Polyneuronal innervation of skeletal muscle in new-born rats and its elimination during maturation

Abstract

1. The events taking place during the elimination of polyneuronal innervation in the soleus muscle of new-born rats have been studied using a combination of electrophysiological and anatomical techniques. 2. Each immature muscle fibre is supplied by two or more motor axons which converge on to a single end-plate. There was no sign of electrical coupling between muscle fibres receiving multiple synaptic inputs. By the end of the second week after birth virtually all muscle fibres are innervated by only a single motor axon. 3. The average tension produced by individual motor units, measured in terms of the percentage of the total muscle twitch tension, declined dramatically during the first 2 weeks after birth. During this period there was no significant change in the number of motor neurones innervating the soleus muscle. Thus, the disappearance of polyneuronal innervation reflects a decrease in the number of peripheral synapses made by each motor neurone. 4. The decline in motor unit size was delayed, but not ultimately prevented, by the early surgical removal of all but a few motor axons to the soleus muscle. This procedure also caused a delay in the removal of polyneuronal innervation involving the remaining motor units. 5. Following a crush of the soleus nerve in neonatal animals, regenerating axons usually returned to the original end-plates. Polyneuronal innervation was extensive at early stages of re-innervation and it disappeared during the second week after birth just as in normal muscles. 6. Cross-innervation of neonatal muscles by an implanted foreign nerve caused a rapid disappearance of cholinesterase at denervated original end-plates and in most fibres prevented re-innervation by the original nerve. In the small proportion of fibres that did become innervated through both the foreign and original nerves the end-plates were more than 1 mm apart, and both foreign and original nerve end-plates could persist indefinitely. 7. Many cross-innervated fibres received multiple inputs through the foreign nerve. Some foreign end-plates were separated by distances ranging up to 1 mm. Polyneuronal innervation through the foreign nerve was completely eliminated during maturation but over a slightly longer period than in normal muscles. Apparently the elimination process can act over a distance up to but not much more than 1 mm. 8. These observations suggest that there are several factors influencing the elimination of redundant inputs in immature muscles. Individual motor neurones appear to have an inherent tendency to withdraw the majority of their original complement of peripheral terminals. The determination of which particular synapses are to survive, however, seems to be made in the periphery by a selection among all the synapses that innervate a limited region of each muscle fibre. There may be a competitive interaction among synapses in which those belonging to smaller motor units are less likely to be eliminated, thereby leading to a relatively uniform size of the motor units in the soleus.