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Cerebral Cortex Advance Access published online on October 26, 2006
Cerebral Cortex, doi:10.1093/cercor/bhl104
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© 2006 The Authors This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.0/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Article

Extensive Overlap of µ-Opioid and Nicotinic Sensitivity in Cortical Interneurons

Isabelle Férézou 1, Elisa L. Hill 1, Bruno Cauli 1, Nathalie Gibelin 1, Takeshi Kaneko 2, Jean Rossier 1, and Bertrand Lambolez 1 *

1 Laboratoire de Neurobiologie et Diversité Cellulaire, CNRS UMR 7637, École Supérieure de Physique et de Chimie Industrielles, 75005 Paris, France
2 Department of Morphological Brain Science, Graduate School of Medicine, Kyoto University, Kyoto 606-8501, Japan

* To whom correspondence should be addressed.
Bertrand Lambolez, E-mail: bertrand.lambolez{at}snv.jussieu.fr


  Abstract

We studied µ-opioid transmission in acute slices of rat neocortex using whole-cell recordings and single-cell reverse transcription-polymerase chain reaction. The µ-opioid receptor (MOR) was found in {gamma}-aminobutyric acidergic (GABAergic) interneurons that were either layer I cells frequently expressing neuropeptide Y or layers II-V cells expressing vasoactive intestinal peptide and enkephalin (Enk). We found that µ-opioid agonists inhibit these interneurons that are selectively excited by nicotinic agonists. The extensive overlap of µ-opioid and nicotinic responsiveness allowed µ-opioid agonists to inhibit nicotinic excitation of responsive interneurons and of their GABAergic output onto pyramidal cells. Finally, nicotinic stimulation resulted in a dynamic sequence where GABAergic transmission was first enhanced and then depressed below its baseline. This latter disinhibitory effect was prevented by a µ-opioid antagonist, indicating that excitation of nicotinic-responsive interneurons induced the release of endogenous Enk, which in turn led to MOR activation. Our results suggest that neocortical µ-opioid transmission acts as an inhibitory feedback onto nicotinic-responsive interneurons, which may change network excitability and inhibition patterns during cholinergic excitation.

Keywords: enkephalin; GABAergic interneuron; µ-opioid receptor; neocortex; nicotinic receptor.
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