Torsional dynamics and cross-coupling in the human vestibulo-ocular reflex during active head rotation

Six subjects fixated an imagined space-fixed target in darkness, or a visible target against a structured visual background, while rotating their heads actively in yaw, pitch and roll at four different frequencies, from 0.3 to 2.4 Hz. We used search coils to measure the 3-dimensional rotations of the head and eye, and described the relation between them--the input-output function of the rotational vestibulo-ocular reflex (VOR)--using gain matrices. We found consistent cross-coupling in which torsional head rotation evoked horizontal eye rotation. The reason may be that the eyes are above the axis of torsional head rotation, and therefore may translate horizontally during the head motion, so the VOR rotates them horizontally to compensate. Torsional gain was lower than horizontal or vertical, more variable from subject to subject and decreased at low frequencies. One reason for the low gain may be that torsional head rotation produces little retinal slip near the fovea; hence little compensatory eye motion is needed, and so the VOR reduces its torsional gain to save energy or to approximate Listing's law by keeping ocular torsion near zero. In addition, the human VOR has little experience with purely torsional head rotations and so its adaptive networks may be poorly trained for such stimuli. The drop in torsional gain at low frequencies can be explained based on the leak in the neural integrator that helps convert torsional eye-velocity commands into eye-position commands.