Canal-otolith interactions after off-vertical axis rotations I. Spatial reorientation of horizontal vestibuloocular...

We examined the three-dimensional (3-D) spatial orientation of postrotatory eye velocity after horizontal off-vertical axis rotations by varying the final body orientation with respect to gravity. Three rhesus monkeys were oriented in one of two positions before the onset of rotation: pitched 24 degrees nose-up or 90 degrees nose-up (supine) relative to the earth-horizontal plane and rotated at +/-60 degrees /s around the body-longitudinal axis. After 10 turns, the animals were stopped in 1 of 12 final positions separated by 30 degrees. An empirical analysis of the postrotatory responses showed that the resultant response plane remained space-invariant, i.e., accurately represented the actual head tilt plane at rotation stop. The alignment of the response vector with the spatial vertical was less complete. A complementary analysis, based on a 3-D model that implemented the spatial transformation and dynamic interaction of otolith and lateral semicircular canal signals, confirmed the empirical description of the spatial response. In addition, it allowed an estimation of the low-pass filter time constants in central otolith and semicircular canal pathways as well as the weighting ratio between direct and inertially transformed canal signals in the output. Our results support the hypothesis that the central vestibular system represents head velocity in gravity-centered coordinates by sensory integration of otolith and semicircular canal signals.