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Graded Inhibitory Synaptic Transmission Between Leech Interneurons: Assessing the Roles of Two Kinetically Distinct Low-Threshold Ca Currents

Department of Biology, Emory University, Atlanta, Georgia

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

In leeches, two pairs of reciprocally inhibitory heart interneurons that form the core oscillators of the pattern-generating network for heartbeat possess both high- and low-threshold (HVA and LVA) Ca channels. LVA Ca current has two kinetically distinct components (one rapidly activating/inactivating, I_CaF, and another slowly activating/inactivating, I_CaS) that mediate graded transmission, generate plateau potentials driving burst formation, and modulate spike-mediated transmission between heart interneurons. Here we used different stimulating protocols and inorganic Ca channel blockers to separate the effects of I_CaF and I_CaS on graded synaptic transmission and determine their interaction and relative efficacy. Ca²⁺ entering by I_CaF channels is more efficacious in mediating release than that entering by I_CaS channels. The rate of Ca²⁺ entry by LVA Ca channels appears to be as critical as the amount of delivered Ca²⁺ for synaptic transmission. LVA Ca currents and associated graded transmission were selectively blocked by 1 mM Ni²⁺, leaving spike-mediated transmission unaffected. Nevertheless, 1 mM Ni²⁺ affected homosynaptic enhancement of spike-mediated transmission that depends on background Ca²⁺ provided by LVA Ca channels. Ca²⁺ provided by both I_CaF and I_CaS depletes a common pool of readily releasable synaptic vesicles. The balance between availability of vesicles and Ca²⁺ concentration and its time course determine the strength of inhibitory transmission between heart interneurons. We argue that Ca²⁺ from multichannel domains arising from I_CaF channels, clustered near but not directly associated with the release trigger, and Ca²⁺ radially diffusing from generally distributed I_CaS channels interact at common release sites to mediate graded transmission.

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