Brain criticality predicts individual levels of inter-areal synchronization in human electrophysiological data

The brain has been proposed to operate near a critical transition between order and disorder, controlled by a balance between inhibition and excitation. Here, the authors show that individual variability in long-range synchronization between brain regions can be explained by an individual's proximity to this phase transition. Neuronal oscillations and their synchronization between brain areas are fundamental for healthy brain function. Yet, synchronization levels exhibit large inter-individual variability that is associated with behavioral variability. We test whether individual synchronization levels are predicted by individual brain states along an extended regime of critical-like dynamics - the Griffiths phase (GP). We use computational modelling to assess how synchronization is dependent on brain criticality indexed by long-range temporal correlations (LRTCs). We analyze LRTCs and synchronization of oscillations from resting-state magnetoencephalography and stereo-electroencephalography data. Synchronization and LRTCs are both positively linearly and quadratically correlated among healthy subjects, while in epileptogenic areas they are negatively linearly correlated. These results show that variability in synchronization levels is explained by the individual position along the GP with healthy brain areas operating in its subcritical and epileptogenic areas in its supercritical side. We suggest that the GP is fundamental for brain function allowing individual variability while retaining functional advantages of criticality.

Automated summary

This study suggests that variability in long-range synchronization between brain regions can be explained by an individual's position along the critical transition between order and disorder. Neuronal oscillations and synchronization are essential for healthy brain function, and the variability in synchronization is associated with behavioral variability. Computational modeling shows that synchronization is dependent on brain criticality, and these results demonstrate the importance of the individual's position along the critical transition for synchronization levels.