Neural Activity in Guinea Pig Vestibular Nuclei During Volitional Head Movements

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DESCRIPTION (provided by applicant): Voluntary rapid eye and head movements are used to shift gaze in space. Rapid eye movements are shorter in duration than head movements necessitating compensatory ocular counter-rotation during head turns in order to stabilize the retinal image and direction of gaze in space (equal to the sum of eye and head position). It is widely accepted that the vestibulo-ocular reflex (VOR) produces the compensatory eye movement. However, recently published data demonstrate that when gaze stability is a behavioral goal, guinea pigs use extra-vestibular signals (e.g., efference copy of head movement) in place of the VOR to compensate for active head movement. This response is anticipatory because it occurs with zero latency relative to the head movement. We hypothesize that the extra-vestibular signal is encoded in the vestibular nucleus and/or cerebellum from either an efference copy of the intended head movement or proprioceptive feedback related to the head movement. Since the anticipatory response must replace the VOR, the reafference that results from the active head movement must also be cancelled. We hypothesize that an internal model of the vestibular sensorium is used to transform the extra-vestibular signal into a signal that cancels the reafference. Specifically, we hypothesize a neural circuit that includes a subset of vestibular-only (VO) and eye movement sensitive (ES) neurons in the vestibular nucleus and Purkinje cells in the cerebellar flocculus perform this cancellation and produce the anticipatory eye movement. The specific aims of this proposal are designed (1) to directly test this hypothesis by recording from secondary vestibular neurons of head-unrestrained guinea pigs during passive and active head turns and (2) to refine and demonstrate the effectiveness of two novel devices: a miniature micro-drive and a 6-dof motion sensor to record single unit data and head movements in multiple dimensions from a head unrestrained animal.