Inertial representation of angular motion in the vestibular system of rhesus monkeys. I. Vestibuloocular reflex

1. The spatial organization of the vestibuloocular reflex (VOR) was studied in six rhesus monkeys by applying fast, short-lasting, passive head and body tilts immediately after constant-velocity rotation (±90°/s) about an earth-vertical axis. Two alternative hypotheses were investigated regarding the reference frame used for coding angular motion. 1) If the vestibular system is organized in head-centered coordinates, postrotatory eye velocity would decay invariably along the direction of applied head angular acceleration. 2) Alternatively, if the vestibular system codes angular motion in inertial, gravity-centered coordinates, postrotatory eye velocity would decay along the direction of gravity. 2. Horizontal VOR was studied with the monkeys upright. Pitch (roll) tilts away from upright elicited a transient vertical (torsional) VOR and shortened the time constant of the horizontal postrotatory slow phase velocity. In addition, an orthogonal torsional (after pitch tilts) or vertical (after roll tilts) response gradually built up. As a result, the eye velocity vector transiently deviated in the roll (pitch) plane and then gradually rotated in the same direction as gravity in the pitch (roll) head plane until the orthogonal component reached a peak value. 3. The time constant of the horizontal postrotatory response was maximal in upright position (21.5 ± 5.7 s, mean ± SD) and minimal after tilts to prone (3.8 ± 0.7 s), supine (4.5 ± 1.2 s), and ear-down (5.2 ± 1.6 s) positions. 4. Torsional VOR was studied with the monkeys in supine or prone position. Pitch (yaw) tilts from the supine or prone position toward upright (ear- down) position elicited a transient vertical (horizontal) VOR and shortened the time constant of the torsional postrotatory response while a horizontal (vertical) orthogonal component slowly built up. As a result the eye velocity vector gradually rotated in the pitch (yaw) plane until the orthogonal component reached a peak value. 5. The time constant of the torsional postrotatory response in supine/prone positions was 16.5 ± 6.8 s. After tilts from supine/prone positions toward upright position, time constants decreased and were minimal after tilts to upright position (2.7 ± 0.7 s). 6. Vertical VOR was examined in ear-down positions. Roll (yaw) tilts from ear- down toward upright (supine/prone) position shortened the time constant of the vertical postrotatory slow phase velocity while an orthogonal horizontal (after roll tilts) or torsional (after yaw tilts) component slowly built up. As a result the eye velocity vector gradually rotated in the roll (yaw) plane away from the pitch head axis until residual postrotatory velocity decayed along a line approximately parallel to gravity. 7. The time constant of the vertical postrotatory slow phase velocity in ear-down positions was 18.0 ± 6.3 s (upward slow phase velocity) and 12.8 ± 4.6 s (downward slow phase velocity). 8. As a general finding for all three VOR planes, postrotatory eye velocity decayed ultimately along the line of gravity and not along the axis of semicircular canal stimulation. 9. Two dynamic phases could be distinguished during the spatial reorientation of postrotatory eye velocity: First there was a marked decrease of the principal postrotatory eye velocity immediately after the tilt while the orthogonal response component built up. Second, after the orthogonal response had reached its peak amplitude, both the principal and orthogonal postrotatory components decayed to zero at a slower rate. 10. The magnitudes of the principal and orthogonal response components, measured at the time when the orthogonal component peaked, varied sinusoidally as a function of tilt angle. 11. For horizontal VOR, peak amplitudes of the torsional and vertical orthogonal components (after pitch and roll tilts) were sinusoidally modulated with the same period as that of tilt angle, i.e., they were zero in upright position and maximal in supine/prone or ear-down positions. For torsional and vertical VOR the period of modulation was half that of the tilt angle after tilts in the yaw plane and took intermediate values after tilts in the pitch and roll planes. 12. These differences suggest that the spatiotemporal transformation of postrotatory vestibuloocular velocity from head-fixed to gravity-centered coordinates is based on two different mechanisms. 1) Reorientation of the horizontal eye velocity is best described as a rotation of postrotatory VOR activity, accompanied by a reduction in magnitude (dumping). 2) Reorientation of vertical and torsional eye velocity can be described as a projection of postrotatory VOR activity onto the direction of gravity. 13. The spatial reorientation of postrotatory eye velocity after a head tilt depended little on the spatial or temporal configuration of the tilt.