Competitive interaction between foreign nerves innervating frog skeletal muscle.

Abstract

Competition between 2 foregin nerves innervating frog skeletal muscle was studied by using pairs of somatic motor nerves (SMNT) or 1 SMN and the preganglionic splanchnic nerve (SPM) implanted into a denervated sartorius muscle that was transplanted to the lymph sac of the back. A single SMN implanted into the muscle succeeded in innervating essentially every fiber within 2-3 mo.; tetanic stimulation of the nerve elicited 90-100% of the maximal direct tetanus tension. Most of the EPP were suprathreshold, since a single indirect stimulus evoked a twitch 60-100% as large as that to a direct stimulus. If SMN were implanted simultaneously, tetanic stimulation of either elicited 80-100% of the maximal tension to direct stimulation. If 1 nerve was implanted 2-3 mo. before the other, the 2nd, although usually less effective than the 1st, normally innervated 50-100% of the fibers, with about the same time course of innervation as a single SMN. Mutual synaptic repression was seen on examination of twitch tensions. With either simultaneous or staggered innervation, stimulation of each SMN resulted in a twitch of 30-50% of the total direct twitch tension, with little overlap between the fields driven by the 2 nerves. Intracellular recordings showed that the distribution of subthreshold and spike-producing EPP reflected the existence of separate twitch fields. Even if 1 SMN was implanted several months before the other and had time to establish suprathreshold junctions on most muscle fibers, an SMN implanted later was able to reduce sharply the effectiveness of many junctions from the earlier nerve while itself innervating most muscle fibers. The subthreshold EPP had low quantal content, typically 10 or fewer quanta EPP. The minmum EPP frequency was very low, while minimum EPP amplitude appeared to be normal. In the vast majority of muscle fibers, junctions from the 2 nerves were not within recording distance of each other. The competitive interaction was mediated somehow via the muscle fiber. The preganglionic splanchnic nerve, which also successfully reinnervated frog skeletal muscle, competed with a foreign SMN in ways which differ qualitatively from the competition by a 2nd SMN. After 6-8 mo. of dual innervation by SMN and SPN the SMN became almost totally dominant. If the SMN was then sectioned, the SPN became as effective, within about 1 wk, as it would have been in the absence of the SMN.