Linking neuronal avalanches with oscillatory and broadband 1/factivities in the resting human brain
Authors: Dellavale Damián , Rabuffo Giovanni , Lopez Emahnuel Troisi , Romano Antonella , Sorrentino Pierpaolo 
Published: February 2024

Objective

Brain oscillations, broadband 1/factivity and neuronal avalanches (NA) are valuable conceptualizations extensively used to interpret brain data, yet, these perspectives have mainly progressed in parallel with no current consensus on a rationale linking them. This study aims to reconcile these viewpoints using source-reconstructed MEG data obtained in healthy humans during eyes-closed resting state.

Methods

We analyzed NA in source-reconstructed MEG data from 47 subjects. For this, we introduced custom measures and a comprehensive array of features characterizing the statistical, spatiotemporal and spectral properties of NA. By using the complex baseband representation of signals we provide an analytical description of the mechanisms underlying the emergence of NA from the Fourier spectral constituents of the brain activity.

Results

The observed NA disclose a significant spectral signature in the alpha band, suggesting that the large-scale spreading of alpha bursts occurs mainly via brain avalanches. Besides, the NA detected in our MEG dataset can be segregated based on their spectral signature in two main groups having different propagation patterns, where cluster 2 avalanches is mainly related to the spread of narrowband alpha bursts across the brain network, whereas cluster 1 avalanches correspond to more spatially localized fluctuations promoted by the broadband 1/factivity. We also provide an analytical framework for the evidence showing that a) spectral group delay consistency in specific narrow frequency bands, b) transient cross-regional coherent oscillations and c) broadband 1/factivity, are all key ingredients for the emergence of realistic avalanches.

Significance

The proposed analytical arguments, supported by extensive model and experimental evidence, show how NA emerge from narrowband oscillations and broad-band arrhythmic activity co-existing in the human brain. Our results suggest that large-scale spreading of specific narrowband oscillations takes place in a transient manner mainly via NA, which may play a functional role as a long-range interaction mechanism in the resting human brain.

Highlights

Neuronal avalanches propagating across the brain during spontaneous resting state activity, are highly structured in terms of their spatial, temporal and spectral properties.

The link between local above-threshold fluctuations and oscillations can be understood in terms of the group delay consistency across the spectral components of the neuronal activity (spectral group delay consistency).

Spectral group delay consistency, transient cross-regional coherent oscillations and broadband 1/factivity, are all key ingredients for the emergence of realistic avalanches.

Observed neuronal avalanches can be segregated based on their spectral signature in two main groups having different propagation patterns, where cluster 2 avalanches is specifically related to the spread of narrowband alpha bursts across the brain network, whereas cluster 1 avalanches correspond to more spatially localized fluctuations promoted by the broadband 1/factivity.

Large-scale spreading of alpha bursts occurs mainly via brain avalanches, which may play a functional role as a long-range interaction mechanism in the resting human brain.