We have studied the influence of the K(+)-current mutations eag and Sh and the Na(+)-current mutation napts upon two well-defined neural circuits that underlie flight and an escape response in Drosophila, recording from dorsal longitudinal and tergotrochanteral muscles. Mutations of Sh and eag affected refractory period and following frequency, but not latency, of the jump-and-flight escape response. The napts mutation altered these 3 physiological parameters of the "jump" (TTM), but not the "flight" (DLM), branch, suggesting differences in the vulnerability of different circuit components to the mutation. In contrast to their interaction in some other systems, napts did not counteract the effects of eag and Sh upon these physiological parameters in eag Sh; nap triple mutants. In eag Sh double mutants, in which multiple K+ currents may be diminished, flight muscles showed abnormal rhythmic activity not associated with flight, and some flies also had an abnormal wings-down posture. The low-frequency spikes probably originated in the flight muscle motoneurons, but the coordination between muscle fibers during this "non-flight activity" was distinct from flight. Nevertheless, in spite of the presence of this non-flight activity in resting eag Sh flies, those animals with normal wing posture were also able to fly, with a normal pattern of muscle activity. This suggests that in these mutants, the DLM motoneuron circuit is able to switch between two patterns of output, non-flight activity and flight.(ABSTRACT TRUNCATED AT 250 WORDS)