EXPERIMENTAL TESTS OF A SUPERPOSITION HYPOTHESIS TO EXPLAIN THE RELATIONSHIP BETWEEN THE VESTIBULOOCULAR REFLEX AND SMOOTH PURSUIT DURING HORIZONTAL COMBINED EYE-HEAD TRACKING IN HUMANS

1. We used a modeling approach to test the hypothesis that, in humans, the smooth pursuit (SP) system provides the primary signal for canceling the vestibuloocular reflex (VOR) during combined eye-head tracking (CEHT) of a target moving smoothly in the horizontal plane. Separate models for SP and the VOR were developed. The optimal values of parameters of the two models were calculated using measured responses of four subjects to trials of SP and the visually enhanced VOR. After optimal parameter values were specified, each model generated waveforms that accurately reflected the subjects' responses to SP and vestibular stimuli. The models were then combined into a CEHT model wherein the final eye movement command signal was generated as the linear summation of the signals from the SP and VOR pathways. 2. The SP-VOR superposition hypothesis was tested using two types of CEHT stimuli, both of which involved passive rotation of subjects in a vestibular chair. The first stimulus consisted of a "chair brake" or sudden stop of the subject's head during CEHT; the visual target continued to move. The second stimulus consisted of a sudden change from the visually enhanced VOR to CEHT ("delayed target onset" paradigm); as the vestibular chair rotated past the angular position of the stationary visual stimulus, the latter started to move in synchrony with the chair. Data collected during experiments that employed these stimuli were compared quantitatively with predictions made by the CEHT model. 3. During CEHT, when the chair was suddenly and unexpectedly stopped, the eye promptly began to move in the orbit to track the moving target. Initially, gaze velocity did not completely match target velocity, however; this finally occurred approximately 100 ms after the brake onset. The model did predict the prompt onset of eye-in-orbit motion after the brake, but it did not predict that gaze velocity would initially be only approximately 70% of target velocity. One possible explanation for this discrepancy is that VOR gain can be dynamically modulated and, during sustained CEHT, it may assume a lower value. Consequently, during CEHT, a smaller-amplitude SP signal would be needed to cancel the lower-gain VOR. This reduction of the SP signal could account for the attenuated tracking response observed immediately after the brake. We found evidence for the dynamic modulation of VOR gain by noting differences in responses to the onset and offset of head rotation in trials of the visually enhanced VOR. 4. If, during the visually enhanced VOR, the visual target suddenly began to move in synchrony with the head ("delayed target onset" paradigm), eye velocity in the head was sustained for approximately 130 ms (compensatory for the head motion and in the opposite direction of target motion) and then declined to zero, after which gaze velocity matched target velocity. The model accurately predicted the transition from the visually enhanced VOR to CEHT, with the dynamics of CEHT onset being similar to SP onset; however, the latency of onset of CEHT was somewhat shorter than that predicted by the model. Sections of eye velocity waveforms after, but not before, the onset of target motion exhibited "ringing" similar to that observed with SP onset. These results suggest that SP is activated only while tracking a moving target and that when subjects view a stationary target the VOR is supplemented by other visual mechanisms with simpler dynamics. 5. We conclude that a linear superposition of SP and VOR signals accounts for most, but not all, aspects of CEHT during passive rotation of subjects in a vestibular chair. We postulate that a parametric adjustment of the VOR, consisting of a reduction of gain, contributes to CEHT behavior.