Corrective saccades in acute vestibular neuritis: studying the role of prediction with automated passively induced head impulses

Abstract

When the demands for visual stabilization during head rotations overwhelm the ability of the vestibulo-ocular reflex (VOR) to produce compensatory eye movements, the brain produces corrective saccades that bring gaze towards the fixation target, even without visual cues (covert saccades). What triggers covert saccades and what might be the role of prediction in their generation are unknown. We studied 14 subjects with acute vestibular neuritis. To minimize variability of the stimulus, head impulses were imposed using a motorized torque generator with the subject on a bite-bar. Predictable and unpredictable (timing, amplitude, direction) stimuli were compared. Distributions of covert corrective saccade latencies were analyzed with a 'LATER' (linear approach to threshold with ergodic rate) approach. On the affected side, VOR gain was higher (0.47±0.28 vs. 0.39±0.22, p<<0.001) with predictable than unpredictable head impulses, and gaze error at the end of the head movement was less (5.4±3.3 vs 6.9±3.3 deg p<<0.001). Analyzing trials with covert saccades, gaze error at saccade end was significantly less with predictable than unpredictable head impulses (4.2 ±2.8 vs 5.5 ±3.2 deg, p<<0.001). Furthermore, covert corrective saccades occurred earlier with predictable than unpredictable head impulses (140±37 vs. 153±37 ms p<<0.001). Using a LATER analysis with reciprobit plots, we were able to divide covert corrective saccades into two classes - early and late - with a break point in the range of 88-98ms. We hypothesized two rise-to-threshold decision mechanisms for triggering early and late covert corrective saccades, with the first being most engaged when stimuli are predictable.