Effects of deep brain stimulation on quantitative sleep electroencephalogram during non-rapid eye movement in Parkinson’s disease
IntroductionSleep 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...
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Frontiers Media S.A.
2023-09-01
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| Series: | Frontiers in Human Neuroscience |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fnhum.2023.1269864/full |
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| author | Adeel A. Memon Brandon S. Edney Alexander J. Baumgartner Alexander J. Baumgartner Alan J. Gardner Corina Catiul Zachary T. Irwin Allen Joop Svjetlana Miocinovic Amy W. Amara |
| author_facet | Adeel A. Memon Brandon S. Edney Alexander J. Baumgartner Alexander J. Baumgartner Alan J. Gardner Corina Catiul Zachary T. Irwin Allen Joop Svjetlana Miocinovic Amy W. Amara |
| author_sort | Adeel A. Memon |
| collection | DOAJ |
| description | IntroductionSleep 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.MethodsIn 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.ResultsThe 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.ConclusionThis 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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| last_indexed | 2024-03-11T22:35:09Z |
| publishDate | 2023-09-01 |
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| spelling | doaj.art-ba81ac2a4911420c8c539848611a7d162023-09-22T15:33:04ZengFrontiers Media S.A.Frontiers in Human Neuroscience1662-51612023-09-011710.3389/fnhum.2023.12698641269864Effects of deep brain stimulation on quantitative sleep electroencephalogram during non-rapid eye movement in Parkinson’s diseaseAdeel A. Memon0Brandon S. Edney1Alexander J. Baumgartner2Alexander J. Baumgartner3Alan J. Gardner4Corina Catiul5Zachary T. Irwin6Allen Joop7Svjetlana Miocinovic8Amy W. Amara9Department of Neurology, West Virginia University Rockefeller Neuroscience Institute, Morgantown, WV, United StatesSchool of Medicine, University of Alabama at Birmingham, Birmingham, AL, United StatesDepartment of Neurology, University of Colorado Anschutz Medical Campus, Aurora, CO, United StatesDepartment of Neurosurgery, University of Colorado Anschutz Medical Campus, Aurora, CO, United StatesNeuroscience Undergraduate Program, University of Alabama at Birmingham, Birmingham, AL, United StatesDepartment of Neurology, University of Alabama at Birmingham, Birmingham, AL, United StatesDepartment of Neurosurgery, University of Alabama at Birmingham, Birmingham, AL, United StatesSchool of Medicine, University of Alabama at Birmingham, Birmingham, AL, United StatesDepartment of Neurology, Emory University, Atlanta, GA, United StatesDepartment of Neurology, University of Colorado Anschutz Medical Campus, Aurora, CO, United StatesIntroductionSleep 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.MethodsIn 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.ResultsThe 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.ConclusionThis 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.https://www.frontiersin.org/articles/10.3389/fnhum.2023.1269864/fullParkinson’s diseasesleep spindlessleepcognitionsleep qEEGDeep brain stimulation |
| spellingShingle | Adeel A. Memon Brandon S. Edney Alexander J. Baumgartner Alexander J. Baumgartner Alan J. Gardner Corina Catiul Zachary T. Irwin Allen Joop Svjetlana Miocinovic Amy W. Amara Effects of deep brain stimulation on quantitative sleep electroencephalogram during non-rapid eye movement in Parkinson’s disease Frontiers in Human Neuroscience Parkinson’s disease sleep spindles sleep cognition sleep qEEG Deep brain stimulation |
| 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 | Parkinson’s disease sleep spindles sleep cognition sleep qEEG Deep brain stimulation |
| url | https://www.frontiersin.org/articles/10.3389/fnhum.2023.1269864/full |
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