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Cerebral Cortex Advance Access originally published online on October 26, 2006
Cerebral Cortex 2007 17(8):1948-1957; 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.

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

Isabelle Férézou1, Elisa L. Hill1, Bruno Cauli1, Nathalie Gibelin1, Takeshi Kaneko2, Jean Rossier1 and Bertrand Lambolez1

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

Address correspondence to Dr Bertrand Lambolez, NPA, CNRS UMR 7102, UPMC, 9 quai St Bernard, 75005 Paris, France. Email: bertrand.lambolez{at}snv.jussieu.fr.

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.

Key Words: enkephalin • GABAergic interneuron • µ-opioid receptor • neocortex • nicotinic receptor

Funding to pay the Open Access publication charges for this article was provided by Grant-in-Aid for Scientific Research on Priority Areas (Molecular Brain Science) from the Ministry of Education, Culture, Sports, Science and Technology of Japan (No. 17024055).


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