Semicircular canal afferents similarly encode active and passive head-on-body rotations: implications for the role of vestibular efference

Abstract

The vestibular receptors in the labyrinth receive innervation from centrifugally projecting efferent fibers. The influence of these efferents on information processing by vestibular afferents in primates has not been determined. One commonly held notion is that efferent activation during large-amplitude, active head movements would result in an increase in the resting discharge rate and in a reduction of the rotational sensitivity of afferents. Such an effect would increase the dynamic range of afferents involved in the encoding of head movements. To test this hypothesis, we recorded from afferents innervating the semicircular canals in alert macaques during passive head-on-body rotations and during active head movements that included gaze shifts and gaze pursuit. Extracellular, single-unit recordings were obtained from 24 afferent fibers innervating the horizontal, superior, and posterior canals. Based on the normalized coefficient of variation of the interspike interval for these units, our sample contained six regularly discharging, six intermediate, and 12 irregularly discharging afferents. Responses were analyzed using a least squares regression to determine the bias discharge rate of each unit and sensitivity to head velocity and acceleration. We found no difference in bias discharge rate or rotational sensitivity of the afferent responses for the different stimulus conditions tested. Our results indicate that semicircular canal afferents encode information about head rotation similarly for self generated and passively applied head-on-body movements.