EEG state-trajectory instability and speed reveal global principles of intrinsic spatiotemporal neural dynamics

Abstract

Spatiotemporal dynamics of EEG/MEG (electro-/magneto-encephalogram) have typically been investigated by applying time-frequency decomposition and examining amplitude-amplitude, phase-phase, or phase-amplitude associations between combinations of frequency bands and scalp sites, primarily to identify neural correlates of behaviors and traits. Instead, we directly extracted global EEG spatiotemporal dynamics as trajectories of k-dimensional state vectors (k = the number of estimated current sources) to investigate potential global rules governing neural dynamics. We chose timescale-dependent measures of trajectory instability (approximately the 2nd temporal derivative) and speed (approximately the 1st temporal derivative) as state variables, that succinctly characterized trajectory forms. We compared trajectories across posterior, central, anterior, and lateral scalp regions as the current sources under those regions may serve distinct functions. We recorded EEG while participants rested with their eyes closed (likely engaged in spontaneous thoughts) to investigate intrinsic neural dynamics. Some potential global rules emerged. Time-averaged trajectory instability from all five regions tightly converged (with their variability minimized) at the level of generating nearly unconstrained but slightly conservative turns ([~]100{degrees} on average) on the timescale of [~]25 ms, suggesting that spectral-amplitude profiles are globally adjusted to maintain this convergence. Further, within-frequency and cross-frequency phase relations appear to be independently coordinated to reduce average trajectory speed and increase the variability in trajectory speed and instability in a relatively timescale invariant manner, and to make trajectories less oscillatory. Future research may investigate the functional relevance of these intrinsic global-dynamics rules by examining how they adjust to various sensory environments and task demands or remain invariant. The current results also provide macroscopic constraints for quantitative modeling of neural dynamics as the timescale dependencies of trajectory instability and speed are relatable to oscillatory dynamics.