Swimming activity evoked by light tactile stimulation of a body wall flap in dissected leech preparations undergoes habituation (5). In this study, we examine the activity of several interneurons (cell 204, cell 205, the S cell, and cell 208) during habituation trials to study further the neuronal mechanisms that mediate this decline in responsiveness. Light tactile stimulation of the leech body wall evoked initially a marked excitatory response in cell 204 homologs (segmental swim-initiating neurons) that preceded the initiation of swimming activity. This response decreased over the course of repeated stimulus trials; however, no marked decline in cell 204 activity accompanied the cessation of swim initiation. A similar activity pattern was observed in cell 205. Thus the habituation of swimming activity to stroking of the body wall is not due solely to reduced input to cell 204 and cell 205. The early activity of cell 204 was not correlated to the duration of subsequent swim episodes. However, the impulse frequency of cell 204 during swim episodes was negatively correlated to the period of swim cycles. This correlation between cell 204 activity and cycle period occurred both within individual episodes as well as between trials in a habituation series. Direct stimulation of cell 204 with current pulses evoked swimming activity reliably for an average of 72 trials. Therefore, habituation that results from stroking the body wall (which occurs after approximately 6 trials) is not mediated by plasticity in the connections between cell 204 and the swim oscillator. The S cell fired repeatedly in response to light tactile stimulation. This response declined with repeated trials. Intense intracellular stimulation of the S cell was sufficient to initiate swimming activity in some preparations. The magnitude and duration of the excitation required to initiate swimming by this means were far greater, however, than that which occurred during stroking the body wall. The response of cell 208 (a swim oscillator cell) to body wall stimulation during habituation trials was variable; usually an initial hyperpolarization was followed by some depolarization. No aspect of this response correlated with the onset of habituation. Our results are consistent with the idea that cell 204 and cell 205 are part of the pathway that mediates swimming activity in response to light tactile stimulation of the leech body wall, and that habituation occurs, in part, as the result of reduced sensory input to this cell.(ABSTRACT TRUNCATED AT 400 WORDS)