse. It appears that the frog neuromuscular synapse is not a static structure, but is in a state of permanent remodelling.

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References

  • Barker, D. &Ip, M. C. (1966) Sprouting and degeneration of mammalian motor axons in normal and deafferentated skeletal muscle.Proceedings of the Royal Society of London, Series B 163, 538–54.

    Google Scholar 

  • Berg, D. K. &Hall, Z. W. (1975) Increased extrajunctional acetylcholine sensitivity produced by chronic post-synaptic neuromuscular blockade.Journal of Physiology 244, 659–76.

    PubMed  Google Scholar 

  • Birks, R., Huxley, H. E. &Ratz, B. (1960) The fine structure of the neuromuscular junction of the frog.Journal of Physiology 150, 134–44.

    PubMed  Google Scholar 

  • Birks, R., Katz, B. &Miledi, R. (1959) Dissociation of the ‘surface membrane complex’ in atrophic muscle fibres.Nature 184, 1507–8.

    PubMed  Google Scholar 

  • Birks, R., Katz, B. &Miledi, R. (1960) Physiological and structural changes at the amphibian myoneural junction in the course of nerve degeneration.Journal of Physiology 150, 145–68.

    PubMed  Google Scholar 

  • Bodian, D. (1936) A new method for staining nerve fibres and nerve endings in mounted paraffin sections.Anatomical Record 65, 89–97.

    Google Scholar 

  • Bowden, R. E. M. &Ducken, L. W. (1976) The anatomy and pathology of the neuromuscular junction.In Neuromuscular Junction (edited byZaimis, E.), pp. 23–29. Berlin, Heidelberg, New York: Springer-Verlag.

    Google Scholar 

  • Brown, M. C., Goodwin, G. M. &Ironton, R. (1977) Prevention of motor nerve sprouting in botulinum toxin poisoned mouse soleus muscles by direct stimulation of the muscle.Journal of Physiology 267, 42–3P.

    Google Scholar 

  • Brown, M. C. &Ironton, R. (1977a) Motor neuron sprouting induced by prolonged tetrodotoxin block of nerve action potentials.Nature 265, 459–61.

    PubMed  Google Scholar 

  • Brown, M. C. &Ironton, R. (1977b) Suppression of motor nerve terminal sprouting in partially denervated mouse muscles,Journal of Physiology 272, 70–1P.

    Google Scholar 

  • Brown, M. C. &Ironton, R. (1978) Sprouting and regression of neuromuscular synapses in partially denervated mammalian muscles.Journal of Physiology 278, 325–48.

    PubMed  Google Scholar 

  • Cohen, M. W. (1972) The development of neuromuscular connexions in the presence of d-tubocurarine.Brain Research 41, 457–63.

    PubMed  Google Scholar 

  • Couteaux, R. (1960) Motor end-plate structure. InStructure and Function of Muscle (edited byBourne, G. H.), pp. 337–380. New York: Academic Press.

    Google Scholar 

  • Couteaux, R. (1975) Facteurs de la différenciation des ‘zones actives’ des membranes présynaptiques.Comptes rendus des Séances de l'Académie des Sciences (D) 280, 299–301.

    Google Scholar 

  • Couteaux, R. &Pécot-Dechavassine, M. (1968) Particularités structurales du sarcoplasme sous-neural.Comptes rendus des Séances de l'Académie des Sciences (D) 266, 8–10.

    Google Scholar 

  • Crain, S. M. &Peterson, E. M. (1971) Development of paired explants of foetal spinal cord and adult skeletal muscle during chronic exposure to curare and hemicholinium.In vitro 6, 373–81.

    Google Scholar 

  • Duchen, L. W. (1970) Changes in motor innervation and cholinesterase localization induced by botulinum toxin in skeletal muscle of the mouse: differences between fast and slow muscles.Journal' of Neurology, Neurosurgery and Psychiatry 33, 40–54.

    Google Scholar 

  • Duchen, L. W. (1971) An electron microscopic study of the changes induced by botulinum toxin in the motor end-plates of slow and fast skeletal muscle fibres of the mouse.Journal of the Neurological Sciences 14, 47–60.

    PubMed  Google Scholar 

  • Duchen, L. W. &Strich, S. J. (1968) The effects of botulinum toxin on the pattern of innervation of skeletal muscle in the mouse.Quarterly Journal of Experimental Physiology 53, 84–9.

    Google Scholar 

  • Duchen, L. W. &Tonge, D. A. (1973) The effects of tetanus toxin on neuromuscular transmission and on the morphology of motor endplates in slow and fast skeletal muscle of the mouse.Journal of Physiology 228, 157–72.

    PubMed  Google Scholar 

  • Edds, M. V. (1953) Collateral nerve regeneration.Quarterly Review of Biology 28, 260–76.

    PubMed  Google Scholar 

  • Freeman, S. S., Engel, A. G. &Drachman, D. B. (1976) Experimental acetylcholine blockade of the neuromuscular junction. Effects on end-plate and muscle fibre ultrastructure.Annals of the New York Academy of Sciences 266, 46–59.

    Google Scholar 

  • Haimann, C., Mallart, A. &Zilber-Gachelin, N. F. (1976) Competition between motor nerves in the establishment of neuromuscular junctions in striated muscles ofXenopus laevis.Neuroscience Letters 2, 15–20.

    Google Scholar 

  • Ip, M. C. (1974) Some morphological features of the myoneural junction in certain normal muscles of the rat.Anatomical Record 180, 605–16.

    PubMed  Google Scholar 

  • Karnovsky, M. J. &Roots, L. (1964) A ‘direct-coloring’ thiocholine method for cholinesterases.Journal of Histochemistry and Cytochemistry 12, 219–21.

    PubMed  Google Scholar 

  • Landmesser, L. (1972) Pharmacological properties, cholinesterase activity and anatomy of nerve-muscle junctions in vagus-innervated frog sartorius.Journal of Physiology 220, 243–56.

    PubMed  Google Scholar 

  • Letinsky, M. S., Fischbeck, K. H. &McMahan, U. J. (1976) Precision of reinnervation of original postsynaptic sites in frog muscle after a nerve crush.Journal of Neurocytology 5, 691–718.

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Lømo, T. &Slater, C. R. (1976) Control of neuromuscular formation. InGif Lectures in Neurobiology on ‘Synaptogenesis’ (edited byTauc, L.), pp. 9–30. Jouy en Josas.

  • Lømo, T. &Slater, C. R. (1978) Control of acetylcholine sensitivity and synapse formation by muscle activity.Journal of Physiology 275, 391–402.

    PubMed  Google Scholar 

  • Müller, H. K. (1976) The frog as an experimental animal. InFrog Neurobiology (edited byLlinas, R. andPrecht, W.), pp. 1023–1039. Berlin, Heidelberg, New York: Springer-Verlag.

    Google Scholar 

  • Pécot-Dechavassine, M. (1968) Evolution de l'activité des cholinestérases et de leur capacité fonctionnelle au niveau des jonctions neuromusculaires et musculotendineuses de la grenouille après section du nerf moteur.Archives internationales de Pharmacodynamie et de Therapie 176, 118–33.

    PubMed  Google Scholar 

  • Pécot-Dechavassine, M. &Wernig, A. (1978) The effect of longtime treatment with curare on the frog neuromuscular synapse.Neuroscience Letters Suppl.1, S39.

    Google Scholar 

  • Pécot-Dechavassine, M., Wernig, A. &Stöver, H. (1979) A combined silver and cholinesterase method for studying exact relations between the pre- and postsynaptic elements at the frog neuromuscular junction.Stain Technology 54, 25–8.

    PubMed  Google Scholar 

  • Pestronk, A. &Drachman, D. B. (1978) Motor nerve sprouting and acetylcholine receptors.Science 199, 1223–5.

    PubMed  Google Scholar 

  • Srihari, T. &Vrbová, G. (1978) The role of muscle activity in the differentiation of neuromuscular junctions in slow and fast chick muscles.Journal of Neurocytology 7, 529–40.

    PubMed  Google Scholar 

  • Thompson, W. (1978) Reinnervation of partially denervated rat soleus muscle.Acta physiologica scandinavica 103, 81–91.

    PubMed  Google Scholar 

  • Tuffery, A. R. (1971) Growth and degeneration of motor end-plates in normal cat hind limb muscles.Journal of Anatomy 110, 221–47.

    PubMed  Google Scholar 

  • Verma, V. (1977)Modifications ultrastructurales et physiologiques de la jonction neuromusculaire après section du nerf moteur. Thèse d'Université. Paris.

    Google Scholar 

  • Verma, V. &Pécot-Dechavassine, M. (1977) A comparative study of physiological and structural changes at the myoneural junction in two species of frog after transection of the motor nerve.Cell and Tissue Research 185, 451–64.

    PubMed  Google Scholar 

  • Watson, W. E. (1969) The response of motoneurones to intramuscular injections of botulinum toxin.Journal of Physiology 202, 611–30.

    PubMed  Google Scholar 

  • Wernig, A. &Stover, H. (1977) Extrajunctional ACh receptors and the formation of foreign nerve synapses after curare and botulinum toxin.Pflügers Archiv Suppl.368, R32.

    Google Scholar 

  • Wernig, A. &Stöver, H. (1979) Sprouting and regression of the nerve at the neuromuscular junction.Pflügers Archiv Suppl.379, R38.

    Google Scholar 

  • Young, J. Z. (1952) Growth and plasticity in the nervous system.Proceedings of the Royal Society of London, Series B 139, 18–37.

    Google Scholar 

Download references

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Authors and Affiliations

  1. Max-Planck-Institut für Psychiatrie, Kraepelinstraβe 2, 8000, München 40, West Germany

    A. Wernig & H. Stöver

  2. Equipe de Recherche du CNRS No. 160, Laboratoire de Cytologie, Université Pierre et Marie Curie, 7, Quai St. Bernard, Paris, France

    M. Pécot-Dechavassine

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  1. A. Wernig
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  2. M. Pécot-Dechavassine
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  3. H. Stöver
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Wernig, A., Pécot-Dechavassine, M. & Stöver, H. Sprouting and regression of the nerve at the frog neuromuscular junction in normal conditions and after prolonged paralysis with curare. J Neurocytol 9, 277–303 (1980). https://doi.org/10.1007/BF01181538

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  • DOI: https://doi.org/10.1007/BF01181538

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