The vestibulo-ocular reflex of the squirrel monkey during eccentric rotation and roll tilt

The vestibulo-ocular reflexes (VOR) are determined not only by angular acceleration, but also by the presence of gravity and linear acceleration. This phenomenon was studied by measuring three-dimensional nystagmic eye movements, with implanted search coils, in six male squirrel monkeys during eccentric rotation. Monkeys were rotated in the dark at a constant velocity of 200 degrees/s (centrally or 79 cm off axis) with the axis of rotation always aligned with gravity and the spinal axis of the upright monkeys. The monkey's orientation (facing-motion or back-to-motion) had a dramatic influence on the VOR. These experiments show that: (a) the axis of eye rotation always shifted toward alignment with gravito-inertial force; (b) the peak value of horizontal slow phase eye velocity was greater with the monkey facing-motion than with back-to-motion; and (c) the time constant of horizontal eye movement decay was smaller with the monkey facing-motion than with back-to-motion. All of these findings were statistically significant and consistent across monkeys. In another set of tests, the same monkeys were rapidly tilted about their naso-occipital (roll) axis. Tilted orientations of 45 degrees and 90 degrees were maintained for 1 min. Other than a compensatory angular VOR during the angular rotation, no consistent eye velocity response was observed during or following the tilt for any of the six monkeys. The absence of any eye movement response following tilt weighs against the possibility that translational linear VOR responses are due to simple high-pass filtering of the otolith signals. The VOR response during eccentric rotation was divided into the more familiar angular VOR and linear VOR components. The angular component is known to depend upon semicircular canal dynamics and central influences. The linear component of the response decays rapidly with a mean duration of only 6.6 s, while the axis of eye rotation rapidly aligns (< 10 s) with gravito-inertial force. These results are consistent with the hypothesis that the measurement of gravito-inertial force by the otolith organs is resolved into central estimates of linear acceleration and gravity, such that the central estimate of gravitational force minus the central estimate of linear acceleration approximately equals the otolith measurement of gravito-inertial force.