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The Journal of Neuroscience, October 15, 2001, 21(20):8145-8153

Excitatory and Inhibitory Circuitry in the Superficial Gray Layer of the Superior Colliculus

Psyche H. Lee¹, Matthias Schmidt^{1, 2}, and William C. Hall¹

¹ Department of Neurobiology, Duke University Medical Center, Durham, North Carolina 27710, and ² Department of Zoology and Neurobiology, Ruhr-University, D-44780 Bochum, Germany

Stratum griseum superficiale (SGS) of the superior colliculus receives a dense cholinergic input from the parabigeminal nucleus. In this study, we examined in vitro the modulatory influence of acetylcholine (ACh) on the responses of SGS neurons that project to the visual thalamus in the rat. We used whole-cell patch-clamp recording to measure the responses of these projection neurons to electrical stimulation of their afferents in the stratum opticum (SO) before and during local pressure injections of ACh. These colliculothalamic projection neurons (CTNs) were identified during the in vitro experiments by prelabeling them from the thalamus with the retrograde axonal tracer wheat germ agglutinin-apo-HRP-gold. In a group of cells that included the prelabeled neurons, EPSCs evoked by SO stimulation were significantly reduced by the application of ACh, whereas IPSC amplitudes were significantly enhanced. Similar effects were observed when the nicotinic ACh receptor agonist lobeline was used. Application of the selective GABA_B receptor antagonist 3-[[(3,4-dichlorophenyl)-methyl]amino]propyl](diethoxymethyl)phosphinic acid blocked ACh-induced reduction in the evoked response. In contrast, the ACh-induced reduction was insensitive to application of the GABA_A receptor antagonist bicuculline. The ACh-induced reduction was also diminished by bath application of muscimol at the low concentrations that selectively activate GABA_C receptors. Because GABA_C receptors may be specifically expressed by GABAergic SGS interneurons (Schmidt et al., 2001), our results support the hypothesis that ACh reduces CTN activity by nicotinic receptor-mediated excitation of local GABAergic interneurons. These interneurons in turn use GABA_B receptors to inhibit the CTNs.

Key words: acetylcholine; nicotinic ACh receptors; muscarinic ACh receptors; cholinergic circuits; interneurons; patch clamp; superior colliculus

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Copyright © 2001 Society for Neuroscience  0270-6474/01/21208145-09$05.00/0

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