Neuronal Mechanisms for Rhythmic Motor Pattern Generation in a Simple System

Abstract

The lobster stomatogastric ganglion is an ideal system with which to study the genesis of rhythmic patterned motor activity. This ganglion operates the striated musculature of the lobster stomach. All muscles operate under direct neural control and the stomach itself can be considered an internalized appendage whose movements are similar to those observed in crustacean locomotory systems. The isolated, deafferented ganglion produces two rhythms, the gastric mill rhythm and the pyloric rhythm, each with a different range of movements and a different pattern of bursts. When the ganglion is connected to the rest of the central nervous system, it receives modulating input over these rhythms from sensory receptors in the wall of the stomach and from higher centers in the central nervous system. The ganglion contains about 30 cells, 23 of which are motor-neurons. The synaptic connectivity between the motorneurons has been determined for both the gastric and pyloric rhythms. Subthreshold activity can be seen in all of the cell bodies and all motorneuron axons can be traced to their muscles and isolated for recording or antidromic stimulation. The mechanism of burst generation for the pyloric rhythm appears to consist of endogenous bursts generated by three electrotonically coupled cells. When the synaptic input to these cells is blocked, the cells continue to oscillate and fire whereas other cells are converted to a free running mode. Similar effects can be observed by hyperpolarizing these three cells to shut off their activity and observing the effects on follower cells. When ramp currents are passed into the bursting cells, they begin to burst at threshold and the burst number and inter-burst interval goes up with depolarization. The mechanism underlying the gastric bursts appears to be the result of the cooperative activity of many non-bursting cells connected primarily by inhibitory synapses. No single cell in the gastric mill network has been found to be capable of endogenous burst generation. When depolarized they fire continuously with some accommodation. Occasionally some single cells fire a spontaneous burst without synaptic input. The burst generation mechanism for the pyloric rhythm, therefore, appears to reside within the membranes of the endogenous bursting cells whereas the burst generation mechanism for the gastric mill network appears to be an emergent property of the network itself. It appears to be entirely reasonable, on the basis of preliminary modeling studies, to suggest that the pyloric rhythm burst generation mechanism can be supplemented by properties emerging from the pyloric network as a whole. Similarly, although the gastric system appears to be predominantly a rhythm generated by cooperative synaptic effects, bursting in some of the cells may also play a part in the overall generation of the gastric mill pattern.