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The Journal of Neuroscience, July 1, 1999, 19(13):5228-5235
Selective Excitation of Subtypes of Neocortical Interneurons by
Nicotinic Receptors
James T.
Porter,
Bruno
Cauli,
Keisuke
Tsuzuki,
Bertrand
Lambolez,
Jean
Rossier, and
Etienne
Audinat
Neurobiologie et Diversité Cellulaire, Centre National de la
Recherche Scientifique, Unité Mixte de Recherche 7637, Ecole
Supérieure de Physique et de Chimie Industrielles, 75231 Paris
Cedex 05, France
The cellular mechanisms by which neuronal nicotinic cholinergic
receptors influence many aspects of physiology and pathology in the
neocortex remain primarily unknown. Whole-cell recordings and
single-cell reverse transcription (RT)-PCR were combined to analyze the
effect of nicotinic receptor agonists on different types of neurons in
acute slices of rat neocortex. Nicotinic receptor agonists had no
effect on pyramidal neurons and on most types of interneurons,
including parvalbumin-expressing fast spiking interneurons and
somatostatin-expressing interneurons, but selectively excited a
subpopulation of interneurons coexpressing the neuropeptides vasoactive
intestinal peptide (VIP) and cholecystokinin. This excitation
persisted in the presence of glutamate, GABA, and muscarinic receptor
antagonists and in the presence of tetrodotoxin and low extracellular
calcium, suggesting that the depolarization was mediated through the
direct activation of postsynaptic nicotinic receptors. The responses
were blocked by the nicotinic receptor antagonists
dihydro- -erythroidine and mecamylamine and persisted in the presence
of the 7 selective nicotinic receptor antagonist methyllycaconitine,
suggesting that the involved nicotinic receptors lacked the 7
subunit. Single-cell RT-PCR analysis indicated that the majority of the
interneurons that responded to nicotinic stimulation coexpressed the
4, 5, and 2 nicotinic receptor subunits. Therefore, these
results provide a role for non- 7 nicotinic receptors in the
selective excitation of a subpopulation of neocortical interneurons. Because the neocortical interneurons expressing VIP have been proposed
previously to regulate regional cortical blood flow and metabolism,
these results also provide a cellular basis for the neuronal regulation
of cortical blood flow mediated by acetylcholine.
Key words:
single-cell PCR; neuropeptides; calcium-binding proteins; methyllycaconitine; dihydro- -erythroidine; acetylcholine; mecamylamine
Copyright © 1999 Society for Neuroscience 0270-6474/99/19135228-08$05.00/0
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