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

Abstract

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.

Rhythmicity of neuronal oscillations delineates their cortical and spectral architecture

“…Neuronal oscillations encompass a wide range of neuronal processes where the phase of the oscillation is the key mechanistically and functionally substantial element 25 , 53 , 54 , they predict visual perception 55 , plays a role in neural coordination 56 , plasticity 57 and reflect phase-specific functional relations between neuronal populations 58 . Phase-synchronization is also a basis for resting-state networks 27 , 59 , 60 . The relationship between phase and amplitude correlations 23 , 61 and that between oscillations of different frequencies 28 have remained an active topic for investigation.…”

Cortex deviates from criticality during action and deep sleep: a temporal renormalization group approach

“…The closer to criticality the system operates, the broader the range of scale-invariant timescales, with the range diverging at criticality 4,5 . In line with this hypothesis, a rich history of studies examining "1/f" power spectra [6][7][8] and long-range temporal correlations [9][10][11] of measured brain activity suggests that the brain often generates temporally scale-invariant population activity.…”

“…For the DFA fluctuation function, we followed the procedure in ref 11 . Briefly, for a given 𝑤𝑤, we split the z-scored spike-count time series into windows of length 𝑤𝑤 (50% overlap between windows), took the cumulative sum within each window, subtracted the leastsquares fit line from this cumulative sum, and calculated the standard deviation of the resulting time series.…”

Node centrality in MEG resting-state networks co-varies with neurotransmitter receptor and transporter density

“…DA, along with NA, has also been proposed to regulate long-range temporal correlations (LRTCs) that are the hallmark of brain critical dynamics, as well as the neuronal exhibition/inhibition (E/I) balance (Pfeffer, 2018). A recent study reported that the level of brain-wide inter-areal phase-connectivity and LRTCs are correlated and dependent on an individual's E/I balance that acts as the main control parameter for critical dynamics (Fuscà et al, 2023). Therefore, our findings imply that NT receptor and transporter densities may influence synchronization and LRTCs within the framework of critical dynamics via the E/I balance.…”