Prediction in the timing of pursuit eye movement initiation revealed by cross-axis vestibular–pursuit training in monkeys

Abstract

The smooth-pursuit system interacts with the vestibular system to maintain the image of a moving target on the fovea. Efficient tracking performance requires information about the velocity and the initiation of target motion. Previous studies in monkeys have shown that training with orthogonal pursuit and whole body rotation results in adapted eye movement direction during chair rotation. In addition, the latency of the pursuit shortens and initial eye velocity increases in a task-dependent manner. To examine whether these adapted eye movements are predictive pursuit, we studied whether our monkeys could predict the timing of smooth eye movement initiation during chair rotation. Two young Japanese monkeys were rotated horizontally in a trapezoidal waveform (20°/s, ±10°) with random inter-trial intervals. A laser spot was moved vertically with the same trajectory at a constant delay ranging from 100 to 700 ms after the onset of the chair motion. The monkeys were required to pursue the spot. After this training, the latencies of pursuit eye movements following the onset of chair motion were examined in the presence of the target motion. The target was also briefly (for 500–700 ms) extinguished at 80 ms after the onset of chair rotation. Pursuit eye movements after training were initiated before the onset of target motion and the latencies were proportional to the delays used for training. The latencies and response magnitudes of pursuit with or without target blanking were similar. The auditory–pursuit training did not induce an initial pursuit response similar to that induced by vestibular–pursuit training. These results indicate that smooth eye movements during the chair rotation after the vestibular–pursuit training included a predictive pursuit component. The monkeys’ estimate of the delays revealed by the latencies of pursuit was shorter by 22–36% than the actual delays.