Adaptive plasticity in the gaze stabilizing synergy of slow and saccadic eye movements

Abstract

When a normal human subject is briefly turned in total darkness while trying to "look" at a spatially fixed target, the vestibulo-ocular reflex (VOR) produces slow-phase compensatory eye movements tending to hold the eyes on target. However, slow-phase compensation per se is generally inadequate in these circumstances. Nevertheless it has recently been found, that even in the dark, this inadequacy tends to be corrected by supplementary saccades usually acting in the compensatory direction. The present study further investigates this phenomenon by measuring the respective contributions of saccadic, slow-phase and overall net compensation in 9 subjects tested before and after 30% adaptive attenuation of VOR slow-phase gain. In each test series, subjects attempted to stabilize their gaze on a previously seen target during each of 40 brief (approximately 0.5 s) whole body rotations (40 degrees/s, 20 degrees amp) conducted in complete darkness. The adaptive experience comprised 2 h of full-field visual suppression of the VOR during sinusoidal rotation of subject and surround at 1/6 Hz and 40 degrees/s velocity amplitude. Before adaptation, the cumulative slow-phase and cumulative saccadic components produced on average 78% and 14% respectively of the ideal (100%) compensation, thus yielding an overall net compensation which was 92% of the desired value. After adaptation, the corresponding values in the same population were 53%, 18% and 71% respectively. Thus after adaptation, the combined saccadic-slow-phase response brought the final gaze position to a point in space that was systematically shifted in the direction of head rotation (i.e. undercompensation). Subjects re-exposed to 30 min of normal visual-vestibular interaction displayed a variety of recovery patterns using different combinations of slow and saccadic eye movements. However, there was a consistent "synergistic" tendency for saccadic eye movements to improve slow-phase performance, regardless of the subject's adaptive state. In one subject, compensatory saccadic eye movements corrected a consistent directional asymmetry in the slow-phase response. It is suggested that a conscious vestibular percept of self-rotation might underlie the combined saccadic-slow-phase response, and that the net under performance after adaptation might reflect attenuation of this percept relative to the actual rotational stimulus.