Inter-areal coupling for cognition through coincident oscillatory transients

Abstract

How do large-scale functional brain networks dynamically emerge to enable cognition? Correlated oscillations, a mechanism for inter-areal interactions, can be expressed as phase coherence or correlated amplitude fluctuations. While the functional role of phase coherence has been addressed in the past, it remains unknown how large-scale amplitude coupling dynamically supports the rapid network reconfigurations necessary for adaptive behavior. Here, we demonstrate that cognitive processing relies on the temporal alignment of brief, high-amplitude oscillatory events across distant cortical regions, rather than sustained coupling of oscillations. Capitalizing on the spatio-temporal resolution of magnetoencephalography (MEG) during a task probing attention and decision-making, we show that oscillatory event coincidences form functionally relevant, transient networks: First, coincidences of high-amplitude oscillatory events in the alpha and beta frequency range increase prior to correct decisions within a parieto-frontal network. Second, transient theta/alpha oscillatory event coincidences within a medial parietal, temporo-parietal junction and lateral prefrontal network track the dynamics of spontaneous, covert spatial attention reallocation. In contrast, transient aperiodic and sustained network components exhibit only weak functional modulations, revealing a spatial and spectral dissociation between transient and sustained amplitude coupling. Overall, our findings demonstrate that efficient cognition relies on large-scale interactions rapidly formed through co-occurring transient oscillatory events. We propose that the brain-wide orchestration of high-amplitude oscillatory events can provide a new framework for understanding how the brain dynamically integrates information to guide flexible behavior.