Near-Critical Dynamics in Stimulus-Evoked Activity of the Human Brain and Its Relation to Spontaneous Resting-State Activity

Abstract

In recent years, numerous studies have found that the brain at resting state displays many features characteristic of a critical state. Here we examine whether stimulus-evoked activity can also be regarded as critical. Additionally, we investigate the relation between resting-state activity and stimulus-evoked activity from the perspective of criticality. We found that cortical activity measured by magnetoencephalography (MEG) is near critical and organizes as neuronal avalanches at both resting-state and stimulus-evoked activities. Moreover, a significantly high intrasubject similarity between avalanche size and duration distributions at both cognitive states was found, suggesting that the distributions capture specific features of the individual brain dynamics. When comparing different subjects, a higher intersubject consistency was found for stimulus-evoked activity than for resting state. This was expressed by the distance between avalanche size and duration distributions of different participants and was supported by the spatial spreading of the avalanches involved. During the course of stimulus-evoked activity, time locked to the stimulus onset, we demonstrate fluctuations in the gain of the neuronal system and thus short timescale deviations from the critical state. Nonetheless, the overall near-critical state in stimulus-evoked activity is retained over longer timescales, in close proximity and with a high correlation to spontaneous (not time-locked) resting-state activity. Spatially, the observed fluctuations in gain manifest through anticorrelative activations of brain sites involved, suggesting a switch between task-negative (default mode) and task-positive networks and assigning the changes in excitation–inhibition balance to nodes within these networks. Overall, this study offers a novel outlook on evoked activity through the framework of criticality.

SIGNIFICANCE STATEMENT The organization of stimulus-evoked activity and ongoing cortical activity is a topic of high importance. The article addresses several general questions. What is the spatiotemporal organization of stimulus-evoked cortical activity in healthy human subjects? Are there deviations from excitation–inhibition balance during stimulus-evoked activity? What is the relationship between stimulus-evoked activity and ongoing resting-state activity? Using magnetoencephalography (MEG), we demonstrate that stimulus-evoked activity in humans follows a critical branching process that produces neuronal avalanches. Additionally, we investigate the spatiotemporal relationship between resting-state activity and stimulus-evoked activity from the perspective of critical dynamics. These analyses reveal new aspects of this complex relationship and offer novel insights into the interplay between excitation and inhibition that were not observed previously using conventional approaches.