White matter microstructure in Parkinson's disease with and without elevated rapid eye movement sleep muscle tone

Remi Patriat, Pramod K. Pisharady, Sommer Amundsen-Huffmaster, Maria Linn-Evans, Michael J Howell, Jae Woo Chung, Matthew N Petrucci, Aleksandar Videnovic, Erin Holker, Joshua De Kam, Paul Tuite, Christophe Lenglet, Noam Harel, Colum D. MacKinnon

Research output: Contribution to journalArticlepeer-review

Abstract

People with Parkinson's disease who have elevated muscle activity during rapid eye movement sleep (REM sleep without atonia) typically have a worse motor and cognitive impairment compared with those with normal muscle atonia during rapid eye movement sleep. This study used tract-based spatial statistics to compare diffusion MRI measures of fractional anisotropy, radial, mean and axial diffusivity (measures of axonal microstructure based on the directionality of water diffusion) in white matter tracts between people with Parkinson's disease with and without rapid eye movement sleep without atonia and controls and their relationship to measures of motor and cognitive function. Thirty-eight individuals with mild-to-moderate Parkinson's disease and 21 matched control subjects underwent ultra-high field MRI (7 T), quantitative motor assessments of gait and bradykinesia and neuropsychological testing. The Parkinson's disease cohort was separated post hoc into those with and without elevated chin or leg muscle activity during rapid eye movement sleep based on polysomnography findings. Fractional anisotropy was significantly higher, and diffusivity significantly lower, in regions of the corpus callosum, projection and association white matter pathways in the Parkinson's group with normal rapid eye movement sleep muscle tone compared with controls, and in a subset of pathways relative to the Parkinson's disease group with rapid eye movement sleep without atonia. The Parkinson's disease group with elevated rapid eye movement sleep muscle tone showed significant impairments in the gait and upper arm speed compared with controls and significantly worse scores in specific cognitive domains (executive function, visuospatial memory) compared with the Parkinson's disease group with normal rapid eye movement sleep muscle tone. Regression analyses showed that gait speed and step length in the Parkinson's disease cohort were predicted by measures of fractional anisotropy of the anterior corona radiata, whereas elbow flexion velocity was predicted by fractional anisotropy of the superior corona radiata. Visuospatial memory task performance was predicted by the radial diffusivity of the posterior corona radiata. These findings show that people with mild-to-moderate severity of Parkinson's disease who have normal muscle tone during rapid eye movement sleep demonstrate compensatory-like adaptations in axonal microstructure that are associated with preserved motor and cognitive function, but these adaptations are reduced or absent in those with increased rapid eye movement sleep motor tone.

Original languageEnglish (US)
Article numberfcac027
JournalBrain Communications
Volume4
Issue number2
DOIs
StatePublished - 2022

Bibliographical note

Publisher Copyright:
© 2022 The Author(s). Published by Oxford University Press on behalf of the Guarantors of Brain.

Keywords

  • 7 T MRI
  • diffusion MRI
  • Parkinson's disease
  • RBD

PubMed: MeSH publication types

  • Journal Article

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