Information theoretic measures of network coordination in high-frequency scalp EEG reveal dynamic patterns associated with seizure termination

Abstract

How a seizure terminates is still under-studied and, despite its clinical importance, remains an obscure phase of seizure evolution. Recent studies of seizure-related scalp EEGs at frequencies >100 Hz suggest that neural activity, in the form of oscillations and/or neuronal network interactions, may play an important role in preictal/ictal seizure evolution [2, 31]. However, the role of high-frequency activity in seizure termination, is unknown, if it exists at all. Using information theoretic measures of network coordination, this study investigated ictal and immediate postictal neurodynamic interactions encoded in scalp EEGs from a relatively small sample of 8 patients with focal epilepsy and multiple seizures originating in temporal and/or frontal brain regions, at frequencies ≤100 Hz and >100 Hz, respectively. Despite some heterogeneity in the dynamics of these interactions, consistent patterns were also estimated. Specifically, in several seizures, linear or non-linear increase in high-frequency neuronal coordination during ictal intervals, coincided with a corresponding decrease in coordination at frequencies <100 Hz, suggesting a potential interference role of high-frequency activity, to disrupt abnormal ictal synchrony at lower frequencies. These changes in network synchrony started at least 20–30 sec prior to seizure offset, depending on the seizure duration. Opposite patterns were estimated at frequencies ≤100 Hz in several seizures. These results raise the possibility that high-frequency interference may occur in the form of progressive network coordination during the ictal interval, which continues during the postictal interval. This may be one of several possible mechanisms that facilitate seizure termination. In fact, inhibition of pairwise interactions between EEGs by other signals in their spatial neighborhood, quantified by negative interaction information, was estimated at frequencies ≤100 Hz, at least in some seizures.

How important is the seizure onset zone for seizure dynamics?

“…Our findings are, however, in line with previous reports on the high relevance of brain outside of the SOZ but within the epileptic network for seizure dynamics 25,26,5,27,28,29,30 . Particularly brain areas neighbouring the SOZ were most often rated as important (using betweenness centrality) pre-ictally and during the first half of a seizure which would characterize these non-focal nearby structures as a bridge between the SOZ and other brain regions.…”

Neocortical gamma oscillations in idiopathic generalized epilepsy

“…Our present findings are in line with the suggestions of these author that a potential interference role of high frequency activity can disrupt abnormal ictal synchrony at lower frequencies. 25 The cause of the intensified gamma power is unknown, but may reflect ion channel or neurotransmitter receptor activity that may relate mechanistically to the production of SWD in the IGE patients. 26,27 Spontaneous gamma activity improves visual cortex excitability, and may serve to ensure more rapid and reliable transmission, 28 and increases in gamma activity accompany perceptual and cognitive processes.…”

Early Psychosocial Neglect Adversely Impacts Developmental Trajectories of Brain Oscillations and Their Interactions

“…Gamma oscillations have been associated with perceptual binding, working memory loads, and attention among other processes (Canolty et al, 2006; Buzsaki & Draguhn, 2004; Ward, 2003; Csibra, David, Spratling, & Johnson, 2000). High-frequency oscillations (>80 Hz) in the human brain are less well understood but have been implicated in pathological processes such as epilepsy (Stamoulis, Schomer, & Chang, 2013; Stamoulis, Gruber, Schomer, & Chang, 2012). …”