Difference in context-dependency between orienting and defense-like responses induced by the superior colliculus

Previous electrical stimulation and lesion experiments have suggested that the crossed descending output pathway from the deeper layers (SCd) of superior colliculus (SC) controls orienting responses, while the uncrossed pathway mediates defense-like behavior. Here we extended these investigations by using selective optogenetic activation of each pathway in mice with channelrhodopsin 2 expression by double viral vector techniques. Brief photo-stimulation of the crossed pathway evoked short latency contraversive orienting-like head turns, while extended stimulation induced contraversive circling responses. In contrast, stimulation of uncrossed pathway induced short-latency upward head movements followed by longer-latency defense-like behaviors including retreat and flight. The novel discovery was that the evoked defense-like responses varied depending on the environment, suggesting that uncrossed output can be influenced by top-down modification of the SC or its downstream. This further suggests that the SCd-defense system can be profoundly modulated by non-motor, affective and cognitive components, in addition to direct sensory inputs.