CALCIUM INFLUX AND RELEASE FROM INTRACELLULAR STORES CONTRIBUTE DIFFERENTIALLY TO ACTIVITY-DEPENDENT NEURONAL FACILITATION IN HERMISSENDA PHOTORECEPTORS

A series of experiments is described that elucidates the sources of Ca 2+ that contribute to activity-dependent neuronal facilitation in Herm issenda B photoreceptors during associative conditioning. In an in vit ro preparation, pairings of a 4-s light with a 3-s mechanical stimulat ion of presynaptic hair cells increased the input resistance and elici ted spike rate (i.e., excitability) of the B photoreceptors in the Her missenda eye, indicative of a Ca2+-dependent process that is analogous to associative conditioning in the intact animal. This increase in ex citability was reduced but not eliminated when hyperpolarizing current was applied to the B cell during the pairings, suggesting that voltag e-dependent influx of Ca2+ contributed only a portion of the total cal cium signal necessary for facilitation. Moreover, no increase in excit ability was observed when a comparable current-induced depolarization of the photoreceptor was substituted for light-induced depolarization. In other experiments, Ca2+-dependent inactivation of a light-induced Na+ current was used as an index of intracellular Ca2+ concentration. It was determined that light caused a large increase in intracellular Ca2+ concentration regardless of whether the photoreceptor was allowed to freely depolarize in response to light or was voltage clamped at i ts resting membrane potential. Current-induced depolarization produced a smaller increase, while presynaptic stimulation had no measurable e ffect. Intracellular injections of either heparin, an antagonist of in tracellular Ca2+ release, or EGTA, a general Ca2+ chelator, induced co mparable reductions of light-induced Ca2+ accumulation. Finally, intra cellular injections of heparin blocked the pairing-induced increases i n B cell excitability as effectively as injections of EGTA. Taken as a whole, these data suggest that Ca2+ release from intracellular stores maybe sufficient for the induction of facilitation in this preparatio n, while Ca2+ influx through voltage-dependent channels may have an ad ditive effect and provide further evidence for the ubiquitous role of Ca2+ in learning-related forms of neuronal plasticity. (C) 1996 Academ ic Press, Inc.