Alterations of Sub-cortical Gray Matter Volume and Their Associations With Disease Duration in Patients With Restless Legs Syndrome

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Abstract

Object: The purpose of this study was to uncover the pathology of restless legs syndrome (RLS) by exploring brain structural alterations and their corresponding functional abnormality.

Method: Surface-based morphometry (SBM) and voxel-based morphometry (VBM) were performed to explore the alterations in cortical and sub-cortical gray matter volume (GMV) in a cohort of 20 RLS and 18 normal controls (NC). Furthermore, resting-state functional connectivity (RSFC) was also performed to identify the functional alterations in patients with RLS.

Results: We found significant alterations of sub-cortical GMV, especially the bilateral putamen (PUT), rather than alterations of cortical GMV in patients with RLS compared to NC using both SBM and VBM. Further sub-regional analysis revealed that GMV alterations of PUT was mostly located in the left dorsal caudal PUT in patients with RLS. In addition, altered RSFC patterns of PUT were identified in patients with RLS compared to NC. Moreover, correlation analyses showed that the GMV of the left caudate and the left ventral rostral PUT were positively correlated with disease duration in patients with RLS.

Conclusions: The alterations of subcortical GMV might imply that the primarily affected areas are located in sub-cortical areas especially in the sub-region of PUT by the pathologic process of RLS, which might be used as potential biomarkers for the early diagnosis of RLS.

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Most cited references 37

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Functional connectivity of human striatum: a resting state FMRI study.

A. Di Martino, A Scheres, D S Margulies … (2008)

Classically regarded as motor structures, the basal ganglia subserve a wide range of functions, including motor, cognitive, motivational, and emotional processes. Consistent with this broad-reaching involvement in brain function, basal ganglia dysfunction has been implicated in numerous neurological and psychiatric disorders. Despite recent advances in human neuroimaging, models of basal ganglia circuitry continue to rely primarily upon inference from animal studies. Here, we provide a comprehensive functional connectivity analysis of basal ganglia circuitry in humans through a functional magnetic resonance imaging examination during rest. Voxelwise regression analyses substantiated the hypothesized motor, cognitive, and affective divisions among striatal subregions, and provided in vivo evidence of a functional organization consistent with parallel and integrative loop models described in animals. Our findings also revealed subtler distinctions within striatal subregions not previously appreciated by task-based imaging approaches. For instance, the inferior ventral striatum is functionally connected with medial portions of orbitofrontal cortex, whereas a more superior ventral striatal seed is associated with medial and lateral portions. The ability to map multiple distinct striatal circuits in a single study in humans, as opposed to relying on meta-analyses of multiple studies, is a principal strength of resting state functional magnetic resonance imaging. This approach holds promise for studying basal ganglia dysfunction in clinical disorders.

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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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Smoothing and cluster thresholding for cortical surface-based group analysis of fMRI data.

Donald J Hagler, Ayse Pinar Saygin, Martin I Sereno (2006)

Cortical surface-based analysis of fMRI data has proven to be a useful method with several advantages over 3-dimensional volumetric analyses. Many of the statistical methods used in 3D analyses can be adapted for use with surface-based analyses. Operating within the framework of the FreeSurfer software package, we have implemented a surface-based version of the cluster size exclusion method used for multiple comparisons correction. Furthermore, we have a developed a new method for generating regions of interest on the cortical surface using a sliding threshold of cluster exclusion followed by cluster growth. Cluster size limits for multiple probability thresholds were estimated using random field theory and validated with Monte Carlo simulation. A prerequisite of RFT or cluster size simulation is an estimate of the smoothness of the data. In order to estimate the intrinsic smoothness of group analysis statistics, independent of true activations, we conducted a group analysis of simulated noise data sets. Because smoothing on a cortical surface mesh is typically implemented using an iterative method, rather than directly applying a Gaussian blurring kernel, it is also necessary to determine the width of the equivalent Gaussian blurring kernel as a function of smoothing steps. Iterative smoothing has previously been modeled as continuous heat diffusion, providing a theoretical basis for predicting the equivalent kernel width, but the predictions of the model were not empirically tested. We generated an empirical heat diffusion kernel width function by performing surface-based smoothing simulations and found a large disparity between the expected and actual kernel widths.

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Author and article information

Contributors

Tian Li: URI : http://loop.frontiersin.org/people/489425/overview

Zhexue Xu: URI : http://loop.frontiersin.org/people/558436/overview

Yuping Wang: URI : http://loop.frontiersin.org/people/431200/overview

Jinping Xu: URI : http://loop.frontiersin.org/people/355675/overview

Journal

Journal ID (nlm-ta): Front Neurol

Journal ID (iso-abbrev): Front Neurol

Journal ID (publisher-id): Front. Neurol.

Title: Frontiers in Neurology

Publisher: Frontiers Media S.A.

ISSN (Electronic): 1664-2295

Publication date (Electronic): 17 December 2018

Publication date Collection: 2018

Volume: 9

Electronic Location Identifier: 1098

Affiliations

[1] ¹Department of Psychology, Faculty of Education, Hubei University , Wuhan, China

[2] ²Institute of Biomedical and Health Engineering, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences , Shenzhen, China

[3] ³Department of Neurology, Xuan Wu Hospital, Capital Medical University , Beijing, China

[4] ⁴Beijing Key Laboratory of Neuromodulation , Beijing, China

[5] ⁵Radiology Department, Shenzhen Traditional Chinese Medicine Hospital , Shenzhen, China

Author notes

Edited by: Fabiana Novellino, Italian National Research Council, Italy

Reviewed by: Maria Salsone, Italian National Research Council, Italy; Ferath Kherif, Lausanne University Hospital (CHUV), Switzerland

*Correspondence: Bibo Xu bluewave2002@ 123456163.com

Yuping Wang wangyuping01@ 123456sina.cn

Jinping Xu jp.xu@ 123456siat.ac.cn

This article was submitted to Neuropharmacology, a section of the journal Frontiers in Neurology

†These authors have contributed equally to this work

Article

DOI: 10.3389/fneur.2018.01098

PMC ID: 6304426

SO-VID: 2e381271-f4be-4b4f-b6a2-b5a79788f9ff

License:

This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

History

Date received : 25 May 2018

Date accepted : 03 December 2018

Page count

Figures: 5, Tables: 3, Equations: 0, References: 44, Pages: 9, Words: 5507

Funding

Funded by: Science and Technology Innovation Program of Shenzhen

Award ID: JCYJ20160531184531506

Funded by: Natural Science Foundation of Guangdong Province 10.13039/501100003453

Award ID: 2017A030313744

Funded by: National Natural Science Foundation of China 10.13039/501100001809

Award ID: 81701297

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Alterations of Sub-cortical Gray Matter Volume and Their Associations With Disease Duration in Patients With Restless Legs Syndrome

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Karger: Neurology and Neuroscience

Most cited references 37

Functional connectivity of human striatum: a resting state FMRI study.

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.

Smoothing and cluster thresholding for cortical surface-based group analysis of fMRI data.

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