Alterations in White Matter Network and Microstructural Integrity Differentiate Parkinson’s Disease Patients and Healthy Subjects
Parkinson’s disease (PD) is a neurodegenerative disease, neuropathologically characterized by progressive loss of neurons in distinct brain areas. We hypothesize that quantifiable network alterations are caused by neurodegeneration. The primary motivation of this study was to assess the specific net...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2019-07-01
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| Series: | Frontiers in Aging Neuroscience |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fnagi.2019.00191/full |
| _version_ | 1818911173412651008 |
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| author | Nabin Koirala Abdul Rauf Anwar Dumitru Ciolac Dumitru Ciolac Dumitru Ciolac Martin Glaser Bogdan Pintea Günther Deuschl Muthuraman Muthuraman Sergiu Groppa |
| author_facet | Nabin Koirala Abdul Rauf Anwar Dumitru Ciolac Dumitru Ciolac Dumitru Ciolac Martin Glaser Bogdan Pintea Günther Deuschl Muthuraman Muthuraman Sergiu Groppa |
| author_sort | Nabin Koirala |
| collection | DOAJ |
| description | Parkinson’s disease (PD) is a neurodegenerative disease, neuropathologically characterized by progressive loss of neurons in distinct brain areas. We hypothesize that quantifiable network alterations are caused by neurodegeneration. The primary motivation of this study was to assess the specific network alterations in PD patients that are distinct but appear in conjunction with physiological aging. 178 subjects (130 females) stratified into PD patients, young, middle-aged and elderly healthy controls (age- and sex-matched with PD patients), were analyzed using 3D-T1 magnetization-prepared rapid gradient-echo (MPRAGE) and diffusion weighted images acquired in 3T MRI scanner. Diffusion modeling and probabilistic tractography analysis were applied for generating voxel-based connectivity index maps from each seed voxel. The obtained connectivity matrices were analyzed using graph theoretical tools for characterization of involved network. By network-based statistic (NBS) the interregional connectivity differences between the groups were assessed. Measures evaluating local diffusion properties for anisotropy and diffusivity were computed for characterization of white matter microstructural integrity. The graph theoretical analysis showed a significant decrease in distance measures – eccentricity and characteristic path length – in PD patients in comparison to healthy subjects. Both measures as well were lower in PD patients when compared to young and middle-aged healthy controls. NBS analysis demonstrated lowered structural connectivity in PD patients in comparison to young and middle-aged healthy subject groups, mainly in frontal, cingulate, olfactory, insula, thalamus, and parietal regions. These specific network differences were distinct for PD and were not observed between the healthy subject groups. Microstructural analysis revealed diffusivity alterations within the white matter tracts in PD patients, predominantly in the body, splenium and tapetum of corpus callosum, corticospinal tract, and corona radiata, which were absent in normal aging. The identified alterations of network connectivity presumably caused by neurodegeneration indicate the disruption in global network integration in PD patients. The microstructural changes identified within the white matter could endorse network reconfiguration. This study provides a clear distinction between the network changes occurring during aging and PD. This will facilitate a better understanding of PD pathophysiology and the direct link between white matter changes and their role in the restructured network topology. |
| first_indexed | 2024-12-19T22:54:29Z |
| format | Article |
| id | doaj.art-ffdb8d5e7da74750b78118f9601741f1 |
| institution | Directory Open Access Journal |
| issn | 1663-4365 |
| language | English |
| last_indexed | 2024-12-19T22:54:29Z |
| publishDate | 2019-07-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Aging Neuroscience |
| spelling | doaj.art-ffdb8d5e7da74750b78118f9601741f12022-12-21T20:02:42ZengFrontiers Media S.A.Frontiers in Aging Neuroscience1663-43652019-07-011110.3389/fnagi.2019.00191423926Alterations in White Matter Network and Microstructural Integrity Differentiate Parkinson’s Disease Patients and Healthy SubjectsNabin Koirala0Abdul Rauf Anwar1Dumitru Ciolac2Dumitru Ciolac3Dumitru Ciolac4Martin Glaser5Bogdan Pintea6Günther Deuschl7Muthuraman Muthuraman8Sergiu Groppa9Department of Neurology, University Medical Center of the Johannes Gutenberg University Mainz, Mainz, GermanyCentre for Biomedical Engineering, University of Engineering and Technology, Lahore, PakistanDepartment of Neurology, University Medical Center of the Johannes Gutenberg University Mainz, Mainz, GermanyDepartment of Neurology, Institute of Emergency Medicine, Chisinau, MoldovaLaboratory of Neurobiology and Medical Genetics, State University of Medicine and Pharmacy “Nicolae Testemit̨anu”, Chisinau, MoldovaDepartment of Neurosurgery, University Medical Center of the Johannes Gutenberg University Mainz, Mainz, GermanyDepartment of Neurosurgery, Bergmannsheil Clinic, Ruhr University Bochum, Bochum, GermanyDepartment of Neurology, Christian-Albrechts-University, Kiel, GermanyDepartment of Neurology, University Medical Center of the Johannes Gutenberg University Mainz, Mainz, GermanyDepartment of Neurology, University Medical Center of the Johannes Gutenberg University Mainz, Mainz, GermanyParkinson’s disease (PD) is a neurodegenerative disease, neuropathologically characterized by progressive loss of neurons in distinct brain areas. We hypothesize that quantifiable network alterations are caused by neurodegeneration. The primary motivation of this study was to assess the specific network alterations in PD patients that are distinct but appear in conjunction with physiological aging. 178 subjects (130 females) stratified into PD patients, young, middle-aged and elderly healthy controls (age- and sex-matched with PD patients), were analyzed using 3D-T1 magnetization-prepared rapid gradient-echo (MPRAGE) and diffusion weighted images acquired in 3T MRI scanner. Diffusion modeling and probabilistic tractography analysis were applied for generating voxel-based connectivity index maps from each seed voxel. The obtained connectivity matrices were analyzed using graph theoretical tools for characterization of involved network. By network-based statistic (NBS) the interregional connectivity differences between the groups were assessed. Measures evaluating local diffusion properties for anisotropy and diffusivity were computed for characterization of white matter microstructural integrity. The graph theoretical analysis showed a significant decrease in distance measures – eccentricity and characteristic path length – in PD patients in comparison to healthy subjects. Both measures as well were lower in PD patients when compared to young and middle-aged healthy controls. NBS analysis demonstrated lowered structural connectivity in PD patients in comparison to young and middle-aged healthy subject groups, mainly in frontal, cingulate, olfactory, insula, thalamus, and parietal regions. These specific network differences were distinct for PD and were not observed between the healthy subject groups. Microstructural analysis revealed diffusivity alterations within the white matter tracts in PD patients, predominantly in the body, splenium and tapetum of corpus callosum, corticospinal tract, and corona radiata, which were absent in normal aging. The identified alterations of network connectivity presumably caused by neurodegeneration indicate the disruption in global network integration in PD patients. The microstructural changes identified within the white matter could endorse network reconfiguration. This study provides a clear distinction between the network changes occurring during aging and PD. This will facilitate a better understanding of PD pathophysiology and the direct link between white matter changes and their role in the restructured network topology.https://www.frontiersin.org/article/10.3389/fnagi.2019.00191/fulldiffusion MRInetwork connectivity analysisParkinson’s diseaseagingwhite matter |
| spellingShingle | Nabin Koirala Abdul Rauf Anwar Dumitru Ciolac Dumitru Ciolac Dumitru Ciolac Martin Glaser Bogdan Pintea Günther Deuschl Muthuraman Muthuraman Sergiu Groppa Alterations in White Matter Network and Microstructural Integrity Differentiate Parkinson’s Disease Patients and Healthy Subjects Frontiers in Aging Neuroscience diffusion MRI network connectivity analysis Parkinson’s disease aging white matter |
| title | Alterations in White Matter Network and Microstructural Integrity Differentiate Parkinson’s Disease Patients and Healthy Subjects |
| title_full | Alterations in White Matter Network and Microstructural Integrity Differentiate Parkinson’s Disease Patients and Healthy Subjects |
| title_fullStr | Alterations in White Matter Network and Microstructural Integrity Differentiate Parkinson’s Disease Patients and Healthy Subjects |
| title_full_unstemmed | Alterations in White Matter Network and Microstructural Integrity Differentiate Parkinson’s Disease Patients and Healthy Subjects |
| title_short | Alterations in White Matter Network and Microstructural Integrity Differentiate Parkinson’s Disease Patients and Healthy Subjects |
| title_sort | alterations in white matter network and microstructural integrity differentiate parkinson s disease patients and healthy subjects |
| topic | diffusion MRI network connectivity analysis Parkinson’s disease aging white matter |
| url | https://www.frontiersin.org/article/10.3389/fnagi.2019.00191/full |
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