The ventral posterior lateral thalamus preferentially encodes externally applied versus active movement: Implications for self-motion perception

Successful interaction with our environment requires that voluntary behaviors be precisely coordinated with our perception of self-motion. The vestibular sensors in the inner ear detect self-motion and in turn send projections via the vestibular nuclei to multiple cortical areas through 2 principal thalamocortical pathways, 1 anterior and 1 posterior. While the anterior pathway has been extensively studied, the role of the posterior pathway is not well understood. Accordingly, here we recorded responses from individual neurons in the ventral posterior lateral thalamus of macaque monkeys during externally applied (passive) and actively generated self-motion. The sensory responses of neurons that robustly encoded passive rotations and translations were canceled during comparable voluntary movement (~80% reduction). Moreover, when both passive and active self-motion were experienced simultaneously, neurons selectively encoded the detailed time course of the passive component. To examine the mechanism underlying the selective elimination of vestibular sensitivity to active motion, we experimentally controlled correspondence between intended and actual head movement. We found that suppression only occurred if the actual sensory consequences of motion matched the motor-based expectation. Together, our findings demonstrate that the posterior thalamocortical vestibular pathway selectively encodes unexpected motion, thereby providing a neural correlate for ensuring perceptual stability during active versus externally generated motion.