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Resting state functional connectivity of the pain matrix and default mode network in irritable bowel syndrome: a graph theoretical analysis.

ABSTRACT: Irritable bowel syndrome (IBS) is a functional disorder of brain-gut interactions. Differential brain responses to rectal distention between IBS and healthy controls (HCs) have been demonstrated, particularly in the pain matrix and the default mode network. This study aims to compare resting-state functional properties of these networks between IBS patients and HCs using graph analysis in two independent cohorts. We used a weighted graph analysis of the adjacency matrix based on partial correlations between time series in the different regions in each subject to determine subject specific graph measures. These graph measures were normalized by values obtained in equivalent random networks. We did not find any significant differences between IBS patients and controls in global normalized graph measures, hubs, or modularity structure of the pain matrix and the DMN in any of our two independent cohorts. Furthermore, we did not find consistent associations between these global network measures and IBS symptom severity or GI-specific anxiety but we found a significant difference in the relationship between measures of psychological distress (anxiety and/or depressive symptoms) and normalized characteristic path length. The responses of these networks to visceral stimulation rather than their organisation at rest may be primarily disturbed in IBS.

SUBMITTER: Kano M

PROVIDER: S-EPMC7335204 | biostudies-literature | 2020 Jul

REPOSITORIES: biostudies-literature

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Resting state functional connectivity of the pain matrix and default mode network in irritable bowel syndrome: a graph theoretical analysis.

Kano Michiko M Grinsvall Cecilia C Ran Qian Q Dupont Patrick P Morishita Joe J Muratsubaki Tomohiko T Mugikura Shunji S Ly Huynh Giao HG Törnblom Hans H Ljungberg Maria M Takase Kei K Simrén Magnus M Van Oudenhove Lukas L Fukudo Shin S

Scientific reports 20200703 1

Irritable bowel syndrome (IBS) is a functional disorder of brain-gut interactions. Differential brain responses to rectal distention between IBS and healthy controls (HCs) have been demonstrated, particularly in the pain matrix and the default mode network. This study aims to compare resting-state functional properties of these networks between IBS patients and HCs using graph analysis in two independent cohorts. We used a weighted graph analysis of the adjacency matrix based on partial correlat ...[more]

PMID: 32620938

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Project description:Interhemispheric connectivity with resting state MEG has been elusive, and demonstration of the default mode network (DMN) yet more challenging. Recent seed-based MEG analyses have shown interhemispheric connectivity using power envelope correlations. The purpose of this study is to compare graph theoretic maps of brain connectivity generated using MEG with and without signal leakage correction to evaluate for the presence of interhemispheric connectivity. Eight minutes of resting state eyes-open MEG data were obtained in 22 normal male subjects enrolled in an IRB-approved study (ages 16-18). Data were processed using an in-house automated MEG processing pipeline and projected into standard (MNI) source space at 7mm resolution using a scalar beamformer. Mean beta-band amplitude was sampled at 2.5second epochs from the source space time series. Leakage correction was performed in the time domain of the source space beam formed signal prior to amplitude transformation. Graph theoretic voxel-wise source space correlation connectivity analysis was performed for leakage corrected and uncorrected data. Degree maps were thresholded across subjects for the top 20% of connected nodes to identify hubs. Additional degree maps for sensory, visual, motor, and temporal regions were generated to identify interhemispheric connectivity using laterality indices. Hubs for the uncorrected MEG networks were predominantly symmetric and midline, bearing some resemblance to fMRI networks. These included the cingulate cortex, bilateral inferior frontal lobes, bilateral hippocampal formations and bilateral cerebellar hemispheres. These uncorrected networks however, demonstrated little to no interhemispheric connectivity using the ROI-based degree maps. Leakage corrected MEG data identified the DMN, with hubs in the posterior cingulate and biparietal areas. These corrected networks demonstrated robust interhemispheric connectivity for the ROI-based degree maps. Graph theoretic analysis of MEG resting state data without signal leakage correction can demonstrate symmetric networks with some resemblance to fMRI networks. These networks however, are an artifact of high local correlation from signal leakage and lack interhemispheric connectivity. Following signal leakage correction, MEG hubs emerge in the DMN, with strong interhemispheric connectivity.

Project description:BackgroundFibromyalgia (FM) is a disabling chronic pain syndrome with unknown pathophysiology. Functional magnetic resonance imaging studies on FM have suggested altered brain connectivity between the insula and the default mode network (DMN). However, this connectivity change has not been characterized through direct neural signals for exploring the embedded spectrotemporal features and the pertinent clinical relevance.MethodsWe recorded the resting-state magnetoencephalographic activities of 28 patients with FM and 28 age- and sex-matched controls, and analyzed the source-based functional connectivity between the insula and the DMN at 1-40 Hz by using the minimum norm estimates and imaginary coherence methods. We also measured the connectivity between the DMN and the primary visual (V1) and somatosensory (S1) cortices as intrapatient negative controls. Connectivity measurement was further correlated with the clinical parameters of FM.ResultsCompared with the controls, patients with FM reported more tender points (15.2±2.0 vs. 5.9±3.7) and higher total tenderness score (TTS; 29.1±7.0 vs. 7.7±5.5; both p < 0.001); they also had decreased insula-DMN connectivity at the theta band (4-8 Hz; left, p = 0.007; right, p = 0.035), but displayed unchanged V1-DMN and S1-DMN connectivity (p > 0.05). When patients with FM and the controls were combined together, the insula-DMN theta connectivity was negatively correlated with the number of tender points (left insula, r = -0.428, p = 0.001; right insula, r = -0.4, p = 0.002) and TTS score (left insula, r = -0.429, p = 0.001; right insula, r = -0.389, p = 0.003). Furthermore, in patients with FM, the right insula-DMN connectivity at the beta band (13-25 Hz) was negatively correlated with the number of tender points (r = -0.532, p = 0.004) and TTS (r = -0.428, p = 0.023), and the bilateral insula-DMN connectivity at the delta band (1-4 Hz) was negatively correlated with FM Symptom Severity (left: r = -0.423, p = 0.025; right: r = -0.437, p = 0.020) and functional disability (Fibromyalgia Impact Questionnaire; left: r = -0.415, p = 0.028; right: r = -0.374, p = 0.050).ConclusionsWe confirmed the frequency-specific reorganization of the insula-DMN connectivity in FM. The clinical relevance of this connectivity change may warrant future studies to elucidate its causal relationship and potential as a neurological signature for FM.

Dataset Information

Resting state functional connectivity of the pain matrix and default mode network in irritable bowel syndrome: a graph theoretical analysis.

Publications

Resting state functional connectivity of the pain matrix and default mode network in irritable bowel syndrome: a graph theoretical analysis.

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