Signal processing by vestibular nuclei neurons is dependent on the current behavioral goal

The vestibular sensory apparatus and associated vestibular nuclei are generally thought to encode angular head velocity during our daily activities. However, in addition to direct inputs from vestibular afferents, the vestibular nuclei receive substantial projections from cortical, cerebellar, and other brainstem structures. Given this diversity of inputs, the question arises: How are the responses of vestibular nuclei neurons to head velocity modified by these additional inputs during naturally occurring behaviors? Here we have focused on the signal processing done by two specific classes of neurons in the vestibular nuclei: (1) position-vestibular-pause (PVP) neurons that mediate the vestibulo-ocular reflex (VOR), and (2) vestibular-only (VO) neurons that are thought to mediate, at least in part, the vestibulo-collic reflex (VCR). We first characterized neuronal responses to passive rotation in the head-restrained condition, and then released the head to record the discharges of the same neurons during self-generated head movements. VOR interneurons (i.e., PVP neurons) faithfully transmitted head velocity signals when the animal stabilized its gaze, regardless of whether the head motion was actively or passively generated; their responses were attenuated only when the monkey's behavioral goal was to redirect its axis of gaze relative to space. In contrast, VCR interneurons (i.e., VO neurons) faithfully transmitted head velocity signals during passive head motion, but their responses were greatly (and similarly) attenuated during all behaviors (i.e., gaze shifts, gaze pursuit, gaze stabilization) during which the monkey's behavioral goal was to move its head relative to the body. To characterize the mechanism(s) that underlie this differential processing, we tested neurons during passive rotation of the head relative to the body, as well as during a task in which a monkey actively "drove" both its head and body together in space. We conclude that neither passive activation of neck proprioceptors nor knowledge of self-generated head-in-space motion directly mediate the observed reductions in head-velocity-related modulation. Instead, we propose that the VOR and VCR pathways use efference copies of oculomotor and neck movement commands, respectively, for the differential processing of vestibular information.