Characteristics of Resting-State Functional Connectivity in Intractable Unilateral Temporal Lobe Epilepsy Patients with Impaired Executive Control Function.

Chao Zhang,Kuncheng Li,Chang Liu,Wen Qin,Nan Chen,Hongyu Yang,Zhigang Qi

doi:10.3389/fnhum.2017.00609

Abstract

Executive control function (ECF) deficit is a common complication of temporal lobe epilepsy (TLE). Characteristics of brain network connectivity in TLE with ECF dysfunction are still unknown. The aim of this study was to investigate resting-state functional connectivity (FC) changes in patients with unilateral intractable TLE with impaired ECF. Forty right-handed patients with left TLE confirmed by comprehensive preoperative evaluation and postoperative pathological findings were enrolled. The patients were divided into normal ECF (G1) and decreased ECF (G2) groups according to whether they showed ECF impairment on the Wisconsin Card Sorting Test (WCST). Twenty-three healthy volunteers were recruited as the healthy control (HC) group. All subjects underwent resting-state functional magnetic resonance imaging (rs-fMRI). Group-information-guided independent component analysis (GIG-ICA) was performed to estimate resting-state networks (RSNs) for all subjects. General linear model (GLM) was employed to analyze intra-network FC (p < 0.05, false discovery rate, FDR correction) and inter-network FC (p < 0.05, Bonferroni correction) of RSN among three groups. Pearson correlations between FC and neuropsychological tests were also determined through partial correlation analysis (p < 0.05). Eleven meaningful RSNs were identified from 40 left TLE and 23 HC subjects. Comparison of intra-network FC of all 11 meaningful RSNs did not reveal significant difference among the three groups (p > 0.05, FDR correction). For inter-network analysis, G2 exhibited decreased FC between the executive control network (ECN) and default-mode network (DMN) when compared with G1 (p = 0.000, Bonferroni correction) and HC (p = 0.000, Bonferroni correction). G1 showed no significant difference of FC between ECN and DMN when compared with HC. Furthermore, FC between ECN and DMN had significant negative correlation with perseverative responses (RP), response errors (RE) and perseverative errors (RPE) and had significant positive correlation categories completed (CC) in both G1 and G2 (p < 0.05). No significant difference of Montreal Cognitive Assessment (MoCA) was found between G1 and G2, while intelligence quotient (IQ) testing showed significant difference between G1and G2.There was no correlation between FC and either MoCA or IQ performance. Our findings suggest that ECF impairment in unilateral TLE is not confined to the diseased temporal lobe. Decreased FC between DMN and ECN may be an important characteristic of RSN in intractable unilateral TLE.

Highlights

Cognitive impairment is a common complication of epilepsy that can decrease quality of life and increase condition-associated costs (Bell et al, 2011; Keezer et al, 2016)
The 11 meaningful resting-state network (RSN) across all subjects were the dorsal sensorimotor-related network, executive control network (ECN), occipital pole visual network, medial VN, anterior default-mode network, left frontoparietal network, right FPN, visuospatial network (VSN), ventral SMN, DMN and posterior part of DMN, that all of the RSNs were consistent with previous reports (Supplementary Figure S1; Mantini et al, 2007; Seeley et al, 2007; Yeo et al, 2011; Wang et al, 2014; Du et al, 2015; Raichle, 2015; de Campos et al, 2016; Ma et al, 2016)
G2 showed significantly decreased functional connectivity (FC) between the DMN and ECN when compared with G1 and healthy control (HC) (Bonferroni corrected, both p < 0.05)

Summary

Introduction

Cognitive impairment is a common complication of epilepsy that can decrease quality of life and increase condition-associated costs (Bell et al, 2011; Keezer et al, 2016). The pathogenetic mechanism of TLE with ECF impairment remains unclear (Royall et al, 2002) Both morphological and diffusion tensor imaging (DTI) researches on ECF in TLE patients had conflicting results. Such as, early studies reported that the hippocampus may be a major contributor to ECF in TLE (Corcoran and Upton, 1993; Giovagnoli, 2001); another study believed that prefrontal cortex (PFC) was a key structure (Keller et al, 2009).

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