Altered spreading of neuronal avalanches in temporal lobe epilepsy relates to cognitive performance: a resting-state hdEEG study

ABSTRACT Objective Large aperiodic bursts of activations named neuronal avalanches have been used to characterize whole-brain activity, as their presence typically relates to optimal dynamics. Epilepsy is characterized by alterations of large-scale brain network dynamics. Here, we exploited neuronal avalanches to characterize differences in the electroencephalography (EEG) basal activity, free from seizures and/or interictal spikes, between patients with temporal lobe epilepsy (TLE) and matched controls. Method We defined neuronal avalanches as starting when the z-scored source-reconstructed EEG signals crossed a specific threshold in any region and ending when all regions went back to baseline. This technique avoids data manipulation or assumptions of signal stationarity, focusing on the aperiodic, scale-free components of the signals. We computed individual avalanche transition matrices, to track the probability of avalanche spreading across any two regions, compared them between patients and controls, and related them to memory performance in patients. Results We observed a robust topography of significant edges clustering in regions functionally and structurally relevant for the TLE, such as the entorhinal cortex, the inferior parietal and fusiform area, the inferior temporal gyrus, and the anterior cingulate cortex. We detected a significant correlation between the centrality of the entorhinal cortex in the transition matrix and the long-term memory performance (delay recall Rey figure test). Significance Our results show that the propagation patterns of large-scale neuronal avalanches are altered in TLE during resting state, suggesting a potential diagnostic application in epilepsy. Furthermore, the relationship between specific patterns of propagation and memory performance supports the neurophysiological relevance of neuronal avalanches. Key Points Investigation of the brain dynamics during resting-state activity in patients with TLE using neuronal avalanches (i.e., large scale patterns of activation) We found higher transition probabilities in patients with TLE in the entorhinal cortex, inferior temporal and fusiform gyri, and anterior cingulate cortex We found higher eigenvector centrality of the left entorhinal cortex in the avalanche transition matrix, which was related to reduced long term memory performance Discussion: of the potential application of the avalanche transition matrix as diagnostic tool in presurgical evaluations and epilepsy types differentiation