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Reconfigured functional network dynamics in adult moyamoya disease: a resting-state fMRI study

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Abstract

Treatment of vascular cognitive impairment (VCI) in adult moyamoya disease (MMD) is still unclear because of its unveiled neural synchronization. This study introduced a dynamic measurement of connectivity number entropy (CNE) to characterize both spatial and temporal dimensions of network interactions. Fifty-one patients with MMD were recruited (27 with VCI and 24 with intact cognition), as well as 26 normal controls (NCs). Static network properties were first examined to confirm its aberrance in MMD with VCI. Then, the dynamic measurement of CNE was used to detect the deteriorated flexibility of MMD with VCI at global, regional, and network levels. Finally, dynamic reconfiguration of flexible and specialized regions was traced across the three groups. Graph theory analysis indicated that MMD exhibited “small-world” network topology but presented with a deviating pattern from NC as the disease progressed in all topologic metrics of integration, segregation, and small-worldness. Subsequent dynamic analysis showed significant CNE differences among the three groups at both global (p < 0.001) and network levels (default mode network, p = 0.004; executive control network, p = 0.001). Specifically, brain regions related to key aspects of information processing exhibited significant CNE changes across the three groups. Furthermore, CNE values of both flexible and specialized regions changed with impaired cognition. This study not only sheds light on both the static and dynamic organizational principles behind network changes in adult MMD for the first time, but also provides a new methodologic viewpoint to acquire more knowledge of its pathophysiology and treatment direction.

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Funding

This study was supported by the National Natural Science Foundation of China (No. 81771237, 81801155 & 11105062); the National Key Research and Development Program (No. SQ2016YFSF110141); the Fundamental Research Funds for the Central Universities (No. lzujbky-2015-119); the Natural Science Foundation and Major Basic Research Program of Shanghai (No. 16JC1420100); the “Dawn” Program of Shanghai Education Commission (No. 16SG02); and the Scientific Research Project of Huashan Hospital, Fudan University (No. 2016QD082).

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Author notes

  1. Yu Lei and Benshen Song have an equal contribution on this work as the first authors.

Authors and Affiliations

  1. Department of Neurosurgery, Huashan Hospital, Fudan University, Wulumuqi Zhong Road 12, Shanghai, 200040, China

    Yu Lei, Liang Chen, Jiabin Su, Xin Zhang, Wei Ni, Bin Xu, Yuxiang Gu & Ying Mao

  2. Institute of Theoretical Physics, Key Laboratory for Magnetism and Magnetic Materials of the Ministry of Education, Lanzhou University, Lanzhou, 730000, China

    Benshen Song & Lianchun Yu

  3. School of Life Science and the State Key Laboratory of Medical Neurobiology, Institutes of Brain Science and the Collaborative Innovation Center for Brain Science, Fudan University, Shanghai, 200040, China

    Yuguo Yu

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  1. Yu Lei
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  2. Benshen Song
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  3. Liang Chen
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  4. Jiabin Su
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  5. Xin Zhang
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  6. Wei Ni
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  9. Lianchun Yu
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Correspondence to Lianchun Yu or Yuxiang Gu.

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This manuscript has been read and approved by all authors, who acknowledge due care in ensuring the integrity of the work. All authors have made substantial contributions to the design, collection, analysis and/or interpretation of data, and many have contributed to the writing and intellectual content of the article.

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All procedures performed in this study involving human participants were approved by the Institutional Ethics Committee of Huashan Hospital of Fudan University, and were conducted in accordance with the 1964 Helsinki declaration and its later amendments.

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Lei, Y., Song, B., Chen, L. et al. Reconfigured functional network dynamics in adult moyamoya disease: a resting-state fMRI study. Brain Imaging and Behavior 14, 715–727 (2020). https://doi.org/10.1007/s11682-018-0009-8

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