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TitleDendritic calcium nonlinearities switch the direction of synaptic plasticity in fast-spiking interneurons.
Publication TypeJournal Article
Year of Publication2014
AuthorsCamiré, Olivier, and Lisa Topolnik
JournalJ Neurosci
Volume34
Issue11
Pagination3864-77
Date Published2014 Mar 12
ISSN1529-2401
KeywordsAction Potentials, Animals, Calcium Channels, L-Type, Calcium Channels, T-Type, Calcium Signaling, Dendrites, Excitatory Postsynaptic Potentials, Female, Interneurons, Male, Mice, Mice, Inbred Strains, Models, Neurological, Neuronal Plasticity, Nonlinear Dynamics, Organ Culture Techniques, Patch-Clamp Techniques, Sodium Channels
Abstract

Postsynaptic calcium (Ca2+) nonlinearities allow neuronal coincidence detection and site-specific plasticity. Whether such events exist in dendrites of interneurons and play a role in regulation of synaptic efficacy remains unknown. Here, we used a combination of whole-cell patch-clamp recordings and two-photon Ca2+ imaging to reveal Ca2+ nonlinearities associated with synaptic integration in dendrites of mouse hippocampal CA1 fast-spiking interneurons. Local stimulation of distal dendritic branches within stratum oriens/alveus elicited fast Ca2+ transients, which showed a steep sigmoidal relationship to stimulus intensity. Supralinear Ca2+ events required Ca2+ entry through AMPA receptors with a subsequent Ca2+ release from internal stores. To investigate the functional significance of supralinear Ca2+ signals, we examined activity-dependent fluctuations in transmission efficacy triggered by Ca2+ signals of different amplitudes at excitatory synapses of interneurons. Subthreshold theta-burst stimulation (TBS) produced small amplitude postsynaptic Ca2+ transients and triggered long-term potentiation. In contrast, the suprathreshold TBS, which was associated with the generation of supralinear Ca2+ events, triggered long-term depression. Blocking group I/II metabotropic glutamate receptors (mGluRs) during suprathreshold TBS resulted in a slight reduction of supralinear Ca2+ events and induction of short-term depression. In contrast, blocking internal stores and supralinear Ca2+ signals during suprathreshold TBS switched the direction of plasticity from depression back to potentiation. These data reveal a novel type of supralinear Ca2+ events at synapses lacking the GluA2 AMPA subtype of glutamate receptors and demonstrate a general mechanism by which Ca2+ -permeable AMPA receptors, together with internal stores and mGluRs, control the direction of plasticity at interneuron excitatory synapses.

DOI10.1523/JNEUROSCI.2253-13.2014
Alternate JournalJ. Neurosci.
PubMed ID24623765
Grant List / / Canadian Institutes of Health Research / Canada