Vertical vestibulo-ocular reflex, smooth pursuit and eye-head tracking dysfunction in internuclear ophthalmoplegia

Vertical smooth eye movements were quantified by magnetic search coil oculography in 7 patients with internuclear ophthalmoplegia (INO), 4 bilateral and 3 unilateral, and compared with age-matched normal subjects. The upward and downward vestibulo-ocular reflex (VOR) had reduced gain and abnormal phase lag in both unilateral and bilateral INO during active head motion at frequencies from 0.25 to 2 Hz. The phase lag was attributed to disruption of vestibular eye velocity signals and relative preservation of eye position signals. Fixation of a stationary target enhanced smooth eye movement gain during vertical head motion but it remained subnormal. Vertical smooth pursuit gain was mildly reduced. All patients had normal gaze (eye plus head) gain when tracking with both the head and eyes despite defective cancellation of the vertical VOR; they employed high amplitude head tracking to compensate for the uncancelled VOR. Cancellation was more impaired than smooth pursuit. Dissociation between cancellation and ocular pursuit was also demonstrated by a model of VOR cancellation that uses measured pursuit gain with the head immobile to predict gaze gain of eye-head tracking. The model predicted eye-head tracking gain in normal subjects but not in patients with INO. The results indicate that the medial longitudinal fasciculi or neighbouring tegmental tracts convey bidirectional signals for vertical pursuit, cancellation, and vestibular smooth eye movements in man, and that smooth pursuit and cancellation of the VOR can be dissociated in INO.