Superior colliculus supports touch-guided corrections during licking in mice

Successful actions require correcting for movement errors in real-time. When grasping an object, unexpected touches at the hand evoke rapid adjustments in grip. Touch-guided corrections require proprioceptive and mechanosensory feedback to be integrated with ongoing motor commands and transformed into an updated plan. To determine how touch events guide ongoing movements, we combined kilohertz frame-rate imaging and a deep neural network to track lingual kinematics in 3D as head-fixed mice retrieved water from a moving spout. We detected the offset of tongue-spout contact on the first lick (L1) of a lick bout and randomly displaced the spout to the left or right such that the next lick (L2) would nick the spout with the side of the tongue. Mice produced rapid nick-guided corrections: left nicks guided the third lick (L3) left, and right nicks guided L3 right. We used electrophysiology and closed-loop photoinhibition to screen cortical, midbrain, and cerebellar regions previously implicated in directional licking. Neural activity in anterolateral motor cortex (ALM) exhibited contact-related information, but surprisingly, bilateral inactivation of ALM, tongue-jaw primary motor or somatosensory cortex (TJM1, TJS1), and the fastigial nucleus of the cerebellum did not impair touch-guided corrections. Interestingly, bilateral photoinhibition of lateral superior colliculus (lSC) impaired lick kinematics to a larger degree than cortical regions, and unilateral photoinhibition of lSC, but not cortical areas, abolished contact-guided corrections to the contralateral side. Consistent with a role for touch-guided re-aiming, lSC neurons were rapidly activated by contact events on the contralateral surface of tongue. For visuomotor control, SC has been shown to have a sensorimotor map in which a novel stimulus in the contralateral visual field directs saccades to unexpected targets. Our findings suggest that the SC may have an analogous somato-sensorimotor map of tongue space for rapid adjustment of tongue kinematics during licking.