The Orienting Reflex Reveals Behavioral States Set by Demanding Contexts: Role of the Superior Colliculus.

Sensory stimuli can trigger an orienting reflex (response) by which animals move the head to position their sensors (e.g., eyes, pinna, whiskers). Orienting responses may be important to evaluate stimuli that call for action (e.g., approach, escape, ignore), but little is known about the dynamics of orienting responses in the context of goal-directed actions. Using mice of either sex, we found that, during a signaled avoidance action, the orienting response evoked by the conditioned stimulus (CS) consisted of a fast head movement containing rotational and translational components that varied substantially as a function of the behavioral and underlying brain states of the animal set by different task contingencies. Larger CS-evoked orienting responses were associated with high-intensity auditory stimuli, failures to produce the appropriate signaled action, and behavioral states resulting from uncertain or demanding situations and the animal's ability to cope with them. As a prototypical orienting neural circuit, we confirmed that the superior colliculus controls and codes the direction of spontaneous exploratory orienting movements. In addition, superior colliculus activity correlated with CS-evoked orienting responses, and either its optogenetic inhibition or excitation potentiated CS-evoked orienting responses, which are likely generated downstream in the medulla. CS-evoked orienting responses may be a useful probe to assess behavioral and related brain states, and state-dependent modulation of orienting responses may involve the superior colliculus.