Static and dynamic interactions within the triple-network model in stroke patients with multidomain cognitive impairments

Yingying Wang; Hongxu Chen; Caihong Wang; Jingchun Liu; Peifang Miao; Ying Wei; Luobing Wu; Xin Wang; Peipei Wang; Yong Zhang; Jingliang Cheng; Siyuan Fan; Guifang Sun

NeuroImage: Clinical (Jan 2024)

Static and dynamic interactions within the triple-network model in stroke patients with multidomain cognitive impairments

Yingying Wang,
Hongxu Chen,
Caihong Wang,
Jingchun Liu,
Peifang Miao,
Ying Wei,
Luobing Wu,
Xin Wang,
Peipei Wang,
Yong Zhang,
Jingliang Cheng,
Siyuan Fan,
Guifang Sun

Affiliations

Yingying Wang: Department of MRI, Henan Key Laboratory of Magnetic Resonance Function and Molecular Imaging, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, China; Huaxi MR Research Center (HMRRC), Functional and Molecular Imaging Key Laboratory of Sichuan Province, Department of Radiology, West China Hospital, Sichuan University, Chengdu, China
Hongxu Chen: Cardiff University Brain Research Imaging Centre, United Kingdom
Caihong Wang: Department of MRI, Henan Key Laboratory of Magnetic Resonance Function and Molecular Imaging, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, China
Jingchun Liu: Department of Radiology, Tianjin Key Laboratory of Functional Imaging, Tianjin Medical University General Hospital, Tianjin, China
Peifang Miao: Department of MRI, Henan Key Laboratory of Magnetic Resonance Function and Molecular Imaging, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, China
Ying Wei: Department of MRI, Henan Key Laboratory of Magnetic Resonance Function and Molecular Imaging, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, China
Luobing Wu: Department of MRI, Henan Key Laboratory of Magnetic Resonance Function and Molecular Imaging, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, China
Xin Wang: Department of MRI, Henan Key Laboratory of Magnetic Resonance Function and Molecular Imaging, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, China
Peipei Wang: Department of MRI, Henan Key Laboratory of Magnetic Resonance Function and Molecular Imaging, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, China
Yong Zhang: Department of MRI, Henan Key Laboratory of Magnetic Resonance Function and Molecular Imaging, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, China
Jingliang Cheng: Department of MRI, Henan Key Laboratory of Magnetic Resonance Function and Molecular Imaging, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, China; Corresponding author at: Department of MRI, Henan Key Laboratory of Magnetic Resonance Function and Molecular Imaging, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, China (J. Cheng); Cardiovascular Center, Liyuan Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China (S. Fan); Department of Neurology, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, China (G. Sun).
Siyuan Fan: Cardiovascular Center, Liyuan Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China; Clinic Center of Human Gene Research, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China; Corresponding author at: Department of MRI, Henan Key Laboratory of Magnetic Resonance Function and Molecular Imaging, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, China (J. Cheng); Cardiovascular Center, Liyuan Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China (S. Fan); Department of Neurology, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, China (G. Sun).
Guifang Sun: Department of Neurology, The First Affiliated Hospital of Zhengzhou University, Henan Province 450052, China; Corresponding author at: Department of MRI, Henan Key Laboratory of Magnetic Resonance Function and Molecular Imaging, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, China (J. Cheng); Cardiovascular Center, Liyuan Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China (S. Fan); Department of Neurology, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, China (G. Sun).

Journal volume & issue: Vol. 43
p. 103655

Abstract

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Background: Internal capsule strokes often result in multidomain cognitive impairments across memory, attention, and executive function, typically due to disruptions in brain network connectivity. Our study examines these impairments by analyzing interactions within the triple-network model, focusing on both static and dynamic aspects. Methods: We collected resting-state fMRI data from 62 left (CI_L) and 56 right (CI_R) internal capsule stroke patients, along with 57 healthy controls (HC). Using independent component analysis to extract the default mode (DMN), executive control (ECN), and salience networks (SAN), we conducted static and dynamic functional network connectivity analyses (DFNC) to identify differences between stroke patients and controls. For DFNC, we used k-means clustering to focus on temporal properties and multilayer network analysis to examine integration and modularity Q, where integration represents dynamic interactions between networks, and modularity Q measures how well the network is divided into distinct modules. We then calculated the correlations between SFNC/DFNC properties with significant inter-group differences and cognitive scales. Results: Compared to HC, both CI_L and CI_R patients showed increased static FCs between SAN and DMN and decreased dynamic interactions between ECN and other networks. CI_R patients also had heightened static FCs between SAN and ECN and maintained a state with strongly positive FNCs across all networks in the triple-network model. Additionally, CI_R patients displayed decreased modularity Q. Conclusion: These findings highlight that stroke can result in the disruption of static and dynamic interactions in the triple network model, aiding our understanding of the neuropathological basis for multidomain cognitive deficits after internal capsule stroke.

Published in NeuroImage: Clinical

ISSN: 2213-1582 (Online)
Publisher: Elsevier
Country of publisher: Netherlands
LCC subjects: Medicine: Medicine (General): Computer applications to medicine. Medical informatics; Medicine: Internal medicine: Neurosciences. Biological psychiatry. Neuropsychiatry: Neurology. Diseases of the nervous system
Website: http://www.journals.elsevier.com/neuroimage-clinical/

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