Role of presynaptic calcium ions and channels in synaptic facilitation and depression at the squid giant synapse.

Abstract

The roles of presynaptic Ca influx and Ca accumulation in synaptic facilitation and depression were explored at the giant synapse in the stellate ganglion of the squid. Ca currents were recorded in the presynaptic terminal, using a 3-electrode voltage clamp and blocking Na and K currents pharmacologically. The Ca influx was constant during pairs or trains of brief depolarizing pulses that elicited facilitating or depressing excitatory post-synaptic potentials [EPSP]. The relationship between Ca influx and transmitter release during brief depolarizing pulses of varying amplitude resembled a power function with exponent of about 2. Presynaptic Ca concentration transients were measured by injecting the dye arsenazo III and detecting absorbance changes microspectrophotometrically. Increments in intracellular free Ca accompanying single action potentials appeared constant for repeated action potentials that elicited facilitating EPSP. The presynaptic Ca concentration remains elevated for several seconds following action potentials. Presynaptic injection of Ca2+ by interbarrel ion-tophoresis evokes a post-synaptic depolarization apparently reflecting a large increase in miniature EPSP frequency. Presynaptic action potentials remain unaffected by this treatment, but EPSP triggered by them are facilitated for several seconds, and then depressed. Results are consistent with the hypothesis that synaptic facilitation is due to the action of residual Ca or a Ca complex remaining in the presynaptic terminal after electrical activity. The late depression of release during Ca injection may be a result of the continual release of transmitter and consequent depletion of a presynaptic store.