Narrow doorways alter brain connectivity and step patterns in isolated REM sleep behaviour disorder

Background: Motor impairments in those with isolated REM sleep behaviour disorder (iRBD) significantly increases the likelihood of developing Lewy body disease (e.g. Parkinson’s disease and Dementia with Lewy Bodies). Objective: This study sought to explore the prodromal process of neurodegeneration...

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Main Authors: Kaylena A. Ehgoetz Martens, Elie Matar, Joseph R. Phillips, James M. Shine, Ron R. Grunstein, Glenda M. Halliday, Simon J.G. Lewis
Format: Article
Language:English
Published: Elsevier 2022-01-01
Series:NeuroImage: Clinical
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2213158222000237
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author Kaylena A. Ehgoetz Martens
Elie Matar
Joseph R. Phillips
James M. Shine
Ron R. Grunstein
Glenda M. Halliday
Simon J.G. Lewis
author_facet Kaylena A. Ehgoetz Martens
Elie Matar
Joseph R. Phillips
James M. Shine
Ron R. Grunstein
Glenda M. Halliday
Simon J.G. Lewis
author_sort Kaylena A. Ehgoetz Martens
collection DOAJ
description Background: Motor impairments in those with isolated REM sleep behaviour disorder (iRBD) significantly increases the likelihood of developing Lewy body disease (e.g. Parkinson’s disease and Dementia with Lewy Bodies). Objective: This study sought to explore the prodromal process of neurodegeneration by examining the neural signature underlying motor deficits in iRBD patients. Methods: A virtual reality (VR) gait paradigm (which has previously been shown to elicit adaptive changes in gait performance whilst navigating doorways in Parkinson’s Disease - PD) was paired with fMRI to investigate whether iRBD patients demonstrated worsened motor performance and altered connectivity across frontoparietal, motor and basal ganglia networks compared to healthy controls. Forty participants (23 iRBD and 17 healthy controls) completed the virtual reality gait task whilst in the MRI scanner, and an additional cohort of 19 Early PD patients completed the behavioural virtual reality gait task. Results: As predicted, iRBD patients demonstrated slower and more variable stepping compared to healthy control participants and demonstrated an exaggerated response when navigating narrow compared to wide doorways, a phenomenon characteristically seen in PD. The iRBD patients also demonstrated less BOLD signal change in the left posterior putamen and right mesencephalic locomotor region, as well as reduced functional connectivity between the frontoparietal network and the motor network, when navigating narrow versus wide doorways compared to healthy control participants. Conclusions: Taken together, this study demonstrates that iRBD patients have altered task-related brain connectivity, which may represent the neural underpinnings of early motor impairments that are evident in iRBD.
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spelling doaj.art-d7b6bac36aad421291637a2427457d782022-12-21T17:24:44ZengElsevierNeuroImage: Clinical2213-15822022-01-0133102958Narrow doorways alter brain connectivity and step patterns in isolated REM sleep behaviour disorderKaylena A. Ehgoetz Martens0Elie Matar1Joseph R. Phillips2James M. Shine3Ron R. Grunstein4Glenda M. Halliday5Simon J.G. Lewis6ForeFront Research Team, Brain and Mind Centre, University of Sydney, Australia; Parkinson’s Disease Research Clinic, Brain and Mind Centre, University of Sydney, Australia; Department of Kinesiology and Health Sciences, University of Waterloo, Waterloo, Canada; Corresponding author at: Department of Kinesiology and Health Sciences, University of Waterloo, Waterloo, Canada.ForeFront Research Team, Brain and Mind Centre, University of Sydney, Australia; Parkinson’s Disease Research Clinic, Brain and Mind Centre, University of Sydney, Australia; Department of Kinesiology and Health Sciences, University of Waterloo, Waterloo, CanadaForeFront Research Team, Brain and Mind Centre, University of Sydney, Australia; Parkinson’s Disease Research Clinic, Brain and Mind Centre, University of Sydney, Australia; School of Social Sciences and Psychology, Western Sydney University, Sydney, AustraliaForeFront Research Team, Brain and Mind Centre, University of Sydney, Australia; Parkinson’s Disease Research Clinic, Brain and Mind Centre, University of Sydney, AustraliaForeFront Research Team, Brain and Mind Centre, University of Sydney, Australia; Department of Kinesiology and Health Sciences, University of Waterloo, Waterloo, CanadaForeFront Research Team, Brain and Mind Centre, University of Sydney, AustraliaForeFront Research Team, Brain and Mind Centre, University of Sydney, Australia; Parkinson’s Disease Research Clinic, Brain and Mind Centre, University of Sydney, Australia; Department of Kinesiology and Health Sciences, University of Waterloo, Waterloo, Canada; Sleep and Circadian Group (CIRUS), Woolcock Institute of Medical Research, University of Sydney and Royal Prince Alfred Hospital, AustraliaBackground: Motor impairments in those with isolated REM sleep behaviour disorder (iRBD) significantly increases the likelihood of developing Lewy body disease (e.g. Parkinson’s disease and Dementia with Lewy Bodies). Objective: This study sought to explore the prodromal process of neurodegeneration by examining the neural signature underlying motor deficits in iRBD patients. Methods: A virtual reality (VR) gait paradigm (which has previously been shown to elicit adaptive changes in gait performance whilst navigating doorways in Parkinson’s Disease - PD) was paired with fMRI to investigate whether iRBD patients demonstrated worsened motor performance and altered connectivity across frontoparietal, motor and basal ganglia networks compared to healthy controls. Forty participants (23 iRBD and 17 healthy controls) completed the virtual reality gait task whilst in the MRI scanner, and an additional cohort of 19 Early PD patients completed the behavioural virtual reality gait task. Results: As predicted, iRBD patients demonstrated slower and more variable stepping compared to healthy control participants and demonstrated an exaggerated response when navigating narrow compared to wide doorways, a phenomenon characteristically seen in PD. The iRBD patients also demonstrated less BOLD signal change in the left posterior putamen and right mesencephalic locomotor region, as well as reduced functional connectivity between the frontoparietal network and the motor network, when navigating narrow versus wide doorways compared to healthy control participants. Conclusions: Taken together, this study demonstrates that iRBD patients have altered task-related brain connectivity, which may represent the neural underpinnings of early motor impairments that are evident in iRBD.http://www.sciencedirect.com/science/article/pii/S2213158222000237Isolated REM sleep behaviour disorder (iRBD)Virtual reality (VR)GaitFunctional magnetic resonance imaging (fMRI)Parkinson’s disease (PD)
spellingShingle Kaylena A. Ehgoetz Martens
Elie Matar
Joseph R. Phillips
James M. Shine
Ron R. Grunstein
Glenda M. Halliday
Simon J.G. Lewis
Narrow doorways alter brain connectivity and step patterns in isolated REM sleep behaviour disorder
NeuroImage: Clinical
Isolated REM sleep behaviour disorder (iRBD)
Virtual reality (VR)
Gait
Functional magnetic resonance imaging (fMRI)
Parkinson’s disease (PD)
title Narrow doorways alter brain connectivity and step patterns in isolated REM sleep behaviour disorder
title_full Narrow doorways alter brain connectivity and step patterns in isolated REM sleep behaviour disorder
title_fullStr Narrow doorways alter brain connectivity and step patterns in isolated REM sleep behaviour disorder
title_full_unstemmed Narrow doorways alter brain connectivity and step patterns in isolated REM sleep behaviour disorder
title_short Narrow doorways alter brain connectivity and step patterns in isolated REM sleep behaviour disorder
title_sort narrow doorways alter brain connectivity and step patterns in isolated rem sleep behaviour disorder
topic Isolated REM sleep behaviour disorder (iRBD)
Virtual reality (VR)
Gait
Functional magnetic resonance imaging (fMRI)
Parkinson’s disease (PD)
url http://www.sciencedirect.com/science/article/pii/S2213158222000237
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