Ca²⁺-activated K current in the ARC muscle of Aplysia

1. This work continues our examination of the electrophysiology and contractions of single, functionally intact fibers dissociated from a widely studied molluscan muscle, the accessory radula closer (ARC) muscle of Aplysia californica, aimed at understanding its excitation-contraction mechanisms and their modulation. Extensive previous work has characterized a number of ion currents in the fibers. 2. Here we describe an additional major current that could not be studied earlier because, unlike all of the other currents in the ARC muscle fibers, it becomes prominent only during contraction of the fiber. It is a Ca²⁺-activated K current, associated with contraction most likely because both are activated by the same elevation in intracellular free Ca²⁺. 3. We used several manipulations to elicit the Ca²⁺-activated K current and contraction: depolarizing voltage steps in the presence of extracellular Ca²⁺, application of caffeine in the presence or absence of extracellular Ca²⁺ (and thus presumably working by releasing Ca²⁺ from intracellular stores), application of the Ca²⁺-ionophore A23187, and direct iontophoretic injection of Ca²⁺ into the fiber. 4. The Ca²⁺-activated K current reversed around -70 mV, not far from E(K), and the reversal potential shifted substantially with elevated extracellular K⁺. Activation of the current was not only Ca²⁺ dependent, but also quite strongly voltage dependent, promoted by depolarization. The current was well blocked by tetraethylammonium (K(D) ≃ 2 mM), but not blocked by even 10 mM 4- aminopyridine or low concentrations of the K-current blocking toxins charybdotoxin and apamin. 5. After a depolarizing voltage step in Ca²⁺- containing solution, the Ca²⁺-activated K current appeared, often with some delay, as a large peak of current that soon disintegrated into a prolonged period of individual oscillatory transients of Ca²⁺-activated K current, sometimes correlated with transient contractions. Similar transients could be elicited by caffeine or iontophoretic Ca²⁺ injection. More extensive study of the underlying Ca²⁺ dynamics will be presented elsewhere, but we interpret these phenomena in terms of our hypothesis that the ARC muscle generates both contraction and the Ca²⁺-activated K current by Ca²⁺- induced Ca²⁺ release (CICR), in which a small depolarization-induced influx of extracellular Ca²⁺ releases more Ca²⁺ from intracellular stores. 6. The Ca²⁺-activated K current is significant in the physiological operating voltage range of the ARC muscle, and its predicted hyperpolarizing action and consequent negative-feedback depression of contractions is likely to be an important pan of the integrated set of mechanisms that regulate the muscle's contractility.