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An imbalance between functional segregation and integration in patients with pontine stroke: A dynamic functional network connectivity study

BACKGROUND: Previous studies on brain functional connectivity have revealed the neural physiopathology in patients with pontine stroke (PS). However, those studies focused only on the static features of intrinsic fluctuations, rather than on the time-varying effects throughout the entire scan. In th...

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Autores principales: Wang, Yingying, Wang, Caihong, Miao, Peifang, Liu, Jingchun, Wei, Ying, Wu, Luobing, Wang, Kaiyu, Cheng, Jingliang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Elsevier 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7714678/
https://www.ncbi.nlm.nih.gov/pubmed/33395996
http://dx.doi.org/10.1016/j.nicl.2020.102507
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author Wang, Yingying
Wang, Caihong
Miao, Peifang
Liu, Jingchun
Wei, Ying
Wu, Luobing
Wang, Kaiyu
Cheng, Jingliang
author_facet Wang, Yingying
Wang, Caihong
Miao, Peifang
Liu, Jingchun
Wei, Ying
Wu, Luobing
Wang, Kaiyu
Cheng, Jingliang
author_sort Wang, Yingying
collection PubMed
description BACKGROUND: Previous studies on brain functional connectivity have revealed the neural physiopathology in patients with pontine stroke (PS). However, those studies focused only on the static features of intrinsic fluctuations, rather than on the time-varying effects throughout the entire scan. In the present study, we sought to explore the underlying mechanism of PS using the dynamic functional network connectivity (dFNC) method. METHODS: Resting-state functional magnetic resonance imaging (fMRI) data were collected from 58 patients with PS and 52 healthy controls (HC). Independent component analysis (ICA), the sliding window method, and k-means clustering analysis were performed to extract different functional networks, to calculate dFNC matrices, and to estimate distinct dynamic connectivity states. Additionally, temporal features were compared between the two groups in each state to explore the brain’s preference for different dynamic connectivity states in PS, and global and local efficiency were compared among states to explore the differences of topologic organization across different dFNC states. The correlations between clinical scales and the temporal features that differed between the two groups also were calculated. RESULTS: The dFNC analyses suggested four recurring states; in two of these states, the PS group showed a different duration from that of the HC group. Patients with PS spent significantly more time in a sparsely connected state (State 1), which was characterized by relatively low levels of connectivity within and between all brain networks. In contrast, patients with PS spent significantly less time in a highly segregated state (State 2), which was characterized by high levels of positive connectivities within primary perceptional domains and within higher cognitive control domains, and by high levels of negative inter-functional connectivities (inter-FCs) among primary perceptional and higher cognitive control domains. Additionally, the dwell time in State 2 was positively correlated with HC group’s long-term memory scores in the Rey Auditory Verbal Learning Test (RAVLT-L), whereas there was no correlation between the State-2 dwell time and RAVLT-L scores in the PS group. Furthermore, the sparsely connected state and the highly segregated state mentioned above had the highest global efficiency and the highest local efficiency among the four states, respectively. CONCLUSIONS: In summary, we observed a preference in the aberrant brain for dynamic connectivity states with different network topologic organization in patients with PS, indicating abnormal functional segregation and integration of the whole brain and confirming the imperfection of functional network connectivity in patients with PS. These findings provide new evidence for the dynamic neural mechanisms underlying clinical symptoms in patients with PS.
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spelling pubmed-77146782020-12-09 An imbalance between functional segregation and integration in patients with pontine stroke: A dynamic functional network connectivity study Wang, Yingying Wang, Caihong Miao, Peifang Liu, Jingchun Wei, Ying Wu, Luobing Wang, Kaiyu Cheng, Jingliang Neuroimage Clin Regular Article BACKGROUND: Previous studies on brain functional connectivity have revealed the neural physiopathology in patients with pontine stroke (PS). However, those studies focused only on the static features of intrinsic fluctuations, rather than on the time-varying effects throughout the entire scan. In the present study, we sought to explore the underlying mechanism of PS using the dynamic functional network connectivity (dFNC) method. METHODS: Resting-state functional magnetic resonance imaging (fMRI) data were collected from 58 patients with PS and 52 healthy controls (HC). Independent component analysis (ICA), the sliding window method, and k-means clustering analysis were performed to extract different functional networks, to calculate dFNC matrices, and to estimate distinct dynamic connectivity states. Additionally, temporal features were compared between the two groups in each state to explore the brain’s preference for different dynamic connectivity states in PS, and global and local efficiency were compared among states to explore the differences of topologic organization across different dFNC states. The correlations between clinical scales and the temporal features that differed between the two groups also were calculated. RESULTS: The dFNC analyses suggested four recurring states; in two of these states, the PS group showed a different duration from that of the HC group. Patients with PS spent significantly more time in a sparsely connected state (State 1), which was characterized by relatively low levels of connectivity within and between all brain networks. In contrast, patients with PS spent significantly less time in a highly segregated state (State 2), which was characterized by high levels of positive connectivities within primary perceptional domains and within higher cognitive control domains, and by high levels of negative inter-functional connectivities (inter-FCs) among primary perceptional and higher cognitive control domains. Additionally, the dwell time in State 2 was positively correlated with HC group’s long-term memory scores in the Rey Auditory Verbal Learning Test (RAVLT-L), whereas there was no correlation between the State-2 dwell time and RAVLT-L scores in the PS group. Furthermore, the sparsely connected state and the highly segregated state mentioned above had the highest global efficiency and the highest local efficiency among the four states, respectively. CONCLUSIONS: In summary, we observed a preference in the aberrant brain for dynamic connectivity states with different network topologic organization in patients with PS, indicating abnormal functional segregation and integration of the whole brain and confirming the imperfection of functional network connectivity in patients with PS. These findings provide new evidence for the dynamic neural mechanisms underlying clinical symptoms in patients with PS. Elsevier 2020-11-19 /pmc/articles/PMC7714678/ /pubmed/33395996 http://dx.doi.org/10.1016/j.nicl.2020.102507 Text en © 2020 The Authors http://creativecommons.org/licenses/by-nc-nd/4.0/ This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
spellingShingle Regular Article
Wang, Yingying
Wang, Caihong
Miao, Peifang
Liu, Jingchun
Wei, Ying
Wu, Luobing
Wang, Kaiyu
Cheng, Jingliang
An imbalance between functional segregation and integration in patients with pontine stroke: A dynamic functional network connectivity study
title An imbalance between functional segregation and integration in patients with pontine stroke: A dynamic functional network connectivity study
title_full An imbalance between functional segregation and integration in patients with pontine stroke: A dynamic functional network connectivity study
title_fullStr An imbalance between functional segregation and integration in patients with pontine stroke: A dynamic functional network connectivity study
title_full_unstemmed An imbalance between functional segregation and integration in patients with pontine stroke: A dynamic functional network connectivity study
title_short An imbalance between functional segregation and integration in patients with pontine stroke: A dynamic functional network connectivity study
title_sort imbalance between functional segregation and integration in patients with pontine stroke: a dynamic functional network connectivity study
topic Regular Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7714678/
https://www.ncbi.nlm.nih.gov/pubmed/33395996
http://dx.doi.org/10.1016/j.nicl.2020.102507
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