Ca2+ sparks activate K+ and Cl- channels, resulting in spontaneous transient currents in guinea-pig tracheal myocytes

1. Local changes in cytosolic [Ca2+] were imaged with a wide-field, high-sp eed, digital imaging system while membrane currents were simultaneously rec orded using whole-cell, perforated patch recording in freshly dissociated g uinea-pig tracheal myocytes. 2. Depending on membrane potential, Ca2+ sparks triggered 'spontaneous' tra nsient inward currents (STICs), 'spontaneous' transient outward currents (S TOCs) and biphasic currents in which the outward phase always preceded the inward (STOICs). The outward currents resulted from the opening of large-co nductance Ca2+-activated K+ (BK) channels and the inward currents from Ca2-activated Cl- (Cl-Ca) channels. 3. A single Ca2+ spark elicited both phases of a STOIC, and sparks originat ing from the same site triggered STOCs, STICs and STOICs, depending on memb rane potential. 4. STOCs had a shorter time to peak (TTP) than Ca2+ sparks and a much short er half-time of decay. In contrast, STICs had a somewhat longer TTP than sp arks but the same half-time of decay. Thus, the STIC, not the STOC, more cl osely reflected the time course of cytosolic Ca2+ elevation during a Ca2+ s park. 5. These findings suggest that Cl-Ca channels and BK channels may be organi zed spatially in quite different ways in relation to points of Ca2+ release from intracellular Ca2+ stores. The results also suggest that Ca2+ sparks may have functions in smooth muscle not previously suggested, such as a sta bilizing effect on membrane potential and hence on the contractile state of the cell, or as activators of voltage-gated Ca2+ channels due to depolariz ation mediated by STICs.