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Spike-Mediated and Graded Inhibitory Synaptic Transmission Between Leech Interneurons: Evidence for Shared Release Sites

Department of Biology, Emory University, Atlanta, Georgia

Submitted 17 October 2005; accepted in final form 29 March 2006

Inhibitory synaptic transmission between leech heart interneurons consist of two components: graded, gated by Ca²⁺ entering by low-threshold [low-voltage–activated (LVA)] Ca channels and spike-mediated, gated by Ca²⁺ entering by high-threshold [high-voltage–activated (HVA)] Ca channels. Changes in presynaptic background Ca²⁺ produced by Ca²⁺ influx through LVA channels modulate spike-mediated transmission, suggesting LVA channels have access to release sites controlled by HVA channels. Here we explore whether spike-mediated and graded transmission can use the same release sites and thus how Ca²⁺ influx by HVA and LVA Ca channels might interact to evoke neurotransmitter release. We recorded pre- and postsynaptic currents from voltage-clamped heart interneurons bathed in 0 mM Na⁺/5 mM Ca²⁺ saline. Using different stimulating paradigms and inorganic Ca channel blockers, we show that strong graded synaptic transmission can occlude high-threshold/spike-mediated synaptic transmission when evoked simultaneously. Suppression of LVA Ca currents diminishes graded release and concomitantly increases the ability of Ca²⁺ entering by HVA channels to release transmitter. Uncaging of Ca chelator corroborates that graded release occludes spike-mediated transmission. Our results indicate that both graded and spike-mediated synaptic transmission depend on the same readily releasable pool of synaptic vesicles. Thus Ca²⁺, entering cells through different Ca channels (LVA and HVA), acts to gate release of the same synaptic vesicles. The data argue for a closer location of HVA Ca channels to release sites than LVA Ca channels. The results are summarized in a conceptual model of a heart interneuron release site.

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