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 inHuman brain mapping Vol. 38; no. 8; pp. 3988 - 4008
Main Authors Wen, Hongwei, Liu, Yue, Rekik, Islem, Wang, Shengpei, Zhang, Jishui, Zhang, Yue, Peng, Yun, He, Huiguang
Format Journal Article
LanguageEnglish
Published United States John Wiley & Sons, Inc 01.08.2017
John Wiley and Sons Inc
Subjects
Online AccessGet full text
ISSN1065-9471
1097-0193
1097-0193
DOI10.1002/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.
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
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  organization: University of Chinese Academy of Sciences
BackLink https://www.ncbi.nlm.nih.gov/pubmed/28474385$$D View this record in MEDLINE/PubMed
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Issue 8
Keywords multiple kernel learning
graph theory
topological organization
diffusion MRI
structural network
probabilistic tractography
Tourette syndrome
Language English
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2017 Wiley Periodicals, Inc.
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These authors contributed equally to this work.
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PublicationDate August 2017
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PublicationDate_xml – month: 08
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  text: August 2017
PublicationDecade 2010
PublicationPlace United States
PublicationPlace_xml – name: United States
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PublicationTitle Human brain mapping
PublicationTitleAlternate Hum Brain Mapp
PublicationYear 2017
Publisher John Wiley & Sons, Inc
John Wiley and Sons Inc
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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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StartPage 3988
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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