K channels in enzymatically dispersed circular smooth muscle cells from the canine proximal colon were studied with the patch-clamp technique. The most prominent channel in cell-attached and excised, inside-out patches was a K channel, which had slope conductances of approximately 100 pS at a holding potential of 0 mV in a physiological K+ gradient and approximately 200 pS in symmetrical 140 mM K+ solutions. The relative permeabilities of the channel for monovalent cations were 1.0 K+:0.5 Rb+: less than 0.07 Li+:less than 0.07 Na+. The channels were activated by potential and intracellular Ca2+. At Ca2+ concentrations less than 10(-7) M, channel openings were rare except at very positive potentials. At Ca2+ concentrations between 10(-7) and 10(-6) M the probability of channel opening increased steeply, and the voltage for channel activation shifted to a negative potential range, which cells experience during electrical slow wave events in situ. The effect of Ca2+ on the open-state probability of single channels was mainly due to a decrease in mean close time. Channels were blocked by 1 mM tetraethylammonium applied to the outside of the patch but up to 10 mM tetraethylammonium applied to the inside of the patch, and 4-aminopyridine applied to either side did not block the channel. The data suggest that this channel mediates a current important in the termination of electrical slow waves, which are the primary excitable event in colonic circular muscles.