Serotonin and the small cardioactive peptides differentially modulate two motor neurons that innervate the same muscle fibers in Aplysia

Abstract

The anterior portion of intrinsic buccal muscle 3 (I3a) is innervated by two motor neurons, B3 and B38, which appear to use glutamate as their fast excitatory transmitter. B3 and B38 express the neuropeptides FMRFamide and the small cardioactive peptides (SCPs), respectively. We have shown previously that stimulation of B38 causes release of the SCPs from terminals in the muscle. The I3a muscle also receives input from neurons that use 5HT as a modulatory transmitter. The SCPs and 5HT potently facilitated B38- evoked excitatory junction potentials (EJPs) but had only a small effect on B3-evoked EJPs; however, both the SCPs and 5HT strongly potentiated contractions evoked by both B3 and B38, indicating that the two substances must also act on excitation-contraction coupling. The selective facilitation of B38-evoked EJPs, however, did manifest itself in other parameters. Decreases in the firing frequencies and burst durations that were threshold to evoke contractions and decreases in the latency between the onset of a burst and the onset of the evoked contraction were all much larger for B38 than for B3. Indeed, B38 bursts recorded during feeding-like behavior would be subthreshold for evoking contractions in the absence of this modulation. All of the effects of the SCPs reversed during washout, whereas those of 5HT were persistent, lasting many hours after washout. Thus, the SCPs and 5HT dramatically change the behavioral output of these motor neurons, increasing the amplitude of contractions evoked by both B3 and B38, and shifting the temporal relationship between bursts in B38 and its evoked contractions.