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....
Main Authors: | , , , , , , , |
---|---|
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 |
_version_ | 1818417983276449792 |
---|---|
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. |
first_indexed | 2024-12-14T12:15:27Z |
format | Article |
id | doaj.art-00f19376ae1f485b9a6b11b3a21ca45b |
institution | Directory Open Access Journal |
issn | 1664-2295 |
language | English |
last_indexed | 2024-12-14T12:15:27Z |
publishDate | 2021-02-01 |
publisher | Frontiers Media S.A. |
record_format | Article |
series | Frontiers in Neurology |
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 |
work_keys_str_mv | AT simonjschreiner reducedregionalnremsleepslowwaveactivityisassociatedwithcognitiveimpairmentinparkinsondisease AT simonjschreiner reducedregionalnremsleepslowwaveactivityisassociatedwithcognitiveimpairmentinparkinsondisease AT simonjschreiner reducedregionalnremsleepslowwaveactivityisassociatedwithcognitiveimpairmentinparkinsondisease AT lukaslimbach reducedregionalnremsleepslowwaveactivityisassociatedwithcognitiveimpairmentinparkinsondisease AT lukaslimbach reducedregionalnremsleepslowwaveactivityisassociatedwithcognitiveimpairmentinparkinsondisease AT philippovalko reducedregionalnremsleepslowwaveactivityisassociatedwithcognitiveimpairmentinparkinsondisease AT philippovalko reducedregionalnremsleepslowwaveactivityisassociatedwithcognitiveimpairmentinparkinsondisease AT philippovalko reducedregionalnremsleepslowwaveactivityisassociatedwithcognitiveimpairmentinparkinsondisease AT angelinamaric reducedregionalnremsleepslowwaveactivityisassociatedwithcognitiveimpairmentinparkinsondisease AT angelinamaric reducedregionalnremsleepslowwaveactivityisassociatedwithcognitiveimpairmentinparkinsondisease AT angelinamaric reducedregionalnremsleepslowwaveactivityisassociatedwithcognitiveimpairmentinparkinsondisease AT rinamaqkaj reducedregionalnremsleepslowwaveactivityisassociatedwithcognitiveimpairmentinparkinsondisease AT rinamaqkaj reducedregionalnremsleepslowwaveactivityisassociatedwithcognitiveimpairmentinparkinsondisease AT estherwerth reducedregionalnremsleepslowwaveactivityisassociatedwithcognitiveimpairmentinparkinsondisease AT estherwerth reducedregionalnremsleepslowwaveactivityisassociatedwithcognitiveimpairmentinparkinsondisease AT estherwerth reducedregionalnremsleepslowwaveactivityisassociatedwithcognitiveimpairmentinparkinsondisease AT christianrbaumann reducedregionalnremsleepslowwaveactivityisassociatedwithcognitiveimpairmentinparkinsondisease AT christianrbaumann reducedregionalnremsleepslowwaveactivityisassociatedwithcognitiveimpairmentinparkinsondisease AT christianrbaumann reducedregionalnremsleepslowwaveactivityisassociatedwithcognitiveimpairmentinparkinsondisease AT heidebaumannvogel reducedregionalnremsleepslowwaveactivityisassociatedwithcognitiveimpairmentinparkinsondisease AT heidebaumannvogel reducedregionalnremsleepslowwaveactivityisassociatedwithcognitiveimpairmentinparkinsondisease |