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

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

12 Citations (Scopus)

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.

Original languageEnglish
Pages (from-to)1596-1606
Number of pages11
JournalMovement Disorders
Volume35
Issue number9
DOIs
Publication statusPublished - 1 Sept 2020
Externally publishedYes

Keywords

  • biomarker
  • cognition
  • dual-task
  • functional MRI
  • gait
  • idiopathic REM sleep behavior disorder
  • neurodegeneration
  • virtual reality

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