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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-HT_3A receptor subunit was expressed selectively in a subset of GABAergic interneurons coexpressing cholecystokinin (CCK) and vasoactive intestinal peptide (VIP). The 5-HT_3B subunit was never detected, indicating that 5-HT₃Rs expressed by neocortical interneurons did not contain this subunit. In 5-HT_3A-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-HT_3A 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-HT_3A and 5-HT_3B subunits; tropisetron; EPSC; nicotinic receptor

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Copyright © 2002 Society for Neuroscience  0270-6474/02/22177389-09$05.00/0

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