Effects of Full-Field Visual Input on the Three-Dimensional Properties of the Human Vestibuloocular Reflex 1

The three-dimensional (3-D) properties of the vestibuloocular reflex (VOR) were studied in six normal human subjects during passive whole-body rotations in darkness and with full-field visual input in light. Subjects were asked to fixate a point target stationary in space straight ahead or to imagine such a target in darkness. Using a 3-D rotating chair, subjects were rotated sinusoidally (frequency .3 Hz, maximum speed 37.5°/s) about an earth-vertical axis for horizontal stimulation and about an earth-horizontal axis for vertical and torsional stimulation. The subject faced forward for vertical stimulation, 90° to the side for torsional stimulation, or 15° to the right or left side for combined vertical and torsional stimulation. Left eye position was measured using 3-D search coils. The VOR response was quantified using the 3-D analogue of gain, a 3 × 3 matrix where each element describes the dependence of one component – torsional, vertical, or horizontal – of eye velocity on one component of head velocity. Average gain matrices were calculated for three cycles of rotation (10 s). Major findings were: (1) Gain values for the VOR were higher in light than in darkness for all directions. In light, vertical and horizontal responses were fully compensatory in both magnitude and direction, whereas the torsional responses were still weak. (2) Intersubject variability, large in the dark, was very small in the light for the vertical and horizontal responses but still considerable for the torsional. (3) Crosscoupling, in the form of partially horizontal eye movements in response to a torsional head rotation, was present in darkness but disappeared in light. (4) The VOR showed the same eye position dependence in darkness and in light; that is, if the eye is looking x° away from straight ahead, the eye rotation axis in response to a horizontal or vertical head rotation tilts about x°/4 in the same direction as the gaze line. These axis tilts are incompatible with perfect stabilization of the retinal image, but they are qualitatively appropriate for preserving Listing’s law.