The Xenopus embryo has been well studied and the circuitry underlying motor pattern generation largely elucidated. We have extended this analysis by determining the roles of individual voltage- and ligand-gated ion channels in controlling the motor pattern for swimming and two mechanisms that control rundown of this pattern. Xenopus embryo spinal neurons possess at least six classes of ion channel: a fast Na+ channel; a mixture of kinetically similar Ca2+ channels; a fast K+ channel; a slow K+ channel; a Na(+)-dependent K+ channel; and a slowly activating Ca2(+)-dependent K+ channel. The roles of the voltage-gated currents in determining neuronal firing properties and operation of the locomotor circuitry have been examined both pharmacologically and in realistic computer simulations. Model neurons fire repetitively in response to current injection. The Ca2+ current seems essential for repetitive firing. The fast K+ current appears mainly to control spike width, whereas the slow K+ current exerts a powerful influence on repetitive firing. These predictions from the model have been confirmed by the use of specific pharmacological blockers of the fast and slow K+ currents. Both the model network and the real spinal locomotor circuit appear to tolerate a wide variation in the relative strengths of the component synapses but are very sensitive to the magnitudes of the voltage-gated currents. In particular the slow K+ current, despite being a small component of the total outward current, plays a critical role in stabilizing the motor pattern. Like many other rhythmic motor patterns, swimming in the Xenopus embryo is episodic; it undergoes run-down and self-termination even in the absence of sensory inputs. The slow Ca2(+)-dependent K+ current appears to play a role in the self-termination of swimming. However, intrinsic modulation mediated by the release of ATP and production of adenosine in the extracellular space appears to be a very powerful determinant of run-down of the motor pattern.