Globally stable, locally flexible: Dynamic reconfiguration of brain natural frequencies during cognitive processing

Abstract

Neural oscillations are fundamental to brain function and cognition. Conventional analyses often rely on predefined frequency bands to assess power modulations, which may obscure finer-grained spectral variability. In this study, we focused on frequency rather than power to investigate whether the natural frequency of each brain region, typically observed at rest, represents a stable intrinsic property or dynamically reconfigures during cognitive processing. We analysed magnetoencephalography (MEG) data from the Human Connectome Project (HCP) across motor execution, working memory, and language processing tasks. Using a multivariate, data-driven spectral clustering approach, we mapped natural frequencies on a voxel-by-voxel basis without imposing predefined bands or regional boundaries. Results indicated that, while the global spatial organization of natural frequencies remained largely preserved during task engagement, specific cortical regions exhibited systematic, task-dependent shifts. In the sensorimotor cortices, the typical resting frequency of [~]24 Hz decreased to [~]6 Hz during movement preparation and at movement onset, and shifted to high-beta rhythms ([~]30 Hz) following hand movement. Increased working memory demands accelerated parieto-occipital alpha/beta activity (from [~]11/16 Hz to [~]13/20 Hz) and recruited high-gamma oscillations (60 to 80 Hz) in medial temporal regions. Finally, arithmetic processing elicited a [~]5 to 15 Hz increase within the beta/gamma ranges across frontoparietal networks relative to semantic comprehension. Taken together, these findings demonstrate that natural frequencies reflect a hybrid architecture: globally stable, yet locally flexible in response to cognitive demands. Moreover, our results suggest that cognitive engagement tends to accelerate neural rhythms in functionally specialized regions, providing a more nuanced understanding of the spectral architecture of human brain function beyond conventional power- and band-based metrics.