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Research ArticleNegative Results, Cognition and Behavior

Closed-Loop Acoustic Stimulation Enhances Sleep Oscillations But Not Memory Performance

Simon Henin, Helen Borges, Anita Shankar, Cansu Sarac, Lucia Melloni, Daniel Friedman, Adeen Flinker, Lucas C. Parra, Gyorgy Buzsaki, Orrin Devinsky and Anli Liu
eNeuro 11 October 2019, 6 (6) ENEURO.0306-19.2019; DOI: https://doi.org/10.1523/ENEURO.0306-19.2019
Simon Henin
1NYU Comprehensive Epilepsy Center, New York, New York 10016
2New York University Langone Health, New York, NY 10016
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Helen Borges
1NYU Comprehensive Epilepsy Center, New York, New York 10016
2New York University Langone Health, New York, NY 10016
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Anita Shankar
1NYU Comprehensive Epilepsy Center, New York, New York 10016
2New York University Langone Health, New York, NY 10016
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Cansu Sarac
1NYU Comprehensive Epilepsy Center, New York, New York 10016
2New York University Langone Health, New York, NY 10016
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Lucia Melloni
1NYU Comprehensive Epilepsy Center, New York, New York 10016
2New York University Langone Health, New York, NY 10016
3Max Planck Institute for Empirical Aesthetics, 60322 Frankfurt am Main, Germany
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Daniel Friedman
1NYU Comprehensive Epilepsy Center, New York, New York 10016
2New York University Langone Health, New York, NY 10016
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Adeen Flinker
1NYU Comprehensive Epilepsy Center, New York, New York 10016
2New York University Langone Health, New York, NY 10016
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Lucas C. Parra
4Department of Biomedical Engineering, City College of New York, New York, New York 10031
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Gyorgy Buzsaki
2New York University Langone Health, New York, NY 10016
5NYU Neuroscience Institute, New York, New York 10016
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Orrin Devinsky
1NYU Comprehensive Epilepsy Center, New York, New York 10016
2New York University Langone Health, New York, NY 10016
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Anli Liu
1NYU Comprehensive Epilepsy Center, New York, New York 10016
2New York University Langone Health, New York, NY 10016
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  • Figure 1.
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    Figure 1.

    Schema for experiments 1 and 2. Timing of different phases for each experiment. In experiment 1, subjects arrived at the laboratory at 11:00 A.M. Following informed consent, participants performed the encoding portion of the word pair associates and virtual reality (VR) tasks, followed by setup of EEG electrodes. After a 2 h nap opportunity, participants completed the recall portions of the VR and word pair associates tasks, respectively. In experiment 2, participants arrived at the sleep laboratory at 9:00 P.M. for the accommodation night (no memory tasks or stimulation performed). On experimental nights (weeks 1 and 2), participants arrived at the sleep laboratory at 8:00 P.M. for EEG electrode setup, followed by word pair associates encoding at ∼9:00 P.M. Light’s out started at 11:00 P.M., and participants were awoken at ∼6:00 A.M. (e.g., after 7 h). A 1 week delay (washout) occurred between every session.

  • Figure 2.
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    Figure 2.

    Closed-loop stimulation during a daytime nap enhances slow wave–spindle complexes, but does not enhance memory performance. A, Evoked responses from 12 subjects (mean ± SEM) shows that stimulation delivered during slow-wave UP states (red curves; dashed red line indicates the onset of acoustic pulse) enhances ongoing slow-wave oscillations (red) compared with sham stimulation (black). Spindle power is also increased in stimulation (red) compared with sham (black; inset). B, C, Memory performance, as assessed by postnap retention of word pairs (B), and spatial navigation performance, as measured by the number of speed improvements (C), do not exhibit a significant benefit from acoustic stimulation relative to sham (each line represents individual subject performance).

  • Figure 3.
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    Figure 3.

    Acoustic stimulation during nap sleep enhances both fast- and slow-spindle amplitudes but is not related to memory performance. A, Fast-spindle (12–15 Hz) and slow-spindle (9–12 Hz) amplitude at electrode Cz time locked to the negative DOWN state of all off-line detected SO events (t = 0). Both fast- and slow-spindle amplitude showed significant increases in amplitude in the stimulation (red) condition relative to sham (black) stimulation. B, Scatter plots of retention versus peak fast-spindle amplitude (left) and the number of VR improvements versus peak fast-spindle amplitude (right) across individuals in sham and stimulation conditions (no significant correlations in either task).

  • Figure 4.
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    Figure 4.

    Closed-loop stimulation during overnight sleep enhances slow-wave and spindle oscillations, but does not enhance verbal memory performance. A, Mean ± SEM EEG signal (at electrode Cz) averaged (across 19 subjects) time locked to the first auditory stimulus (t = 0 s) for the stimulation (red) and sham (black) conditions. The bottom panel indicates significant differences between conditions. Evoked responses from 19 subjects show that stimulation delivered during slow-wave UP states (red curves; dashed lines indicate onset of acoustic pulse) enhances ongoing slow-wave oscillations relative to sham stimulation (black). B, Memory performance, as assessed by the word pair associates task does not exhibit a significant benefit from acoustic stimulation relative to sham (mean, SEM). C, Correlation (and trend line) between the amount of SWS during the stimulation period and retention on the behavioral task. Correlations were not significant in either condition.

  • Figure 5.
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    Figure 5.

    Acoustic stimulation enhances both fast- and slow-spindle amplitude but is not related to verbal memory consolidation. A, Fast-spindle (12–15 Hz) and slow-spindle (9–12 Hz) amplitude at electrode Cz time locked to the negative DOWN state of all detected SO events (t = 0). B, Scatter plot of retention versus peak fast-spindle amplitude across individuals in sham and stimulation conditions (not significant in either condition).

Tables

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    Table 1.

    Subject characteristics

    Experiment 1 (N = 12)Experiment 2 (N = 19)
    Female (n, %)6.050.0%9.047.4%
    Age, years (mean, SEM)23.30.823.30.9
    Race (n, %)
        Caucasian/white5.041.7%8.042.1%
        African American/black4.033.3%2.010.5%
        Asian3.025.0%5.026.3%
        Biracial0.00.0%1.05.3%
        Not specified0.00.0%3.015.8%
        Hispanic/Latino (n, %)0.00.0%2.010.5%
    Education, years (mean, SEM)15.80.314.70.4
    SSS score visit 1 maximum score = 6
        Pre (mean, SEM)2.90.33.50.4
        Post (mean, SEM)2.20.32.60.2
    SSS score visit 2 maximum score = 6
        Pre (mean, SEM)2.30.23.50.3
        Post (mean, SEM)2.20.32.50.3
    PVT score visit 1
        Pre (mean, SEM)0.30.0
        Post (mean, SEM)0.30.0
    PVT score visit 2
        Pre (mean, SEM)0.30.0
        Post (mean, SEM)0.30.0
    MOCA score maximum score = 30
    (mean, SEM)27.90.428.60.3
    • Demographics table of subjects who participated in experiments 1 and 2.

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    Table 2.

    Mean time spent in each sleep stage during experiment 1 (nap study)

    StimShamp Value
    W7.42% (1.85)6.29% (1.73)0.49
    N120.92% (2.96)20.92% (1.59)0.53
    N230.77% (4.04)33.26% (4.19)0.57
    SWS16.53% (2.73)18.45% (2.03)0.40
    REM22.57% (6.91)21.01% (5.16)0.78
    MA0.08% (0.08)0.07% (0.06)0.92
    TST (mins)83.0 (9.60)79.3 (7.31)0.69
    • Sleep during daytime nap study is characterized with the average time spent in each sleep stage (mean ± SEM). The percentage of time spent in each condition (W, wake; N1, stage 1; N2, stage 2; MA, movement artifact) was similar during the stimulation period, demonstrating that stimulation did not disrupt sleep or increase the overall time spent in non-REM sleep.

    • View popup
    Table 3.

    Slow-oscillation characteristics during afternoon nap closed-loop stimulation (experiment 1)

    StimShamp Value
    Number of SOs166.67 (27.76)154.58 (17.65)0.52
    SO amplitude (μV)147.36 (13.04)143.17 (9.89)0.40
    SO slope (μV/s)278.68 (26.09)275.92 (20.30)0.83
    Duration (s)1.13 (0.01)1.15 (0.01)0.04
    • Mean ± SEM number of slow oscillations (identified off-line; see Materials and Methods) during the entire recording, amplitude (negative half-wave-to-peak), slope, and duration between stim and sham conditions. Duration of SO in the stimulation condition was significantly shorter compared with the sham condition, suggesting that the induced SO oscillation peaked at a higher frequency compared with the sham condition (∼1 Hz)

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    Table 4.

    Bayesian paired-samples t test for memory tests in experiments 1 and 2

    BF10Error %
    Experiment 1
        Word pair retention
            Stim-sham0.3020.019
        VR speed improvements
            Stim-sham0.2990.019
    Experiment 2
        Word pair retention
            Stim-sham0.2490.012
    • Bayes factor (BF10) and proportional error of the BF for paired-samples t test of the hypothesis the memory performance scores in the stim and sham sessions are equal. A Bayes factor <1 indicates evidence in favor of the null hypothesis (e.g., stim = sham)

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    Table 5.

    Mean ± SEM spent in each sleep stage during experiment 2 (overnight study)

    StimShamp Value
    W1.55% (0.69)4.11% (3.21)0.44
    N13.61% (1.00)2.19% (0.64)0.23
    N244.50% (3.47)39.33% (3.89)0.33
    SWS39.69% (3.34)40.85% (4.32)0.83
    REM9.25% (1.35)7.39% (1.48)0.36
    MA1.39% (0.29)0.89% (0.20)0.17
    Total sleep time (min)394.4 (15.6)398.5 (11.1)0.83
    • Sleep characteristics during the 210 min stimulation period showing the average time spent in each sleep stage demonstrates that the percentage of time spent in each condition (W, wake; N1, stage 1; N2, stage 2; MA, muscle artifact) was similar during the stimulation period, suggesting that stimulation did not disrupt sleep or increase the overall time spent in NREM sleep.

    • View popup
    Table 6.

    Characteristics of slow oscillations during overnight closed-loop stimulation (experiment 2).

    StimShamp Value
    Number of SOs (stimulation period)529.37 (74.71)477.05 (60.75)0.59
    Number of SOs (entire night)1356.37 (111.47)1338.89 (106.62)0.87
    SO amplitude (μV)141.93 (9.16)128.62 (10.06)0.24
    SO slope (μV/s)277.64 (21.97)244.02 (20.80)0.14
    Duration (s)1.18 (0.01)1.14 (0.07)0.49
    • Mean ± SEM number of slow oscillations (SOs identified off-line; see Materials and Methods) during SWS epochs of the stimulation period and the entire night, amplitude (negative half-wave to positive-peak), slope, and duration between stim and sham conditions.

    • View popup
    Table 7.

    Comparison of previous studies using acoustic stimulation to boost slow oscillations and spindle and their effects on memory

    StudyStudy designBehavioral resultsEEG results
    Ngo et al., 2013N = 11 healthy young adults (mean ± SD age, 24.2 ± 2.98 years)Stimulation protocolHedges gav = 1.07
    Retention (presleep − postsleep):
    Stim: 22.2 ± 2.3 words
    Sham: 13.0 ± 2.5 words
    Increase in slow-wave and spindle power
    Closed-loop
    Two-pulse stimulation
    overnight sleep (7 h)
    Memory tests
    120 semantically related word pairs
    Cox et al., 2014bN = 12 healthy adults (age range, 18–23 years; 11 females)Stimulation protocolNo behavioral effect observedIncreased slow-wave amplitude and spindle band power with sounds targeted at up-state
    Closed-loop
    One-pulse stimulation
    Evening nap (2 h)
    Memory tests
    Sound stimulus memory task
    Ong et al., 2016N = 16 healthy young adults (mean ± SD age, 22 &#x00B1; 1.4 years)Stimulation protocolHedges gav = 0.41Retention (presleep − postsleep):Sham: −1.72 ± 4.16 SDsStim: 0.0 ± 3.76 SDsIncreased slow-wave amplitude, theta, and fast-spindle activity
    Closed-loopFive consecutive pulsesAfternoon nap (1.5 h)
    Memory tests
    40 semantically related word pairs
    Weigenand et al., 2016N = 26 healthy young adults (mean age, 22.2 years; age range, 18– 28 years)Stimulation protocolNo behavioral effect observedIncrease in slow-wave and increase in spindle power with first pulse
    Open-loopThree consecutive pulse stimulationOvernight sleep (7 h)
    Memory tests
    120 semantically related word pairs1
    Leminen et al., 2017N = 15 healthy adults (mean age, 30.5 years; range, 23–42 years)Stimulation protocolHedges gav = 0.65Retention (presleep – postsleep):Stim: 21.1 ± 7.7 SDsSham: 15.6 ± 8.1 SDsNo behavioral effect on face–name memory, finger tapping, or picture memory (tasks 2–4)Increase in slow-wave and spindle power
    Closed-loopSingle-pulse stimulationOvernight sleep (7 h)
    Memory tests
    120 semantically related word pairs2 Face–name association testFinger-tapping testPicture recognition task
    Papalambros et al., 2017N = 13 healthy older adults (mean age, 75.2 years; age range, 60–84 years)Stimulation protocolHedges gav = 0.77Retention (presleep – postsleep):Stim: 9.2 ± 7.93 SDsSham: 3.1 ± 6.85 SDsIncrease in slow-wave and spindle power
    Closed-loopFive-pulse, phase-locked loop stimulationOvernight sleep (8 h)
    Memory tests
    88 semantically related word pairs
    Ngo et al., 2019N = 24 healthy young adults (mean ± SD age, 23.9 ± 3.42 years)Stimulation protocolNo behavioral effect observedAcute increase in slow-wave and spindle power, but no effect on total overnight slow-wave and spindle power
    Closed-loopSeven-click spindle stimulationOvernight sleep (7 h)
    Memory tests
    120 semantically related word pairs1
    • For each study, the brief description of the subject pool, stimulation and memory protocols, effect size (Hedges gav) of the behavioral effect (if applicable), and overall electrophysiological findings are provided.

    • ↵1 Same word lists used in Ngo et al., 2013.

    • ↵2 Translated from list used in Ngo et al., 2013.

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Closed-Loop Acoustic Stimulation Enhances Sleep Oscillations But Not Memory Performance
Simon Henin, Helen Borges, Anita Shankar, Cansu Sarac, Lucia Melloni, Daniel Friedman, Adeen Flinker, Lucas C. Parra, Gyorgy Buzsaki, Orrin Devinsky, Anli Liu
eNeuro 11 October 2019, 6 (6) ENEURO.0306-19.2019; DOI: 10.1523/ENEURO.0306-19.2019

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Closed-Loop Acoustic Stimulation Enhances Sleep Oscillations But Not Memory Performance
Simon Henin, Helen Borges, Anita Shankar, Cansu Sarac, Lucia Melloni, Daniel Friedman, Adeen Flinker, Lucas C. Parra, Gyorgy Buzsaki, Orrin Devinsky, Anli Liu
eNeuro 11 October 2019, 6 (6) ENEURO.0306-19.2019; DOI: 10.1523/ENEURO.0306-19.2019
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Keywords

  • acoustic stimulation
  • declarative memory
  • memory
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  • sleep
  • spindles

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