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..

Predicting Trial-by-Trial Variation in Oculomotor Behavior Using Multivariate Electroencephalography Theta Phase

“…Using the inverted encoding model [42] and others, several studies have shown how stimulus orientation information is maintained in working memory [43]- [47] and modeled the effect of attention [48] on the oriented visual stimulus. A recent study represented visual and pursuit motion information in multivariate EEG activity during smooth pursuit eye movements [22]. These studies all used multivariate pattern analysis to extract the specific stimulus information of interest (for example, stimulus orientation), which is a step forward in EEG research and applications.…”

“…The data of the remaining 15 participants were analyzed and are presented in this paper (three females; 12 males; age range: 21-32 years). A portion of the data used has been published in a study in which an unrelated aspect was observed and analyzed [22]. All participants gave informed consent, and experimental procedures and methods were approved by the Institutional Review Board at Sungkyunkwan University.…”

“…Finally, we removed ICs classified as artifacts using the ADJUST EEGLab plugin [35]. We band-pass filtered the preprocessed EEG signal into theta (4-8 Hz), alpha (8-13 Hz), beta (13)(14)(15)(16)(17)(18)(19)(20)(21)(22)(23)(24)(25)(26)(27)(28)(29)(30), and gamma . We epoched the preprocessed and filtered signals from −400 to 600 ms relative to the visual stimulus onset in each trial.…”

Multivariate EEG activity reflects the Bayesian integration and the integrated Galilean relative velocity of sensory motion during sensorimotor behavior

“…Previous studies suggest that sensory information integration drives the initiation of smooth pursuit eye movements. A few studies have investigated the neural representation of motion during smooth pursuit eye movements in humans 15 , 47 , 48 . A recent study in our laboratory investigated neural representations using multivariate analysis of EEG activity 48 .…”

“…A few studies have investigated the neural representation of motion during smooth pursuit eye movements in humans 15 , 47 , 48 . A recent study in our laboratory investigated neural representations using multivariate analysis of EEG activity 48 . Using multivariate analysis, we successfully extracted motion direction information and demonstrated the temporal dynamics of the representation, which was consistent with the current knowledge of information processes in the smooth pursuit of eye movements.…”