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Presynaptic kainate receptors (KARs) modulate transmission between dentate granule cells and CA3 pyramidal neurons. Whether presynaptic KARs affect other synapses made by granule cell axons [mossy fibers (MFs)], on hilar mossy cells or interneurons, is not known. Nor is it known whether glutamate release from a single MF is sufficient to activate these receptors. Here, we monitor Ca(2+) in identified MF boutons traced from granule cell bodies. We show that a single action potential in a single MF activates both presynaptic KARs and Ca(2+) stores, contributing to use-dependent facilitation at MF-CA3 pyramidal cell synapses. Rapid local application of kainate to the giant MF bouton has no detectable effect on the resting Ca(2+) but facilitates action-potential-evoked Ca(2+) entry through a Ca(2+) store-dependent mechanism. Localized two-photon uncaging of the Ca(2+) store receptor ligand IP(3) directly confirms the presence of functional Ca(2+) stores at these boutons. In contrast, presynaptic Ca(2+) kinetics at MF synapses on interneurons or mossy cells are insensitive to KAR blockade, to local kainate application or to photolytic release of IP(3). Consistent with this, postsynaptic responses evoked by activation of a single MF show KAR-dependent paired-pulse facilitation in CA3 pyramidal cells, but not in interneurons or mossy cells. Thus, KAR-Ca(2+) store coupling acts as a synapse-specific, short-range autoreceptor mechanism.

Original publication

DOI

10.1523/JNEUROSCI.2932-08.2008

Type

Journal article

Journal

J Neurosci

Publication Date

03/12/2008

Volume

28

Pages

13139 - 13149

Keywords

Animals, Calcium, Calcium Signaling, Glutamic Acid, Hippocampus, Indicators and Reagents, Interneurons, Male, Mossy Fibers, Hippocampal, Neural Pathways, Neuronal Plasticity, Organ Culture Techniques, Patch-Clamp Techniques, Presynaptic Terminals, Pyramidal Cells, Rats, Receptors, Kainic Acid, Synaptic Transmission