Altered Functional and Structural Connectivity Networks in Psychogenic Non-Epileptic Seizures

Ju-Rong Ding,Jinmei Li,Guo-Rong Wu,Dong Zhou,Dongmei An,Olaf Sporns,Qiang Xu,Zhiliang Long,Wei Liao,Huafu Chen,Qiyong Gong,Marcus Kaiser

doi:10.1371/journal.pone.0063850

Abstract

Psychogenic non-epileptic seizures (PNES) are paroxysmal behaviors that resemble epileptic seizures but lack abnormal electrical activity. Recent studies suggest aberrant functional connectivity involving specific brain regions in PNES. Little is known, however, about alterations of topological organization of whole-brain functional and structural connectivity networks in PNES. We constructed functional connectivity networks from resting-state functional MRI signal correlations and structural connectivity networks from diffusion tensor imaging tractography in 17 PNES patients and 20 healthy controls. Graph theoretical analysis was employed to compute network properties. Moreover, we investigated the relationship between functional and structural connectivity networks. We found that PNES patients exhibited altered small-worldness in both functional and structural networks and shifted towards a more regular (lattice-like) organization, which could serve as a potential imaging biomarker for PNES. In addition, many regional characteristics were altered in structural connectivity network, involving attention, sensorimotor, subcortical and default-mode networks. These regions with altered nodal characteristics likely reflect disease-specific pathophysiology in PNES. Importantly, the coupling strength of functional-structural connectivity was decreased and exhibited high sensitivity and specificity to differentiate PNES patients from healthy controls, suggesting that the decoupling strength of functional-structural connectivity might be an important characteristic reflecting the mechanisms of PNES. This is the first study to explore the altered topological organization in PNES combining functional and structural connectivity networks, providing a new way to understand the pathophysiological mechanisms of PNES.

Highlights

Psychogenic non-epileptic seizures (PNES) are paroxysmal behaviors, such as involuntary movement, sensation, or experience, which resemble epileptic seizures, but are not accompanied by abnormal electrical activity in the brain [1,2]
Increased bWi and bBi were found in bilateral superior parietal gyrus, putamen, left caudate nucleus, inferior occipital gyrus, and postcentral gyrus, and increased bWi was found in bilateral orbital part of superior frontal gyrus, right caudate nucleus, hippocampus and amygdala; decreased bWi and bBi were found in bilateral insula, and decreased bWi was found in right parahippocampal gyrus, superior temporal pole, and left superior temporal gyrus (Fig. 3C and Fig. S2C). For both weighted and binarized functional connectivity networks, we found no significant differences of nodal characteristics in PNES patients
We found that regions with decreased characteristics in PNES patients were mainly involved in attention, sensorimotor and default-mode networks, and increased regional characteristics were mainly in subcortical systems and some other regions

Summary

Introduction

Psychogenic non-epileptic seizures (PNES) are paroxysmal behaviors, such as involuntary movement, sensation, or experience, which resemble epileptic seizures, but are not accompanied by abnormal electrical activity in the brain [1,2]. Aetiology facilitated the pathophysiology of PNES, the condition is still mysterious, and only a few lines of evidence from multiple modalities have indicated underlying distributed cortical abnormalities. An EEG synchronization study revealed decreased prefrontal and parietal synchronization in PNES, reflecting dysfunction of fronto-parietal networks [7]. A resting-state functional MRI (fMRI) study implied increased functional connectivity between emotional, executive control and sensorimotor networks in PNES [8]. Together, these studies point to an aberrant functional connectivity in specific brain networks. Little is known, yet, about changes in whole-brain large-scale functional and structural connectivity network in patients with PNES

Methods

Results

Discussion

Conclusion