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Effects of evoked and spontaneous motoneuronal firing on synapse competition and elimination in skeletal muscle

  • Published:
Journal of Neurocytology

Abstract

Synapse elimination is a general feature of the development of neural connections, including the connections of motoneurons to skeletal muscle fibers. Our work addressed two questions: (1) how the action potentials generated in the set of motoneurons innervating an individual muscle (i.e., in a motor pool) are correlated in time during development in vivo; (2) what influence different firing patterns exert on the processes of polyneuronal innervation and synapse elimination which characterize the establishment of muscle innervation.

We recorded the spontaneous electromyographic activity of the tibialis anterior and soleus muscles of late embryonic and neonatal rats, identifying the firing of at least two single motor unit signals in each record. We found that a striking switch occurs a few days after birth from a highly synchronous type of firing to an asynchronous one, the first thus characterizing embryonic while the second one adult motoneurons. We also investigated the effects of an evoked synchronous type of discharge on neuromuscular synapse formation, measuring polyneuronal innervation and synapse elimination. This was done in an adult in vivo model of de novo synapse formation, while a chronic TTX nerve conduction block, placed centrally with respect to the stimulating electrodes, eliminated the natural activity of motoneurons. We found that the imposed synchronous activity greatly inhibits synapse elimination, causing polyneuronal innervation to persist. We conclude that the early synchronous firing, favors the establishment of polyneuronal innervation while the subsequent switch to an asynchronous one promotes synapse elimination.

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References

  • BALICE-GORDON, R. J. & LICHTMAN, J. W. (1994) Long-term synapse loss induced by focal blockade of postsynaptic receptors. Nature 372, 51–524.

    PubMed  Google Scholar 

  • BENOIT, P. & CHANGEUX, J. P. (1975) Consequences of tenotomy on the evolution of multiinnervation in developing rat soleus muscle. Brain Research 99, 35–358.

    PubMed  Google Scholar 

  • BROWN, M. C., JANSEN, J. K. S. & VAN ESSEN, D. C. (1976) Polyneuronal innervation of skeletal muscle in new-born rats and its elimination during maturation. Journal of Physiology 261, 38–424.

    PubMed  Google Scholar 

  • BUFFELLI, M., BURGESS, R. W., FENG, G., LOBE, C., LICHTMAN, J. W. & SANES, J. R. (2003) Genetic evidence that relative synaptic efficacy biases the outcome of synaptic competition. Nature 424, 43–434.

    PubMed  Google Scholar 

  • BUFFELLI, M., BUSETTO, G., CANGIANO, L. & CANGIANO, A. (2002) Perinatal switch from synchronous to asynchronous activity of motoneurons: Link with synapse elimination. Proc. Natl. Acad. Sci. USA 99, 1320–13205.

    PubMed  Google Scholar 

  • BUSETTO, G., BUFFELLI, M., TOGNANA, E., BELLICO, F. & CANGIANO, A. (2000) Hebbian mechanisms revealed by electrical stimulation at developing rat neuromuscular junctions. Journal of Neuroscience 20, 68–695.

    PubMed  Google Scholar 

  • CHANG, Q., GONZALEZ, M., PINTER, M. J. & BALICE-GORDON, R. J. (1999) Gap junctional coupling and patterns of connexin expression among neonatal rat lumbar spinal motor neurons. Journal of Neuroscience 19, 1081–10828.

    PubMed  Google Scholar 

  • COSTANZO, E. M., BARRY, J. A. & RIBCHESTER, R. R. (2000) Competition at silent synapses in reinnervated skeletal muscle. Nature Neuroscience 3, 69–700.

    PubMed  Google Scholar 

  • HEBB, D. (1949) The Organization of Behavior. New York: Wiley.

    Google Scholar 

  • HENNIG, R. & LØMO, T. (1985) Firing patterns of motor units in normal rats. Nature 314, 16–166.

    PubMed  Google Scholar 

  • JANSEN, J. K. & FLADBY, T. (1990) The perinatal reorganization of the innervation of skeletal muscle in mammals. Progress in Neurobiology 34, 3–90.

    PubMed  Google Scholar 

  • PERSONIUS, K. E. & BALICE-GORDON, R. J. (2001) Loss of correlated motor neuron activity during synaptic competition at developing neuromuscular synapses. Neuron 31, 39–408.

    PubMed  Google Scholar 

  • PURVES, D. & LICHTMAN, J. (1985) Principles of Neural Development. Sunderland, MA, USA: Sinauer Associates.

    Google Scholar 

  • REDFERN, P. (1970) Neuromuscular transmission in newborn rats. Journal of Physiology 209, 70–709.

    PubMed  Google Scholar 

  • RIBCHESTER, R. R. (1993) Coexistence and elimination of convergent motor nerve terminals in reinnervated and paralysed adult rat skeletal muscle. Journal of Physiology 466, 42–441.

    PubMed  Google Scholar 

  • RICH, M. M. & LICHTMAN, J. W. (1989) In vivo visualization of pre-and postsynaptic changes during synapse elimination in reinnervatedmousemuscle. Journal of Neuroscience 9, 178–1805.

    PubMed  Google Scholar 

  • ROTHWELL, J. (1994) Control of Human Voluntary Movement. London: Chapman & Hall.

    Google Scholar 

  • STENT, G. S. (1973) A physiological mechanism for Hebb's postulate of learning. Proc. Natl. Acad. Sci. USA 70, 99–1001.

    PubMed  Google Scholar 

  • THOMPSON, W. & JANSEN, J. K. (1977) The extent of sprouting of remaining motor units in partly denervated immature and adult rat soleus muscle. Neuroscience 2, 52–535.

    PubMed  Google Scholar 

  • THOMPSON, W. J. (1983) Synapse elimination in neonatal rat muscle is sensitive to the pattern of muscle use. Nature 302, 61–616.

    PubMed  Google Scholar 

  • THOMPSON, W. J., KUFFLER, D. P. & JANSEN, J. K. S. (1979) The effect of prolonged reversible block of nerve impulses on the elimination of polyneuronal innervation of new-born rat skeletal muscle. Neuroscience 4, 27–281.

    PubMed  Google Scholar 

  • TRESCH, M. C. & KIEHN, O. (2002) Synchronization of motor neurons during locomotion in the neonatal rat: Predictors and mechanisms. Journal of Neuroscience 22, 999–10008.

    PubMed  Google Scholar 

  • WALTON, K. D. & NAVARRETE, R. (1991) Postnatal changes in motoneurone electrotonic coupling studied in the in vitro rat lumbar spinal cord. Journal of Physiology 433, 28–305.

    PubMed  Google Scholar 

  • WESTERGA, J. & GRAMSBERGEN, A. (1994) Development of the EMG of the soleus muscle in the rat. Developmental Brain Research 80, 23–243.

    PubMed  Google Scholar 

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Correspondence to A. Cangiano.

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Busetto, G., Buffelli, M., Cangiano, L. et al. Effects of evoked and spontaneous motoneuronal firing on synapse competition and elimination in skeletal muscle. J Neurocytol 32, 795–802 (2003). https://doi.org/10.1023/B:NEUR.0000020624.48032.ed

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  • DOI: https://doi.org/10.1023/B:NEUR.0000020624.48032.ed

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