Effect of Prior Direction Expectation on the Accuracy and Precision of Smooth Pursuit Eye Movements

The integration of sensory with top-down cognitive signals for generating appropriate sensory-motor behaviors is an important issue in understanding the brain's information processes. Recent studies have demonstrated that the interplay between sensory and high-level signals in oculomotor behavior could be explained by Bayesian inference. Specifically, prior knowledge for motion speed introduces a bias in the speed of smooth pursuit eye movements. The other important prediction of Bayesian inference is variability reduction by prior expectation; however, there is insufficient evidence in oculomotor behaviors to support this prediction. In the present study, we trained monkeys to switch the prior expectation about motion direction and independently controlled the strength of the motion stimulus. Under identical sensory stimulus conditions, we tested if prior knowledge about the motion direction reduced the variability of open-loop smooth pursuit eye movements. We observed a significant reduction when the prior expectation was strong; this was consistent with the prediction of Bayesian inference. Taking advantage of the open-loop smooth pursuit, we investigated the temporal dynamics of the effect of the prior to the pursuit direction bias and variability. This analysis demonstrated that the strength of the sensory evidence depended not only on the strength of the sensory stimulus but also on the time required for the pursuit system to form a neural sensory representation. Finally, we demonstrated that the variability and directional bias change by prior knowledge were quantitatively explained by the Bayesian observer model.