Estimating direction in brain-behavior interactions: Proactive and reactive brain states in driving

•Traditional neuroscience studies investigate localized task-evoked responses•Our approach examines continuous tracking of brain-behavior interactions in oscillatory activity•Brain leads behavior in a Proactive state, while brain follows behavior in a Reactive state•Reactive states are largely carried by alpha activity in regions sensitive to environmental statistics•Proactive states rely more on a diffuse delta-beta network, particularly when linked with steering behavior

Conventional neuroimaging analyses have ascribed function to particular brain regions, exploiting the power of the subtraction technique in fMRI and event-related potential analyses in EEG. Moving beyond this convention, many researchers have begun exploring network-based neurodynamics and coordination between brain regions as a function of behavioral parameters or environmental statistics; however, most approaches average evoked activity across the experimental session to study task-dependent networks. Here, we examined on-going oscillatory activity as measured with EEG and use a methodology to estimate directionality in brain-behavior interactions. After source reconstruction, activity within specific frequency bands (delta: 2-3 Hz; theta: 4-7 Hz; alpha: 8-12 Hz; beta: 13-25 Hz) in a priori regions of interest was linked to continuous behavioral measurements, and we used a predictive filtering scheme to estimate the asymmetry between brain-to-behavior and behavior-to-brain prediction using a variant of Granger causality. We applied this approach to a simulated driving task and examined directed relationships between brain activity and continuous driving performance (steering behavior or vehicle heading error). Our results indicated that two neuro-behavioral states may be explored with this methodology: a Proactive brain state that actively plans the response to the sensory information and is characterized by delta-beta activity, and a Reactive brain state that processes incoming information and reacts to environmental statistics primarily within the alpha band.

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