Vestibular-pursuit interactions: gaze-velocity and target-velocity signals in the monkey frontal eye fields

Visual information about a moving object is obtained by accurate tracking with the eyes using the smooth pursuit system, which must interact with the vestibular system during head movement. Such pursuit-vestibular interactions require calculation of gaze (i.e., eye in space) in order to match eye velocity in space to actual target velocity, using vestibular, retinal-image velocity, and eye-velocity information. To understand the role the frontal eye fields (FEFs) play in pursuit-vestibular interactions, we examined responses of pursuit-related neurons near the arcuate sulcus in head-stabilized monkeys during visual tracking tasks that dissociate eye movement in the orbit from that in space. The activity of the majority of pursuit-related neurons was related to gaze velocity. They also responded to passive body rotation in complete darkness. When the monkeys fixated the stationary target, similar modulation was observed, reflecting the velocity signal of a second test target. Muscimol infusion into the FEF pursuit areas severely impaired smooth gaze tracking. These results suggest that the region near the arcuate sulcus coordinates its various inputs to provide signals for target velocity in space and accurate gaze-velocity command during pursuit-vestibular interactions.