Membrane currents from single smooth muscle cells enzymatically isolated from canine renal artery were recorded using the patch-clamp technique in the whole-cell and cell-attached configurations. These cells exhibited a mean resting potential, input resistance, membrane time constant, and cell capacitance of −51.8±2.1 mV, 5.2±0.98GΩ, 116.2±16.4 msec, and 29.1±2.0 pF, respectively. Inward current, when elicited from a holding potential of —80 mV, activated near —50 mV, reached a maximum near 0 mV and was sensitive to the dihydropyridine agonist Bay K 8644 and dihydropyridine antagonist nisoldipine. Two components of macroscopic outward current were identified from voltage-step and ramp depolarizations. The predominant charge carrier of the net outward current was identified as K+by tail-current experiments (reversal potential, −61.0±0.8 mV in 10.8 mM [K+]o/140 mM [K+]i). The first component was a small, low-noise, voltage- and time-dependent current that activated between —40 and —30 mV (IK(dr)), and the second component was a larger, noisier, voltage- and time-dependent current that activated at potentials positive to +10 mV (IK(Ca)). Both IK(dr)and lK(Ca)displayed little inactivation during long (4-second) voltage steps. IK(Ca)and lK(dr)could be pharmacologically separated by using various Ca2' and K+channel blockers. IK(Ca)was substantially inhibited by external NiCI2(500 μM), CdCI2(300 μM), EGTA (5 mM), tetraethylammonium (Kiat +60 mV, 307 μM), and charybdotoxin (100 nM) but was insensitive to 4-aminopyridine (0.1–10 mM). IK(dr)was inhibited by 4-aminopyridine (Kiat +10 mV, 723 μM) and tetraethylammonium (Kiat +10 mV, 908 μM) but was insensitive to external NiCI2(500 μM), CdCI2(300 μM), EGTA (5 mM), and charybdotoxin (100 nM). Two types of single K+channels were identified in cell-attached patches. The most abundant K+channel that was recorded exhibited voltage-dependent activation, was blocked by external tetraethylammonium (250 μM), and had a large single-channel conductance (232±f12 pS with 150 mM K+in the patch pipette, 130±17 pS with 5.4 mM K+in the patch pipette). The second channel was also voltage dependent, was blocked by 4-aminopyridine (5 mM), and exhibited a smaller single-channel conductance (104±8 pS with 150 mM K+in the patch pipette, 57±6 pS with 5.4 mM K+in the patch pipette). These results suggest that depolarization of canine renal artery cells opens dihydropyridine-sensitive Ca2+channels and at least two K+channels. The two time-dependent K+currents (IK(Ca)and IK(dr)) reflect the behavior of two distinct K' channels. According to the pharmacology of the whole-cell and single-channel experiments, IK(Ca)is primarily carried by the large conductance Ca2+-activated K+channel, and IK(dr)is carried by the smaller conductance delayed rectifier K' channel.