Eye-position error influence over \"open-loop\" smooth pursuit initiation

Abstract

The oculomotor system integrates a variety of visual signals into appropriate motor plans, but such integration can have widely varying time scales. For example, smooth pursuit eye movements to follow a moving target are slower and longer-lasting than saccadic eye movements, and it has been suggested that initiating a smooth pursuit eye movement involves an obligatory open-loop interval, in which new visual motion signals presumably cannot influence the ensuing motor plan for up to 100 ms after movement initiation. However, this view runs directly contrary to the idea that the oculomotor periphery has privileged access to short-latency visual signals. Here we show that smooth pursuit initiation is sensitive to visual inputs, even in \"open-loop\" intervals. We instructed male rhesus macaque monkeys to initiate saccade-free smooth pursuit eye movements, and we injected a transient, instantaneous eye position error signal at different times relative to movement initiation. We found robust short-latency modulations in eye velocity and acceleration, starting only [~]50 ms after transient signal occurrence, and even during \"open-loop\" pursuit initiation. Critically, the spatial direction of the injected position error signal had predictable effects on smooth pursuit initiation, with forward errors increasing eye acceleration and backwards errors reducing it. Catch-up saccade frequencies and amplitudes were also similarly altered [~]50 ms after transient signals, much like well-known effects on microsaccades during fixation. Our results demonstrate that smooth pursuit initiation is highly sensitive to visual signals, and that catch-up saccade generation is reset after a visual transient.