Functional consequences of activity-dependent synaptic enhancement at a crustacean neuromuscular junction

Abstract

This study provides evidence that activity-dependent synaptic enhancement at a neuromuscular junction modifies the characteristics of force production of the receiving muscle during rhythmic motor neuron discharge patterns. Long-lasting augmentation of the excitatory junction potentials (EJPs) quickens and strengthens the muscle response to a given motor pattern. We used the muscle gm6 of the crab Cancer pagurus to study the functional consequences and temporal dynamics of facilitation and augmentation. This stomach muscle is driven by the rhythmic activity of the gastric mill central pattern generator in the stomatogastric nervous system. We tested the response of this muscle to rhythmic motor drive using a variety of gastric mill-like stimulations. EJPs recorded in muscle gm6 were initially small but are summated and facilitated strongly with continuous stimulation. Facilitation increased with shorter interspike intervals and possessed a time constant of decay <1 s. During gastric mill rhythms, motor neuron activity was by contrast represented by bursts of activity with intermittent pauses of several seconds. Recordings in intact animals and in the isolated nervous system showed a great variability in firing frequency and temporal distribution of motor neuron bursts. Train stimulations with various stimulus frequencies (5 Hz, 10 Hz, 20 Hz) and inter-train intervals (2 s, 4 s, 8 s, 16 s, 32 s) revealed that augmentation acted in addition to facilitation. Augmentation increased muscle EJPs during stimulations with inter-train intervals of 16 s or less. The effects of augmentation increased with shorter inter-train intervals, but were independent of stimulus frequency. Augmentation also contributed to the electrical response of the muscle during gastric mill rhythms, which were obtained in vitro and in vivo, and was also reflected by an increase of muscle force and the slope of force development during repetitive train stimulation. We conclude that the augmentation of EJPs at the neuromuscular junction tunes the muscle response to support force production during rhythmic motor patterns.