Asymmetry of ocular motor and perceptual vestibular processing in humans with unilateral vestibular deafferentation

Abstract

To investigate the effect of asymmetrical vestibular input on the perceived straight-ahead direction, we compared 7 subjects (age $59\pm 8$ yrs, mean ± SD) who had chronic ( $\mathrm{>}10$ mos) unilateral vestibular deafferentation with 10 age matched controls (age $61\pm 6$ younger controls (age $28\pm 7$ yrs). Despite the age difference, the two control groups performed similarly and were therefore pooled. Eye and head movements were recorded using search coils as subjects underwent 30 s trials of sinusoidal, whole body oscillation (0.4–2 Hz, peak velocities $0\text{–}{120}^{\circ }$ /s) in darkness while attempting to maintain gaze on a remembered target 5 m distant. As a control, most stimulus oscillations were randomly superimposed on an imperceptible, constant velocity of $\pm 0.5^{\circ }$ /s that produced a whole-body offest of ${15}^{\circ }$ by the end of the trial. Following oscillation, subjects remained motionless in darkness and were asked to orient both gaze and a manipulandum to the remembered target location. In control subjects, mean final gaze and manipulandum positions were within ${15}^{\circ }$ of the target for all testing conditions. There was no dependence of final gaze and manipulandum positions on the frequency or velocity of the preceding whole-body oscillations ( $\mathit{p}\mathrm{>}0.05$ ). In four of seven unilaterally deafferented subjects there was an ipsilesional bias of final eye position of $⩾{10}^{\circ }$ . These subjects moved both eye and manipulandum to the ipsilesional side, with the error increasing at higher stimulus velocities. For the ${120}^{\circ }$ /s peak head velocity, mean ipsilesional gaze bias ranged from $10\text{–}{37}^{\circ }$ and mean manipulandum bias ranged from $26\text{–}{108}^{\circ }$ . Although the errors depended on velocity $\mathit{p}\mathrm{<}0.01$ ), errors were independent of frequency ( $\mathit{p}\mathrm{>}0.1$ ). In the remaining three subjects with vestibular deafferentation, final gaze and manipulandum positions were not statistically different from controls. Early gain (eye velocity / head velocity) of the VOR averaged $0.82\pm 0.01$ for the first 10 s of all trials and was similar in all groups ( $\mathit{p}\mathrm{>}0.1$ ). Gain during the final 10 s gain averaged $0.78\pm 0.01$ for control subjects, but was significantly lower at $0.70\pm 0.01$ for unilaterally deafferented subjects, whose eye positions reached the limit of the ocular motor range. We conclude that many humans with chronic unilateral vestibular deafferentation have a large ipsilesional dynamic bias of eye position and the perceived straight ahead direction reflecting persistent asymmetry of vestibular processing.