Neural control of swimming in Aplysia brasiliana. I. Innervation of parapodial muscle by pedal ganglion motoneurons

D. R. McPherson and J. E. Blankenship Marine Biomedical Institute, University of Texas Medical Branch, Galveston 77550. 1. Swimming is an oscillatory locomotor behavior in Aplysia accomplished by rhythmic undulating movements of the parapodia, winglike flaps that cover the dorsum of the body. As part of an analysis of the neural basis of this behavior, we have identified and characterized motoneurons in the pedal ganglia that directly innervate parapodial muscle and fire phasically during fictive swimming. 2. Parapodial musculature is organized into at least eight discrete layers. Fibers of adjacent layers are directed orthogonally. 3. Motoneurons were localized to the middle and rostral portions of the dorsal surface of each pedal ganglion by the use of backfill staining and intracellular dyes. These neurons were defined as motoneurons on the basis of additional physiological evidence for peripheral axons and their ability to cause excitatory junction potentials (EJPs; average amplitude, 2-5 mV) in muscle fibers and discrete contractions of parapodial muscles. Muscle fibers are polyneuronally innervated. Fibers had an average resting potential of -79 mV and no over-shooting action potentials. 4. There are probably at least 50 motoneurons. Their average resting potential was -48 mV, and they do not appear to be directly connected synaptically to one another. One identifiable motoneuron is described in detail. It participates in the opener (downstroke) phase of swimming and causes contraction of one of the described muscle layers. 5. Divalent ion concentrations were altered centrally and peripherally during motoneuron activity to demonstrate that the motoneurons directly innervate muscle fibers. Blockage of EJPs by hexamethonium and the presence of specific anticholinesterase staining in parapodial nerves and muscle fibers strongly suggest that many of the motoneurons are cholinergic. 6. Studies of excitation-contraction coupling showed that single or a few spikes in motoneurons rarely cause an EJP. Bursts of motoneuron spikes produced facilitating EJPs. With approximately 10 spikes in a 1-s motoneuron burst, adequate depolarization occurred in muscle fibers to initiate a small, slow contraction. Increased spike frequency led to greater depolarization, because of EJP summation, and larger contractions. Contraction requires depolarization of the muscle above a threshold, beyond which the force of contraction depends on both the duration and degree of depolar