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Volume 17, Number 19, Issue of October 1, 1997 pp. 7404-7414
Copyright ©1997 Society for Neuroscience

All-or-None Ca²⁺ Release from Intracellular Stores Triggered by Ca²⁺ Influx through Voltage-Gated Ca²⁺ Channels in Rat Sensory Neurons

Received May 12, 1997; revised July 21, 1997; accepted July 23, 1997.

Yuriy M. Usachev and Stanley A. Thayer

Department of Pharmacology, University of Minnesota Medical School, Minneapolis, Minnesota 55455

Ca²⁺-induced Ca²⁺ release (CICR) from intracellular stores amplifies the Ca²⁺ signal that results from depolarization. In neurons, the amplification has been described as a graded process. Here we show that regenerative CICR develops as an all-or-none event in cultured rat dorsal root ganglion neurons in which ryanodine receptors have been sensitized to Ca²⁺ by caffeine. We used indo-1-based microfluorimetry in combination with whole-cell patch-clamp recording to characterize the relationship between Ca²⁺ influx and Ca²⁺ release. Regenerative release of Ca²⁺ was triggered when action potential-induced Ca²⁺ influx increased the intracellular Ca²⁺ concentration ([Ca²⁺]_i) above threshold. The threshold was modulated by caffeine and intraluminal Ca²⁺. A relative refractory period followed CICR. The pharmacological profile of the response was consistent with Ca²⁺ influx through voltage-gated Ca²⁺ channels triggering release from ryanodine-sensitive stores. The activation of a suprathreshold response increased more than fivefold the amplitude and duration of the [Ca²⁺]_i transient. The switch to a suprathreshold response was regulated very precisely in that addition of a single action potential to the stimulus train was sufficient for this transformation. Confocal imaging experiments showed that CICR facilitated propagation of the Ca²⁺ signal from the plasmalemma to the nucleus. This all-or-none reaction may serve as a switch that determines whether a given electrical signal will be transduced into a local or widespread increase in [Ca²⁺]_i.

Key words: Ca²⁺-induced Ca²⁺ release; ryanodine receptors; dorsal root ganglion; intracellular Ca²⁺; Ca²⁺ stores; voltage-gated Ca²⁺ channels; nucleoplasmic Ca²⁺

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