Eye-position dependence of three-dimensional ocular rotation-axis orientation during head impulses in humans

If horizontal saccades or smooth-pursuit eye movements are made with the li ne-of-sight at different elevations, the three-dimensional (3D) angular rot ation axis of the globe tilts by half the vertical eye eccentricity. This p henomenon is named "half-angle rule" and is a consequence of Listing's law. It was recently found that the ocular rotation axis during the horizontal vestibuloocular reflex (VOR) on a turntable also tilts in the direction of the line-of-sight by about a quarter of the eye's vertical eccentricity. Th is is surprising, since, in a "perfect" VOR, the angular rotation axis of t he eye should be independent from the position of the eye to fully compensa te for the 3D angular head rotation. We asked whether this quarter-angle st rategy is a general property of the VOR or whether the 3D kinematics of ocu lar movements evoked by vestibular stimulation would be less eye-position d ependent at higher stimulus frequencies. Nine healthy subjects were exposed to horizontal head impulses (peak velocity similar to 250 degrees/s). The line-of-sight was systematically changed along the vertical meridian of a t angent screen. Three-dimensional eye and head movements were monitored with dual search coils. The 3D orientation of the angular eye-in-head rotation axis was determined by calculating the average angular velocity vectors of the initial 10 degrees displacements. Then, the difference between the tilt angles of the ocular rotation axis during upward and downward viewing was determined and divided by the difference of vertical eccentricity ("tilt an gle coefficient"). Control experiments included horizontal saccades, smooth -pursuit eye movements, and eye movements evoked by slow, passive head rota tions at the same vertical eye eccentricities. On average, the ocular rotat ion axis during horizontal head-impulse testing at different elevations of the line-of-sight was closely aligned with the rotation axis of the head (t ilt angle coefficient of pooled abducting and adducting eye movements: 0.11 +/-0.17 SD). Values for slow head impulses, however, exceeded somewhat the quarter angle (0.33+/-0.12), while smooth-pursuit movements (0.50+/-0.09) a nd saccades (0.44+/-0.11) were closest to the half angle. These results dem onstrate that the 3D orientation of the ocular rotation axis during rapid h ead thrusts is relatively independent of the direction of the line-of-sight and that ocular rotations elicited by head impulses are kinematically diff erent from saccades, despite similar movement dynamics.