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Disrupted cerebellar connectivity reduces whole-brain network efficiency in multiple system atrophy

Authors

  • Chia-Feng Lu PhD,

    1. Department of Biomedical Imaging and Radiological Sciences, National Yang-Ming University, Taipei, Taiwan, ROC
    2. Integrated Brain Research Laboratory, Department of Medical Research and Education, Taipei Veterans General Hospital, Taipei, Taiwan, Republic of China
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    • Chia-Feng Lu and Bing-Wen Soong contributed equally to this article.

  • Bing-Wen Soong MD, PhD,

    1. Department of Neurology, National Yang-Ming University School of Medicine, Taipei, Taiwan, Republic of China
    2. Department of Neurology, the Neurological Institute, Taipei Veterans General Hospital, Taipei, Taiwan, Republic of China
    3. Brain Research Center, National Yang-Ming University, Taipei, Taiwan, Republic of China
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    • Chia-Feng Lu and Bing-Wen Soong contributed equally to this article.

  • Hsiu-Mei Wu MD,

    1. Department of Radiology, Taipei Veterans General Hospital, Taipei, Taiwan, Republic of China
    2. Department of Radiology, School of Medicine, National Yang-Ming University, Taipei, Taiwan, Republic of China
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  • Shin Teng BSc,

    1. Department of Biomedical Imaging and Radiological Sciences, National Yang-Ming University, Taipei, Taiwan, ROC
    2. Integrated Brain Research Laboratory, Department of Medical Research and Education, Taipei Veterans General Hospital, Taipei, Taiwan, Republic of China
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  • Po-Shan Wang MD,

    Corresponding author
    1. Brain Research Center, National Yang-Ming University, Taipei, Taiwan, Republic of China
    2. The Neurological Institute, Taipei Municipal Gan-Dau Hospital, Taipei, Taiwan, Republic of China
    3. Institute of Brain Science, National Yang-Ming University, Taipei, Taiwan, Republic of China
    • Department of Neurology, National Yang-Ming University School of Medicine, Taipei, Taiwan, Republic of China
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  • Yu-Te Wu PhD

    Corresponding author
    1. Integrated Brain Research Laboratory, Department of Medical Research and Education, Taipei Veterans General Hospital, Taipei, Taiwan, Republic of China
    2. Brain Research Center, National Yang-Ming University, Taipei, Taiwan, Republic of China
    • Department of Biomedical Imaging and Radiological Sciences, National Yang-Ming University, Taipei, Taiwan, ROC
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  • Funding agencies: This study was funded in part by the Taipei Veterans General Hospital, Taipei, Taiwan, Republic of China (V99C1-155, V100C-129, V101C-045, VGHUST100-G7-3-2,VGHUST101-G4-2-4, VGHUST101-G7-3-1), the National Science Council, Taipei, Taiwan, Republic of China (NSC100-2221-E-010-009, NSC 101-2221-E-010-004-MY2), the National Science Council supported for the Center for Dynamical Biomarkers and Translational Medicine, National Central University, Jhongli City, Taoyuan County, Taiwan, Republic of China (NSC 100-2911-I-008-001), the Brain Research Center, National Yang-Ming University, Taipei, Taiwan, Republic of China, and a grant from the Ministry of Education, Aim for the Top University Plan.

  • Relevant conflicts of interest/financial disclosures: Nothing to report.

Correspondence to: Dr. Yu-Te Wu and Dr. Po-Shan Wang, Professors, Department of Biomedical Imaging and Radiological Sciences, National Yang-Ming University, No. 155, Li-Nong Street, Section 2, Pei-Tou, Taipei, 112, Taiwan, ROC; ytwu@ym.edu.tw

ABSTRACT

Multiple system atrophy of the cerebellar type is a sporadic neurodegenerative disorder of the central nervous system. We hypothesized that the white matter degeneration of the cerebellum and pons in this disease may cause a breakdown of cerebellar structural networks and further reduce the network efficiency of cerebellar-connected cerebral regions. Diffusion tensor tractography was used to construct the structural networks of 19 cerebellar-type multiple system atrophy patients, who were compared with 19 age- and sex-matched controls. Graph theory was used to assess the small-world properties and topological organization of structure networks in both the control and patient groups. Our results showed that the cerebellar-type multiple system atrophy patients exhibited altered small-world architecture with significantly increased characteristic shortest path lengths and decreased clustering coefficients. We also found that white matter degeneration in the cerebellum was characterized by reductions in network strength (number and integrity of fiber connections) of the cerebellar regions, which further induced extensively decreased network efficiency for numerous cerebral regions. Finally, we found that the reductions in nodal efficiency of the cerebellar lobules and bilateral sensorimotor, prefrontal, and basal ganglia regions negatively correlated with the severity of ataxia for the cerebellar-type multiple system atrophy patients. This study demonstrates for the first time that the brains of cerebellar-type multiple system atrophy patients exhibit disrupted topological organization of white matter structural networks. Thus, this study provides structural evidence of the relationship between abnormalities of white matter integrity and network efficiency that occurs in cerebellar-type multiple system atrophy. © 2013 Movement Disorder Society

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