The joint representation of self-motion and touch in superior colliculus neurons supporting active sensation

Localizing objects using active sensing requires the brain to integrate a map sensory space against an ongoing estimate of body position. While such computations are often ascribed to the cerebral cortex, we examined the midbrain superior colliculus (SC), due to its close relationship with the sensory periphery as well as higher, motor-related brain regions. Using high-density electrophysiology and movement tracking, we discovered that the on-going kinematics of whisker motion and locomotion speed accurately predict the firing rate of mouse SC neurons. Neural activity was best predicted by movements occurring either in the past, present, or future, revealing that the SC population continuously estimates a trajectory of self-motion. Neural selectivity for combinations of kinematic features built an accurate representation of whisker position with high temporal resolution. Half of all self-motion encoding neurons displayed a touch response as an object entered the active whisking field. Trial-to-trial variation in the size of this response was explained by the position of the whisker upon touch. Taken together, these data indicate that SC neurons linearly combine an internal estimate of body movements with external stimulation to enable active tactile localization.