Disrupted topological organization of structural networks revealed by probabilistic diffusion tractography in Tourette syndrome children
Tourette syndrome (TS) is a childhood‐onset neurobehavioral disorder. Although previous TS studies revealed structural abnormalities in distinct corticobasal ganglia circuits, the topological alterations of the whole‐brain white matter (WM) structural networks remain poorly understood. Here, we used...
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| Published in | Human brain mapping Vol. 38; no. 8; pp. 3988 - 4008 |
|---|---|
| Main Authors | , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
John Wiley & Sons, Inc
01.08.2017
John Wiley and Sons Inc |
| Subjects | |
| Online Access | Get full text |
| ISSN | 1065-9471 1097-0193 1097-0193 |
| DOI | 10.1002/hbm.23643 |
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| Abstract | Tourette syndrome (TS) is a childhood‐onset neurobehavioral disorder. Although previous TS studies revealed structural abnormalities in distinct corticobasal ganglia circuits, the topological alterations of the whole‐brain white matter (WM) structural networks remain poorly understood. Here, we used diffusion MRI probabilistic tractography and graph theoretical analysis to investigate the topological organization of WM networks in 44 drug‐naive TS children and 41 age‐ and gender‐matched healthy children. The WM networks were constructed by estimating inter‐regional connectivity probability and the topological properties were characterized using graph theory. We found that both TS and control groups showed an efficient small‐world organization in WM networks. However, compared to controls, TS children exhibited decreased global and local efficiency, increased shortest path length and small worldness, indicating a disrupted balance between local specialization and global integration in structural networks. Although both TS and control groups showed highly similar hub distributions, TS children exhibited significant decreased nodal efficiency, mainly distributed in the default mode, language, visual, and sensorimotor systems. Furthermore, two separate networks showing significantly decreased connectivity in TS group were identified using network‐based statistical (NBS) analysis, primarily composed of the parieto‐occipital cortex, precuneus, and paracentral lobule. Importantly, we combined support vector machine and multiple kernel learning frameworks to fuse multiple levels of network topological features for classification of individuals, achieving high accuracy of 86.47%. Together, our study revealed the disrupted topological organization of structural networks related to pathophysiology of TS, and the discriminative topological features for classification are potential quantitative neuroimaging biomarkers for clinical TS diagnosis. Hum Brain Mapp 38:3988–4008, 2017. © 2017 Wiley Periodicals, Inc. |
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| AbstractList | Tourette syndrome (TS) is a childhood‐onset neurobehavioral disorder. Although previous TS studies revealed structural abnormalities in distinct corticobasal ganglia circuits, the topological alterations of the whole‐brain white matter (WM) structural networks remain poorly understood. Here, we used diffusion MRI probabilistic tractography and graph theoretical analysis to investigate the topological organization of WM networks in 44 drug‐naive TS children and 41 age‐ and gender‐matched healthy children. The WM networks were constructed by estimating inter‐regional connectivity probability and the topological properties were characterized using graph theory. We found that both TS and control groups showed an efficient small‐world organization in WM networks. However, compared to controls, TS children exhibited decreased global and local efficiency, increased shortest path length and small worldness, indicating a disrupted balance between local specialization and global integration in structural networks. Although both TS and control groups showed highly similar hub distributions, TS children exhibited significant decreased nodal efficiency, mainly distributed in the default mode, language, visual, and sensorimotor systems. Furthermore, two separate networks showing significantly decreased connectivity in TS group were identified using network‐based statistical (NBS) analysis, primarily composed of the parieto‐occipital cortex, precuneus, and paracentral lobule. Importantly, we combined support vector machine and multiple kernel learning frameworks to fuse multiple levels of network topological features for classification of individuals, achieving high accuracy of 86.47%. Together, our study revealed the disrupted topological organization of structural networks related to pathophysiology of TS, and the discriminative topological features for classification are potential quantitative neuroimaging biomarkers for clinical TS diagnosis. Hum Brain Mapp 38:3988–4008, 2017. © 2017 Wiley Periodicals, Inc. Tourette syndrome (TS) is a childhood-onset neurobehavioral disorder. Although previous TS studies revealed structural abnormalities in distinct corticobasal ganglia circuits, the topological alterations of the whole-brain white matter (WM) structural networks remain poorly understood. Here, we used diffusion MRI probabilistic tractography and graph theoretical analysis to investigate the topological organization of WM networks in 44 drug-naive TS children and 41 age- and gender-matched healthy children. The WM networks were constructed by estimating inter-regional connectivity probability and the topological properties were characterized using graph theory. We found that both TS and control groups showed an efficient small-world organization in WM networks. However, compared to controls, TS children exhibited decreased global and local efficiency, increased shortest path length and small worldness, indicating a disrupted balance between local specialization and global integration in structural networks. Although both TS and control groups showed highly similar hub distributions, TS children exhibited significant decreased nodal efficiency, mainly distributed in the default mode, language, visual, and sensorimotor systems. Furthermore, two separate networks showing significantly decreased connectivity in TS group were identified using network-based statistical (NBS) analysis, primarily composed of the parieto-occipital cortex, precuneus, and paracentral lobule. Importantly, we combined support vector machine and multiple kernel learning frameworks to fuse multiple levels of network topological features for classification of individuals, achieving high accuracy of 86.47%. Together, our study revealed the disrupted topological organization of structural networks related to pathophysiology of TS, and the discriminative topological features for classification are potential quantitative neuroimaging biomarkers for clinical TS diagnosis. Hum Brain Mapp 38:3988-4008, 2017. © 2017 Wiley Periodicals, Inc.Tourette syndrome (TS) is a childhood-onset neurobehavioral disorder. Although previous TS studies revealed structural abnormalities in distinct corticobasal ganglia circuits, the topological alterations of the whole-brain white matter (WM) structural networks remain poorly understood. Here, we used diffusion MRI probabilistic tractography and graph theoretical analysis to investigate the topological organization of WM networks in 44 drug-naive TS children and 41 age- and gender-matched healthy children. The WM networks were constructed by estimating inter-regional connectivity probability and the topological properties were characterized using graph theory. We found that both TS and control groups showed an efficient small-world organization in WM networks. However, compared to controls, TS children exhibited decreased global and local efficiency, increased shortest path length and small worldness, indicating a disrupted balance between local specialization and global integration in structural networks. Although both TS and control groups showed highly similar hub distributions, TS children exhibited significant decreased nodal efficiency, mainly distributed in the default mode, language, visual, and sensorimotor systems. Furthermore, two separate networks showing significantly decreased connectivity in TS group were identified using network-based statistical (NBS) analysis, primarily composed of the parieto-occipital cortex, precuneus, and paracentral lobule. Importantly, we combined support vector machine and multiple kernel learning frameworks to fuse multiple levels of network topological features for classification of individuals, achieving high accuracy of 86.47%. Together, our study revealed the disrupted topological organization of structural networks related to pathophysiology of TS, and the discriminative topological features for classification are potential quantitative neuroimaging biomarkers for clinical TS diagnosis. Hum Brain Mapp 38:3988-4008, 2017. © 2017 Wiley Periodicals, Inc. Tourette syndrome (TS) is a childhood‐onset neurobehavioral disorder. Although previous TS studies revealed structural abnormalities in distinct corticobasal ganglia circuits, the topological alterations of the whole‐brain white matter (WM) structural networks remain poorly understood. Here, we used diffusion MRI probabilistic tractography and graph theoretical analysis to investigate the topological organization of WM networks in 44 drug‐naive TS children and 41 age‐ and gender‐matched healthy children. The WM networks were constructed by estimating inter‐regional connectivity probability and the topological properties were characterized using graph theory. We found that both TS and control groups showed an efficient small‐world organization in WM networks. However, compared to controls, TS children exhibited decreased global and local efficiency, increased shortest path length and small worldness, indicating a disrupted balance between local specialization and global integration in structural networks. Although both TS and control groups showed highly similar hub distributions, TS children exhibited significant decreased nodal efficiency, mainly distributed in the default mode, language, visual, and sensorimotor systems. Furthermore, two separate networks showing significantly decreased connectivity in TS group were identified using network‐based statistical (NBS) analysis, primarily composed of the parieto‐occipital cortex, precuneus, and paracentral lobule. Importantly, we combined support vector machine and multiple kernel learning frameworks to fuse multiple levels of network topological features for classification of individuals, achieving high accuracy of 86.47%. Together, our study revealed the disrupted topological organization of structural networks related to pathophysiology of TS, and the discriminative topological features for classification are potential quantitative neuroimaging biomarkers for clinical TS diagnosis. Hum Brain Mapp 38:3988–4008, 2017 . © 2017 Wiley Periodicals, Inc. |
| Author | Zhang, Jishui Zhang, Yue Peng, Yun Rekik, Islem Liu, Yue He, Huiguang Wen, Hongwei Wang, Shengpei |
| AuthorAffiliation | 6 Department of Neurology Beijing Children's Hospital, Capital Medical University Beijing China 3 University of Chinese Academy of Sciences Beijing China 1 Research Center for Brain‐inspired Intelligence, Institute of Automation, Chinese Academy of Sciences Beijing China 5 CVIP, Computing, School of Science and Engineering University of Dundee UK 4 Department of Radiology Beijing Children's Hospital, Capital Medical University Beijing China 2 Center for Excellence in Brain Science and Intelligence Technology, Chinese Academy of Sciences Beijing China |
| AuthorAffiliation_xml | – name: 2 Center for Excellence in Brain Science and Intelligence Technology, Chinese Academy of Sciences Beijing China – name: 6 Department of Neurology Beijing Children's Hospital, Capital Medical University Beijing China – name: 1 Research Center for Brain‐inspired Intelligence, Institute of Automation, Chinese Academy of Sciences Beijing China – name: 3 University of Chinese Academy of Sciences Beijing China – name: 4 Department of Radiology Beijing Children's Hospital, Capital Medical University Beijing China – name: 5 CVIP, Computing, School of Science and Engineering University of Dundee UK |
| Author_xml | – sequence: 1 givenname: Hongwei surname: Wen fullname: Wen, Hongwei organization: University of Chinese Academy of Sciences – sequence: 2 givenname: Yue surname: Liu fullname: Liu, Yue organization: Beijing Children's Hospital, Capital Medical University – sequence: 3 givenname: Islem surname: Rekik fullname: Rekik, Islem organization: University of Dundee – sequence: 4 givenname: Shengpei surname: Wang fullname: Wang, Shengpei organization: University of Chinese Academy of Sciences – sequence: 5 givenname: Jishui surname: Zhang fullname: Zhang, Jishui organization: Beijing Children's Hospital, Capital Medical University – sequence: 6 givenname: Yue surname: Zhang fullname: Zhang, Yue organization: Beijing Children's Hospital, Capital Medical University – sequence: 7 givenname: Yun surname: Peng fullname: Peng, Yun email: ppengyun@yahoo.com organization: Beijing Children's Hospital, Capital Medical University – sequence: 8 givenname: Huiguang orcidid: 0000-0001-9991-378X surname: He fullname: He, Huiguang email: huiguang.he@ia.ac.cn organization: University of Chinese Academy of Sciences |
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| Keywords | multiple kernel learning graph theory topological organization diffusion MRI structural network probabilistic tractography Tourette syndrome |
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| Snippet | Tourette syndrome (TS) is a childhood‐onset neurobehavioral disorder. Although previous TS studies revealed structural abnormalities in distinct corticobasal... Tourette syndrome (TS) is a childhood-onset neurobehavioral disorder. Although previous TS studies revealed structural abnormalities in distinct corticobasal... |
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| SubjectTerms | Abnormalities Adolescent Algorithms Area Under Curve Attention Deficit Disorder with Hyperactivity - complications Attention Deficit Disorder with Hyperactivity - diagnostic imaging Biomarkers Brain Brain - diagnostic imaging Child Child, Preschool Children Circuits Classification Cortex (parietal) Diffusion Magnetic Resonance Imaging - methods diffusion MRI Diffusion Tensor Imaging - methods Female Ganglia Gilles de la Tourette syndrome Graph theory Humans Image Processing, Computer-Assisted - methods Integration Learning algorithms Magnetic resonance imaging Male Medical imaging multiple kernel learning Networks Neural networks Neural Pathways - diagnostic imaging Neuroimaging Neurology Obsessive-Compulsive Disorder - complications Obsessive-Compulsive Disorder - diagnostic imaging Occipital lobe probabilistic tractography ROC Curve Sensorimotor system Shortest-path problems Specialization structural network Substantia alba Support Vector Machine Theoretical analysis topological organization Tourette syndrome Tourette Syndrome - classification Tourette Syndrome - complications Tourette Syndrome - diagnostic imaging Visual cortex Visual pathways |
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| Title | Disrupted topological organization of structural networks revealed by probabilistic diffusion tractography in Tourette syndrome children |
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