Swimming behavior in the marine mollusc Tritonia diomedea is episodic, consisting of a series of alternating dorsal and ventral flexions initiated by a brief sensory stimulus. The swim motor pattern is generated by a network formed of four groups of premotor interneurons: cerebral cell 2 (C2), dorsal swim interneurons (DSIs), and two types of ventral swim interneurons (VSI-A and VSI-B). The initiation and maintenance of swimming depends on the establishment of a long-lasting ramp depolarization in both the premotor, pattern-generating interneurons, and the motor neurons (i.e., flexion neurons). Voltage clamp was used to measure the membrane current responsible for the ramp depolarization. In all cell classes the current had two components: a tonic inward current, which decayed as the swim progressed, and phasic inward current waves, which provided the synaptic drive during each swim burst. The ramp current in the flexion neurons and in C2 was generated largely by activity within the interneuronal pattern-generating network (PGN). The ramp current could be mimicked by driving activity in the pattern-generating interneurons. In VSI-B, the tonic component of the ramp current was independent of activity within the PGN and appeared to be derived from the long-lasting effect of an extrinsic input. The phasic components of the ramp, however, were dependent on PGN activity. The phasic inward current waves were blocked when pattern generation was prevented. In addition, phasic inward currents similar to those occurring during swimming could be produced by driving the C2. The tonic component of the ramp current in a DSI was dependent both on extrinsic inputs and PGN activity. Extrinsic inputs appeared to control the first 10-15 s of the tonic current. At longer times, activity within the DSI population itself maintained the ramp current. When one DSI was driven in a quiescent preparation, all other DSIs were inhibited, yet the DSIs are known to be coupled by monosynaptic, reciprocal excitatory synapses. This effect could be explained by the action of an unidentified inhibitory interneuron (I-neuron), which was excited by DSIs and in turn inhibited all other DSIs. The DSIs were therefore coupled reciprocally by both monosynaptic excitation and polysynaptic inhibition. Activity in C2 switched the DSI-DSI interaction from inhibition to excitation by inhibiting the I-neuron.(ABSTRACT TRUNCATED AT 400 WORDS)