CANAL OTOLITH INTERACTIONS DRIVING VERTICAL AND HORIZONTAL EYE-MOVEMENTS IN THE SQUIRREL-MONKEY

The vestibule-ocular reflex (VOR) was studied in three squirrel monkey s subjected to rotations with the head either centered over, or displa ced eccentrically from, the axis of rotation. This was done for severa l different head orientations relative to gravity in order to determin e how canal-mediated angular (aVOR) and otolith-mediated Linear (lVOR) components of the VOR are combined to generate eye movement responses in three-dimensional space. The aVOR was stimulated in isolation by r otating the head about the axis of rotation in the upright (UP), right -side down (RD), or nose-up (NU) orientations. Horizontal and vertical aVOR responses were compensatory for head rotation over the frequency range 0.25-4.0 Hz, with mean gains near 0.9. The horizontal aVOR was relatively constant across the frequency range, while vertical aVOR ga ins increased with increasing stimulation frequency. In the NU orienta tion, compensatory torsional aVOR responses were of relatively low gai n (0.54) compared with horizontal and vertical responses, and gains re mained constant over the frequency range. When the head was displaced eccentrically, rotation provided the same angular stimuli but added li near stimulus components, due to the centripetal and tangential accele rations acting on the head. By manipulating the orientation of the hea d relative to gravity and relative to the axis of rotation, the lVOR r esponse could be combined with, or isolated from, the aVOR response. E ccentric rotation in the UP and RD orientations generated aVOR and lVO R responses which acted in the same head plane. Horizontal aVOR-lVOR i nteractions were recorded when the head was in the UP orientation and facing toward (''nose-in'') or away from (''nose-out'') the rotation a xis. Similarly, vertical responses were recorded with the head RD and in the nose-out or nose-in positions. For both horizontal and vertical responses, gains were dependent on both the frequency of stimulation and the directions and relative amplitudes of the angular and linear m otion components. When subjects were positioned nose-out, the angular and linear stimuli produced synergistic interactions, with the lVOR dr iving the eyes in the same direction as the aVOR. Gains increased with increasing frequency, consistent with an addition of broad-band aVOR and high-pass lVOR components. When subjects were nose-in, angular and linear stimuli generated eye movements in opposing directions, and ga ins declined with increasing frequency, consistent with a subtraction of the lVOR from the aVOR. This response pattern was identical for hor izontal and vertical eye movements. aVOR and lVOR interactions were al so assessed when the two components acted in orthogonal response plane s. By rotating the monkeys into the NU orientation, the aVOR acted pri marily in the roll plane, generating torsional ocular responses, while the translational (lVOR) component generated horizontal or vertical o cular responses, depending on whether the head was oriented such that linear accelerations acted along the interaural or dorsoventral axes, respectively. Horizontal and vertical lVOR responses were negligible a t 0.25 Hz and increased dramatically with increasing frequency. Compar ison of the combined responses (UP and RD orientations) with the isola ted aVOR (head-centered) and lVOR (NU orientation) responses, indicate s that these VOR components sum in a linear fashion during complex hea d motion.