Excitatory and inhibitory circuitry in the superficial gray layer of the superior colliculus

Stratum griseum superficiale (SGS) of the superior colliculus receives a de nse cholinergic input from the parabigeminal nucleus. In this study, we exa mined in vitro the modulatory influence of acetylcholine (ACh) on the respo nses 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 project ion neurons to electrical stimulation of their afferents in the stratum opt icum (SO) before and during local pressure injections of ACh. These collicu lothalamic projection neurons (CTNs) were identified during the in vitro ex periments by prelabeling them from the thalamus with the retrograde axonal tracer wheat germ agglutinin-apo-HRP-gold. In a group of cells that include d the prelabeled neurons, EPSCs evoked by SO stimulation were significantly reduced by the application of ACh, whereas IPSC amplitudes were significan tly enhanced. Similar effects were observed when the nicotinic ACh receptor agonist lobeline was used. Application of the selective GABA(B) receptor a ntagonist 3-[[(3,4-dichlorophenyl)-methyl]amino]propyl]( diethoxymethyl)pho sphinic acid blocked ACh-induced reduction in the evoked response. In contr ast, the ACh-induced reduction was insensitive to application of the GABA(A ) receptor antagonist bicuculline. The ACh-induced reduction was also dimin ished by bath application of muscimol at the low concentrations that select ively activate GABA(C) receptors. Because GABA(C) receptors may be specific ally expressed by GABAergic SGS interneurons (Schmidt et al., 2001), our re sults support the hypothesis that ACh reduces CTN activity by nicotinic rec eptor-mediated excitation of local GABAergic interneurons. These interneuro ns in turn use GABA(B) receptors to inhibit the CTNs.