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The Journal of Neuroscience, February 15, 2003, 23(4):1206

Modulation of Spike-Mediated Synaptic Transmission by Presynaptic Background Ca²⁺ in Leech Heart Interneurons

Andrei I. Ivanov and Ronald L. Calabrese

Biology Department, Emory University, Atlanta, Georgia 30322

At the core of the rhythmically active leech heartbeat central pattern generator are pairs of mutually inhibitory interneurons. Synaptic transmission between these interneurons consists of spike-mediated and graded components, both of which wax and wane on a cycle-by-cycle basis. Low-threshold Ca²⁺ currents gate the graded component. Ca imaging experiments indicate that these low-threshold currents are widespread in the neurons and that they contribute to neuron-wide changes in internal background Ca²⁺ concentration (Ivanov and Calabrese, 2000). During normal rhythmic activity, background Ca²⁺ concentration oscillates, and thus graded synaptic transmission waxes and wanes as the neurons move from the depolarized to the inhibited phases of their activity.

Here we show that in addition to gating graded transmitter release, the background Ca²⁺ concentration changes evoked by low-threshold Ca²⁺ currents modulate spike-mediated synaptic transmission. We develop stimulation paradigms to simulate the changes in baseline membrane potential that accompany rhythmic bursting. Using Ca imaging and electrophysiological measurements, we show that the strength of spike-mediated synaptic transmission follows the changes in background Ca²⁺ concentration that these baseline potential changes evoke and that it does not depend on previous spike activity. Moreover, we show using internal EGTA and photo-release of caged Ca²⁺ and caged Ca²⁺ chelator that changes in internal Ca²⁺ concentration modulate spike-mediated synaptic transmission. Thus activity-dependent changes in background Ca²⁺, which have been implicated in homeostatic regulation of intrinsic membrane currents and synaptic strength, may also regulate synaptic transmission in an immediate way to modulate synaptic strength cycle by cycle in rhythmically active networks.

Key words: central pattern generator; leech heart interneurons; Ca currents; presynaptic background Ca2+; synaptic transmission; short-term synaptic plasticity; photo-release of caged Ca2+/Ca2+ chelator

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Copyright © 2003 Society for Neuroscience  0270-6474/03/2341206-13$05.00/0

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