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The Journal of Neuroscience, September 1, 2002, 22(17):7389-7397
5-HT3 Receptors Mediate Serotonergic Fast Synaptic Excitation of Neocortical Vasoactive Intestinal Peptide/Cholecystokinin Interneurons
Isabelle Férézou1, Bruno Cauli1, Elisa L. Hill1, Jean Rossier1, Edith Hamel2, and Bertrand Lambolez1 1 Laboratoire de Neurobiologie et Diversité Cellulaire, Centre National de la Recherche Scientifique, Unité Mixte de Rechérche 7637, Ecole Superieure de Physique et Chíme Industrielles de la ville de Paris, 75005 Paris, France, and 2 Complex Neural Systems Neurobiology Unit, Montreal Neurological Institute, McGill University, Montreal, Quebec, Canada H3AZB4
Neocortical neurons expressing the serotonin 5-HT3 receptor (5-HT3R) were characterized in rat acute slices by using patch-clamp recordings combined with single-cell RT-PCR and histochemical labeling. The 5-HT3A receptor subunit was expressed selectively in a subset of GABAergic interneurons coexpressing cholecystokinin (CCK) and vasoactive intestinal peptide (VIP). The 5-HT3B subunit was never detected, indicating that 5-HT3Rs expressed by neocortical interneurons did not contain this subunit. In 5-HT3A-expressing VIP/CCK interneurons, serotonin induced fast membrane potential depolarizations by activating an inward current that was blocked by the selective 5-HT3R antagonist tropisetron. Furthermore, we observed close appositions between serotonergic fibers and the dendrites and somata of 5-HT3R-expressing neurons, suggestive of possible synaptic contacts. Indeed, in interneurons exhibiting rapid excitation by serotonin, local electrical stimulations evoked fast EPSCs of large amplitude that were blocked by tropisetron. Finally, 5-HT3R-expressing neurons were also excited by a nicotinic agonist, indicating that serotonergic and cholinergic fast synaptic transmission could converge onto VIP/CCK interneurons. Our results establish a clear correlation between the presence of the 5-HT3A receptor subunit in neocortical VIP/CCK GABAergic interneurons, its functional expression, and its synaptic activation by serotonergic afferent fibers from the brainstem raphe nuclei.
Key words: neocortex; GABAergic interneurons; vasoactive intestinal peptide; cholecystokinin; single-cell RT-PCR; raphe nucleus; serotonin; 5-HT3 receptor; 5-HT3A and 5-HT3B subunits; tropisetron; EPSC; nicotinic receptor
Copyright © 2002 Society for Neuroscience 0270-6474/02/22177389-09$05.00/0
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