Dataset Information

Aberrant functional metastability and structural connectivity are associated with rumination in individuals with major depressive disorder.

ABSTRACT: Rumination is a repetitive and compulsive thinking focusing on oneself, and the nature and consequences of distress. It is a core characteristic in psychiatric disorders characterized by affective dysregulation, and emerging evidence suggests that rumination is associated with aberrant dynamic functional connectivity and structural connectivity. However, the underlying neural mechanisms remain poorly understood. Here, we adopted a multimodal approach and tested the hypothesis that white matter connectivity forms the basis of the implications of temporal dynamics of functional connectivity in the rumination trait. Fifty-three depressed and ruminative individuals and a control group of 47 age- and gender-matched individuals with low levels of rumination underwent resting-state fMRI and diffusion tensor imaging. We found that lower global metastability and higher global synchrony of the dynamic functional connectivity were associated with higher levels of rumination. Specifically, the altered global synchrony and global metastability mediated the association between white matter integrity of the genu of the corpus callosum to rumination. Hence, our findings offered the first line of evidence for the intricate role of (sub)optimal transition of functional brain states in the connection of structural brain connectivity in ruminative thinking.

SUBMITTER: Zhang R

PROVIDER: S-EPMC8693354 | biostudies-literature | 2021 Dec

REPOSITORIES: biostudies-literature

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Aberrant functional metastability and structural connectivity are associated with rumination in individuals with major depressive disorder.

Zhang Ruibin R Tam Sammi-Kenzie T S STS Wong Nichol M L NML Wu Jingsong J Tao Jing J Chen Lidian L Lin Kangguang K Lee Tatia M C TMC

NeuroImage. Clinical 20211214

Rumination is a repetitive and compulsive thinking focusing on oneself, and the nature and consequences of distress. It is a core characteristic in psychiatric disorders characterized by affective dysregulation, and emerging evidence suggests that rumination is associated with aberrant dynamic functional connectivity and structural connectivity. However, the underlying neural mechanisms remain poorly understood. Here, we adopted a multimodal approach and tested the hypothesis that white matter c ...[more]

PMID: 34923200

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Project description:Thalamocortical circuitry has a substantial impact on emotion and cognition. Previous studies have demonstrated alterations in thalamocortical functional connectivity (FC), characterized by region-dependent hypo- or hyper-connectivity, among individuals with major depressive disorder (MDD). However, the dynamical reconfiguration of the thalamocortical system over time and potential abnormalities in dynamic thalamocortical connectivity associated with MDD remain unclear. Hence, we analyzed dynamic FC (dFC) between ten thalamic subregions and seven cortical subnetworks from resting-state functional magnetic resonance images of 48 patients with MDD and 57 healthy controls (HCs) to investigate time-varying changes in thalamocortical FC in patients with MDD. Moreover, dynamic laterality analysis was conducted to examine the changes in functional lateralization of the thalamocortical system over time. Correlations between the dynamic measures of thalamocortical FC and clinical assessment were also calculated. We identified four dynamic states of thalamocortical circuitry wherein patients with MDD exhibited decreased fractional time and reduced transitions within a negative connectivity state that showed strong correlations with primary cortical networks, compared with the HCs. In addition, MDD patients also exhibited increased fluctuations in functional laterality in the thalamocortical system across the scan duration. The thalamo-subnetwork analysis unveiled abnormal dFC variability involving higher-order cortical networks in the MDD cohort. Significant correlations were found between increased dFC variability with dorsal attention and default mode networks and the severity of symptoms. Our study comprehensively investigated the pattern of alteration of the thalamocortical dFC in MDD patients. The heterogeneous alterations of dFC between the thalamus and both primary and higher-order cortical networks may help characterize the deficits of sensory and cognitive processing in MDD.

Project description:Major depressive disorder (MDD) is a complex mood disorder characterized by persistent and overwhelming depression. Previous studies have identified abnormalities in large scale functional brain networks in MDD, yet most of them were based on static functional connectivity. In contrast, here we explored disrupted topological organization of dynamic functional network connectivity (dFNC) in MDD based on graph theory. One hundred and eighty-two MDD patients and 218 healthy controls were included in this study, all Chinese Han people. By applying group information guided independent component analysis (GIG-ICA) to resting-state functional magnetic resonance imaging (fMRI) data, the dFNCs of each subject were estimated using a sliding window method and k-means clustering. Network properties including global efficiency, local efficiency, node strength and harmonic centrality, were calculated for each subject. Five dynamic functional states were identified, three of which demonstrated significant group differences in their percentage of state occurrence. Interestingly, MDD patients spent much more time in a weakly-connected State 2, which includes regions previously associated with self-focused thinking, a representative feature of depression. In addition, the FNCs in MDD were connected differently in different states, especially among prefrontal, sensorimotor, and cerebellum networks. MDD patients exhibited significantly reduced harmonic centrality primarily involving parietal lobule, lingual gyrus and thalamus. Moreover, three dFNCs with disrupted node properties were commonly identified in different states, and also correlated with depressive symptom severity and cognitive performance. This study is the first attempt to investigate the dynamic functional abnormalities in MDD in a Chinese population using a relatively large sample size, which provides new evidence on aberrant time-varying brain activity and its network disruptions in MDD, which might underscore the impaired cognitive functions in this mental disorder.

Project description:BackgroundMajor depressive disorder (MDD) is a debilitating mental illness that has been linked to increases in markers of inflammation, as well as to changes in brain functional and structural connectivity, particularly between the insula and the subgenual anterior cingulate cortex (sgACC). In this study, we directly related inflammation and dysconnectivity in treatment-resistant MDD by concurrently measuring the following: microglial activity with [18F]N-2-(fluoroethoxyl)benzyl-N-(4phenoxypyridin-3-yl)acetamide ([18F]FEPPA) positron emission tomography (PET); the severity of MDD; and functional or structural connectivity among insula or sgACC nodes.MethodsTwelve patients with treatment-resistant MDD (8 female, 4 male; mean age ± standard deviation 54.9 ± 4.5 years and 23 healthy controls (11 female, 12 male; 60.3 ± 8.5 years) completed a hybrid [18F]FEPPA PET and MRI acquisition. From these, we extracted relative standardized uptake values for [18F]FEPPA activity and Pearson r-to-z scores representing functional connectivity from our regions of interest. We extracted diffusion tensor imaging metrics from the cingulum bundle, a key white matter bundle in MDD. We performed regressions to relate microglial activity with functional connectivity, structural connectivity and scores on the 17-item Hamilton Depression Rating Scale.ResultsWe found significantly increased [18F]FEPPA uptake in the left sgACC in patients with treatment-resistant MDD compared to healthy controls. Patients with MDD also had a reduction in connectivity between the sgACC and the insula. The [18F]FEPPA uptake in the left sgACC was significantly related to functional connectivity with the insula, and to the structural connectivity of the cingulum bundle. [18F]FEPPA uptake also predicted scores on the Hamilton Depression Rating Scale.Limitations: A relatively small sample size, lack of functional task data and concomitant medication use may have affected our findings.ConclusionWe present preliminary evidence linking a network-level dysfunction relevant to the pathophysiology of depression and related to increased microglial activity in MDD.

Dataset Information

Aberrant functional metastability and structural connectivity are associated with rumination in individuals with major depressive disorder.

Publications

Aberrant functional metastability and structural connectivity are associated with rumination in individuals with major depressive disorder.

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