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.

The framework of criticality provides a unifying perspective on neuronal dynamics from in vitro cortical cultures to functioning human brains. Recent findings suggest that a healthy cortex displays critical dynamics, giving rise to scale-free spatiotemporal cascades of activity, termed neuronal avalanches. Pharmacological manipulations of the excitation-inhibition balance (EIB) in cortical cultures were previously shown to result in deviations from criticality and from the power law scaling of avalanche size distribution. To examine the sensitivity of neuronal avalanche metrics to altered EIB in humans, we focused on epilepsy, a neurological disorder characterized by hyperexcitable networks. Using magnetoencephalography, we quantitatively assessed deviations from criticality in the brain dynamics of patients with epilepsy during interictal (between-seizures) activity. Compared with healthy control subjects, epilepsy patients tended to exhibit a higher neural gain and larger avalanches, particularly during interictal epileptiform activity. Moreover, deviations from scalefree behavior were exclusively connected to brief intervals at epileptiform discharges, strengthening the association between deviations from criticality and the instantaneous changes in EIB. The avalanches collected during interictal epileptiform activity had not only a stereotypical size range but also involved particular spatial patterns of activations, as expected for periods of epileptic network dominance. Overall, the neuronal avalanche metrics provide a quantitative novel description of interictal brain activity of patients with epilepsy.

The relation between spontaneous and stimulated global brain activity is a fundamental problem in the understanding of brain functions. This question is investigated both theoretically and experimentally within the context of nonequilibrium fluctuation-dissipation relations. We consider the stochastic coarse-grained Wilson-Cowan model in the linear noise approximation and compare analytical results to experimental data from magnetoencephalography of the human brain. The short-time behavior of the autocorrelation function for spontaneous activity is characterized by a double-exponential decay, with two characteristic times, differing by two orders of magnitude. Conversely, the response function exhibits a single-exponential decay in agreement with experimental data for evoked activity under visual stimulation. Results suggest that the brain response to weak external stimuli can be predicted from the observation of spontaneous activity and pave the way to controlled experiments on the brain response under different external perturbations.

Neuronal avalanches are a hallmark feature of critical dynamics in the brain. While the theoretical framework of a critical branching processes is generally accepted for describing avalanches during ongoing brain activity, there is a current debate about the corresponding dynamical description during stimulus-evoked activity. As the brain activity evoked by external stimuli considerably varies in magnitude across time, it is not clear whether the parameters that govern the neuronal avalanche analysis (a threshold or a temporal scale) should be adaptively altered to accommodate these changes. Here, the relationship between neuronal avalanches and time-frequency representations of stimulus-evoked activity is explored. We show that neuronal avalanche metrics, calculated under a fixed threshold and temporal scale, reflect genuine changes in the underlying dynamics. In particular, event-related synchronization and de-synchronization are shown to align with variations in the power-law exponents of avalanche size distributions and the branching parameter (neural gain), as well as in the spatio-temporal spreading of avalanches. Nonetheless, the scale-invariant behavior associated with avalanches is shown to be a robust feature of healthy brain dynamics, preserved across various periods of stimulus-evoked activity and frequency bands. Taken together, the combined results suggest that throughout stimulus-evoked responses the operating point of the dynamics may drift within an extended-critical-like region.

Video-EEG monitoring (VEM) is imperative in seizure classification and presurgical assessment of epilepsy patients. Analysis of VEM is currently performed in most institutions using a freeform report, a time-consuming process resulting in a non-standardized report, limiting the use of this essential diagnostic tool. Herein we present a pilot feasibility study of our experience with “Digital Semiology” (DS), a novel seizure encoding software. It allows semiautomated annotation of the videos of suspected events from a predetermined, hierarchal set of options, with highly detailed semiologic descriptions, somatic localization, and timing. In addition, the software's semiologic extrapolation functions identify characteristics of focal seizures and PNES, sequences compatible with a Jacksonian march, and risk factors for SUDEP. Sixty episodes from a mixed adult and pediatric cohort from one level 4 epilepsy center VEM archives were analyzed using DS and the reports were compared with the standard freeform ones, written by the same epileptologists. The behavioral characteristics appearing in the DS and freeform reports overlapped by 78–80%. Encoding of one episode using DS required an average of 18 min 13 s (standard deviation: 14 min and 16 s). The focality function identified 19 out of 43 focal episodes, with a sensitivity of 45.45% (CI 30.39–61.15%) and specificity of 87.50% (CI 61.65–98.45%). The PNES function identified 6 of 12 PNES episodes, with a sensitivity of 50% (95% CI 21.09–78.91%) and specificity of 97.2 (95% CI 88.93–99.95%). Eleven events of GTCS triggered the SUDEP risk alert. Overall, these results show that video recordings of suspected seizures can be encoded using the DS software in a precise manner, offering the added benefit of semiologic alerts. The present study represents an important step toward the formation of an annotated video archive, to be used for machine learning purposes. This will further the goal of automated VEM analysis, ultimately contributing to wider utilization of VEM and therefore to the reduction of the treatment gap in epilepsy.