Human angular vestibulo-ocular reflex initiation: relationship to Listing's law.

An ideal vestibulo-ocular reflex (VOR) generates ocular rotations compensatory for head motion. During visually guided movements, Listing's law (LL) constrains eye rotation to axes in Listing's plane (LP). Recently, it has been reported that the VOR axis is not collinear with the rotation axis of the head, but is influenced by eye position in the orbit. Elaborate models have been proposed suggesting dynamic neural control of the VOR axis. By examining the variability and time course of changes in VOR axis orientation, we sought to test plausibility of these models. Binocular LPs were defined in eight humans. The VOR was evoked by a highly repeatable, transient, whole-body yaw rotation in darkness at peak acceleration 2800 deg/s2. Immediately prior to rotation, subjects regarded targets at eye level, 20 degrees up, or 20 degrees down. Eye and head positions were expressed in LP coordinates for comparison with LL. Eye position generally followed head position and departed LP when the head axis tilted out of LP. In the velocity domain the VOR axis tilted 28 +/- 9% of the change in vertical eye position, but there was significant intrasubject variation (14% to 41%). This roughly "quarter-angle" behavior began with the earliest detectable VOR. Given the brief latency and marked interindividual variability of the eye position dependence of the VOR rotational axis, and the small deviation of the VOR from LL in the position domain, it is speculated that this behavior is largely due to orbital mechanics interacting with the basic neural commands that initiate the VOR.