INTERACTION OF SMOOTH-PURSUIT AND THE VESTIBULOOCULAR REFLEX IN 3 DIMENSIONS

1. What is the neural mechanism of vestibuloocular reflex (VOR) cancel lation when a subject fixates a target moving with the head? One theor y is that the moving target evokes pursuit eye movements that add to a nd cancel the VOR. A recent finding with implications for this theory is that eye velocity vectors of both pursuit and the VOR vary with eye position, but in different ways, because pursuit follows Listing's la w whereas the VOR obeys a ''half-Listing'' strategy. As a result, purs uit cannot exactly cancel the VOR in most eye positions, and so the pu rsuit superposition theory predicts an eye-position-dependent pattern of residual eye velocities during cancellation. To test these predicti ons, we measured eye velocity vectors in humans during VOR, pursuit, a nd cancellation in response to torsional, vertical, and horizontal sti muli with tile eyes in different positions. 2. For example. if a subje ct is rolling clockwise (CW, frequency 0.3 Hz, maximum speed 37.5 deg/ s) while looking 20 deg up, the VOR generates an eye velocity that is mainly counterclockwise (CCW), but also leftward. If we then turn on a small target light, located 20 deg up and moving with the subject, th en pursuit super position predicts that the CCW component of eye veloc ity will shrink and the horizontal component will reverse, from leftwa rd to rightward. This pattern was seen in all subjects. 3. Velocities depended on rye position in the predicted way; when subjects looked 20 dee down, instead of 20 deg up, during CW roll, the reversal of horiz ontal eye velocity went the other way, from rightward to leftward. And when gaze was 20 deg right or left, analogous reversals occurred in t he vertical eye velocity, again as predicted, 4. Analogous predictions for horizontal and vertical stimulation were also borne out by the da ta. Far example, when subjects rotated rightward while looking 20 deg up, the VOR response was leftward and CCW. When the target;light switc hed on, the torsional component of the response reversed, becoming CW. And analogous predictions far other eye positions and for vertical st imulation also held. 5. For all axes of stimulation and all eye positi ons, eye velocity during cancellation was roughly parallel with the ga ze line. This alignment is predicted by pursuit superposition and has the effect of reducing retinal image slip over the fovea. 6. The fact that the complex dependence of eye velocity on the stimulation axis an d eye position predicted by pursuit superposition was seen in all subj ects and conditions suggests strongly that the VOR indeed is canceled additively by pursuit. However, eye velocities during cancellation wer e consistently smaller than predicted. This shrinkage indicates that a second mechanism, besides pursuit superposition, attenuates eye veloc ities during cancellation. The results can be explained if VOR gain is reduced by similar to 30%, and if, in addition, pursuit is driven by retinal slip rather than reconstructed target velocity in space.