Vertical eye position responses to steady-state sinusoidal fore-aft head translation in monkeys

A major function of the otolith organ is to detect linear acceleration generated by two different head conditions, dynamic linear translation and static tilt relative to gravity. To investigate these sensory functions of the otolith organ, we analyzed vertical eye position in response to steady-state sinusoidal fore-aft translation over a range of frequencies (0.5-4 Hz) and amplitudes (0.10-0.33 g) in three monkeys. Vertical vestibuloocular reflexes elicited by linear acceleration (LVORs) during sinusoidal fore-aft translation were divided into translational LVOR component and tilt LVOR component taking vertical gaze-dependent properties into account. Based on geometrical considerations, the translational LVOR component, but not the tilt LVOR component, depended on vertical gaze eccentricity. To quantify these two components, we used a V-shaped function model, plotting vertical eye sensitivities (deg/cm) against vertical gaze eccentricities (deg). The slope (deg/cm per degree) and intercept (sensitivity at zero gaze eccentricity) of this function approximately reflected the translational and tilt LVOR components, respectively. Our data show that the tilt LVOR component is independent of the reciprocal of the fixation distance (MA), whereas the translational LVOR component is almost linearly related to MA. The gain of the tilt LVOR component, characterized by low-pass dynamics, was greatest (0.36) at 0.5 Hz. Visual information clearly reduced the gain of the tilt LVOR component, by approximately 50%. There was no difference between the effects of large-field and small-spot stimuli. These findings demonstrate that steady-state sinusoidal fore-aft translation at lower frequencies stimulates the otolith organs and produces a pseudo-pitch tilt in cooperation with the gravito-inertial force and as a result elicits an ocular response equivalent to the tilt LVOR.