Altered resting state brain dynamics in temporal lobe epilepsy can be observed in spectral power, functional connectivity and graph theory metrics

Abstract

Despite a wealth of EEG epilepsy data that accumulated for over half a century, our ability to understand brain dynamics associated with epilepsy remains limited. Using EEG data from 15 controls and 9 left temporal lobe epilepsy (LTLE) patients, in this study we characterize how the dynamics of the healthy brain differ from the "dynamically balanced" state of the brain of epilepsy patients treated with anti-epileptic drugs in the context of resting state. We show that such differences can be observed in band power, synchronization and network measures, as well as deviations from the small world network (SWN) architecture of the healthy brain. The θ (4-7 Hz) and high α (10-13 Hz) bands showed the biggest deviations from healthy controls across various measures. In particular, patients demonstrated significantly higher power and synchronization than controls in the θ band, but lower synchronization and power in the high α band. Furthermore, differences between controls and patients in graph theory metrics revealed deviations from a SWN architecture. In the θ band epilepsy patients showed deviations toward an orderly network, while in the high α band they deviated toward a random network. These findings show that, despite the focal nature of LTLE, the epileptic brain differs in its global network characteristics from the healthy brain. To our knowledge, this is the only study to encompass power, connectivity and graph theory metrics to investigate the reorganization of resting state functional networks in LTLE patients.

Figure 1. a) Total power over the range 2–20 Hz from healthy controls and LTLE patients for the EC and EO conditions.

Figures b and c show the same across the various frequency bands as labeled on the figures for eyes closed and eyes open, respectively. Asterisks indicate where the difference between healthy controls and patients resulted in p<0.05 from a Kruskal-Wallis test. d) Topographical maps of spectral power for the EC and the EO condition showing the regions where power is greater in controls than patients (top) and where power is greater in patients than controls (bottom) for EC and EO as labelled.

Figure 2. a) Group averaged power asymmetry (eqn. 1) contrasting brain activity in the high and low frequency bands, where a positive value indicates more power in the d and q bands compared to a_h and b.

The asterisks indicate statistical significance based on a Kruskal-Wallis test. The p vales are displayed on the plots in figure b. b) Same as figure a but for the individual subjects in the EC condition (top) and EO condition (bottom).

Figure 3. a) Mean synchronization computed by averaging synchronization between all pairs of electrodes in a given frequency band for EC (top) and EO (bottom).

The asterisks indicate statistical significance in a Kruskal-Wallis test. b) Mean synchronization for every electrode computed by averaging the synchronization values between a given electrode and every other electrode in a given frequency band as labeled on the plots. The p values are obtained from a Kurkas-Wallis test and indicate statistical significance in the control to patient contrast for the specific band. Asterisks indicates channels that show statistically significant differences (p<0.05) between patients and controls.

Figure 4. Connectivity matrices showing synchronization between each pair of electrodes in the a) q band and b) a_h band for EC and EO as labeled on the plots.

The spatial distribution is shown in the network diagrams in the right panels for the two cases where large differences were seen in the controls vs LTLE patient contrast. The line thickness indicates the connection strength. All figures are thresholded at p<0.05.

Figure 5. Graph theory metrics ε (top row), γ (middle row) and σ (bottom row) in the θ and α_h bands as labelled on the figure.

The metrics are plotted against a proportional threshold in the range 0.3

Figure 6. a) Graph theory efficiency metric for each electrode computed by averaging the efficiency of the electrode with all other electrodes.

b) Graph theory clustering coefficient metric for each electrode. c) Clustering coefficient versus efficiency. For all three figures the left plots are for the q band while the right are for the a_h band. The asterisks indicate statistical significance from a Kruskal-Wallis test. All results are for the EC condition. Topology of electrodes showing statistical significance on a Kurkas-Wallis test in figures a and b are shown in the abscissa.