The effect of binocular eye position and head rotation plane on the human torsional vestibuloocular reflex

Abstract

We examined how the gain of the torsional vestibulo-ocular reflex (VOR) (defined as the instantaneous eye velocity divided by inverted head velocity) in normal humans is affected by eye position, target distance, and the plane of head rotation. In six normal subjects we measured three-dimensional (3D) eye and head rotation axes using scleral search coils, and 6D head position using a magnetic angular and linear position measurement device, during low-amplitude (∼20°), high-velocity (∼200°/s), high-acceleration (∼4000°/s 2) rapid head rotations or ‘impulses.’ Head impulses were imposed manually and delivered in five planes: yaw (horizontal canal plane), pitch, roll, left anterior-right posterior canal plane (LARP), and right anterior-left posterior canal plane (RALP). Subjects were instructed to fix on one of six targets at eye level. Targets were either straight-ahead, 20° left or 20° right from midline, at distance 15 or 124 cm from the subject. Two subjects also looked at more eccentric targets, 30° left or 30° right from midline. We found that the vertical and horizontal VOR gains increased with the proximity of the target to the subject. Previous studies suggest that the torsional VOR gain should decrease with target proximity. We found, however, that the torsional VOR gain did not change for all planes of head rotation and for both target distances. We also found a dynamic misalignment of the vertical positions of the eyes during the torsional VOR, which was greatest during near viewing with symmetric convergence. This dynamic vertical skew during the torsional VOR arises, in part, because when the eyes are converged, the optical axes are not parallel to the naso-occipital axes around which the eyes are rotating. In five of six subjects, the average skew ranged 0.9°–2.9° and was reduced to <0.4° by a ‘torsional’ quick-phase (around the naso-occipital axis) occurring <110 ms after the onset of the impulse. We propose that the torsional quick-phase mechanism during the torsional VOR could serve at least three functions: (1) resetting the retinal meridians closer to their usual orientation in the head, (2) correcting for the ‘skew’ deviation created by misalignment between the axes around which the eyes are rotating and the line of sight, and (3) taking the eyes back toward Listing’s plane.