Reduced Regional NREM Sleep Slow-Wave Activity Is Associated With Cognitive Impairment in Parkinson Disease

Growing evidence implicates a distinct role of disturbed slow-wave sleep in neurodegenerative diseases. Reduced non-rapid eye movement (NREM) sleep slow-wave activity (SWA), a marker of slow-wave sleep intensity, has been linked with age-related cognitive impairment and Alzheimer disease pathology....

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Main Authors: Simon J. Schreiner, Lukas L. Imbach, Philipp O. Valko, Angelina Maric, Rina Maqkaj, Esther Werth, Christian R. Baumann, Heide Baumann-Vogel
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-02-01
Series:Frontiers in Neurology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fneur.2021.618101/full
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author Simon J. Schreiner
Simon J. Schreiner
Simon J. Schreiner
Lukas L. Imbach
Lukas L. Imbach
Philipp O. Valko
Philipp O. Valko
Philipp O. Valko
Angelina Maric
Angelina Maric
Angelina Maric
Rina Maqkaj
Rina Maqkaj
Esther Werth
Esther Werth
Esther Werth
Christian R. Baumann
Christian R. Baumann
Christian R. Baumann
Heide Baumann-Vogel
Heide Baumann-Vogel
author_facet Simon J. Schreiner
Simon J. Schreiner
Simon J. Schreiner
Lukas L. Imbach
Lukas L. Imbach
Philipp O. Valko
Philipp O. Valko
Philipp O. Valko
Angelina Maric
Angelina Maric
Angelina Maric
Rina Maqkaj
Rina Maqkaj
Esther Werth
Esther Werth
Esther Werth
Christian R. Baumann
Christian R. Baumann
Christian R. Baumann
Heide Baumann-Vogel
Heide Baumann-Vogel
author_sort Simon J. Schreiner
collection DOAJ
description Growing evidence implicates a distinct role of disturbed slow-wave sleep in neurodegenerative diseases. Reduced non-rapid eye movement (NREM) sleep slow-wave activity (SWA), a marker of slow-wave sleep intensity, has been linked with age-related cognitive impairment and Alzheimer disease pathology. However, it remains debated if SWA is associated with cognition in Parkinson disease (PD). Here, we investigated the relationship of regional SWA with cognitive performance in PD. In the present study, 140 non-demented PD patients underwent polysomnography and were administered the Montréal Cognitive Assessment (MoCA) to screen for cognitive impairment. We performed spectral analysis of frontal, central, and occipital sleep electroencephalography (EEG) derivations to measure SWA, and spectral power in other frequency bands, which we compared to cognition using linear mixed models. We found that worse MoCA performance was associated with reduced 1–4 Hz SWA in a region-dependent manner (F2, 687 =11.67, p < 0.001). This effect was driven by reduced regional SWA in the lower delta frequencies, with a strong association of worse MoCA performance with reduced 1–2 Hz SWA (F2, 687 =18.0, p < 0.001). The association of MoCA with 1–2 Hz SWA (and 1–4 Hz SWA) followed an antero-posterior gradient, with strongest, weaker, and absent associations over frontal (rho = 0.33, p < 0.001), central (rho = 0.28, p < 0.001), and occipital derivations, respectively. Our study shows that cognitive impairment in PD is associated with reduced NREM sleep SWA, predominantly in lower delta frequencies (1–2 Hz) and over frontal regions. This finding suggests a potential role of reduced frontal slow-wave sleep intensity in cognitive impairment in PD.
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spelling doaj.art-00f19376ae1f485b9a6b11b3a21ca45b2022-12-21T23:01:37ZengFrontiers Media S.A.Frontiers in Neurology1664-22952021-02-011210.3389/fneur.2021.618101618101Reduced Regional NREM Sleep Slow-Wave Activity Is Associated With Cognitive Impairment in Parkinson DiseaseSimon J. Schreiner0Simon J. Schreiner1Simon J. Schreiner2Lukas L. Imbach3Lukas L. Imbach4Philipp O. Valko5Philipp O. Valko6Philipp O. Valko7Angelina Maric8Angelina Maric9Angelina Maric10Rina Maqkaj11Rina Maqkaj12Esther Werth13Esther Werth14Esther Werth15Christian R. Baumann16Christian R. Baumann17Christian R. Baumann18Heide Baumann-Vogel19Heide Baumann-Vogel20Department of Neurology, University Hospital Zurich, University of Zurich, Zurich, SwitzerlandClinical Neuroscience Center, University Hospital Zurich, University of Zurich, Zurich, SwitzerlandSleep & Health Zurich, University of Zurich, Zurich, SwitzerlandDepartment of Neurology, University Hospital Zurich, University of Zurich, Zurich, SwitzerlandClinical Neuroscience Center, University Hospital Zurich, University of Zurich, Zurich, SwitzerlandDepartment of Neurology, University Hospital Zurich, University of Zurich, Zurich, SwitzerlandClinical Neuroscience Center, University Hospital Zurich, University of Zurich, Zurich, SwitzerlandSleep & Health Zurich, University of Zurich, Zurich, SwitzerlandDepartment of Neurology, University Hospital Zurich, University of Zurich, Zurich, SwitzerlandClinical Neuroscience Center, University Hospital Zurich, University of Zurich, Zurich, SwitzerlandSleep & Health Zurich, University of Zurich, Zurich, SwitzerlandDepartment of Neurology, University Hospital Zurich, University of Zurich, Zurich, SwitzerlandClinical Neuroscience Center, University Hospital Zurich, University of Zurich, Zurich, SwitzerlandDepartment of Neurology, University Hospital Zurich, University of Zurich, Zurich, SwitzerlandClinical Neuroscience Center, University Hospital Zurich, University of Zurich, Zurich, SwitzerlandSleep & Health Zurich, University of Zurich, Zurich, SwitzerlandDepartment of Neurology, University Hospital Zurich, University of Zurich, Zurich, SwitzerlandClinical Neuroscience Center, University Hospital Zurich, University of Zurich, Zurich, SwitzerlandSleep & Health Zurich, University of Zurich, Zurich, SwitzerlandDepartment of Neurology, University Hospital Zurich, University of Zurich, Zurich, SwitzerlandClinical Neuroscience Center, University Hospital Zurich, University of Zurich, Zurich, SwitzerlandGrowing evidence implicates a distinct role of disturbed slow-wave sleep in neurodegenerative diseases. Reduced non-rapid eye movement (NREM) sleep slow-wave activity (SWA), a marker of slow-wave sleep intensity, has been linked with age-related cognitive impairment and Alzheimer disease pathology. However, it remains debated if SWA is associated with cognition in Parkinson disease (PD). Here, we investigated the relationship of regional SWA with cognitive performance in PD. In the present study, 140 non-demented PD patients underwent polysomnography and were administered the Montréal Cognitive Assessment (MoCA) to screen for cognitive impairment. We performed spectral analysis of frontal, central, and occipital sleep electroencephalography (EEG) derivations to measure SWA, and spectral power in other frequency bands, which we compared to cognition using linear mixed models. We found that worse MoCA performance was associated with reduced 1–4 Hz SWA in a region-dependent manner (F2, 687 =11.67, p < 0.001). This effect was driven by reduced regional SWA in the lower delta frequencies, with a strong association of worse MoCA performance with reduced 1–2 Hz SWA (F2, 687 =18.0, p < 0.001). The association of MoCA with 1–2 Hz SWA (and 1–4 Hz SWA) followed an antero-posterior gradient, with strongest, weaker, and absent associations over frontal (rho = 0.33, p < 0.001), central (rho = 0.28, p < 0.001), and occipital derivations, respectively. Our study shows that cognitive impairment in PD is associated with reduced NREM sleep SWA, predominantly in lower delta frequencies (1–2 Hz) and over frontal regions. This finding suggests a potential role of reduced frontal slow-wave sleep intensity in cognitive impairment in PD.https://www.frontiersin.org/articles/10.3389/fneur.2021.618101/fullParkinson diseasesleepslow-wave sleepcognitioncognitive impairmentpolysomnography
spellingShingle Simon J. Schreiner
Simon J. Schreiner
Simon J. Schreiner
Lukas L. Imbach
Lukas L. Imbach
Philipp O. Valko
Philipp O. Valko
Philipp O. Valko
Angelina Maric
Angelina Maric
Angelina Maric
Rina Maqkaj
Rina Maqkaj
Esther Werth
Esther Werth
Esther Werth
Christian R. Baumann
Christian R. Baumann
Christian R. Baumann
Heide Baumann-Vogel
Heide Baumann-Vogel
Reduced Regional NREM Sleep Slow-Wave Activity Is Associated With Cognitive Impairment in Parkinson Disease
Frontiers in Neurology
Parkinson disease
sleep
slow-wave sleep
cognition
cognitive impairment
polysomnography
title Reduced Regional NREM Sleep Slow-Wave Activity Is Associated With Cognitive Impairment in Parkinson Disease
title_full Reduced Regional NREM Sleep Slow-Wave Activity Is Associated With Cognitive Impairment in Parkinson Disease
title_fullStr Reduced Regional NREM Sleep Slow-Wave Activity Is Associated With Cognitive Impairment in Parkinson Disease
title_full_unstemmed Reduced Regional NREM Sleep Slow-Wave Activity Is Associated With Cognitive Impairment in Parkinson Disease
title_short Reduced Regional NREM Sleep Slow-Wave Activity Is Associated With Cognitive Impairment in Parkinson Disease
title_sort reduced regional nrem sleep slow wave activity is associated with cognitive impairment in parkinson disease
topic Parkinson disease
sleep
slow-wave sleep
cognition
cognitive impairment
polysomnography
url https://www.frontiersin.org/articles/10.3389/fneur.2021.618101/full
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