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      Enhancing Slow Oscillations and Increasing N3 Sleep Proportion with Supervised, Non-Phase-Locked Pink Noise and Other Non-Standard Auditory Stimulation During NREM Sleep

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          Abstract

          Purpose

          In non-rapid eye movement (NREM) stage 3 sleep (N3), phase-locked pink noise auditory stimulation can amplify slow oscillatory activity (0.5–1 Hz). Open-loop pink noise auditory stimulation can amplify slow oscillatory and delta frequency activity (0.5–4 Hz). We assessed the ability of pink noise and other sounds to elicit delta power, slow oscillatory power, and N3 sleep.

          Participants and Methods

          Participants ( n = 8) underwent four consecutive inpatient nights in a within-participants design, starting with a habituation night. A registered polysomnographic technologist live-scored sleep stage and administered stimuli on randomized counterbalanced Enhancing and Disruptive nights, with a preceding Habituation night (night 1) and an intervening Sham night (night 3). A variety of non-phase-locked pink noise stimuli were used on Enhancing night during NREM; on Disruptive night, environmental sounds were used throughout sleep to induce frequent auditory-evoked arousals.

          Results

          Total sleep time did not differ between conditions. Percentage of N3 was higher in the Enhancing condition, and lower in the Disruptive condition, versus Sham. Standard 0.8 Hz pink noise elicited low-frequency power more effectively than other pink noise, but was not the most effective stimulus. Both pink noise on the “Enhancing” night and sounds intended to Disrupt sleep administered on the “Disruptive” night increased momentary delta and slow-wave activity (ie, during stimulation versus the immediate pre-stimulation period). Disruptive auditory stimulation degraded sleep with frequent arousals and increased next-day vigilance lapses versus Sham despite preserved sleep duration and momentary increases in delta and slow-wave activity.

          Conclusion

          These findings emphasize sound features of interest in ecologically valid, translational auditory intervention to increase restorative sleep. Preserving sleep continuity should be a primary consideration if auditory stimulation is used to enhance slow-wave activity.

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          Most cited references33

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          AASM Scoring Manual Updates for 2017 (Version 2.4)

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            Auditory closed-loop stimulation of the sleep slow oscillation enhances memory.

            Brain rhythms regulate information processing in different states to enable learning and memory formation. The <1 Hz sleep slow oscillation hallmarks slow-wave sleep and is critical to memory consolidation. Here we show in sleeping humans that auditory stimulation in phase with the ongoing rhythmic occurrence of slow oscillation up states profoundly enhances the slow oscillation rhythm, phase-coupled spindle activity, and, consequently, the consolidation of declarative memory. Stimulation out of phase with the ongoing slow oscillation rhythm remained ineffective. Closed-loop in-phase stimulation provides a straight-forward tool to enhance sleep rhythms and their functional efficacy. Copyright © 2013 Elsevier Inc. All rights reserved.
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              Cumulative sleepiness, mood disturbance, and psychomotor vigilance performance decrements during a week of sleep restricted to 4-5 hours per night.

              To determine whether a cumulative sleep debt (in a range commonly experienced) would result in cumulative changes in measures of waking neurobehavioral alertness, 16 healthy young adults had their sleep restricted 33% below habitual sleep duration, to an average 4.98 hours per night [standard deviation (SD) = 0.57] for seven consecutive nights. Subjects slept in the laboratory, and sleep and waking were monitored by staff and actigraphy. Three times each day (1000, 1600, and 2200 hours) subjects were assessed for subjective sleepiness (SSS) and mood (POMS) and were evaluated on a brief performance battery that included psychomotor vigilance (PVT), probed memory (PRM), and serial-addition testing, Once each day they completed a series of visual analog scales (VAS) and reported sleepiness and somatic and cognitive/emotional problems. Sleep restriction resulted in statistically robust cumulative effects on waking functions. SSS ratings, subscale scores for fatigue, confusion, tension, and total mood disturbance from the POMS and VAS ratings of mental exhaustion and stress were evaluated across days of restricted sleep (p = 0.009 to p = 0.0001). PVT performance parameters, including the frequency and duration of lapses, were also significantly increased by restriction (p = 0.018 to p = 0.0001). Significant time-of-day effects were evident in SSS and PVT data, but time-of-day did not interact with the effects of sleep restriction across days. The temporal profiles of cumulative changes in neurobehavioral measures of alertness as a function of sleep restriction were generally consistent. Subjective changes tended to precede performance changes by 1 day, but overall changes in both classes of measure were greatest during the first 2 days (P1, P2) and last 2 days (P6, P7) of sleep restriction. Data from subsets of subjects also showed: 1) that significant decreases in the MSLT occurred during sleep restriction, 2) that the elevated sleepiness and performance deficits continued beyond day 7 of restriction, and 3) that recovery from these deficits appeared to require two full nights of sleep. The cumulative increase in performance lapses across days of sleep restriction correlated closely with MSLT results (r = -0.95) from an earlier comparable experiment by Carskadon and Dement (1). These findings suggest that cumulative nocturnal sleep debt had a dynamic and escalating analog in cumulative daytime sleepiness and that asymptotic or steady-state sleepiness was not achieved in response to sleep restriction.
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                Author and article information

                Journal
                Nat Sci Sleep
                Nat Sci Sleep
                NSS
                nss
                Nature and Science of Sleep
                Dove
                1179-1608
                09 July 2020
                2020
                : 12
                : 411-429
                Affiliations
                [1 ]Biobehavioral Health, Pennsylvania State University , University Park, PA, USA
                [2 ]Proactive Life, Inc ., New York, NY, USA
                Author notes
                Correspondence: Orfeu M Buxton The Pennsylvania State University , 221 Biobehavioral Health Building, University Park, PA16802, USATel +1 814 867-5707 Email orfeu@psu.edu
                [*]

                These authors contributed equally to this work

                Author information
                http://orcid.org/0000-0001-5057-633X
                Article
                243204
                10.2147/NSS.S243204
                7364346
                32765139
                9037eb5e-917e-404c-8ac6-a16eba54ccbb
                © 2020 Schade et al.

                This work is published and licensed by Dove Medical Press Limited. The full terms of this license are available at https://www.dovepress.com/terms.php and incorporate the Creative Commons Attribution – Non Commercial (unported, v3.0) License ( http://creativecommons.org/licenses/by-nc/3.0/). By accessing the work you hereby accept the Terms. Non-commercial uses of the work are permitted without any further permission from Dove Medical Press Limited, provided the work is properly attributed. For permission for commercial use of this work, please see paragraphs 4.2 and 5 of our Terms ( https://www.dovepress.com/terms.php).

                History
                : 28 December 2019
                : 11 May 2020
                Page count
                Figures: 7, Tables: 5, References: 42, Pages: 19
                Funding
                Funded by: National Science Foundation (NSF)
                Award ID: 1622766
                Funded by: National Center for Advancing Translational Sciences, National Institutes of Health
                Award ID: UL1TR002014
                Funded by: College of Health and Human Development of the Pennsylvania State University
                Award ID: R43AG056250
                The current work was supported by the National Science Foundation (NSF) under grant #1622766 awarded to Gartenberg (PI; CEO Proactive Life Inc, formerly Mobile Sleep Technologies LLC (DBA SleepSpace)). Work was conducted at Pennsylvania State University (via subcontract) and further supported by the Pennsylvania State University Clinical and Translational Sciences Institute (funded by the National Center for Advancing Translational Sciences, National Institutes of Health, through Grant UL1TR002014) and institutional funds from the College of Health and Human Development of the Pennsylvania State University to Dr. Buxton. Collaboration also included a separate project: NIH/NIA SBIR R43AG056250 to Gartenberg (PI; CEO Proactive Life Inc) “Non-pharmacological improvement of sleep structure in midlife and older adults” via subcontract to Pennsylvania State University. The content is solely the responsibility of the authors and does not necessarily represent the official views of the NSF or NIH.
                Categories
                Original Research

                electroencephalographic spectral analysis,neurobehavioral performance,slow-wave sleep,sleep fragmentation,delta power,slow oscillation

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