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J Neurophysiol 88: 1318-1327, 2002;
0022-3077/02 $5.00
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The Journal of Neurophysiology Vol. 88 No. 3 September 2002, pp. 1318-1327
Copyright ©2002 by the American Physiological Society

Two Types of Nicotinic Receptors Mediate an Excitation of Neocortical Layer I Interneurons

Elodie Christophe,1 Aline Roebuck,2 Jochen F. Staiger,3 Daniel J. Lavery,2 Serge Charpak,1 and Etienne Audinat1

 1Laboratoire de Neurophysiologie, Institut National de la Santé et de la Recherche Médicale EPI 0002, ESPCI, 75231 Paris Cedex 5, France;  2GlaxoSmithKline SA, Institut de Biologie Cellulaire et de Morphologie, 1005 Lausanne, Switzerland; and  3Heinrich-Heine University, C & O Vogt-Institute for Brain Research, D-40001 Dusseldorf, Germany

Christophe, Elodie, Aline Roebuck, Jochen F. Staiger, Daniel J. Lavery, Serge Charpak, and Etienne Audinat. Two Types of Nicotinic Receptors Mediate an Excitation of Neocortical Layer I Interneurons. J. Neurophysiol. 88: 1318-1327, 2002. Nicotinic acetylcholine receptors are widely expressed in the neocortex but their functional roles remain largely unknown. Here we investigated the effect of nicotinic receptor activation on interneurons of layer I, which contains a high density of cholinergic fiber terminals. Ninety-seven of 101 neurons recorded in whole cell configuration in rat acute slices were excited by local pressure application of nicotinic agonists, acetylcholine (500 µM), 1,1-dimethyl-4-phenyl-piperazinium (500 µM) or choline (10 mM). Biocytin labeling confirmed that our sample included different morphological types of layer I interneurons. The responses to nicotinic agonists persisted in presence of glutamate and muscarinic receptor antagonists and on further addition of Cd2+ or tetrodotoxin, indicating that they were mediated by direct activation of postsynaptic nicotinic receptors. The kinetics of the currents and their sensitivity to nicotinic receptor antagonists, methyllycaconitine (1-10 nM) or dihydro-beta -erythroidine (500 nM), suggested that early and late components of the responses were mediated by alpha 7 and non-alpha 7 types of receptors. Both components had inwardly rectifying I-V curves, which differed when intracellular spermine was omitted. Single-cell RT-PCR experiments identified alpha 4, alpha 7, and beta 2 as the predominantly expressed mRNAs, suggesting that the receptors consisted of alpha 7 homomers and alpha 4beta 2 heteromers. Finally, selective excitation of layer I interneurons through activation of their nicotinic receptors resulted in a tetrodotoxin-sensitive increase of inhibitory synaptic currents recorded in nonpyramidal cells but not in pyramidal cells of layer II/III. These results suggest that acetylcholine released in layer I may induce a disinhibition of the cortical network through activation of nicotinic receptors expressed by layer I interneurons.




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