Real-Time Excitation of Slow Oscillations during Deep Sleep Using Acoustic Stimulation
Language English Country Switzerland Media electronic
Document type Journal Article
Grant support
NV18-07-00272
Ministerstvo Zdravotnictví Ceské Republiky
SGS21/140/OHK4/2T/17
České Vysoké Učení Technické v Praze
LO1611
NIMH NIH HHS - United States
PubMed
34372405
PubMed Central
PMC8347755
DOI
10.3390/s21155169
PII: s21155169
Knihovny.cz E-resources
- Keywords
- acoustic stimulation, inter trial phase clustering, phase-locked loop, slow-wave activity,
- MeSH
- Acoustic Stimulation MeSH
- Electroencephalography MeSH
- Humans MeSH
- Sleep, Slow-Wave * MeSH
- Sleep MeSH
- Physical Therapy Modalities MeSH
- Check Tag
- Humans MeSH
- Publication type
- Journal Article MeSH
Slow-wave synchronous acoustic stimulation is a promising research and therapeutic tool. It is essential to clearly understand the principles of the synchronization methods, to know their performances and limitations, and, most importantly, to have a clear picture of the effect of stimulation on slow-wave activity (SWA). This paper covers the mentioned and currently missing parts of knowledge that are essential for the appropriate development of the method itself and future applications. Artificially streamed real sleep EEG data were used to quantitatively compare the two currently used real-time methods: the phase-locking loop (PLL) and the fixed-step stimulus in our own implementation. The fixed-step stimulation method was concluded to be more reliable and practically applicable compared to the PLL method. The sleep experiment with chronic insomnia patients in our sleep laboratory was analyzed in order to precisely characterize the effect of sound stimulation during deep sleep. We found that there is a significant phase synchronization of delta waves, which were shown to be the most sensitive metric of the effect of acoustic stimulation compared to commonly used averaged signal and power analyses. This finding may change the understanding of the effect and function of the SWA stimulation described in the literature.
3rd Faculty of Medicine Charles University Ruská 87 100 00 Prague Czech Republic
Faculty of Biomedical Engineering Czech Technical University Prague 272 01 Kladno Czech Republic
National Institute of Mental Health 250 67 Klecany Czech Republic
See more in PubMed
Diykh M., Li Y., Abdulla S. EEG sleep stages identification based on weighted undirected complex networks. Comput. Methods Programs Biomed. 2020;184:105116. doi: 10.1016/j.cmpb.2019.105116. PubMed DOI
Ko L.W., Su C.H., Yang M.H., Liu S.Y., Su T.P. A pilot study on essential oil aroma stimulation for enhancing slow-wave EEG in sleeping brain. Sci. Rep. 2021;11:1–11. doi: 10.1038/s41598-020-80171-x. PubMed DOI PMC
Cox R., Fell J. Analyzing human sleep EEG. Sleep Med. Rev. 2020;54:101353. doi: 10.1016/j.smrv.2020.101353. PubMed DOI
Iber C. The AASM Manual for Scoring of Sleep and Associated Events: Rules, Terminology and Technical Specifications. AASM; Westchester, IL, USA: 2017.
Jirakittayakorn N., Wongsawat Y. A Novel Insight of Effects of a 3-Hz Binaural Beat on Sleep Stages During Sleep. Front. Hum. Neurosci. 2018;12:387. doi: 10.3389/fnhum.2018.00387. PubMed DOI PMC
Danilenko K.V., Kobelev E., Yarosh S.V., Khazankin G.R., Brack I.V., Miroshnikova P.V., Aftanas L.I. Effectiveness of Visual vs. Acoustic Closed-Loop Stimulation on EEG Power Density during NREM Sleep in Humans. Clocks Sleep. 2020;2:172–181. doi: 10.3390/clockssleep2020014. PubMed DOI PMC
Mander B.A., Marks S.M., Vogel J.W., Rao V., Lu B., Saletin J.M., Ancoli-Israel S., Jagust W.J., Walker M.P. β-amyloid disrupts human NREM slow waves and related hippocampus-dependent memory consolidation. Nat. Neurosci. 2015;18:1051–1057. doi: 10.1038/nn.4035. PubMed DOI PMC
Koo P.C., Mölle M., Marshall L. Efficacy of slow oscillatory-transcranial direct current stimulation on EEG and memory—Contribution of an inter-individual factor. Eur. J. Neurosci. 2018;47:812–823. doi: 10.1111/ejn.13877. PubMed DOI
Leger D., Debellemaniere E., Rabat A., Bayon V., Benchenane K., Chennaoui M. Slow-wave sleep. Sleep Med. Rev. 2018;41:113–132. doi: 10.1016/j.smrv.2018.01.008. PubMed DOI
Harrington M.O., Ashton J.E., Ngo H.V.V., Cairney S.A. Phase-locked auditory stimulation of theta oscillations during rapid eye movement sleep. Sleep. 2021;44:zsaa227. doi: 10.1093/sleep/zsaa227. PubMed DOI
Born J. Slow-wave sleep and the consolidation of long-term memory. World J. Biol. Psychiatry. 2010;11:16–21. doi: 10.3109/15622971003637637. PubMed DOI
Mölle M., Born J. Slow oscillations orchestrating fast oscillations and memory consolidation. Prog. Brain Res. 2011;193:93–110. PubMed
Diekelmann S., Born J. The memory function of sleep. Nat. Rev. Neurosci. 2010;11:114–126. doi: 10.1038/nrn2762. PubMed DOI
Rasch B., Born J. About sleep’s role in memory. Physiol. Rev. 2013 doi: 10.1152/physrev.00032.2012. PubMed DOI PMC
Kurth S., Riedner B.A., Dean D.C., O’Muircheartaigh J., Huber R., Jenni O.G., Deoni S.C.L., LeBourgeois M.K. Traveling Slow Oscillations During Sleep. Sleep. 2017;40 doi: 10.1093/sleep/zsx121. PubMed DOI PMC
Onojima T., Kitajo K., Mizuhara H., Alain C. Ongoing slow oscillatory phase modulates speech intelligibility in cooperation with motor cortical activity. PLoS ONE. 2017;12:e0183146. doi: 10.1371/journal.pone.0183146. PubMed DOI PMC
Salfi F., D’Atri A., Tempesta D., De Gennaro L., Ferrara M. Boosting Slow Oscillations during Sleep to Improve Memory Function in Elderly People: A Review of the Literature. Brain Sci. 2020;10:300. doi: 10.3390/brainsci10050300. PubMed DOI PMC
Grimaldi D., Papalambros N.A., Zee P.C., Malkani R.G. Neurostimulation techniques to enhance sleep and improve cognition in aging. Neurobiol. Dis. 2020;141:104865. doi: 10.1016/j.nbd.2020.104865. PubMed DOI
Garcia-Molina G., Tsoneva T., Jasko J., Steele B., Aquino A., Baher K., Pastoor S., Pfundtner S., Ostrowski L., Miller B., et al. Closed-loop system to enhance slow-wave activity. J. Neural Eng. 2018;15:066018. doi: 10.1088/1741-2552/aae18f. PubMed DOI
Ngo H.V.V., Claussen J.C., Born J., Molle M. Induction of slow oscillations by rhythmic acoustic stimulation. J. Sleep Res. 2013;22:22–31. doi: 10.1111/j.1365-2869.2012.01039.x. PubMed DOI
Cox R., Korjoukov I., de Boer M., Talamini L.M. Sound Asleep. PLoS ONE. 2014;9:e101567. doi: 10.1371/journal.pone.0101567. PubMed DOI PMC
Ngo H.V.V., Martinetz T., Born J., Mölle M. Auditory Closed-Loop Stimulation of the Sleep Slow Oscillation Enhances Memory. Neuron. 2013;78:545–553. doi: 10.1016/j.neuron.2013.03.006. PubMed DOI
Ngo H.V.V., Miedema A., Faude I., Martinetz T., Mölle M., Born J. Driving Sleep Slow Oscillations by Auditory Closed-Loop Stimulation—A Self-Limiting Process. J. Neurosci. 2015;35:6630–6638. doi: 10.1523/JNEUROSCI.3133-14.2015. PubMed DOI PMC
Besedovsky L., Ngo H.V.V., Dimitrov S., Gassenmaier C., Lehmann R., Born J. Auditory closed-loop stimulation of EEG slow oscillations strengthens sleep and signs of its immune-supportive function. Nat. Commun. 2017;8:1–8. doi: 10.1038/s41467-017-02170-3. PubMed DOI PMC
Costa M.S., Weigenand A., Ngo H.V.V., Marshall L., Born J., Martinetz T., Claussen J.C., Daunizeau J. A Thalamocortical Neural Mass Model of the EEG during NREM Sleep and Its Response to Auditory Stimulation. PLoS Comput. Biol. 2016;12:e1005022. doi: 10.1371/journal.pcbi.1005022. PubMed DOI PMC
Santostasi G., Malkani R., Riedner B., Bellesi M., Tononi G., Paller K.A., Zee P.C. Phase-locked loop for precisely timed acoustic stimulation during sleep. J. Neurosci. Methods. 2016;259:101–114. doi: 10.1016/j.jneumeth.2015.11.007. PubMed DOI PMC
Papalambros N.A., Santostasi G., Malkani R.G., Braun R., Weintraub S., Paller K.A., Zee P.C. Acoustic Enhancement of Sleep Slow Oscillations and Concomitant Memory Improvement in Older Adults. Front. Hum. Neurosci. 2017;11 doi: 10.3389/fnhum.2017.00109. PubMed DOI PMC
Ong J.L., Lo J.C., Chee N.I., Santostasi G., Paller K.A., Zee P.C., Chee M.W. Effects of phase-locked acoustic stimulation during a nap on EEG spectra and declarative memory consolidation. Sleep Med. 2016;20:88–97. doi: 10.1016/j.sleep.2015.10.016. PubMed DOI
Navarrete M., Schneider J., Ngo H.V.V., Valderrama M., Casson A.J., Lewis P.A. Examining the optimal timing for closed-loop auditory stimulation of slow-wave sleep in young and older adults. Sleep. 2020;43:zsz315. doi: 10.1093/sleep/zsz315. PubMed DOI PMC
Weigenand A., Mölle M., Werner F., Martinetz T., Marshall L. Timing matters: Open-loop stimulation does not improve overnight consolidation of word pairs in humans. Eur. J. Neurosci. 2016;44:2357–2368. doi: 10.1111/ejn.13334. PubMed DOI PMC
Leminen M., Virkkala J., Saure E., Paajanen T., Zee P., Santostasi G., Hublin C., Müller K., Porkka-Heiskanen T., Huotilainen M., et al. Enhanced memory consolidation via automatic sound stimulation during non-REM sleep. Sleep. 2017;40 doi: 10.1093/sleep/zsx003. PubMed DOI PMC
Debellemaniere E., Chambon S., Pinaud C., Thorey V., Dehaene D., Léger D., Chennaoui M., Arnal P.J., Galtier M.N. Performance of an Ambulatory Dry-EEG Device for Auditory Closed-Loop Stimulation of Sleep Slow Oscillations in the Home Environment. Front. Hum. Neurosci. 2018;12:88. doi: 10.3389/fnhum.2018.00088. PubMed DOI PMC
Grimaldi D., Papalambros N., Reid K., Abbott S., Malkani R., Gendy M., Iwanaszko M., Braun R., Sanchez D., Paller K., et al. Strengthening sleep-autonomic interaction via acoustic enhancement of slow oscillations. Sleep. 2019;42 doi: 10.1093/sleep/zsz036. PubMed DOI PMC
Simor P., Steinbach E., Nagy T., Gilson M., Farthouat J., Schmitz R., Gombos F., Ujma P.P., Pamula M., Bódizs R., et al. Lateralized rhythmic acoustic stimulation during daytime NREM sleep enhances slow waves. Sleep. 2018;41 doi: 10.1093/sleep/zsy176. PubMed DOI
Fattinger S., Heinzle B.B., Ramantani G., Abela L., Schmitt B., Huber R. Closed-Loop Acoustic Stimulation During Sleep in Children With Epilepsy: A Hypothesis-Driven Novel Approach to Interact With Spike-Wave Activity and Pilot Data Assessing Feasibility. Front. Hum. Neurosci. 2019;13:166. doi: 10.3389/fnhum.2019.00166. PubMed DOI PMC
Bin Heyat M.B., Akhtar F., Ansari M., Khan A., Alkahtani F., Khan H., Lai D. Progress in Detection of Insomnia Sleep Disorder: A Comprehensive Review. Curr. Drug Targets. 2021;22:672–684. doi: 10.2174/1389450121666201027125828. PubMed DOI
Hamdy R.C., Kinser A., Dickerson K., Kendall-Wilson T., Depelteau A., Copeland R., Whalen K. Insomnia and mild cognitive impairment. Gerontol. Geriatr. Med. 2018;4:2333721418778421. doi: 10.1177/2333721418778421. PubMed DOI PMC
Melo D.L.M., Carvalho L.B.C., Prado L.B.F., Prado G.F. Biofeedback therapies for chronic insomnia: A systematic review. Appl. Psychophysiol. Biofeedback. 2019;44:259–269. doi: 10.1007/s10484-019-09442-2. PubMed DOI
Merica H., Blois R., Gaillard J.M. Spectral characteristics of sleep EEG in chronic insomnia. Eur. J. Neurosci. 1998;10:1826–1834. doi: 10.1046/j.1460-9568.1998.00189.x. PubMed DOI
Carrier J., Land S., Buysse D.J., Kupfer D.J., Monk T.H. The effects of age and gender on sleep EEG power spectral density in the middle years of life (ages 20–60 years old) Psychophysiology. 2001;38:232–242. doi: 10.1111/1469-8986.3820232. PubMed DOI
Schneider J., Lewis P.A., Koester D., Born J., Ngo H.V.V. Susceptibility to auditory closed-loop stimulation of sleep slow oscillations changes with age. Sleep. 2020;43 doi: 10.1093/sleep/zsaa111. PubMed DOI PMC
Papalambros N.A., Weintraub S., Chen T., Grimaldi D., Santostasi G., Paller K.A., Zee P.C., Malkani R.G. Acoustic enhancement of sleep slow oscillations in mild cognitive impairment. Ann. Clin. Transl. Neurol. 2019;6:1191–1201. doi: 10.1002/acn3.796. PubMed DOI PMC
Diep C., Ftouni S., Manousakis J., Nicholas C., Drummond S., Anderson C. Acoustic slow wave sleep enhancement via a novel, automated device improves executive function in middle-aged men. Sleep. 2020;43 doi: 10.1093/sleep/zsz197. PubMed DOI
Wunderlin M., Züst M.A., Hertenstein E., Fehér K.D., Schneider C.L., Klöppel S., Nissen C. Modulating overnight memory consolidation by acoustic stimulation during slow-wave sleep: A systematic review and meta-analysis. Sleep. 2021:zsaa296. doi: 10.1093/sleep/zsaa296. PubMed DOI
Klinzing J.G., Niethard N., Born J. Mechanisms of systems memory consolidation during sleep. Nat. Neurosci. 2019;22:1598–1610. doi: 10.1038/s41593-019-0467-3. PubMed DOI
Fehér K.D., Wunderlin M., Maier J.G., Hertenstein E., Schneider C., Mikutta C., Züst M.A., Klöppel S., Nissen C. Shaping the slow waves of sleep: A systematic and integrative review of sleep slow wave modulation in humans using non-invasive brain stimulation. Sleep Med. Rev. 2021;58:101438. doi: 10.1016/j.smrv.2021.101438. PubMed DOI
Piorecka V. Easys2matlab, Version 1.0.0. [(accessed on 25 May 2021)]; Available online: https://github.com/vaclavapiorecka/easys2matlab.
Kurth S., Jenni O.G., Riedner B.A., Tononi G., Carskadon M.A., Huber R. Characteristics of Sleep Slow Waves in Children and Adolescents. Sleep. 2010;33:475–480. doi: 10.1093/sleep/33.4.475. PubMed DOI PMC
Crecraft D., Gergely S. 11—Signal generation. In: Crecraft D., Gergely S., editors. Analog Electronics. Butterworth-Heinemann; Oxford, UK: 2002. pp. 263–281. DOI
Best R. Phase Locked Loops, Pennsylvania Plaza New York. 6th ed. McGraw-Hill Professional; New York, NY, USA: 2007.
Razavi B. Monolithic Phase-Locked Loops and Clock Recovery Circuits: Theory and Design. Wiley-IEEE Press; Hoboken, NJ, USA: 1996. Design of Monolithic PhaseLocked Loops and Clock Recovery Circuits A Tutorial; pp. 1–39. DOI
Abramovitch D. Lyapunov redesign of classical digital phase-lock loops; Proceedings of the 2003 American Control Conference; Denver, CO, USA. 4–6 June 2003; pp. 2401–2406. DOI
Harikrushna D., Tiwari M., Singh J.K., Khare A. Design, Implementation and Characterization of Xor Phase Detector for Dpll in 45 Nm Cmos Technology. Adv. Comput. Int. J. 2011;2 doi: 10.5121/acij.2011.2605. DOI
Scher A. Simulating Phase Locked Loops (PLLs) with MATLAB. [(accessed on 25 May 2021)]; Available online: http://aaronscher.com/phase_locked_loop/matlab_pll.html.
Oostenveld R., Fries P., Maris E., Schoffelen J.M. FieldTrip: Open Source Software for Advanced Analysis of MEG, EEG, and Invasive Electrophysiological Data. Comput. Intell. Neurosci. 2011;2011:156869. doi: 10.1155/2011/156869. PubMed DOI PMC
Cohen M.X. Analyzing Neural Time Series Data. The MIT Press; Cambridge, MA, USA: 2014.
Smith J.O. Mathematics of the Discrete Fourier Transform (DFT) [(accessed on 25 May 2021)]; Available online: https://ccrma.stanford.edu/~jos/st/mdft-citation.html.
Berens P. CircStat: A MATLAB Toolbox for Circular Statistics. J. Stat. Softw. Artic. 2009;31:1–21. doi: 10.18637/jss.v031.i10. DOI
Maris E., Oostenveld R. Nonparametric statistical testing of EEG- and MEG-data. J. Neurosci. Methods. 2007;164:177–190. doi: 10.1016/j.jneumeth.2007.03.024. PubMed DOI
Suh S., Nowakowski S., Bernert R.A., Ong J.C., Siebern A.T., Dowdle C.L., Manber R. Clinical significance of night-to-night sleep variability in insomnia. Sleep Med. 2012;13:469–475. doi: 10.1016/j.sleep.2011.10.034. PubMed DOI PMC
Stone K.L., Ensrud K.E., Ancoli-Israel S. Sleep, insomnia and falls in elderly patients. Sleep Med. 2008;9:S18–S22. doi: 10.1016/S1389-9457(08)70012-1. PubMed DOI
Kumar N., Kumar M. Design of low power and high speed phase detector; Proceedings of the 2016 2nd International Conference on Contemporary Computing and Informatics (IC3I); Greater Noida, India. 14–17 December 2016; pp. 676–680. DOI
Closed-loop auditory stimulation of slow-wave sleep in chronic insomnia: a pilot study