Summary
This study provides morphological evidence for axon retraction during the elimination of polyneuronal innervation in postnatal rat soleus muscle. The motor innervation of muscles from animals 7–15 days and two months of age was examined in silver-stained preparations at the light microscopic level and in serial sections with the electron microscope. Transection of the soleus nerve in immature muscles revealed that the pattern of terminal and preterminal degeneration was similar to, but much more rapid than, that reported for adult muscles. During normal development, less than 1% of the preterminal axons sampled exhibited a denervation-like morphology and none of the neuromuscular junctions exhibited dense terminal degeneration. This indicates that autotomy and phagocytosis of the excess axons play a minor role in the development of connections.
From estimates of the number of axons lost per day, about 20% of the endplates in 14-day-old muscles would be expected to have involuting axons associated with them. Slender axons terminating in vesicle-laden enlargements were associated with 18% of the endplates examined ultrastructurally which is consistent with the predicted rate of axon removal. These structures are interpreted as morphological manifestations of axon retraction because they were not present in adult material and they were not produced by nerve transection. Furthermore, they are comparable in shape and location to the putative retraction fibres identified in silver-stained sections at the light microscopic level. The present results indicate that retraction is the major means by which all but one of the multiple inputs per endplate are removed during the establishment of the adult pattern of motor innervation.
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Bagust, J., Lewis, D. M. &Westerman, R. A. (1974) Polyneuronal innervation of kitten skeletal muscle. Journal of Physiology 229, 241–55.
Bennett, M. R. &Pettigrew, A. G. (1974) The formation of synapses in striated muscle during development. Journal of Physiology 241, 515–45.
Brown, M. C., Jansen, J. K. S. &Van Essen, D. (1976) Polyneuronal innervation of skeletal muscle in new-born rats and its elimination during maturation. Journal of Physiology 261, 387–422.
Conradi, S. &Ronnevi, L. O. (1975) Spontaneous elimination of synapses on cat spinal motoneurons after birth: do half of the synapses on the cell bodies disappear? Brain Research 92, 505–10.
Heuser, J. &Reese, T. (1973) Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. Journal of Cell Biology 57, 315–44.
Kelly, A. M. &Zacks, S. I. (1969) The fine structure of motor endplate morphogenesis. Journal of Cell Biology 42, 154–69.
Korneliussen, H. &Jansen, J. K. S. (1976) Morphological aspects of the elimination of polyneuronal innervation of skeletal muscle fibers in newborn rats. Journal of Neurocytology 5, 591–604.
Manolov, S. (1974) Initial changes in the neuromuscular synapses of denervated rat diaphragm. Brain Research 65, 303–16.
O'brien, R. A. D., Östberg, A. J. C. &Vrbová, G. (1978) Observations on the elimination of polyneuronal innervation on developing mammalian skeletal muscle. Journal of Physiology 282, 571–82.
Redfern, P. A. (1970) Neuromuscular transmission in new-born rats. Journal of Physiology 209, 701–9.
Reier, P. J. &Hughes, A. (1972) Evidence for spontaneous axon degeneration during peripheral nerve maturation. American Journal of Anatomy 135, 147–52.
Rile Y. D. A. (1976) Multiple axon branches innervating single endplates in kitten soleus muscles. Brain Research 110, 158–161.
Riley, D. A. (1977a) Spontaneous elimination of nerve terminals from the endplates of developing skeletal myofibers. Brain Research 134, 279–85.
Riley, D. A. (1977b) Multiple innervation of fiber types in the soleus muscles of postnatal rats. Experimental Neurology 56, 400–9.
Riley, D. A. (1978) Tenotomy delays the postnatal development of the motor innervation of the rat soleus. Brain Research 143, 162–7.
Rosenthal, J. L. &Taraskevich, P. S. (1977) Reduction of multiaxonal innervation at the neuromuscular junction of the rat during development. Journal of Physiology 270, 299–310.
Winlow, W. &Usherwood, P. N. R. (1975) Ultrastructural studies of normal and degenerating mouse neuromuscular junctions. Journal of Neurocytology 4, 377–94.
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Riley, D.A. Ultrastructural evidence for axon retraction during the spontaneous elimination of polyneuronal innervation of the rat soleus muscle. J Neurocytol 10, 425–440 (1981). https://doi.org/10.1007/BF01262414
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DOI: https://doi.org/10.1007/BF01262414