Activity of multiple identified motor neurons recorded intracellularly during evoked feedinglike motor programs in Aplysia

Abstract

1. The firing patterns of 22 motor neurons were determined by simultaneously recording intracellularly from up to 7 neurons during evoked feedinglike buccal motor programs (BMPs). Intracellular stimulation of cerebral-buccal interneuron 2 (CBI-2) or tactile stimulation of the odontophore were used to elicit BMPs in a reduced preparation. 2. Evoked BMPs were identified as either ingestive-like (iBMP) or egestive-like (eBMP) on the basis of their similarity to those previously recorded in select neurons in freely behaving animals. Neurons were divided into the p-group, r-group, or c-group, on the basis of the phase relationships of rhythmic membrane depolarizations and hyperpolarizations during evoked BMPs. Depolarization of the p-, r-, and c-group neurons was associated with radular protraction, retraction, and closure, respectively. With one exception, the motor neurons segregated into the same groups during iBMPs and eBMPs. The exception, B7, was categorized as a c-group neuron during iBMPs, but as an r-group neuron during eBMPs. 3. Every motor neuron exhibited cyclic membrane depolarizations and hyperpolarizations, and over one-half of the neurons fired bursts of action potentials, during both iBMPs and eBMPs. The neurons fired in patterns that would be likely to release both their conventional and peptide transmitters. 4. A marked hyperpolarizing step in the p-group neurons coincident with a depolarization in the r-group neurons was observed during both iBMPs and eBMPs, suggesting a degree of shared premotor circuitry for the two BMPs. 5. A shift in the timing of activity in c-group neurons relative to that in p- and r-group neurons during iBMPs and eBMPs was observed and correlates well with the shift in phase of radular closure relative to protraction and retraction, which is useful in distinguishing ingestion from egestion in the behaving animal. 6. The firing patterns recorded in neurons that innervate overlapping populations of muscle fibers suggested that there would be complex interactions of multiple transmitters. This is particularly intriguing in the case of I3a muscle fibers, which are innervated by two excitatory and one inhibitory neuron. The firing patterns recorded in these neurons suggest that the inhibitory motor neuron may serve to not only block inappropriate contractions, but also to specifically shape evoked contractions during feeding.