Evaluating oscillatory mechanisms underlying flexible neural communication in the human brain

Abstract

How the brain orchestrates the flow of information between its multiple functional units flexibly, quickly, and accurately, remains a fundamental question in neuroscience. Multiple theories identify neural oscillations as a likely basis for this process. However, a lack of empirical validation of proposed theories, particularly at the whole-brain scale, has hampered consensus on oscillatory principles governing neural communication, limiting our understanding of a process central to perception and cognition and its integration into experiments and clinical applications. Here, we empirically validate previously proposed neural-oscillatory communication mechanisms in the human brain - specifically those involving power and interareal phase coherence - at the whole-brain scale. We do this by estimating the dependence of inferred communication on oscillatory measures that have been theorised to facilitate communication, in source-localised resting-state magnetoencephalography (MEG) recordings. We find that power and phase coherence in the alpha, beta, and high-gamma bands track communication better than others. Crucially, the relation between communication and oscillatory measures varied across regions, indicating spatial heterogeneity in routing mechanisms. Notably, power and coherence-based principles tracked communication patterns of unimodal regions better than those of transmodal regions. In sum, these findings suggest that the human brain implements regionally specific communication mechanisms with complex neural-oscillatory dependence. Significance statementFlexible and dynamic routing of information between neural elements is vital for human brain function. Despite its importance, the mechanisms underlying flexible communication in the brain are not fully understood. Several lines of evidence suggest that neural oscillations might mediate flexible communication, but whether such mechanisms operate at whole-brain scales remains uncertain. Here, we investigate the oscillatory underpinnings of communication by assessing how well observed communication patterns from magnetoencephalography data align with the predictions of established theories. Our findings suggest that the brain follows complex region-specific routing principles to realise flexible communication. Knowledge of these principles can develop our fundamental understanding of functions like perception and cognition, refine models of interareal interactions, and help develop more effective stimulation-based clinical interventions.