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J Neurophysiol 94: 3893-3902, 2005. First published August 17, 2005; doi:10.1152/jn.00211.2005
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Nicotinic Acetylcholine Receptor Subtypes Involved in Facilitation of GABAergic Inhibition in Mouse Superficial Superior Colliculus

Toshiaki Endo1, Yuchio Yanagawa2,3,4, Kunihiko Obata5 and Tadashi Isa1,3,6

1Department of Developmental Physiology, National Institute for Physiological Sciences, Myodaiji, Okazaki; 2Department of Genetic and Behavioral Neuroscience, Gunma University Graduate School of Medicine, Maebashi; 3Core Research for Evolutional Science and Technology and 4Solution Oriented Research for Science and Technology of the Japan Science and Technology Corporation, Kawaguchi; 5Neuronal Circuit Mechanisms Research Group, RIKEN Brain Science Institute, Wako; and 6The Graduate University for Advanced Studies, Hayama, Kanagawa, Japan

Submitted 28 February 2005; accepted in final form 10 August 2005

The superficial superior colliculus (sSC) is a key station in the sensory processing related to visual salience. The sSC receives cholinergic projections from the parabigeminal nucleus, and previous studies have revealed the presence of several different nicotinic acetylcholine receptor (nAChR) subunits in the sSC. In this study, to clarify the role of the cholinergic inputs to the sSC, we examined current responses induced by ACh in GABAergic and non-GABAergic sSC neurons using in vitro slice preparations obtained from glutamate decarboxylase 67-green fluorescent protein (GFP) knock-in mice in which GFP is specifically expressed in GABAergic neurons. Brief air pressure application of acetylcholine (ACh) elicited nicotinic inward current responses in both GABAergic and non-GABAergic neurons. The inward current responses in the GABAergic neurons were highly sensitive to a selective antagonist for {alpha}3{beta}2- and {alpha}6{beta}2-containing receptors, {alpha}-conotoxin MII ({alpha}CtxMII). A subset of these neurons exhibited a faster {alpha}-bungarotoxin-sensitive inward current component, indicating the expression of {alpha}7-containing nAChRs. We also found that the activation of presynaptic nAChRs induced release of GABA, which elicited a burst of miniature inhibitory postsynaptic currents mediated by GABAA receptors in non-GABAergic neurons. This ACh-induced GABA release was mediated mainly by {alpha}CtxMII-sensitive nAChRs and resulted from the activation of voltage-dependent calcium channels. Morphological analysis revealed that recorded GFP-positive neurons are interneurons and GFP-negative neurons include projection neurons. These findings suggest that nAChRs are involved in the regulation of GABAergic inhibition and modulate visual processing in the sSC.

Address for reprint requests and other correspondence: T. Endo, Dept. of Developmental Physiology, National Institute for Physiological Sciences, Myodaiji, Okazaki 444-8585, Japan (E-mail: tendo{at}nips.ac.jp)




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