High-conductance (BK or maxi) K(+) channels were observed in cell-attached patches of the apical membrane of the isolated split-open rat connecting tubule (CNT). These channels were quite rare in cells identified visually as principal cells (PCs; 5/162 patches) but common in intercalated cells (ICs; 24/26 patches). The BK-expressing intercalated cells in the CNT and cortical collecting duct (CCD) were characterized by a low membrane potential (-36 mV) under short-circuit conditions, measured from the reversal potential of the channel currents with similar K(+) concentrations on both sides of the membrane. Under whole-cell clamp conditions with low intracellular Ca(2+), ICs had a very low K(+) conductance. When cell Ca(2+) was increased to 200 nM, a voltage-dependent, tetraethylammonium (TEA)-sensitive outward conductance was activated with a limiting value of 90 and 140 nS/cell in the CNT and CCD, respectively. Feeding animals a high-K diet for 1 wk did not increase these currents. TEA-sensitive currents were much smaller in PCs and usually below detection limits. To examine the possibility that the ICs participate in transepithelial K(+) secretion, we measured Na/K pump activity as a ouabain-sensitive current. Although these currents were easily observed in PCs, averaging 79 +/- 14 and 250 +/- 50 pA/cell in the CCD and CNT, respectively, they were below the level of detection in the ICs. We conclude that ICs have BK channel densities that are sufficient to support renal secretion of K(+) if cell Ca(2+) is elevated. However. a pathway for K(+) entry into these cells has not been identified.