Motion direction representation in multivariate electroencephalography activity for smooth pursuit eye movements

Abstract

Visually-guided smooth pursuit eye movements are composed of initial open-loop and later steady-state periods. Feedforward sensory information dominates the motor behavior during the open-loop pursuit, and a more complex feedback loop regulates the steady-state pursuit. To understand the neural representations of motion direction during open-loop and steady-state smooth pursuits, we recorded electroencephalography (EEG) responses from human observers while they tracked random dot kinematograms as pursuit targets. We estimated population direction tuning curves from multivariate EEG activity using an inverted encoding model. We found significant direction tuning curves as early as 20 ms from motion onset. Direction tuning responses were generalized to later times during the open-loop smooth pursuit, but they became more dynamic during the later steady-state pursuit. The encoding quality of retinal motion direction information estimated from the early direction tuning curves was predictive of trial-by-trial variation in initial pursuit directions. These results suggest that the movement directions of open-loop smooth pursuit are guided by the representation of the retinal motion present in the multivariate EEG activity.