Structure-function coupling and decoupling during movie-watching and resting-state: Novel insights bridging EEG and structural imaging

Abstract

The intricate structural and functional architecture of the brain enables a wide range of cognitive processes ranging from perception and action to higher-order abstract thinking. Despite important progress, the relationship between the brains structural and functional properties is not yet fully established. In particular, the way the brains anatomy shapes its electrophysiological dynamics remains elusive. The electroencephalography (EEG) activity recorded during naturalistic tasks is thought to exhibit patterns of coupling with the underlying brain structure that vary as a function of behavior. Yet these patterns have not yet been sufficiently quantified. We address this gap by jointly examining individual Diffusion-Weighted Imaging (DWI) scans and continuous EEG recorded during video-watching and resting state, using a Graph Signal Processing (GSP) framework. By decomposing the structural graph into Eigenmodes and expressing the EEG activity as an extension of anatomy, GSP provides a way to quantify the structure-function coupling. We elucidate how the structure shapes function during naturalistic tasks such as movie-watching and how this association is modulated by tasks. We quantify the coupling relationship in a region-, time-, frequency-resolved manner. First of all, our findings indicate that the EEG activity in the sensorimotor cortex is strongly coupled with brain structure, while the activity in higher-order systems is less constrained by anatomy, i.e., shows more flexibility. In addition, we found that watching videos was associated with stronger structure-function coupling in the sensorimotor cortex, as compared to resting-state data. Second, time-resolved analysis revealed that the unimodal systems undergo minimal temporal fluctuation in structure-function association, and the transmodal system displays highest temporal fluctuations, with the exception of PCC seeing low fluctuations. Lastly, our frequency-resolved analysis revealed a consistent topography across different EEG rhythms, suggesting a similar relationship with the anatomical structure across frequency bands. Together, this unprecedented characterization of the link between structure and function using continuous EEG during naturalistic behavior underscores the role of anatomy in shaping ongoing cognitive processes. Taken together, by combining the temporal and spectral resolution of EEG and the methodological advantages of GSP, our work sheds new light onto the anatomo-functional organization of the brain.