Disrupted Global and Regional Structural Networks and Subnetworks in Children with Localization-Related Epilepsy

Abstract

Background and purpose: Structural connectivity has been thought to be a less sensitive measure of network changes relative to functional connectivity in children with localization-related epilepsy. The aims of this study were to investigate the structural networks in children with localization-related epilepsy and to assess the relation among structural connectivity, intelligence quotient, and clinical parameters.

Materials and methods: Forty-five children with nonlesional localization-related epilepsy and 28 healthy controls underwent DTI. Global network (network strength, clustering coefficient, characteristic path length, global efficiency, and small-world parameters), regional network (nodal efficiency), and the network-based statistic were compared between patients and controls and correlated with intelligence quotient and clinical parameters.

Results: Patients showed disrupted global network connectivity relative to controls, including reduced network strength, increased characteristic path length and reduced global efficiency, and reduced nodal efficiency in the frontal, temporal, and occipital lobes. Connectivity in multiple subnetworks was reduced in patients, including the frontal-temporal, insula-temporal, temporal-temporal, frontal-occipital, and temporal-occipital lobes. The frontal lobe epilepsy subgroup demonstrated more areas with reduced nodal efficiency and more impaired subnetworks than the temporal lobe epilepsy subgroup. Network parameters were not significantly associated with intelligence quotient, age at seizure onset, or duration of epilepsy.

Conclusions: We found disruption in global and regional networks and subnetworks in children with localization-related epilepsy. Regional efficiency and subnetworks were more impaired in frontal lobe epilepsy than in temporal lobe epilepsy. Future studies are needed to evaluate the implications of disrupted networks for surgical resection and outcomes for specific epileptogenic zones and the relation of disrupted networks to more complex cognitive function.

Fig 1.

Reduced nodal efficiency in localization-related epilepsy (A), frontal lobe epilepsy (B), and temporal lobe epilepsy (C) in patients relative to controls. The disrupted nodes with reduced nodal efficiency are shown in red, and the unaffected nodes are shown in blue. The size of the nodes is related to the significance of between-group differences in nodal efficiency, with larger nodes representing more significant (lower P value) reduced nodal efficiency in patients relative to controls.

Fig 2.

Results of the network-based statistic analysis of the following: A, Patients with localization-related epilepsy relative to controls, showing reduced connectivity involving the frontal-temporal, insula-temporal, temporal-temporal, frontal-occipital, and temporal-occipital lobes. B, Patients with frontal lobe epilepsy relative to controls, showing reduced connectivity involving the frontal-temporal, insula-temporal, temporal-temporal, temporal-occipital, and occipital-occipital lobes. C, Patients with temporal lobe epilepsy relative to controls, showing reduced connectivity involving the frontal-temporal, insula-temporal, temporal-temporal, temporal-occipital, and frontal-occipital lobes.