Effects of exercise on sleep spindles in Parkinson's disease

Adeel Ali Memon; Corina Catiul; Zachary Irwin; Jennifer Pilkington; Raima A Memon; Allen Joop; Kimberly H Wood; Gary Cutter; Marcas Bamman; Svjetlana Miocinovic; Amy W Amara

doi:10.3389/fresc.2022.952289

Effects of exercise on sleep spindles in Parkinson's disease

Front Rehabil Sci. 2022 Aug 11:3:952289. doi: 10.3389/fresc.2022.952289. eCollection 2022.

Authors

Adeel Ali Memon¹, Corina Catiul¹, Zachary Irwin², Jennifer Pilkington¹, Raima A Memon³, Allen Joop¹, Kimberly H Wood^{1

4}, Gary Cutter⁵, Marcas Bamman^{6

7}, Svjetlana Miocinovic⁸, Amy W Amara^{1

6}

Affiliations

¹ Department of Neurology, University of Alabama at Birmingham, Birmingham, AL, United States.
² Department of Neurosurgery, University of Alabama at Birmingham, Birmingham, AL, United States.
³ Department of Pathology, University of Alabama at Birmingham, Birmingham, AL, United States.
⁴ Department of Psychology, Samford University, Birmingham, AL, United States.
⁵ Department of Biostatistics, University of Alabama at Birmingham, Birmingham, AL, United States.
⁶ UAB Center for Exercise Medicine, University of Alabama at Birmingham, Birmingham, AL, United States.
⁷ Florida Institute for Human and Machine Cognition, Pensacola, FL, United States.
⁸ Department of Neurology, Emory University, Atlanta, GA, United States.

Abstract

Background: In a randomized, controlled trial, we showed that high-intensity rehabilitation, combining resistance training and body-weight interval training, improves sleep efficiency in Parkinson's disease (PD). Quantitative sleep EEG (sleep qEEG) features, including sleep spindles, are altered in aging and in neurodegenerative disease.

Objective: The objective of this post-hoc analysis was to determine the effects of exercise, in comparison to a sleep hygiene, no-exercise control group, on the quantitative characteristics of sleep spindle morphology in PD.

Methods: We conducted an exploratory post-hoc analysis of 24 PD participants who were randomized to exercise (supervised 3 times/week for 16 weeks) versus 26 PD participants who were assigned to a sleep hygiene, no-exercise control group. At baseline and post-intervention, all participants completed memory testing and underwent polysomnography (PSG). PSG-derived sleep EEG central leads (C3 and C4) were manually inspected, with rejection of movement and electrical artifacts. Sleep spindle events were detected based on the following parameters: (1) frequency filter = 11-16 Hz, (2) event duration = 0.5-3 s, and (3) amplitude threshold 75% percentile. We then calculated spindle morphological features, including density and amplitude. These characteristics were computed and averaged over non-rapid eye movement (NREM) sleep stages N2 and N3 for the full night and separately for the first and second halves of the recording. Intervention effects on these features were analyzed using general linear models with group x time interaction. Significant interaction effects were evaluated for correlations with changes in performance in the memory domain.

Results: A significant group x time interaction effect was observed for changes in sleep spindle density due to exercise compared to sleep hygiene control during N2 and N3 during the first half of the night, with a moderate effect size. This change in spindle density was positively correlated with changes in performance on memory testing in the exercise group.

Conclusions: This study is the first to demonstrate that high-intensity exercise rehabilitation has a potential role in improving sleep spindle density in PD and leading to better cognitive performance in the memory domain. These findings represent a promising advance in the search for non-pharmacological treatments for this common and debilitating non-motor symptom.

Keywords: Parkinson’s disease; cognition; exercise; sleep; sleep spindles.

Abstract

Grants and funding