Silent calcium channels in skeletal muscle fibers of the crustacean Atya lanipes

The superficial (tonic) abdominal flexor muscles of Atya lanipes do not gen erate Ca2+ action potentials when depolarized and have no detectable inward Ca2+ current. These fibers, however, are strictly dependent on Ca2+ influx for contraction, suggesting that they depend on Ca2+-induced Ca2+ release for contractile activation. The nature of the communication between Ca2+ ch annels in the sarcolemmal/tubular membrane and Ca2+ release channels in the sarcoplasmic reticulum in this crustacean muscle was investigated. The eff ects of dihydropyridines on tension generation and the passive electrical r esponse were examined in current-clamped fibers: Bay K 8644 enhanced tensio n about 100% but did not alter the passive electrical response; nifedipine inhibited tension by about 70%. Sr2+ and Ba2+ action potentials could be el icited in Ca2+-free solutions. The spikes generated by these divalent catio ns were abolished by nifedipine. As the Sr2+ Or Ba2+ concentrations were in creased, the amplitudes of the action potentials and their maximum rate of rise, V-max, increased and tended towards saturation. Three-microelectrode voltage-clamp experiments showed that even at high (138 mM) extracellular C a2+ concentration the channels were silent, i.e., no inward Ca2+ current wa s detected. In Ca2+-free solutions, inward currents carried by 138 mM Sr2or Ba2+ were observed. The currents activated at voltages above -40 mV and peaked at about 0 mV. This voltage-activation profile and the sensitivity o f the channels to dihydropyridines indicate that they resemble L-type Ca2channels. Peak inward current density values were low, ca. -33 mu A/cm(2) f or Sr2+ and -14 mu A/cm(2) for Ba2+, suggesting that Ca2+ channels are pres ent at a very low density. It is concluded that Ca2+-induced Ca2+ release i n this crustacean muscle operates with an unusually high gain: Ca2+ influx through the silent Ca2+ channels is too low to generate a macroscopic inwar d current, but increases sufficiently the local concentration of Ca2+ in th e immediate vicinity of the sarcoplasmic reticulum Ca2+ release channels to trigger the highly amplified release of Ca2+ required for tension generati on.