Age-dependent long-term adaptation of crayfish phasic motor axon synapses to altered activity

Abstract

Crustacean tonic and phasic motoneurons have neuromuscular synaptic properties corresponding with their functional requirements. Phasic axon synapses produce large excitatory postsynaptic potentials (EPSPs) which depress rapidly during repetitive activation. Tonic axon synapses generally produce smaller EPSPs which are more resistant to fatigue. To test whether nerve impulse activity of the motoneuron plays a role in the establishment of these synaptic properties, a phasic axon was tonically stimulated in vivo. The 'fast' closer excitor of the crayfish claw, which normally fires few impulses, was stimulated for 2 hr/day at 5 Hz, through implanted electrodes. In young crayfish, this stimulation produced an 11-fold decrease in synaptic fatigue at the fast axon's neuromuscular synapses, as determined from measurements of EPSPs during 5 Hz stimulation of the fast axon for 30 min. In comparison with EPSPs of the contralateral control claw, the initial EPSP amplitude was 44% smaller and the final EPSP amplitude was 4.3 times larger for the chronically stimulated fast axon. These changes in EPSP amplitude are due to changes in transmitter release. This long-term adaptation of the fast axon to imposed tonic activity persists for at least 10 days after the effect has been established. The same chronic stimulation regimen produces significant, although less dramatic, results in adult crayfish. Compared to the contralateral control, the chronically stimulated fast axon showed no change in initial EPSP amplitude and only a 2-fold increase in the EPSP amplitude after 30 min of stimulation at 5 Hz. Thus, the decrease in synaptic fatigue was only 2- to 3-fold, much less than in young crayfish. During normal growth, the fast axon synapses become better suited to their phasic pattern of activation, showing progressive increase in initial EPSP amplitude and greater synaptic fatigue during prolonged activation. In light of our findings, it is suggested that activity levels during development may play a role in the establishment of the adult synaptic properties.