1. Do slow phase eye velocities generated by the vestibuloocular reflex (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 subjects 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. Thus, during yaw head rotation, the axis of eye rotation was roughly aligned with the head axis when the subject looked straight ahead, but tilted up when the gaze direction was up, and down when gaze was down. The 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 degrees change in the gaze direction. 3. During roll stimulation, the axis 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 degrees down, the eye rotation axis tilted 12.0 degrees up; when the gaze 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 stay 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 stay parallel with the gaze direction. When subjects looked straight ahead, 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 at explaining the above findings. The orbital mechanics hypothesis (that VOR responses change with eye position because of the changing geometry 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 the gaze line. 6. The minimum-velocity hypothesis stated that the VOR attempts to stabilize images only on the fovea, rather than the entire retina, choosing the smallest eye velocity compatible with this task. This 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 vector 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 the VOR adopts a compromise strategy halfway between optimal retinal image stabilization and perfect compliance with Listing's law (i.e., where the reflex tolerates some retinal slip to reduce deviations from Listing's law) correctly predicted all the qualitative and mean quantitative observations (averaged across the 6 subjects) in this paper. This strategy also results in a torsional VOR gain that is only one-half as strong as vertical and horizontal.
