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 restingstate 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.

Deviations from Critical Dynamics in Interictal Epileptiform Activity

“…Indeed, the above analyses have shortcomings: (1) intermixing data of several subjects, which may differ in temporal organization of neuronal avalanches and distance from critical dynamics, may obscure our results; (2) the model inversion of the duration distributions suffers from an underrepresentation at short durations and from a narrow effective range in which a power law regimen can exist; and (3) the shape collapse analysis was applied to only a relatively small range of durations and the obtained shapes were not smooth, suggesting sensitivity to the relatively small amount of avalanches used in averaging over these temporal profiles. Nonetheless, the scaling exponent reported here is in agreement with previous results (Arviv et al, 2015). Although noisy at longer durations, the avalanche shape does not seem to be parabolic (Friedman et al, 2012).…”

“…However, the duration distributions, as opposed to the size distributions, have a particularly narrow range of effective power law regimen due to the smaller magnitudes involved. Moreover, as reported previously (Arviv et al, 2015), there is a consistent, across all subjects, underrepresentation of small durations than would have been expected from a power law (see Fig. 4A).…”

“…Epilepsy, a chronic neurological disorder that affects ϳ1% of the world's population (World Health Organization, 2015), is associated with an altered excitation-inhibition balance (EIB) in the cortex (Eichler and Meier, 2008;Fritschy, 2008;Badawy et al, 2012). The manifestation of hyperexcitable networks and the underlying epileptic processes are mediated by changes in numerous physiological and dynamical factors of both the excitatory and inhibitory circuits (Wendling et al, 2005;Eichler and Meier, 2008;Fritschy, 2008).…”

“…The manifestation of hyperexcitable networks and the underlying epileptic processes are mediated by changes in numerous physiological and dynamical factors of both the excitatory and inhibitory circuits (Wendling et al, 2005;Eichler and Meier, 2008;Fritschy, 2008). Accordingly, it has been suggested that cortical excitability in patients with epilepsy is constantly changing (Badawy et al, 2012). Along with the occurrence of recurrent seizures (Banerjee et al, 2009), interictal (between-seizures) periods are likewise characterized by distinct excitability features (McCormick and Contreras, 2001;Badawy et al, 2012).…”

“…Accordingly, it has been suggested that cortical excitability in patients with epilepsy is constantly changing (Badawy et al, 2012). Along with the occurrence of recurrent seizures (Banerjee et al, 2009), interictal (between-seizures) periods are likewise characterized by distinct excitability features (McCormick and Contreras, 2001;Badawy et al, 2012). A magnetoencephalography (MEG) or EEG trace often shows interictal epileptiform activity (IEA), namely, abnormal waveforms not associated with seizure symptoms.…”