Linking neuronal avalanches with oscillatory and broadband 1/f activities in the resting human brain

Abstract

ObjectiveNarrowband oscillations (NOs) and Broadband Arrhythmic Activity (BAA) are valuable conceptualizations extensively used to interpret brain data, with NOs linked to communication and synchronization and BAA encompassing scale-free dynamics and neuronal avalanches. Although both frameworks offer critical in-sights into brain function, they have largely evolved in parallel, with limited integration and no unifying mechanistic account of how these dynamics interact to generate transient, Salient Events (SEs). This gap is particularly pressing given recent interest in how SEs--brief ({approx} 100 ms) bursts of activity coordinated across brain regions--relate to large-scale brain function and cognition. To address this, we introduce a signal-level framework that links the Fourier spectral properties (oscillation-domain) of neural signals to the emergence of realistic SEs in the time-domain from NOs and BAA. MethodsOur approach is grounded in a novel concept--Spectral Group Delay Consistency (SGDC)--along with associated measures that quantify the temporal alignment of spectral components and capture the conditions under which Nos and BAA coalesce into transient, burst-like events. Unlike traditional power- or phase-based measures, or higher-order statistical metrics such as kurtosis and cokurtosis, SGDC provides a signal-level mechanistic account of how local and large-scale SEs emerge from the spectral structure of the underlying signals. Empirical validation is provided using source-reconstructed MEG data from a large cohort and a comprehensive array of features characterizing the statistical, spatiotemporal and spectral properties of observed SEs. ResultsWe found that the SEs identified in our empirical MEG dataset can be segregated based on their spectral signature in two main groups having different propagation patterns. Using generative models based on the SGDC mechanism we provide a theoretical framework to interpret these experimental results showing that cluster 2 events are specifically related to the long-range spread of narrowband alpha bursts across the brain network (i.e., SNEs: Salient Network Events), whereas cluster 1 events correspond to more short-lived and spatially localized fluctuations mainly promoted by the BAA (i.e., SLEs: Salient Local Events). We also provide analytical arguments and numerical simulations showing that a) high SGDC in specific narrow frequency bands, b) transient cross-regional coherent NOs and c) BAA, are all key ingredients for the emergence of realistic SNEs. SignificanceWe combine experimental evidence supported by a signal-level analytical framework and numerical simulations based on generative models to demonstrate that transient phase-structured alpha bursts, shaped by the SGDC mechanism, contribute to long-range coordination during rest. This extends the communication-through-coherence hypothesis to the transient domain. Additionally, SGDC links to findings that NOs interact with fast microstates ({approx}100 - 200 ms) and may modulate long-range dependencies across timescales. While previous studies have described SEs within the framework of neuronal avalanches, they often lacked a generative, signal-level account. Here, we bridge that divide by offering a mathematically grounded and empirically validated framework that accounts for oscillatory and aperiodic bursts perspectives on brain activity. HighlightsO_LISalient network events propagating across the brain during spontaneous resting state activity, are highly structured in terms of their spatial, temporal and spectral properties. C_LIO_LIThe spectral group delay consistency framework provides a signal-level mechanism that accounts for transient salient network events emerging from oscillatory components of the brain activity. C_LIO_LINarrowband oscillations and broadband arrhythmic activity interact to shape the timing and spatial extent of salient events. C_LIO_LISpectral group delay consistency, transient cross-regional coherent narrowband oscillations and broadband arrhythmic activity, are all key ingredients for the emergence of realistic salient network events. C_LIO_LISalient network events during rest reflect large-scale spreading of synchronized alpha band activity, which may play a functional role as a long-range interaction mechanism in the human brain. C_LI