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Effects of deep brain stimulation on quantitative sleep electroencephalogram during non-rapid eye movement in Parkinson’s disease

INTRODUCTION: Sleep dysfunction is frequently experienced by people with Parkinson’s disease (PD) and negatively influences quality of life. Although subthalamic nucleus (STN) deep brain stimulation (DBS) can improve sleep in PD, sleep microstructural features such as sleep spindles provide addition...

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Autores principales: Memon, Adeel A., Edney, Brandon S., Baumgartner, Alexander J., Gardner, Alan J., Catiul, Corina, Irwin, Zachary T., Joop, Allen, Miocinovic, Svjetlana, Amara, Amy W.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10551142/
https://www.ncbi.nlm.nih.gov/pubmed/37810765
http://dx.doi.org/10.3389/fnhum.2023.1269864
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author Memon, Adeel A.
Edney, Brandon S.
Baumgartner, Alexander J.
Gardner, Alan J.
Catiul, Corina
Irwin, Zachary T.
Joop, Allen
Miocinovic, Svjetlana
Amara, Amy W.
author_facet Memon, Adeel A.
Edney, Brandon S.
Baumgartner, Alexander J.
Gardner, Alan J.
Catiul, Corina
Irwin, Zachary T.
Joop, Allen
Miocinovic, Svjetlana
Amara, Amy W.
author_sort Memon, Adeel A.
collection PubMed
description INTRODUCTION: Sleep dysfunction is frequently experienced by people with Parkinson’s disease (PD) and negatively influences quality of life. Although subthalamic nucleus (STN) deep brain stimulation (DBS) can improve sleep in PD, sleep microstructural features such as sleep spindles provide additional insights about healthy sleep. For example, sleep spindles are important for better cognitive performance and for sleep consolidation in healthy adults. We hypothesized that conventional STN DBS settings would yield a greater enhancement in spindle density compared to OFF and low frequency DBS. METHODS: In a previous within-subject, cross-sectional study, we evaluated effects of low (60 Hz) and conventional high (≥130 Hz) frequency STN DBS settings on sleep macroarchitectural features in individuals with PD. In this post hoc, exploratory analysis, we conducted polysomnography (PSG)-derived quantitative electroencephalography (qEEG) assessments in a cohort of 15 individuals with PD who had undergone STN DBS treatment a median 13.5 months prior to study participation. Fourteen participants had unilateral DBS and 1 had bilateral DBS. During three nonconsecutive nights of PSG, the participants were assessed under three different DBS conditions: DBS OFF, DBS LOW frequency (60 Hz), and DBS HIGH frequency (≥130 Hz). The primary objective of this study was to investigate the changes in sleep spindle density across the three DBS conditions using repeated-measures analysis of variance. Additionally, we examined various secondary outcomes related to sleep qEEG features. For all participants, PSG-derived EEG data underwent meticulous manual inspection, with the exclusion of any segments affected by movement artifact. Following artifact rejection, sleep qEEG analysis was conducted on frontal and central leads. The measures included slow wave (SW) and spindle density and morphological characteristics, SW-spindle phase-amplitude coupling, and spectral power analysis during non-rapid eye movement (NREM) sleep. RESULTS: The analysis revealed that spindle density was significantly higher in the DBS HIGH condition compared to the DBS LOW condition. Surprisingly, we found that SW amplitude during NREM was significantly higher in the DBS LOW condition compared to DBS OFF and DBS HIGH conditions. However, no significant differences were observed in the other sleep qEEG features during sleep at different DBS conditions. CONCLUSION: This study presents preliminary evidence suggesting that conventional HIGH frequency DBS settings enhance sleep spindle density in PD. Conversely, LOW frequency settings may have beneficial effects on increasing slow wave amplitude during sleep. These findings may inform mechanisms underlying subjective improvements in sleep quality reported in association with DBS. Moreover, this work supports the need for additional research on the influence of surgical interventions on sleep disorders, which are prevalent and debilitating non-motor symptoms in PD.
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spelling pubmed-105511422023-10-06 Effects of deep brain stimulation on quantitative sleep electroencephalogram during non-rapid eye movement in Parkinson’s disease Memon, Adeel A. Edney, Brandon S. Baumgartner, Alexander J. Gardner, Alan J. Catiul, Corina Irwin, Zachary T. Joop, Allen Miocinovic, Svjetlana Amara, Amy W. Front Hum Neurosci Human Neuroscience INTRODUCTION: Sleep dysfunction is frequently experienced by people with Parkinson’s disease (PD) and negatively influences quality of life. Although subthalamic nucleus (STN) deep brain stimulation (DBS) can improve sleep in PD, sleep microstructural features such as sleep spindles provide additional insights about healthy sleep. For example, sleep spindles are important for better cognitive performance and for sleep consolidation in healthy adults. We hypothesized that conventional STN DBS settings would yield a greater enhancement in spindle density compared to OFF and low frequency DBS. METHODS: In a previous within-subject, cross-sectional study, we evaluated effects of low (60 Hz) and conventional high (≥130 Hz) frequency STN DBS settings on sleep macroarchitectural features in individuals with PD. In this post hoc, exploratory analysis, we conducted polysomnography (PSG)-derived quantitative electroencephalography (qEEG) assessments in a cohort of 15 individuals with PD who had undergone STN DBS treatment a median 13.5 months prior to study participation. Fourteen participants had unilateral DBS and 1 had bilateral DBS. During three nonconsecutive nights of PSG, the participants were assessed under three different DBS conditions: DBS OFF, DBS LOW frequency (60 Hz), and DBS HIGH frequency (≥130 Hz). The primary objective of this study was to investigate the changes in sleep spindle density across the three DBS conditions using repeated-measures analysis of variance. Additionally, we examined various secondary outcomes related to sleep qEEG features. For all participants, PSG-derived EEG data underwent meticulous manual inspection, with the exclusion of any segments affected by movement artifact. Following artifact rejection, sleep qEEG analysis was conducted on frontal and central leads. The measures included slow wave (SW) and spindle density and morphological characteristics, SW-spindle phase-amplitude coupling, and spectral power analysis during non-rapid eye movement (NREM) sleep. RESULTS: The analysis revealed that spindle density was significantly higher in the DBS HIGH condition compared to the DBS LOW condition. Surprisingly, we found that SW amplitude during NREM was significantly higher in the DBS LOW condition compared to DBS OFF and DBS HIGH conditions. However, no significant differences were observed in the other sleep qEEG features during sleep at different DBS conditions. CONCLUSION: This study presents preliminary evidence suggesting that conventional HIGH frequency DBS settings enhance sleep spindle density in PD. Conversely, LOW frequency settings may have beneficial effects on increasing slow wave amplitude during sleep. These findings may inform mechanisms underlying subjective improvements in sleep quality reported in association with DBS. Moreover, this work supports the need for additional research on the influence of surgical interventions on sleep disorders, which are prevalent and debilitating non-motor symptoms in PD. Frontiers Media S.A. 2023-09-21 /pmc/articles/PMC10551142/ /pubmed/37810765 http://dx.doi.org/10.3389/fnhum.2023.1269864 Text en Copyright © 2023 Memon, Edney, Baumgartner, Gardner, Catiul, Irwin, Joop, Miocinovic and Amara. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Human Neuroscience
Memon, Adeel A.
Edney, Brandon S.
Baumgartner, Alexander J.
Gardner, Alan J.
Catiul, Corina
Irwin, Zachary T.
Joop, Allen
Miocinovic, Svjetlana
Amara, Amy W.
Effects of deep brain stimulation on quantitative sleep electroencephalogram during non-rapid eye movement in Parkinson’s disease
title Effects of deep brain stimulation on quantitative sleep electroencephalogram during non-rapid eye movement in Parkinson’s disease
title_full Effects of deep brain stimulation on quantitative sleep electroencephalogram during non-rapid eye movement in Parkinson’s disease
title_fullStr Effects of deep brain stimulation on quantitative sleep electroencephalogram during non-rapid eye movement in Parkinson’s disease
title_full_unstemmed Effects of deep brain stimulation on quantitative sleep electroencephalogram during non-rapid eye movement in Parkinson’s disease
title_short Effects of deep brain stimulation on quantitative sleep electroencephalogram during non-rapid eye movement in Parkinson’s disease
title_sort effects of deep brain stimulation on quantitative sleep electroencephalogram during non-rapid eye movement in parkinson’s disease
topic Human Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10551142/
https://www.ncbi.nlm.nih.gov/pubmed/37810765
http://dx.doi.org/10.3389/fnhum.2023.1269864
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