Evidence for Transdifferentiation of Alpha Motoneuron Terminals during Reinnervation of Muscle Spindles

  • Richard Butler


It is quite clear that during synaptogenesis, the transformation of growing axons into specialized nerve terminals is largely regulated by their synaptic targets. This is especially true for vertebrate neuromuscular junctions where evidence points to local control of peripheral axon terminal differentiation by the target’s basal lamina. Such dynamic influence by the target apparently exists in mature adult tissue as well. For example, the results earlier experiments on cat muscle indicate that sometimes single regenerating alpha motoneurons can reinnervate two different types of intrafusal muscle fibers simultaneously (slow twitch and fast twitch) with focal plates and ‘en grappe’ terminals occurring on different branches of the same motoneuron, simultaneously. This led to the converse series of experiments (using rats) in which motoneurons were left intact while their targets were made to degenerate and subsequently allowed to regenerate around the axons. By transplanting a very different target (slow tonic extraocular eye muscle) into the normal regenerating leg muscle target, the intact neurons and their terminals have the option to innervate this very different target as well and my observations indicate that they do. The results also suggest that some existing plate terminals are modified to multiple ‘en grappe’ terminals on the transplanted target, thus providing evidence for the continuing dynamic influence of targets on adult neuromuscular junctions. However, the stability of the new junctions over time is unknown.


Muscle Spindle Motor Endplate Alpha Motoneuron Synaptic Target Intact Neuron 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Bennett, M.R., Pettigrew, A.G., and Taylor, R.S., 1973, The formation of synapses in reinnervated and cross-reinnervated adult avian muscle, J. Physiol., 230, 331–357.PubMedGoogle Scholar
  2. Benoit, P.W., and Belt, W.D., 1970, Destruction and regeneration of skeletal muscle after treatment with a local anaesthetic, bupivacaine (Marcaine), J, Anat., 107, 547–556.Google Scholar
  3. Brown, M.C., and Butler, R.G., 1976, Regeneration of afferent and efferent fibres to muscle spindles after nerve injury in adult cats, J. Physiol., 260, 253–266.PubMedGoogle Scholar
  4. Buller, A.J., Eccles, J.C., and Eccles, R.M., 1960, Interactions between motoneurons and muscles in respect of the characteristic speeds of their responses, J. Physiol., 150, 417–439.PubMedGoogle Scholar
  5. Butler, R., 1980, Can a regenerating alpha motoneuron innervate two different types of intrafusal muscle fibre simultaneously?, Neurosci. Abst., 6: 92.Google Scholar
  6. Butler, R., 1985a, Evidence for the continuing role of targets in controlling motoneuron terminals in adult mammals, Neurosci. Abst., 11: 1102.Google Scholar
  7. Butler, R., 1985b, Plasticity of regenerating and intact alpha motoneuron terminals, Proc. Can. Fed. Biol. Sci., 28: 143.Google Scholar
  8. Butler, R., 1986, Motoneuron-target interactions during regeneration, Abst. for “The Current Status of Peripheral Nerve Regeneration”, a satellite symposium to XXX IUPS Congress, Edmonton, July 1986.Google Scholar
  9. Carlson, B.M., 1972, “The Regeneration of Minced Muscles”, Karger, Basel, Switzerland.Google Scholar
  10. Carlson, B.M., 1976, A quantitative study of muscle fiber survival and regeneration in normal, predenervated, and Marcaine-treated free muscle grafts in the rat, Exp. Neurol., 52, 421–432.PubMedCrossRefGoogle Scholar
  11. Glicksman, M.A., and Sanes, J.R., 1983, Differentiation of motor nerve terminals formed in the absence of muscle fibres, J. Neurocytol., 12, 661–671.PubMedCrossRefGoogle Scholar
  12. Hall-Craggs, E.C.B., 1974, Rapid degeneration and regeneration of a whole skeletal muscle following treatment with bupivacaine (Marcain), Exp. Neurol., 43, 349–358.PubMedCrossRefGoogle Scholar
  13. Hall-Craggs, E.C.B., 1980, Early ultrastructural changes in skeletal muscle exposed to the local anaesthetic bupivacaine (Marcaine), Br. J. exp. Path., 61, 139–149.Google Scholar
  14. Hall-Craggs, E.C.B., and Seyan, H.S., 1975, Histochemical changes in innervated and denervated skeletal muscle fibers following treatment with bupivacaine (Marcain), Exp. Neurol., 46, 345–354.PubMedCrossRefGoogle Scholar
  15. Huang, C.L.-H., and Keynes, R.J., 1983, Terminal sprouting of mouse motor nerves when the post-synaptic membrane degenerates, Brain Res., 274, 225–229.PubMedCrossRefGoogle Scholar
  16. Jirmanova, I., 1975, Ultrastructure of motor endplates during pharmacologically induced degeneration and subsequent regeneration of skeletal muscle, J. Neurocytol., 4, 141–155.PubMedCrossRefGoogle Scholar
  17. Jirmanova, I., and Thesleff, S., 1972, Ultrastructural study of experimental muscle degeneration and regeneration in the adult rat, Z. Zellforsch., 131, 77–97.PubMedCrossRefGoogle Scholar
  18. Libelius, R., Sonneson, B., Stamenovic, B.A., and Thesleff, S., 1970, Denervation-like changes in skeletal muscle after treatment with a local anaesthetic (Marcaine), J. Anat., 106, 297–309.PubMedGoogle Scholar
  19. Mayr, R., 1971, Structure and distribution of fibre types in the external eye muscles of the rat, Tissue & Cell, 3, 433–462.CrossRefGoogle Scholar
  20. McMahan, U.J., Edgington, D.R., and Kuffler, D.P., 1980, Factors that influence regeneration of the neuromuscular junction, J. exp. Biol., 89, 31–42.PubMedGoogle Scholar
  21. Milburn, A., 1976, The effect of the local anaesthetic bupivacaine on the muscle spindle of the rat, J. Neurocytol., 5, 425–446.PubMedCrossRefGoogle Scholar
  22. Purves, D., 1975, Functional and structural changes in mammalian neurones following interruption of their axons, J. Physiol., 252, 429–463.PubMedGoogle Scholar
  23. Purves, D., and Lichtman, J.W., 1985, Principles of Neural Development, Sinauer Associates Inc., Sunderland, Mass.Google Scholar
  24. Rees, R.P., 1978, The morphology of interneuronal synaptogenesis — a review, Fed. Proc., 37, 2000–2004.PubMedGoogle Scholar
  25. Ruskell, G.L., 1978, The fine structure of innervated myotendinous cylinders in extraocular muscles of rhesus monkeys, J. Neurocytol., 7: 693–708.CrossRefGoogle Scholar
  26. Sanes, J.R., 1987, Cell lineage and the origin of muscle fiber types, Trends in Neurosciences, 10, 219–221.CrossRefGoogle Scholar
  27. Sanes, J.R., Marshall, L.M., and McMahan, U.J., 1978, Reinnervation of muscle fiber basal lamina after removal of myofibers, J. Cell Biol., 78, 176–198.PubMedCrossRefGoogle Scholar
  28. Sokoll, M.D., Sonesson, B., and Thesleff, S., 1968, Denervation changes produced in an innervated skeletal muscle by long-continued treatment with a local anaesthetic, Eur. J. Pharmacol., 4, 179–187.PubMedCrossRefGoogle Scholar
  29. Studitsky, A.N., 1959, Experimental Surgery of Muscles (In Russian), Izdatel, Akad. Nauk. S.S.S.R., Moscow.Google Scholar
  30. Wernig, A., Carmody, J.J., Anzil, A.P., Hansert, E., Marciniak, M. and Zucker, H., 1984, Persistence of nerve sprouting with features of synaptic remodelling in soleus muscles of adult mice, Neuroscience, 11, 241–253.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1988

Authors and Affiliations

  • Richard Butler
    • 1
  1. 1.Department of AnatomyMcMaster UniversityHamiltonCanada

Personalised recommendations