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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 scale-free 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.

Deviations from Critical Dynamics in Interictal Epileptiform Activity