Jesse H. Goldberg, PhD

Abstract

Accurate goal-directed movements require information about effector position and ongoing motion to be integrated into sensory feedback. Here, with high-speed videography, we examined three-dimensional tongue kinematics as mice re-aimed their licks by reacting to subtle tactile events on the left, center or right surface of the tongue. Because a tactile event on the left side of the tongue can specify a centered spout on right licks, or a left spout on straight licks, task performance requires a coordinate transformation from a tongue- to head-based reference frame. In past work, we showed that superior colliculus (SC) neurons encode tactile events in tongue, head, and mixed reference frames, suggesting that the SC implements a coordinate transformation necessary for touch-based re-aiming. Yet another possibility is that the SC inherits these representations from lower levels of the sensory hierarchy. To test this idea, we recorded neurons in the brainstem spinal trigeminal nucleus (SpV), the first relay center for tongue tactile inputs into the brain with projections going to SC. As expected, SpV neurons represented tactile events at low latencies (<10 ms) in a tongue-based reference frame, with a strong bias in activation from ipsilateral contacts. Yet surprisingly, SpV neurons could also represent tactile signals in mixed frames at similarly low latencies. This suggests that precise tongue position at a moment of spout contact is already incorporated into tactile feedback signals at the lowest possible level of the central sensory hierarchy. Notably, SpV signals additionally represented diverse aspects of task structure, including go cue responses, memory of spout position, and detailed lick cycle information. Our findings show that task-related information, including that necessary for a tongue-to-head based coordinate transformation, is already present at the lowest level of the central sensory hierarchy.