Axis of Eye Rotation Changes with Head-Pitch Orientation during Head Impulses about Earth-Vertical

The goal of this study was to assess how the axis of head rotation, Listing's law, and eye position influence the axis of eye rotation during brief, rapid head rotations. We specifically asked how the axis of eye rotation during the initial angular vestibuloocular reflex (VOR) changed when the pitch orientation of the head relative to Earth-vertical was varied, but the initial position of the eye in the orbit and the orientation of Listing's plane with respect to the head were fixed. We measured three-dimensional eye and head rotation axes in eight normal humans using the search coil technique during head-and-trunk (whole-body) and head-on-trunk (head-only) “impulses” about an Earth-vertical axis. The head was initially oriented at one of five pitch angles (30° nose down, 15° nose down, 0°, 15° nose up, 30° nose up). The fixation target was always aligned with the nasooccipital axis. Whole-body impulses were passive, unpredictable, manual, rotations with peak-amplitude of ∼20°, peak-velocity of ∼80°/s, and peak-acceleration of ∼1000°/s2. Head-only impulses were also passive, unpredictable, manual, rotations with peak-amplitude of ∼20°, peak-velocity of ∼150°/s, and peak-acceleration of ∼3000°/s2. During whole-body impulses, the axis of eye rotation tilted in the same direction, and by an amount proportional (0.51 ± 0.09), to the starting pitch head orientation (P < 0.05). This proportionality constant decreased slightly to 0.39 ± 0.08 (P < 0.05) during head-only impulses. Using the head-only impulse data, with the head pitched up, we showed that only 50% of the tilt in the axis of eye rotation could be predicted from vectorial summation of the gains (eye velocity/head velocity) obtained for rotations about the pure yaw and roll head axes. Thus, even when the orientation of Listing's plane and eye position in the orbit are fixed, the axis of eye rotation during the VOR reflects a compromise between the requirements of Listing's law and a perfectly compensatory VOR.