Swimming in Aplysia brasiliana: behavioral and cellular effects of serotonin.

1. Aplysia brasiliana is a marine mollusk that swims by repeated metachronal flapping movements of its bilateral fleshy parapodia. Animals with bilateral cerebropedal connective (CPC) lesions do not swim when suspended above the substrate, although tonic CPC stimulation can elicit normal parapodial flapping. Although the parapodial opener-phase (POP) cells, a previously identified group of neurons, fire synchronous bursts of efferent spikes in-phase with parapodial opening movements in both intact animals and dissected preparations, they are not likely to be primary parapodial motoneurons. These cells receive one or more large, apparently monosynaptic excitatory postsynaptic potentials (EPSPs) during CPC stimulation that are effective in producing the swimming motor program (SMP). 2. In suspended CPC-lesioned animals, injections of serotonin (5-HT) that produce an average hemolymph concentration of 10(-5) M induced full-amplitude parapodial flapping. Selected episodes of flapping were similar in frequency to normal suspended swimming. 3. In suspended CPC-lesioned animals, 5-HT injections elicited an apparently normal swimming motor program that was associated with synchronous bursts of large-amplitude efferent spikes in the parapodial nerves. In many semi-intact preparations, exposing the circumoesophageal ganglia to 5-HT elicited a similar rhythmic motor program, but usually at a lower frequency than during normal swimming or during tonic CPC stimulation. 4. In isolated-ganglion preparations, bath application of 5-HT produced immediate depolarization and tonic firing of individual POP neurons, followed by smooth and regular bursting in the apparent absence of synaptic input. In such preparations, the motor program elicited by bath-applied 5-HT differed from the one elicited by tonic CPC stimulation in that the 5-HT-elicited rhythmic bursting usually was not synchronous in different POP neurons. Tonic CPC stimulation during bath applications of 5-HT produced immediate synchronization of bursts among the POP neurons. 5. Hyperpolarization (or depolarization) of a POP neuron during bath application of 5-HT increased (or decreased) the burst period, but membrane polarization did not change the burst period elicited during tonic CPC stimulation.