Gain Control in Predictive Smooth Pursuit Eye Movements: Evidence for an Acceleration-Based Predictive Mechanism

Abstract

The smooth pursuit eye movement system incorporates various control features enabling adaptation to specific tracking situations. In this work we analyzed the interplay between two of these mechanisms, gain control and predictive pursuit. We tested human responses to high-frequency perturbations during step-ramp pursuit, as well as pursuit of a periodically moving target. For the latter task, we found a non-linear interaction between perturbation response and carrier acceleration. Responses to perturbations where the initial perturbation acceleration was contra-directional to carrier acceleration increased with carrier velocity, in a similar way as observed during step-ramp pursuit. In contrast, responses to perturbations with ipsi-directional initial perturbation and carrier acceleration were large for all carrier velocities. Modelling the pursuit system suggests that gain control and short-term prediction are separable elements. The observed effect may be explained by combining the standard gain control mechanism with a derivative-based short-term predictive mechanism. The non-linear interaction between perturbation and carrier acceleration can be reproduced by assuming a signal saturation, which is acting on the derivative of the target velocity signal. Our results therefore argue for the existence of an internal estimate of target acceleration as a basis for a simple yet efficient short-term predictive mechanism.

Significance Statement Due to its modest complexity, analysis of the smooth pursuit control system offers a promising approach for understanding the principle mechanisms that transform visual perception into motor action. While previous studies investigated smooth pursuit gain control and predictive pursuit separately, here we investigated for the first time the interaction between them. We present strong evidence for the utilization of an internal estimate of target acceleration in the pursuit control circuit. Electrophysiological studies have shown that such signal might be extracted from neuronal responses in the extrastriate visual cortex. Our results therefore suggest an extended functional role for this area in sensorimotor transformation. Further, we propose a physiologically plausible modification of the standard pursuit model which reproduces the observed system behavior.