GABAergic mechanisms for shaping transient visual responses in the mouse superior colliculus

Abstract

An object that suddenly appears in the visual field should be quickly detected and responded to because it could be beneficial or harmful. The superficial layer of the superior colliculus (sSC) is a brain structure capable of such functions, as sSC neurons exhibit sharp transient spike discharges with short latency in response to the appearance of a visual stimulus. However, how transient activity is generated in the sSC is poorly understood. Here, we show that inhibitory inputs actively shape transient activity in the sSC. Juxtacellular recordings from anesthetized mice demonstrate that almost all types of sSC neurons, which were identified by post hoc histochemistry, show transient spike discharges, i.e., ON activity, immediately after visual stimulus onset. ON activity was followed by a pause before the visual stimulus was turned off. To determine whether the pause reflected the absence of excitatory drive or inhibitory conductance, we injected depolarizing currents juxtasomally, which enabled us to observe inhibition as decreased discharges. The pause was observed even under this condition, suggesting that inhibitory input caused the pause. We further found that local application of a mixture of GABAA and GABAB receptor antagonists additively diminished the pause. These results indicate that GABAergic inputs produce transient ON responses by attenuating excitatory activity through the cooperative activation of GABAA and GABAB receptors, allowing sSC neurons to act as a saliency detector.