Connectome analysis with diffusion MRI in idiopathic Parkinson's disease: Evaluation using multi-shell, multi-tissue, constrained spherical deconvolution

Parkinson's disease (PD) is a progressive neurodegenerative disorder that affects extensive regions of the central nervous system. In this work, we evaluated the structural connectome of patients with PD, as mapped by diffusion-weighted MRI tractography and a multi-shell, multi-tissue (MSMT) co...

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Main Authors: Koji Kamagata, Andrew Zalesky, Taku Hatano, Maria Angelique Di Biase, Omar El Samad, Shinji Saiki, Keigo Shimoji, Kanako K. Kumamaru, Kouhei Kamiya, Masaaki Hori, Nobutaka Hattori, Shigeki Aoki, Christos Pantelis
Format: Article
Language:English
Published: Elsevier 2018-01-01
Series:NeuroImage: Clinical
Online Access:http://www.sciencedirect.com/science/article/pii/S2213158217302875
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author Koji Kamagata
Andrew Zalesky
Taku Hatano
Maria Angelique Di Biase
Omar El Samad
Shinji Saiki
Keigo Shimoji
Kanako K. Kumamaru
Kouhei Kamiya
Masaaki Hori
Nobutaka Hattori
Shigeki Aoki
Christos Pantelis
spellingShingle Koji Kamagata
Andrew Zalesky
Taku Hatano
Maria Angelique Di Biase
Omar El Samad
Shinji Saiki
Keigo Shimoji
Kanako K. Kumamaru
Kouhei Kamiya
Masaaki Hori
Nobutaka Hattori
Shigeki Aoki
Christos Pantelis
Connectome analysis with diffusion MRI in idiopathic Parkinson's disease: Evaluation using multi-shell, multi-tissue, constrained spherical deconvolution
NeuroImage: Clinical
author_facet Koji Kamagata
Andrew Zalesky
Taku Hatano
Maria Angelique Di Biase
Omar El Samad
Shinji Saiki
Keigo Shimoji
Kanako K. Kumamaru
Kouhei Kamiya
Masaaki Hori
Nobutaka Hattori
Shigeki Aoki
Christos Pantelis
author_sort Koji Kamagata
title Connectome analysis with diffusion MRI in idiopathic Parkinson's disease: Evaluation using multi-shell, multi-tissue, constrained spherical deconvolution
title_short Connectome analysis with diffusion MRI in idiopathic Parkinson's disease: Evaluation using multi-shell, multi-tissue, constrained spherical deconvolution
title_full Connectome analysis with diffusion MRI in idiopathic Parkinson's disease: Evaluation using multi-shell, multi-tissue, constrained spherical deconvolution
title_fullStr Connectome analysis with diffusion MRI in idiopathic Parkinson's disease: Evaluation using multi-shell, multi-tissue, constrained spherical deconvolution
title_full_unstemmed Connectome analysis with diffusion MRI in idiopathic Parkinson's disease: Evaluation using multi-shell, multi-tissue, constrained spherical deconvolution
title_sort connectome analysis with diffusion mri in idiopathic parkinson's disease: evaluation using multi-shell, multi-tissue, constrained spherical deconvolution
publisher Elsevier
series NeuroImage: Clinical
issn 2213-1582
publishDate 2018-01-01
description Parkinson's disease (PD) is a progressive neurodegenerative disorder that affects extensive regions of the central nervous system. In this work, we evaluated the structural connectome of patients with PD, as mapped by diffusion-weighted MRI tractography and a multi-shell, multi-tissue (MSMT) constrained spherical deconvolution (CSD) method to increase the precision of tractography at tissue interfaces. The connectome was mapped with probabilistic MSMT-CSD in 21 patients with PD and in 21 age- and gender-matched controls. Mapping was also performed by deterministic single-shell, single tissue (SSST)-CSD tracking and probabilistic SSST-CSD tracking for comparison. A support vector machine was trained to predict diagnosis based on a linear combination of graph metrics. We showed that probabilistic MSMT-CSD could detect significantly reduced global strength, efficiency, clustering, and small-worldness, and increased global path length in patients with PD relative to healthy controls; by contrast, probabilistic SSST-CSD only detected the difference in global strength and small-worldness. In patients with PD, probabilistic MSMT-CSD also detected a significant reduction in local efficiency and detected clustering in the motor, frontal temporoparietal associative, limbic, basal ganglia, and thalamic areas. The network-based statistic identified a subnetwork of reduced connectivity by MSMT-CSD and probabilistic SSST-CSD in patients with PD, involving key components of the cortico–basal ganglia–thalamocortical network. Finally, probabilistic MSMT-CSD had superior diagnostic accuracy compared with conventional probabilistic SSST-CSD and deterministic SSST-CSD tracking. In conclusion, probabilistic MSMT-CSD detected a greater extent of connectome pathology in patients with PD, including those with cortico–basal ganglia–thalamocortical network disruptions. Connectome analysis based on probabilistic MSMT-CSD may be useful when evaluating the extent of white matter connectivity disruptions in PD. Keywords: Connectome, Diffusion MRI, Diffusion tensor imaging, Lewy bodies, Neurodegenerative disorders, Support vector machine
url http://www.sciencedirect.com/science/article/pii/S2213158217302875
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spelling doaj-9888deb477c74a4f974e9bc1449ee9292020-11-25T02:15:34ZengElsevierNeuroImage: Clinical2213-15822018-01-0117518529Connectome analysis with diffusion MRI in idiopathic Parkinson's disease: Evaluation using multi-shell, multi-tissue, constrained spherical deconvolutionKoji Kamagata0Andrew Zalesky1Taku Hatano2Maria Angelique Di Biase3Omar El Samad4Shinji Saiki5Keigo Shimoji6Kanako K. Kumamaru7Kouhei Kamiya8Masaaki Hori9Nobutaka Hattori10Shigeki Aoki11Christos Pantelis12Department of Radiology, Juntendo University Graduate School of Medicine, Tokyo, Japan; Melbourne Neuropsychiatry Centre, Department of Psychiatry, The University of Melbourne & Melbourne Health, Parkville, VIC, Australia; Corresponding author at: Department of Radiology, Juntendo University School of Medicine, 2-1-1 Hongo, Bunkyo-ku, Tokyo 113-8421, Japan.Melbourne Neuropsychiatry Centre, Department of Psychiatry, The University of Melbourne & Melbourne Health, Parkville, VIC, Australia; Melbourne School of Engineering, University of Melbourne, Melbourne, AustraliaDepartment of Neurology, Juntendo University Graduate School of Medicine, Tokyo, JapanMelbourne Neuropsychiatry Centre, Department of Psychiatry, The University of Melbourne & Melbourne Health, Parkville, VIC, AustraliaDepartment of Computing and Information Systems, University of Melbourne, Parkville, AustraliaDepartment of Neurology, Juntendo University Graduate School of Medicine, Tokyo, JapanDepartment of Radiology, Juntendo University Graduate School of Medicine, Tokyo, Japan; Department of Diagnostic Radiology, Tokyo Metropolitan Geriatric Hospital, Tokyo, JapanDepartment of Radiology, Juntendo University Graduate School of Medicine, Tokyo, JapanDepartment of Radiology, The University of Tokyo, Bunkyo, Tokyo, JapanDepartment of Radiology, Juntendo University Graduate School of Medicine, Tokyo, JapanDepartment of Neurology, Juntendo University Graduate School of Medicine, Tokyo, JapanDepartment of Radiology, Juntendo University Graduate School of Medicine, Tokyo, JapanMelbourne Neuropsychiatry Centre, Department of Psychiatry, The University of Melbourne & Melbourne Health, Parkville, VIC, Australia; Melbourne School of Engineering, University of Melbourne, Melbourne, Australia; Centre for Neural Engineering, Department of Electrical and Electronic Engineering, The University of Melbourne, Carlton, VIC, AustraliaParkinson's disease (PD) is a progressive neurodegenerative disorder that affects extensive regions of the central nervous system. In this work, we evaluated the structural connectome of patients with PD, as mapped by diffusion-weighted MRI tractography and a multi-shell, multi-tissue (MSMT) constrained spherical deconvolution (CSD) method to increase the precision of tractography at tissue interfaces. The connectome was mapped with probabilistic MSMT-CSD in 21 patients with PD and in 21 age- and gender-matched controls. Mapping was also performed by deterministic single-shell, single tissue (SSST)-CSD tracking and probabilistic SSST-CSD tracking for comparison. A support vector machine was trained to predict diagnosis based on a linear combination of graph metrics. We showed that probabilistic MSMT-CSD could detect significantly reduced global strength, efficiency, clustering, and small-worldness, and increased global path length in patients with PD relative to healthy controls; by contrast, probabilistic SSST-CSD only detected the difference in global strength and small-worldness. In patients with PD, probabilistic MSMT-CSD also detected a significant reduction in local efficiency and detected clustering in the motor, frontal temporoparietal associative, limbic, basal ganglia, and thalamic areas. The network-based statistic identified a subnetwork of reduced connectivity by MSMT-CSD and probabilistic SSST-CSD in patients with PD, involving key components of the cortico–basal ganglia–thalamocortical network. Finally, probabilistic MSMT-CSD had superior diagnostic accuracy compared with conventional probabilistic SSST-CSD and deterministic SSST-CSD tracking. In conclusion, probabilistic MSMT-CSD detected a greater extent of connectome pathology in patients with PD, including those with cortico–basal ganglia–thalamocortical network disruptions. Connectome analysis based on probabilistic MSMT-CSD may be useful when evaluating the extent of white matter connectivity disruptions in PD. Keywords: Connectome, Diffusion MRI, Diffusion tensor imaging, Lewy bodies, Neurodegenerative disorders, Support vector machinehttp://www.sciencedirect.com/science/article/pii/S2213158217302875