CANAL-OTOLITH INTERACTIONS IN THE SQUIRREL-MONKEY VESTIBULOOCULAR REFLEX AND THE INFLUENCE OF FIXATION DISTANCE

Natural head movements include angular and linear components of motion . Two classes of vestibuloocular reflex (VOR), mediated by the semicir cular canals and otoliths (the angular and linear VOR, or AVOR and LVO R, respectively), compensate for head movements and help maintain bino cular fixation on targets in space. In this study, AVOR/LVOR interacti ons were quantified during complex head motion over a broad range of f ixation distances at a fixed stimulus frequency of 4.0 Hz. Binocular e ye movements were recorded (search-coil technique) in squirrel monkeys while fixation distance (assessed by vergence) was varied using brief presentations of earth-fixed targets at various distances. Stimuli co nsisted of rotations around an earth-vertical axis and therefore alway s activated the AVOR. Horizontal and vertical AVORs were assessed when the head was centered over the axis of rotation and oriented upright (UP) and right-side-down (RD), respectively. AVOR gains increased slig htly with increasing vergence in darkness, as expected given the small anterior position of the eyes in the head. Combined AVOR/LVOR respons es were recorded when subjects were displaced eccentrically from the r otation axis. Eccentric rotations activated the AVOR just as when the head was centered, but added a translational stimulus which generated an LVOR component in response to interaural (IA) or dorsoventral (DV) tangential accelerations, depending on whether the head was UP or RD, respectively. When the head was eccentric and facing nose-out, the AVO R and LVOR produced ocular responses in the same plane and direction ( coplanar and synergistic), and response magnitudes increased with incr easing vergence. With the head facing nose-in, AVOR and LVOR response components were oppositely directed (coplanar and antagonistic). The A VOR dominated the response when fixation distance was far, and phase w as compensatory for head rotation. As fixation distance decreased towa rd the rotation axis, responses declined to near zero, and when fixati on distance approached even closer, the LVOR component dominated and r esponse phase inverted. The same pattern was observed for both horizon tal (head UP) and vertical (head RD) responses. The LVOR was recorded directly by rotating subjects eccentrically but in the nose-up (NU) or ientation. The AVOR then generated torsional responses to head roll, c oexistent with either horizontal or vertical LVOR responses to tangent ial acceleration when the subject was oriented head-out or right-side- out, respectively. Only the LVOR response components were modulated by vergence. A vectorial analysis of AVOR, LVOR, and combined responses supports the conclusion that AVOR and LVOR response components combine linearly during complex head motion.