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The Journal of Neuroscience, January 26, 2005, 25(4):990-1001; doi:10.1523/JNEUROSCI.4388-04.2005

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Cellular/Molecular
Differential Regulation of Metabotropic Glutamate Receptor- and AMPA Receptor-Mediated Dendritic Ca²⁺ Signals by Presynaptic and Postsynaptic Activity in Hippocampal Interneurons

Lisa Topolnik, Patrice Congar, and Jean-Claude Lacaille

Département de Physiologie, Centre de Recherche en Sciences Neurologiques, Université de Montréal, Montréal, Quebec, Canada H3C 3J7

Calcium plays a crucial role as a ubiquitous second messenger and has a key influence in many forms of synaptic plasticity in neurons. The spatiotemporal properties of dendritic Ca²⁺ signals in hippocampal interneurons are relatively unexplored. Here we use two-photon calcium imaging and whole-cell recordings to study properties of dendritic Ca²⁺ signals mediated by different glutamate receptors and their regulation by synaptic activity in oriens/alveus (O/A) interneurons of rat hippocampus. We demonstrate that O/A interneurons express Ca²⁺-permeable AMPA receptors (CP-AMPARs) providing fast Ca²⁺ signals. O/A cells can also coexpress CP-AMPARs, Ca²⁺-impermeable AMPARs (CI-AMPARs), and group I/II metabotropic glutamate receptors (mGluRs) (including mGluR1a), in the same cell. CI-AMPARs are often associated with mGluRs, resulting in longer-lasting Ca²⁺ signals than CP-AMPAR-mediated responses. Finally, CP-AMPAR- and mGluR-mediated Ca²⁺ signals demonstrate distinct voltage dependence and are differentially regulated by presynaptic and postsynaptic activity: weak synaptic stimulation produces Ca²⁺ signals mediated by CP-AMPARs, whereas stronger stimulation, or weak stimulation coupled with postsynaptic depolarization, recruits Ca²⁺ signals mediated by mGluRs. Our results suggest that differential activation of specific glutamate receptor-mediated Ca²⁺ signals within spatially restricted dendritic microdomains may serve distinct signaling functions and endow oriens/alveus interneurons with multiple forms of Ca²⁺-mediated synaptic plasticity. Specific activation of mGluR-mediated Ca²⁺ signals by coincident presynaptic and postsynaptic activity fulfills the conditions for Hebbian pairing and likely underlies their important role in long-term potentiation induction at O/A interneuron synapses.

Key words: Ca²⁺-permeable AMPA receptor; group I mGluR; Ca²⁺ microdomains; synaptic Ca²⁺ signals; two-photon confocal imaging; dendritic microdomains

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Received July 15, 2004; revised November 30, 2004; accepted December 2, 2004.

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