Spontaneous sarcoplasmic reticulum calcium release in rat and rabbit cardiac muscle: Relation to transient and rested-state twitch tension

Scattered light intensity fluctuations (SLIF) (which monitor spontaneous Ca²⁺ release from the sarcoplasmic reticulum [SR] and resting and twitch tension were measured during intervals after stimulation in rat and rabbit papillary muscles. For 1 to 5 seconds after stimulation of rat muscle bathed in 1.5 mM [Ca²⁺] (Ca₀), twitch and resting tension are depressed and SLIF are transiently abolished. SLIF and resting tension then recover simultaneously and monotonically but lag behind the restitution of twitch tension. In the absence of further stimulation, SLIF persist and the rested state twitch amplitude remains potentiated. When Ca₀ is increased above 2.5 mM, the restitution of all parameters following stimulation is accelerated and becomes oscillatory; the lag of SLIF and resting tension restitution behind that of the twitch increases such that twitch amplitude increases, overshoots, and decreases to a nadir as SLIF and resting tension reach their initial maximum. In a given muscle, the maximum twitch amplitude occurs at approximately the same level of SLIF; when this level is exceeded, either transiently during monotonic or oscillatory recovery after stimulation in a given Ca₀ or in the steady rested state by an increase in Ca₀, twitch tension decreases. Ryanodine (1 μM), caffeine (10 mM), or replacement of Ca₀ with strontium abolishes SLIF and causes twitch amplitude to decay with rest. In contrast to rat, twitch amplitude in rabbit muscle bathed in physiological Ca₀ decays with rest and SLIF are nonmeasurable at any interval following stimulation. When Ca₀ is increased to 20 mM during rest, SLIF occur and the rest decay of the twitch is abolished. We interpret the parallel behavior of SLIF and rest potentiation to indicate that in the presence of SLIF, the average SR Ca²⁺ load within the tissue is high. Depolarization of a tissue exhibiting SLIF causes a large twitch but also a transient depletion of the average SR Ca²⁺ load. That the restitution of SLIF lags behind recovery of twitch amplitude suggests that the onset of spontaneous SR Ca²⁺ release requires a delay following SR Ca²⁺ replenishment. The simultaneous occurrence of spontaneous Ca²⁺ release in a sufficient number of cells places an upper limit on twitch amplitude either during recovery following stimulation or at rest.