Disrupted Structural and Functional Networks and Their Correlation with Alertness in Right Temporal Lobe Epilepsy: A Graph Theory Study

Abstract

Previous studies have shown that temporal lobe epilepsy (TLE) involves abnormal structural or functional connectivity in specific brain areas. However, limited comprehensive studies have been conducted on TLE associated changes in the topological organization of structural and functional networks. Additionally, epilepsy is associated with impairment in alertness, a fundamental component of attention. In this study, structural networks were constructed using diffusion tensor imaging tractography, and functional networks were obtained from resting-state functional MRI temporal series correlations in 20 right temporal lobe epilepsy (rTLE) patients and 19 healthy controls. Global network properties were computed by graph theoretical analysis, and correlations were assessed between global network properties and alertness. The results from these analyses showed that rTLE patients exhibit abnormal small-world attributes in structural and functional networks. Structural networks shifted toward more regular attributes, but functional networks trended toward more random attributes. After controlling for the influence of the disease duration, negative correlations were found between alertness, small-worldness, and the cluster coefficient. However, alertness did not correlate with either the characteristic path length or global efficiency in rTLE patients. Our findings show that disruptions of the topological construction of brain structural and functional networks as well as small-world property bias are associated with deficits in alertness in rTLE patients. These data suggest that reorganization of brain networks develops as a mechanism to compensate for altered structural and functional brain function during disease progression.

Resting‐state brain entropy in right temporal lobe epilepsy and its relationship with alertness

“…MRI studies have revealed that brain functional connectivity, the amplitude of low‐frequency fluctuations (ALFFs), regional homogeneity (ReHo), the fractional anisotropy (FA) of white matter fibers, topological properties, and many other indicators are altered in patients with TLE (Bernhardt, Hong, Bernasconi, & Bernasconi, ; DeSalvo, Douw, Tanaka, Reinsberger, & Stufflebeam, ; Jiang, Li, Chen, Ye, & Zheng, ; Liao et al, ); thus, the function and structure of the brain in TLE patients are damaged to varying degrees. However, how the regularity and complexity of rs‐fMRI time series are altered in rTLE patients is still unknown.…”

Progressive topological disorganization of brain network in focal epilepsy

“…2,5 The small-world network is characterized by a high level of integration and segregation. [11][12][13][14][15] However, of these modalities, the DTI has been rarely used to investigate the connectivity in patients with focal epilepsy, [12][13][14][15] despite the reproducibility of graph theory metrics from structural connectomes based on DTI being remarkably accurate. [11][12][13][14][15] However, of these modalities, the DTI has been rarely used to investigate the connectivity in patients with focal epilepsy, [12][13][14][15] despite the reproducibility of graph theory metrics from structural connectomes based on DTI being remarkably accurate.…”

“…17,18 In addition, they are highly modulated by attention, medications, and cognitive state. [12][13][14][15] Previous studies in patients with focal epilepsy using graph theory analysis have revealed various results, including both a more regular 4,20 and a more random network topology. Only a few studies investigated graph theoretical analysis in patients with focal epilepsy based on DTI, and most of them recruited patients with mesial temporal lobe epilepsy.…”

“…6 Recently, there has also been an emerging role of graph theory in the research of epilepsy, 2 and various modalities have been used to evaluate the topological properties, such as electroencephalography (EEG), 7 magnetoencephalography (MEG), 8 resting state-functional magnetic resonance imaging (rs-fMRI), 9 cortical thickness or volumes, 4,10 and diffusion tensor image (DTI). [11][12][13][14][15] However, of these modalities, the DTI has been rarely used to investigate the connectivity in patients with focal epilepsy, [12][13][14][15] despite the reproducibility of graph theory metrics from structural connectomes based on DTI being remarkably accurate. 16 Compared to DTI study, studies of functional connectivity based on EEG, MEG, and rs-fMRI have dynamic properties over time and a level of within-subject variability that is caused by changes in signal transmission time delay and local interactions between cells.…”

“…Only a few studies investigated graph theoretical analysis in patients with focal epilepsy based on DTI, and most of them recruited patients with mesial temporal lobe epilepsy. [12][13][14][15] Previous studies in patients with focal epilepsy using graph theory analysis have revealed various results, including both a more regular 4,20 and a more random network topology. 21,22 These discrepancies across studies may originate from the differences in the modality of connectivity measures but are likely also influenced by epilepsyrelated factors, such as duration of epilepsy.…”