Adaptive eye movements induced by cross-axis pursuit--vestibular interactions in trained monkeys

We showed previously that smooth pursuit training combined with whole-body rotation in the orthogonal plane induces adaptive cross-axis vestibulo-ocular reflex (VOR). To gain an insight into the possible pathways and the nature of error signals for cross-axis VOR adaptation, we examined further properties of adaptive responses. In the first series, we trained monkeys for vertical pursuit during sinusoidal yaw rotation at 0.5 Hz (+/- 10 degrees) by presenting a target spot either in phase with, or with phase shifts (lead or lag) of 90 degrees to, the chair for 1 h. After training, sinusoidal or trapezoidal yaw rotation was tested in complete darkness without a target. Different training conditions resulted in different amounts of phase shift in cross-axis VOR. Trapezoidal yaw rotation (peak acceleration approximately 780 degrees/s2) revealed further differences in the direction, latency and time course of the adaptive responses depending on the conditions of the pursuit task. At least two (fast and slow) components with different latencies were induced in the cross-axis VOR by trapezoidal rotation after in-phase and phase-shift training. Adaptive responses were accurately simulated by the weighted sum of these two components. In the second series, we examined the effects of sequentially flashed (10 microseconds) targets in the horizontal plane during pitch rotation. The monkeys learned to track such targets by smooth pursuit, and cross-axis VOR was also induced after such apparent motion stimuli without retinal slip of the target image. These results indicate the importance of eye velocity for cross-axis VOR and suggest that this adaptation occurs most probably in the smooth pursuit pathways.