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

Abstract

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.

Topographic Organization of Excitatory and Inhibitory Commissural Connections in the Superior Colliculi and Their Functional Roles in Saccade Generation

“…In cases that were used for double labeling, injections of WGA conjugated to apo-HRP conjugated to gold particles (GPs) (15-nm particle size, E-Y Laboratories) was injected into the left SC (Lee et al 2001). The survival period after the GP injection was 7-28 days.…”

Regulation of Burst Activity through Presynaptic and Postsynaptic GABABReceptors in Mouse Superior Colliculus

“…Previous studies suggested that GABA C Rs expressed predominantly in SGS GABAergic neurons have a role in disinhibitory circuitry (Lee et al, 2001;Schmidt et al, 2001). We investigated the effect of muscimol, which activates GABA C Rs and inhibits specifically GABAergic neurons, on the bursts evoked under our experimental condition.…”

“…Its superficial layers [stratum griseum superficiale (SGS) and stratum opticum (SO)] receive visual information from the retina and primary visual cortex, and its deeper layers [stratum griseum intermediale (SGI) and stratum griseum profundum (SGP)] send descending motor commands to the brainstem reticular formation and spinal cord. Previous studies showed that stimulation of the superficial layers induces excitatory synaptic responses in the deeper layers in slice preparations (Lee et al, 1997(Lee et al, , 2001Isa et al, 1998;Helms et al, 2004). In particular, when the slices were treated with GABA A receptor (GABA A R) antagonists such as bicuculline or gabazine, stimulation with single current pulses of the superficial layers elicits bursting responses in deeper layer neurons including crossed tecto-reticular neurons, output neurons projecting to the brainstem gaze center (Saito and Isa, 2003;Sooksawate et al, 2005).…”

AnIn VitroStudy of Horizontal Connections in the Intermediate Layer of the Superior Colliculus

“…This cholinergic pathway reduces the level of activity of superficial layer cells (Lee et al, 2001) and may provide a spatially selective modulation of visual signals relayed to SGI. Moreover, the adjacent midbrain tegmentum contains GABAergic cells that project to the superior colliculus (Appell and Behan, 1990) and may mediate global inhibition.…”