Skip to main content
SpringerLink
Log in

Electroencephalographic and Electromyographic Events During Spontaneous and Final Arousal from Sleep: Study of the Sequence of Appearance and Significance

  • Original Article
  • Published:
Sleep and Vigilance Aims and scope Submit manuscript

Abstract

Objective

Though there are excellent reviews on the functional significance of spontaneous arousals during sleep, associated electroencephalographic (EEG) and electromyographic (EMG) changes need further studies. Moreover, a comparison of these changes with early morning arousal from sleep will help in improving our understanding of sleep–wake regulations.

Methods

The study conducted on 15 healthy young volunteers showed that the spontaneous arousals, with associated EEG and EMG changes, occurred almost uniformly throughout non-rapid eye movement (NREM) sleep and rapid eye movement (REM) sleep.

Results

EEG changes preceded EMG changes in majority of the events. There was a delay of more than a second in between EEG and EMG changes, in both spontaneous arousals and early morning awakenings. Compared to the pre-arousal values, there was a significant increase in the delta power and all the frequency bands during spontaneous arousals. Though similar changes in EEG happened during the early morning awakenings, there were significant differences in beta and sigma EEG powers and computed root mean square EMG during the early morning awakenings.

Conclusion

The differences in the characteristic features of EEG and EMG changes during spontaneous arousal and early morning arousal indicated the probable role of these changes in facilitating the continuance of sleep in the former, and waking up from sleep in the case of the latter.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Availability of Data and Materials

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

Code Availability

Not applicable.

References

  1. Halasz P, Terzano M, Parrino L, Bodizs R. The nature of arousal in sleep. J Sleep Res. 2004;13:1–23. https://doi.org/10.1111/j.1365-2869.2004.00388.x.

    Article  PubMed  Google Scholar 

  2. ASDA. EEG arousals: scoring rules and examples: a preliminary report from the Sleep Disorders Atlas Task Force of the American Sleep Disorders Association. Sleep. 1992;15:173–84.

    Article  Google Scholar 

  3. Azarbarzin A, Ostrowski M, Younes M, Keenan BT, Pack AI, Staley B, et al. Arousal responses during overnight polysomnography and their reproducibility in healthy young adults. Sleep. 2015;38:1313–21. https://doi.org/10.5665/sleep.4916.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Togo F, Cherniack N, Natelson B. Electroencephalogram characteristics of autonomic arousals during sleep in healthy men. Clin Neurophysiol. 2006;117:2597–603. https://doi.org/10.1016/j.clinph.2006.07.314.

    Article  PubMed  PubMed Central  Google Scholar 

  5. American Academy of Sleep Medicine. The AASM manual for the scoring of sleep and associated events. Darien; 2020.

  6. Mesquita J, Poree F, Carrault G, Fiz JA, Abad J, Jane R. Respiratory and spontaneous arousals in patients with sleep apnea hypopnea syndrome. IEEE, 2012, p. 6337–40. https://doi.org/10.1109/EMBC.2012.6347443.

  7. Colten H, Altevogt B. Sleep disorders and sleep deprivation: an unmet public health problem. Washington, D.C.: National Academies Press; 2006.

    Google Scholar 

  8. Loredo JS, Clausen JL, Ancoli-Israel S, Dimsdale JE. Night-to-night arousal variability and interscorer reliability of arousal measurements. Sleep. 1999;22:916–20. https://doi.org/10.1093/sleep/22.7.916.

    Article  CAS  PubMed  Google Scholar 

  9. Zampi C, Fagioli I, Salzarulo P. Time course of EEG background activity level before spontaneous awakening in infants. J Sleep Res. 2002;11:283–7. https://doi.org/10.1046/j.1365-2869.2002.00313.x.

    Article  PubMed  Google Scholar 

  10. Colrain IM. The K-complex: a 7-decade history. Sleep. 2005;28:255–73. https://doi.org/10.1093/sleep/28.2.255.

    Article  PubMed  Google Scholar 

  11. Halász P. The K-complex as a special reactive sleep slow wave—a theoretical update. Sleep Med Rev. 2016;29:34–40. https://doi.org/10.1016/j.smrv.2015.09.004.

    Article  PubMed  Google Scholar 

  12. Halász P. Hierarchy of micro-arousals and the microstructure of sleep. Neurophysiol Clin Neurophysiol. 1998;28:461–75. https://doi.org/10.1016/S0987-7053(99)80016-1.

    Article  Google Scholar 

  13. Hornyak M, Cejnar M, Elam M, Matousek M, Wallin BG. Sympathetic muscle nerve activity during sleep in man. Brain. 1991;114:1281–95. https://doi.org/10.1093/brain/114.3.1281.

    Article  PubMed  Google Scholar 

  14. Latreille V, von Ellenrieder N, Peter-Derex L, Dubeau F, Gotman J, Frauscher B. The human K-complex: insights from combined scalp-intracranial EEG recordings. Neuroimage. 2020;213: 116748. https://doi.org/10.1016/j.neuroimage.2020.116748.

    Article  PubMed  Google Scholar 

  15. Naitoh P, Antony-Baas V, Muzet A, Ehrhart J. Dynamic relation of sleep spindles and K-complexes to spontaneous phasic arousal in sleeping human subjects. Sleep. 1982;5:58–72. https://doi.org/10.1093/sleep/5.1.58.

    Article  CAS  PubMed  Google Scholar 

  16. Sassin JF, Johnson LC. Body motility during sleep and its relation to the K-complex. Exp Neurol. 1968;22:133–44. https://doi.org/10.1016/0014-4886(68)90025-3.

    Article  CAS  PubMed  Google Scholar 

  17. Wauquier A, Aloe L, Declerck A. K-complexes: are they signs of arousal or sleep protective? J Sleep Res. 1995;4:138–43. https://doi.org/10.1111/j.1365-2869.1995.tb00162.x.

    Article  CAS  PubMed  Google Scholar 

  18. Jasper H. Report of the committee on methods of clinical examination in electroencephalography. Electroencephal Clin Neurophysiol. 1958;10:370–5. https://doi.org/10.1016/0013-4694(58)90053-1.

    Article  Google Scholar 

  19. Rechtschaffen A, Kales A. A manual of standardized terminology, techniques and scoring system for sleep stages of human subjects. Bethesda: National Institute of Neurological Diseases and Blindness, Neurological Information Network; 1968.

    Google Scholar 

  20. Hang L-W, Su B-L, Yen C-W. Detecting slow wave sleep via one or two channels of EEG/EOG signals. Int J Signal Process Syst. 2013. https://doi.org/10.12720/ijsps.1.1.84-88.

    Article  Google Scholar 

  21. Okura K, Kato T, Montplaisir JY, Sessle BJ, Lavigne GJ. Quantitative analysis of surface EMG activity of cranial and leg muscles across sleep stages in human. Clin Neurophysiol. 2006;117:269–78. https://doi.org/10.1016/j.clinph.2005.10.003.

    Article  PubMed  Google Scholar 

  22. Lofaso F, Goldenberg F, d’Ortho MP, Coste A, Harf A. Arterial blood pressure response to transient arousals from NREM sleep in nonapneic snorers with sleep fragmentation. Chest. 1998;113:985–91. https://doi.org/10.1378/chest.113.4.985.

    Article  CAS  PubMed  Google Scholar 

  23. Rees K, Spence DP, Earis JE, Calverley PM. Arousal responses from apneic events during non-rapid-eye-movement sleep. Am J Respir Crit Care Med. 1995;152:1016–21. https://doi.org/10.1164/ajrccm.152.3.7663777.

    Article  CAS  PubMed  Google Scholar 

  24. Schieber JP, Muzet A, Ferriere PJ. Phases of spontaneous transitory activation during normal sleep in humans. Arch Sci Physiol (Paris). 1971;25:443–65.

    CAS  Google Scholar 

  25. Terzano MG, Mancia D, Salati MR, Costani G, Decembrino A, Parrino L. The cyclic alternating pattern as a physiologic component of normal NREM sleep. Sleep. 1985;8:137–45. https://doi.org/10.1093/sleep/8.2.137.

    Article  CAS  PubMed  Google Scholar 

  26. Halász P, Kundra O, Rajna P, Pál I, Vargha M. Micro-arousals during nocturnal sleep. Acta Physiol Acad Sci Hung. 1979;54:1–12.

    PubMed  Google Scholar 

  27. Murphy PJ, Rogers NL, Campbell SS. Age differences in the spontaneous termination of sleep. J Sleep Res. 2000;9:27–34. https://doi.org/10.1046/j.1365-2869.2000.00185.x.

    Article  CAS  PubMed  Google Scholar 

  28. Karadeniz O, Besset B. EEG arousals and awakenings in relation with periodic leg movements during sleep. J Sleep Res. 2000;9:273–7. https://doi.org/10.1046/j.1365-2869.2000.00202.x.

    Article  CAS  PubMed  Google Scholar 

  29. Black JE, Guilleminault C, Colrain IM, Carrillo O. Upper airway resistance syndrome: central electroencephalographic power and changes in breathing effort. Am J Respir Crit Care Med. 2000;162:406–11. https://doi.org/10.1164/ajrccm.162.2.9901026.

    Article  CAS  PubMed  Google Scholar 

  30. Forget D, Charles MM, Clyne HB. The role of the spontaneous and evoked K-complex in good-sleeper controls and in individuals with insomnia. Sleep. 2011. https://doi.org/10.5665/SLEEP.1250.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Kuo TBJ, Chen C-Y, Hsu Y-C, Yang CCH. EEG beta power and heart rate variability describe the association between cortical and autonomic arousals across sleep. Auton Neurosci. 2016;194:32–7. https://doi.org/10.1016/j.autneu.2015.12.001.

    Article  PubMed  Google Scholar 

  32. Martynas Z, Vanda L, Ramune G, Raminta M, Osvaldas R. Arousals and macrostructure of sleep: importance of NREM stage 2 reconsidered. Sleep Sci. 2013;6:91–7.

    Google Scholar 

  33. Lim MM, Szymusiak R. Neurobiology of arousal and sleep: updates and insights into neurological disorders. Curr Sleep Med Rep. 2015;1:91–100. https://doi.org/10.1007/s40675-015-0013-0.

    Article  Google Scholar 

  34. McCormick DA, Bal T. Sleep and arousal: thalamocortical mechanisms. Annu Rev Neurosci. 1997;20:185–215. https://doi.org/10.1146/annurev.neuro.20.1.185.

    Article  CAS  PubMed  Google Scholar 

  35. Purcell SM, Manoach DS, Demanuele C, Cade BE, Mariani S, Cox R, et al. Characterizing sleep spindles in 11,630 individuals from the National Sleep Research Resource. Nat Commun. 2017. https://doi.org/10.1038/ncomms15930.

    Article  PubMed  PubMed Central  Google Scholar 

  36. Burgess CR, Peever JH. A noradrenergic mechanism functions to couple motor behavior with arousal state. Curr Biol. 2013;23:1719–25. https://doi.org/10.1016/j.cub.2013.07.014.

    Article  CAS  PubMed  Google Scholar 

  37. Jones BE. Modulation of cortical activation and behavioral arousal by cholinergic and orexinergic systems. Ann NY Acad Sci. 2008;1129:26–34. https://doi.org/10.1196/annals.1417.026.

    Article  CAS  PubMed  Google Scholar 

  38. St. Louis EK, McCarter SJ, Boeve BF, Silber MH, Kantarci K, Benarroch EE, et al. Lesional REM sleep behavior disorder localizes to the dorsomedial pons. Neurology. 2014;83:1871–3. https://doi.org/10.1212/WNL.0000000000000978.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Heister DS, Hayar A, Garcia-Rill E. Cholinergic modulation of GABAergic and glutamatergic transmission in the dorsal subcoeruleus: mechanisms for REM sleep control. Sleep. 2009;32:1135–47. https://doi.org/10.1093/sleep/32.9.1135.

    Article  PubMed  PubMed Central  Google Scholar 

  40. McCarter SJ, Tippmann-Peikert M, Sandness DJ, Flanagan EP, Kantarci K, Boeve BF, et al. Neuroimaging-evident lesional pathology associated with REM sleep behavior disorder. Sleep Med. 2015;16:1502–10. https://doi.org/10.1016/j.sleep.2015.07.018.

    Article  PubMed  Google Scholar 

  41. Boselli M, Parrino L, Smerieri A, Terzano MG. Effect of age on EEG arousals in normal sleep. Sleep. 1998;21:351–7.

    CAS  PubMed  Google Scholar 

  42. Halász P. The role of the nonspecific phasic activation in the sleep regulation and in the mechanism of generalised epilepsy with spikewave pattern. Academic Doctoral Thesis, Semmelweis University; 1982.

  43. Borbély AA. A two process model of sleep regulation. Hum Neurobiol. 1982;1:195–204.

    PubMed  Google Scholar 

Download references

Funding

Not applicable.

Author information

Authors and Affiliations

  1. Department of Physiology, All India Institute of Medical Sciences, New Delhi, 110029, India

    Shaheen Yawar Bhat, Nasreen Akhtar, Trina Sengupta, Ritesh Netam, Velayudhan Mohan Kumar & Hruda Nanda Mallick

  2. Faculty of Medicine and Health Sciences, Department of Physiology, SGT University, Gurugram, Haryana, 122505, India

    Shaheen Yawar Bhat & Hruda Nanda Mallick

  3. All India Institute of Medical Sciences, Jodhpur, 342005, India

    Trina Sengupta

  4. Kerala Chapter, National Academy of Medical Sciences (India), New Delhi, India

    Velayudhan Mohan Kumar

Authors
  1. Shaheen Yawar Bhat
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nasreen Akhtar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Trina Sengupta
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ritesh Netam
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Velayudhan Mohan Kumar
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hruda Nanda Mallick
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceptualization: HNM, NA, data collection: SB, NA, statistical analysis and data presentation: TS, VMK, writing—original draft preparation: TS, SB, VMK, writing—review, and editing: all authors, and supervision: HNM, NA, RN.

Corresponding author

Correspondence to Hruda Nanda Mallick.

Ethics declarations

Conflict of Interest

The author declares no conflict of interest.

Ethics Approval

The study was approved by the Institutional Ethics Committee of All India Institute of Medical Sciences, New Delhi, India.

Consent to Participate

Have been taken.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bhat, S.Y., Akhtar, N., Sengupta, T. et al. Electroencephalographic and Electromyographic Events During Spontaneous and Final Arousal from Sleep: Study of the Sequence of Appearance and Significance. Sleep Vigilance 6, 153–163 (2022). https://doi.org/10.1007/s41782-021-00185-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s41782-021-00185-x

Keywords

Search

Navigation