The Neural Signature of Impaired Dual-Tasking in Idiopathic Rapid Eye Movement Sleep Behavior Disorder Patients

Kaylena A Ehgoetz Martens; Elie Matar; James M Shine; Joseph R Phillips; Matthew J Georgiades; Ron R Grunstein; Glenda M Halliday; Simon J G Lewis

doi:10.1002/mds.28114

The Neural Signature of Impaired Dual-Tasking in Idiopathic Rapid Eye Movement Sleep Behavior Disorder Patients

Mov Disord. 2020 Sep;35(9):1596-1606. doi: 10.1002/mds.28114. Epub 2020 Jun 11.

Authors

Kaylena A Ehgoetz Martens^{1

2

3}, Elie Matar^{1

2}, James M Shine¹, Joseph R Phillips^{2

4}, Matthew J Georgiades^{1

2

3}, Ron R Grunstein^{5

3}, Glenda M Halliday², Simon J G Lewis^{1

2}

Affiliations

¹ ForeFront Research Team, Brain and Mind Centre, University of Sydney, Camperdown, New South Wales, Australia.
² Parkinson's Disease Research Clinic, Brain and Mind Centre, University of Sydney, Camperdown, New South Wales, Australia.
³ Department of Kinesiology, University of Waterloo, Ontario, Canada.
⁴ School of Social Sciences and Psychology, Western Sydney University, Sydney, New South Wales, Australia.
⁵ Sleep and Circadian Group (CIRUS), Woolcock Institute of Medical Research, Glebe, New South Wales, Australia; and University of Sydney and Royal Prince Alfred Hospital, Sydney, New South Wales, Australia.

PMID: 32525224
DOI: 10.1002/mds.28114

Abstract

Dual-task gait can be a useful biomarker for cognitive decline and a sensitive predictor of future neurodegeneration in certain clinical populations, such as patients with idiopathic rapid eye movement sleep behavior disorder.

Objectives: The objective of this cross-sectional study was to determine the neural signature of dual-tasking deficits in idiopathic rapid eye movement sleep behavior disorder using a validated gait paradigm.

Methods: Fifty-eight participants (28 controls; 30 idiopathic rapid eye movement sleep behavior disorder patients) were recruited; 52 participants had functional MRI scans as they performed a validated dual-task virtual reality gait paradigm using foot pedals. Forty-one participants completed single- and dual-task "overground walking" on a pressure sensor carpet.

Results: Idiopathic rapid eye movement sleep behavior disorder patients showed deficits in dual-tasking (i.e., greater mean step time) compared to controls during "overground walking." Functional MRI revealed that idiopathic rapid eye movement sleep behavior disorder patients had reduced blood-oxygen-level-dependent signal change in the dorsal caudate nucleus, and significantly different corticostriatal functional connectivity patterns from controls, when dual-tasking in high versus low cognitive load. While controls showed greater connectivity between frontoparietal and motor networks, idiopathic rapid eye movement sleep behavior disorder patients exhibited less change in this connectivity as a function of cognitive load.

Conclusions: These findings demonstrate evidence of dual-task gait deficits in idiopathic rapid eye movement sleep behavior disorder patients, underpinned by disrupted corticostriatal connectivity. Minimal differences in the level of functional connectivity between dual-tasking conditions of high and low cognitive load suggest that idiopathic rapid eye movement sleep behavior disorder patients recruit cognitive networks to control gait even when the cognitive demands are low. This may indicate a compensatory strategy for early cognitive decline in idiopathic rapid eye movement sleep behavior disorder. © 2020 International Parkinson and Movement Disorder Society.

Keywords: biomarker; cognition; dual-task; functional MRI; gait; idiopathic REM sleep behavior disorder; neurodegeneration; virtual reality.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Cognitive Dysfunction*
Cross-Sectional Studies
Gait
Humans
REM Sleep Behavior Disorder*
Walking