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      DTI and VBM reveal white matter changes without associated gray matter changes in patients with idiopathic restless legs syndrome

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          Abstract

          Background and Purpose

          We evaluated cerebral white and gray matter changes in patients with iRLS in order to shed light on the pathophysiology of this disease.

          Methods

          Twelve patients with iRLS were compared to 12 age- and sex-matched controls using whole-head diffusion tensor imaging (DTI) and voxel-based morphometry (VBM) techniques. Evaluation of the DTI scans included the voxelwise analysis of the fractional anisotropy (FA), radial diffusivity (RD), and axial diffusivity (AD).

          Results

          Diffusion tensor imaging revealed areas of altered FA in subcortical white matter bilaterally, mainly in temporal regions as well as in the right internal capsule, the pons, and the right cerebellum. These changes overlapped with changes in RD. Voxel-based morphometry did not reveal any gray matter alterations.

          Conclusions

          We showed altered diffusion properties in several white matter regions in patients with iRLS. White matter changes could mainly be attributed to changes in RD, a parameter thought to reflect altered myelination. Areas with altered white matter microstructure included areas in the internal capsule which include the corticospinal tract to the lower limbs, thereby supporting studies that suggest changes in sensorimotor pathways associated with RLS.

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          Most cited references51

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          Restless legs syndrome: diagnostic criteria, special considerations, and epidemiology. A report from the restless legs syndrome diagnosis and epidemiology workshop at the National Institutes of Health.

          Richard Allen, Daniel Picchietti, Wayne Hening … (2003)
          Restless legs syndrome is a common yet frequently undiagnosed sensorimotor disorder. In 1995, the International Restless Legs Syndrome Study Group developed standardized criteria for the diagnosis of restless legs syndrome. Since that time, additional scientific scrutiny and clinical experience have led to a better understanding of the condition. Modification of the criteria is now necessary to better reflect that increased body of knowledge, as well as to clarify slight confusion with the wording of the original criteria. The restless legs syndrome diagnostic criteria and epidemiology workshop at the National Institutes of Health. Members of the International Restless Legs Syndrome Study Group and authorities on epidemiology and the design of questionnaires and scales. To modify the current criteria for the diagnosis of restless legs syndrome, to develop new criteria for the diagnosis of restless legs syndrome in the cognitively impaired elderly and in children, to create standardized criteria for the identification of augmentation, and to establish consistent questions for use in epidemiology studies. The essential diagnostic criteria for restless legs syndrome were developed and approved by workshop participants and the executive committee of the International Restless Legs Syndrome Study Group. Criteria were also developed and approved for the additional aforementioned groups.
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            Determinants of anisotropic water diffusion in nerves.

            C Beaulieu, Jonathan Allen (1994)
            We report NMR diffusion measurements of water in three central nervous system models, namely the nonmyelinated olfactory, and the myelinated trigeminal and optic nerves of the spotted and long-nosed garfish. A similar degree of anisotropy of the average diffusion coefficients (DNMR) is observed for all three freshly excised nerve types (DNMR(parallel)/DNMR-(perpendicular) is 3.6 +/- 1.2, 3.2 +/- 0.9, and 2.6 +/- 0.4 for the olfactory, trigeminal, and optic nerves, respectively). The anisotropy of DNMR for the nonmyelinated olfactory nerve argues strongly that myelin is not a necessary determinant of diffusional anisotropy in ordered axonal systems (even though it may contribute when present). Garfish nerves treated with vinblastine, in order to depolymerize microtubules and inhibit fast axonal transport, also exhibit diffusional anisotropy (DNMR(parallel)/DNMR(perpendicular) is 2.6 +/- 0.4, 2.8 +/- 0.8, and 2.2 +/- 0.7 for the olfactory, trigeminal, and optic nerves, respectively) thus excluding a significant role for microtubules and fast axonal transport in that observed anisotropy.
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              White matter pathology isolates the hippocampal formation in Alzheimer's disease.

              D.H. Salat, D.S. Tuch, A.J.W. van der Kouwe … (2010)
              Prior work has demonstrated that the memory dysfunction of Alzheimer's disease (AD) is accompanied by marked cortical pathology in medial temporal lobe (MTL) gray matter. In contrast, changes in white matter (WM) of pathways associated with the MTL have rarely been studied. We used diffusion tensor imaging (DTI) to examine regional patterns of WM tissue changes in individuals with AD. Alterations of diffusion properties with AD were found in several regions including parahippocampal WM, and in regions with direct and secondary connections to the MTL. A portion of the changes measured, including effects in the parahippocampal WM, were independent of gray matter degeneration as measured by hippocampal volume. Examination of regional changes in unique diffusion parameters including anisotropy and axial and radial diffusivity demonstrated distinct zones of alterations, potentially stemming from differences in underlying pathology, with a potential myelin specific pathology in the parahippocampal WM. These results demonstrate that deterioration of neocortical connections to the hippocampal formation results in part from the degeneration of critical MTL and associated fiber pathways.
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                Author and article information

                Journal
                Journal ID (nlm-ta): Brain Behav
                Journal ID (iso-abbrev): Brain Behav
                Journal ID (publisher-id): brb3
                Title: Brain and Behavior
                Publisher: John Wiley & Sons, Ltd (Chichester, UK )
                ISSN (Print): 2162-3279
                ISSN (Electronic): 2162-3279
                Publication date (Print): September 2015
                Publication date (Electronic): 30 July 2015
                Volume: 5
                Issue: 9
                Electronic Location Identifier: e00327
                Affiliations
                [1 ]Department of Neurology, Philipps-University Marburg Baldingerstrasse, Marburg, 35043, Germany
                [2 ]Department of Diagnostic Radiology, Philipps-University Marburg Baldingerstrasse, Marburg, 35043, Germany
                [3 ]Epilepsy Center Franfurt Rhein-Main, Department of Neurology, Johann Wolfgang Goethe University Frankfurt am Main, Germany
                [4 ]Somnomar, Institute for Medical Research and Sleep Medicine Marburg Marburger Strasse 9a, Marburg, 35043, Germany
                Author notes
                Correspondence Susanne Knake, Center of Brain Imaging, Philipps-University Marburg, Department of Neurology, Baldingerstrasse, 35043 Marburg, Germany. Tel: 0049 6421 5865200; Fax: 0049 6421 5865208; E-mail: knake@ 123456staff.uni-marburg.de

                Funding Information No funding information provided.

                [*]

                Equal contribution

                Article
                DOI: 10.1002/brb3.327
                PMC ID: 4589804
                PubMed ID: 26442748
                SO-VID: 5d888a9a-7535-4e75-aa7e-5f2fd507d21c
                Copyright © © 2015 The Authors. Brain and Behavior published by Wiley Periodicals, Inc.
                License:

                This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                Date received : 19 January 2015
                Date accepted : 26 January 2015
                Categories
                Subject: Original Research

                ScienceOpen disciplines: Neurosciences
                Keywords: diffusion tensor imaging,gray matter changes,restless legs syndrome,voxel-based morphometry,white matter changes
                Data availability:
                ScienceOpen disciplines: Neurosciences
                Keywords: diffusion tensor imaging, gray matter changes, restless legs syndrome, voxel-based morphometry, white matter changes

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