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Unilateral Deafferentation and Eye Position Misdirect the Initial Vestibulo-ocular Reflex: A Model-Based Study

¹From the Department of Surgery (Division of Otolaryngology/Head and Neck Surgery), the ²Department of Ophthalmology and Jules Stein Institute, and ³Departments of Neurology, ⁴Bioengineering, and ⁵Neuroscience Interdepartmental Programs, University of California, Los Angeles, California.

PURPOSE. Orbital eye position and vestibular sensitivity have both been postulated to influence vestibulo-ocular reflex (VOR) axis direction. The interaction of these factors in unilateral vestibular deafferentation (UVD) was examined.

METHODS. Initial VOR direction and magnitude were examined in six normal human subjects and five with UVD during transient whole-body yaw at 2800 deg/s². The effect of eye position was evaluated by computing the tilt angle ratio (TAR), the ratio of change in VOR axis orientation relative to change in target direction for targets 20° up or down.

RESULTS. Gain during the initial 50 ms in UVD subjects was 0.66 ± 0.13 (mean ± SD) during contralesional, and 0.30 ± 0.16 during ipsilesional rotation, but 0.87 ± 0.02 in normal control subjects. In control subjects VOR axis direction was independent of stimulus direction. During ipsilesional rotation, subjects with UVD had a significant (P < 0.01) initial forward VOR axis tilt relative to contralesional rotation averaging 9.5 ± 4.9°, which was evident 20 ms after rotation. Initial TAR was 0.18 ± 0.08 in control subjects and 0.32 ± 0.08 in subjects with UVD. Since Listing’s Law (LL) requires 0.5 TAR, whereas a VOR axis perfectly aligned with head axis requires 0, the observed intermediate TAR implies a compromise between the two criteria. In the interval 150 to 200 ms after rotation onset, subjects with UVD had 0.21 ± 0.06 TAR during contralesional rotation and 0.50 ± 0.11 during ipsilesional rotation, suggesting late synergy between the VOR and visual pursuit.

CONCLUSIONS. A vector-based model accounts for observed axis tilt based on semicircular canal directional sensitivity and response saturation. Overall, the deviating effect of eye position on VOR axis is not influenced by UVD, but canal nonlinearity and geometric orientation account for the additional VOR axis error.