The role of the Ca2+-activated K+ current (I(K(Ca))) in crayfish opener muscle fibers is functionally important because it regulates the graded electrical activity that is characteristic of these fibers. Using the cell-attached and inside-out configurations of the patch-clamp technique, we found three different classes of channels with properties that matched those expected of the three different ionic channels mediating the depolarization- activated macroscopic currents previously described (Ca2+, K+, and Ca2+dependent K+ currents). We investigated the properties of the ionic channels mediating the extremely fast activating and persistent (I(K(Ca)). These voltage- and Ca2+-activated channels had a mean single-channel conductance of ~ 70 pS and showed a very fast activation. Both the single- channel open probability and the speed of activation increased with depolarization. Both parameters also increased in inside-out patches, i.e., in high Ca2+ concentration. Intracellular loading with the Ca2+ chelator bis(2-aminophenoxy) ethane-N, N,N',N'-tetraacetic acid gradually reduced and eventually prevented channel openings. The channels opened at very brief delays after the pulse depolarization onset (<5 ms), and the time-dependent open probability was constant during sustained depolarization (≤560 ms), matching both the extremely fast activation kinetics and the persistent nature of the macroscopic (I(K(Ca)). However, the intrinsic properties of these single channels do not account for the partial apparent inactivation of the macroscopic (I(K(Ca)), which probably reflects temporal Ca2+ variations in the whole muscle fiber. We conclude that the channels mediating (I(K(Ca)) in crayfish muscle are voltage- and Ca2+-gated BK channels with relatively small conductance. The intrinsic properties of these channels allow them to act as precise Ca2+ sensors that supply the exact feedback current needed to control the graded electrical activity and therefore the contraction of opener muscle fibers.