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

To investigate the effect of asymmetrical vestibular input on the perceived straight-ahead direction, we compared 7 subjects (age 59 ± 8 yrs, mean ± SD) who had chronic (> 10 mos) unilateral vestibular deafferentation with 10 age matched controls (age 61 ± 6 younger controls (age 28 ± 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 0-120°/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 ±0.5°/s that produced a whole-body offest of 15° 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° 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 (p > 0.05). In four of seven unilaterally deafferented subjects there was an ipsilesional bias of final eye position of ≥ 10°. These subjects moved both eye and manipulandum to the ipsilesional side, with the error increasing at higher stimulus velocities. For the 120°/s peak head velocity, mean ipsilesional gaze bias ranged from 10-37° and mean manipulandum bias ranged from 26-108°. Although the errors depended on velocity (p < 0.01), errors were independent of frequency (p > 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 ± 0.01 for the first 10 s of all trials and was similar in all groups (p > 0.1). Gain during the final 10 s gain averaged 0.78 ± 0.01 for control subjects, but was significantly lower at 0.70 ± 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.