ROTATIONAL KINEMATICS OF THE HUMAN VESTIBULOOCULAR REFLEX .3. LISTINGS LAW

1. Do slow phase eye velocities generated by the vestibuloocular refle x (VOR) depend on eye position? If the purpose of the VOR is simply to stabilize the retinal image, there can be no such dependence, because eye velocity must always be equal and opposite to head velocity. But if the VOR tolerates some retinal slip to achieve other goals, such as reducing eye velocity or following Listing's law, then one should see specific patterns of dependence. We examined VOR responses of human s ubjects to yaw, pitch, and roll rotation looking in various directions to quantify how the input-output properties of the VOR vary with eye position. 2. Eye rotation axes during yaw and pitch tilted in the same direction as the gaze line but only one-quarter as far on average. Th us, during yaw head rotation, the axis of eye rotation was roughly ali gned with the head axis when the subject looked straight ahead, but ti lted up when the gaze direction was up, and down when gaze was down. T he amount of tilt varied between subjects, but on average a 30 degrees change in eye position caused a 7.5 degrees tilt in the eye rotation axis. During pitch, the eye axis tilted right when gaze was right and left when gaze was left, also moving 7.5 degrees on average for a 30 d egrees change in the gaze direction. 3. During roll stimulation, the a xis of eye rotation tilted in the opposite direction to the gaze line, and about one-half as far. On average, when the gaze Line moved 30 de grees down, the eye rotation axis tilted 12.0 degrees up; when the gaz e moved 30 degrees left, the eye axis tilted 15.3 degrees right. 4. It is often argued that the torsional VOR is weak because head rotation about the line of sight causes little image displacement on the fovea. But the line of sight is collinear with the torsional axis only when the subject looks straight ahead. Does the ''weak axis'' of the VOR st ay collinear with the gaze line when the subject looks eccentrically? We calculated the axis of head rotation for which the VOR response is weakest and found that it does vary with eye position, but does not st ay parallel with the gaze direction. When subjects looked straight ahe ad, the weak axis was roughly collinear with the gaze line; when gaze shifted eccentrically, the weak axis shifted in the same direction but only about one-half as far. 5. We examined several hypotheses aimed a t explaining the above findings. The orbital mechanics hypothesis (tha t VOR responses change with eye position because of the changing geome try and mechanics of the extraocular muscles and other orbital tissues ) was rejected because it predicted smaller tilts of the yaw and pitch responses than were actually observed and incorrectly predicted that roll responses would be around axes tilted in the same direction as th e gaze line. 6. The minimum-velocity hypothesis stated that the VOR at tempts to stabilize images only on the fovea, rather than the entire r etina, choosing the smallest eye velocity compatible with this task. T his model predicted the qualitative tilts of the yaw, pitch, and roll responses but made large quantitative errors, predicting yaw and pitch tilts four times larger than those actually observed. 7. The Listing' s law hypothesis, in which the VOR chooses the unique eye velocity vec tor that stabilizes the foveal image while obeying Listing's law, also made the correct qualitative predictions but predicted yaw and pitch tilts twice as large as those actually observed. 8. A model in which t he VOR adopts a compromise strategy halfway between optimal retinal im age stabilization and perfect compliance with Listing's law (i.e., whe re the reflex tolerates some retinal slip to reduce deviations from Li sting's law) correctly predicted all the qualitative and mean quantita tive observations (averaged across the 6 subjects) in this paper. This strategy also results in a torsional VOR gain that is only one-half a s strong as vertical and horizontal.