Does Head Rotation Contribute to Gaze Stability during Passive Translations?

Active translations of human subjects are nearly perfectly compensated by a combined rotation of both the eyes and the head. Because vestibuloocular reflex (VOR) gain is less than perfect during passive translations with near targets in head-fixed subjects, there is a possibility that the compensatory head rotation observed during natural behavior represents a vestibularly driven head reflex [translational vestibulocollic reflex (TVCR)]. The TVCR could elicit a horizontal rotation of the head during lateral linear acceleration that contributes to gaze stabilization. To investigate this hypothesis, we examined whether a horizontal rotation of the head contributes to gaze stability during passive lateral translation in rhesus monkeys whose head was free to rotate in the horizontal plane. Motion frequency was varied between 0.5 and 5 Hz while animals fixated targets at distances of 12-102 cm. We did not find evidence supporting the existence of a TVCR. Specifically, during motion at frequencies between 0.5 and 2 Hz, horizontal head rotation was negligible. During 4- and 5-Hz oscillations, there was a clear and consistent horizontal rotation of the head, but responses were always anticompensatory to gaze stabilization; that is, the head rotated in the same direction as head translation and oppositely to the direction of gaze rotation. Furthermore, there was no difference in gaze stability between the head-free and head-fixed conditions. Thus we conclude that the compensatory head rotation observed in human studies of active gaze movements could represent a strategy and/or a motor command contribution to gaze stabilization, rather than a simple vestibularly driven reflex.