Skip to main content
SpringerLink
Log in

Video polysomnographic analysis of elevated EMG activity and rapid eye movements before abnormal behaviors in REM sleep behavior disorder

  • Original Article
  • Published:
Sleep and Biological Rhythms Aims and scope Submit manuscript

Abstract

The pathogenesis of rapid eye movement (REM) sleep behavior disorder (RBD) is unclear. According to the cortical hypothesis, severe RBD episode (RBDE) occurs when spinal motoneurons are less inhibited and cortical and limbic systems are more active. We made this study to prove the hypothesis for the development of RBDE using video-polysomnography (VPSG). VPSG records of 35 patients with RBD were analyzed. According to severity, RBDEs were classified into three motor events (MEs): ME 1; small movements or jerks, ME 2; proximal movements including violent behavior, and ME 3; axial movements including bed falls. For each ME, we measured the number of MEs preceded or not preceded by both REM sleep without atonia (RWA) and REMs during the 10-s-period immediately before ME onset. In severe RBDE (ME 3), the number of MEs preceded by both RWA and REMs was significantly higher than that of MEs not preceded by both (0.8 vs. 0.2, P = 0.033). This was not the case for mild RBDE (ME 1) and moderate RBDE (ME 2). Our results suggest that both RWA and REMs are associated with the development of severe RBDE.

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

Similar content being viewed by others

References

  1. American Academy of Sleep Medicine. International Classification of Sleep Disorders. 3rd ed. American Academy of Sleep Medicine; 2014.

  2. Hogl B, Stefani A, Videnovic A. A. Idiopathic REM sleep behaviour disorder and neurodegeneration—an update. Nat Rev Neurol. 2018;14:40–55.

    Article  PubMed  Google Scholar 

  3. Stefani A, Holzknecht E, Hogl B. Clinical neurophysiology of REM parasomnias. In: Levin PCKH, editors. Handbook of clinical neurology; 2019. p. 381–396.

  4. Sforza E, Krieger J, Periau C. REM sleep behavior disorder: clinical and physiopathological findings. Sleep Med Rev. 1997;1:57–69.

    Article  CAS  PubMed  Google Scholar 

  5. Olson EJ, Boeve BF, Silber MH. Rapid eye movement sleep behaviour disorder: demographic, clinical and laboratory findings in 93 cases. Brain. 2000;123:331–9.

    Article  PubMed  Google Scholar 

  6. Schenck CH, Mahowald MW. REM sleep behavior disorder: clinical, developmental, and neuroscience perspectives 16 years after its formal identification in SLEEP. Sleep. 2002;25:120–38.

    Article  PubMed  Google Scholar 

  7. Frauscher B, Gschliesser V, Brandauer E, Ulmer H, Peralta CM, Muller J, Poewe W, Hogl B. Video analysis of motor events in REM sleep behavior disorder. Mov Disord. 2007;22:1464–70.

    Article  PubMed  Google Scholar 

  8. Iranzo A. The REM sleep circuit and how its impairment leads to REM sleep behavior disorder. Cell Tissue Res. 2018;373:245–66.

    Article  PubMed  Google Scholar 

  9. Luppi PH, Clement O, Valencia Garcia S, Brischoux F, Fort P. New aspects in the pathophysiology of rapid eye movement sleep behavior disorder: the potential role of glutamate, gamma-aminobutyric acid, and glycine. Sleep Med. 2013;14:714–8.

    Article  PubMed  Google Scholar 

  10. Peever J, Luppi PH, Montplaisir J. Breakdown in REM sleep circuitry underlies REM sleep behavior disorder. Trends Neurosci. 2014;37:279–88.

    Article  PubMed  Google Scholar 

  11. Chase MH. Motor control during sleep and wakefulness: clarifying controversies and resolving paradoxes. Sleep Med Rev. 2013;17:299–312.

    Article  PubMed  Google Scholar 

  12. Desseilles M, Sterpenich V, Dang-Vu TT, Schwartz S. REM sleep and emotion regulation. In: Mallick MN, Pandi-Perumal SR, McCarley RW, Morrison AR, editors. Rapid Eye Movement Sleep: Regulation and Function. Cambridge：Cambridge University Press; 2011. p. 427–36.

  13. Arnulf I. The “scanning hypothesis” of rapid eye movements during REM sleep: a review of the evidence. Arch Ital Biol. 2011;149:367–82.

    CAS  PubMed  Google Scholar 

  14. Valli K, Frauscher B, Gschliesser V, Wolf E, Falkenstetter T, Schonwald SV, Ehrmann L, Zangerl A, Marti I, Boesch SM, Revonsuo A, Poewe W, Hogl B. Can observers link dream content to behaviours in rapid eye movement sleep behaviour disorder? A cross-sectional experimental pilot study. J Sleep Res. 2012;21:21–9.

    Article  PubMed  Google Scholar 

  15. Proserpio P, Terzaghi M, Nobili L. Local cortical activations during REM sleep and implications for RBD. In: Schenck CH, Högl B, Videnovic A, editors. Rapid-eye-movement sleep behavior disorder. Berlin: springer; 2018. p. 389–401.

  16. Iranzo A, Frauscher B, Santos H, Gschliesser V, Ratti L, Falkenstetter T, Sturner C, Salamero M, Tolosa E, Poewe W, Santamaria J, Hogl B, for the SINBAR (Sleep Insbruck Barcerona) Group. Usefulness of the SINBAR electromyographic montage to detect the motor and vocal manifestations occurring in REM sleep behavior disorder. Sleep Med. 2011;12:284–8.

    Article  Google Scholar 

  17. Frauscher B, Iranzo A, Gaig C, Gschliesser V, Guaita M, Raffelseder V, Ehrmann L, Sola N, Salamero M, Tolosa E, Poewe W, Santamaria J, Hogl B, for the SINBAR (Sleep Insbruck Barcerona) Group. Normative EMG values during REM sleep for the diagnosis of REM sleep behavior disorder. Sleep. 2012;35:875–947.

    Google Scholar 

  18. Ioannides AA, Corsi-Cabrera M, Fenwick PB, del Rio Portilla Y, Laskaris NA, Khurshudyan A, Theofilou D, Shibata T, Uchida S, Nakabayashi T, Kostopoulos GK. MEG tomography of human cortex and brainstem activity in waking and REM sleep saccades. Cereb Cortex. 2004;14:56–72.

    Article  PubMed  Google Scholar 

  19. Abe T, Matsuoka T, Ogawa K, Nittono H, Hori T. Gamma band EEG activity is enhanced after the occurrence of rapid eye movement during human REM sleep. Sleep Biol Rhythms. 2008;6:26–33.

    Article  Google Scholar 

  20. Abe T, Ogawa K, Nittono H, Hori T. Neural generators of brain potentials before rapid eye movements during human REM sleep: a study using sLORETA. Clin Neurophysiol. 2008;119:2044–53.

    Article  PubMed  Google Scholar 

  21. Corsi-Cabrera M, Guevara MA, del Rio-Portilla Y. Brain activity and temporal coupling related to eye movements during REM sleep: EEG and MEG results. Brain Res. 2008;1235:82–91.

    Article  CAS  PubMed  Google Scholar 

  22. Corsi-Cabrera M, Velasco F, Del Rio-Portilla Y, Armony JL, Trejo-Martinez D, Guevara MA, Velasco AL. Human amygdala activation during rapid eye movements of rapid eye movement sleep: an intracranial study. J Sleep Res. 2016;25:576–82.

    Article  PubMed  Google Scholar 

  23. Miyauchi S, Misaki M, Kan S, Fukunaga T, Koike T. Human brain activity time-locked to rapid eye movements during REM sleep. Exp Brain Res. 2009;192:657–67.

    Article  PubMed  Google Scholar 

  24. Hong CC, Harris JC, Pearlson GD, Kim JS, Calhoun VD, Fallon JH, Golay X, Gillen JS, Simmonds DJ, van Zijl PC, Zee DS, Pekar JJ. fMRI evidence for multisensory recruitment associated with rapid eye movements during sleep. Hum Brain Mapp. 2009;30:1705–22.

    Article  PubMed  Google Scholar 

  25. Ogawa K, Abe T, Nittono H, Yamazaki K, Hori T. Phasic brain activity related to the onset of rapid eye movements during rapid eye movement sleep: study of event-related potentials and standardized low-resolution brain electromagnetic tomography. J Sleep Res. 2010;19:407–14.

    Article  PubMed  Google Scholar 

  26. American Academy of Sleep Medicine. In: International classification of sleep disorders: diagnostic and coding manual, 2nd ed. American Academy of Sleep Medicine; 2005.

  27. Rechtschaffen A, Kales A. A manual of standardised terminology, techniques and scoring system for sleep stages of human subjects. Washington DC: US Government Printing Office, US Public Health Service; 1968.

  28. Iber C, Ancoli-Israel S, Chesson A, Quan SF. The AASM manual for the scoring of sleep and associated events: rules, terminology and technical specifications. Westchester: American Academy of Sleep Medicine; 2007.

  29. Sixel-Döring F, Schweitzer M, Mollenhauer B, Trenkwalder C. Intraindividual variability of REM sleep behavior disorder in Parkinson’s disease: a comparative assessment using a new REM Sleep Behavior Disorder Severity Scale (RBDSS) for clinical routine. J Clin Sleep Med. 2011;7:75–80.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Mayer G, Kesper K, Ploch T, Canisius S, Penzel T, Oertel W, Stiasny-Kolster K. Quantification of tonic and phasic muscle activity in REM sleep behavior disorder. J Clin Neurophysiol. 2008;25:48–55.

    Article  PubMed  Google Scholar 

  31. Kanda Y. Investigation of the freely available easy-to-use software “EZR” for medical statistics. Bone Marrow Transpl. 2013;48:452–8.

    Article  CAS  Google Scholar 

  32. Frauscher B, Gschliesser V, Brandauer E, Ulmer H, Poewe W, Hogl B. The relation between abnormal behaviors and REM sleep microstructure in patients with REM sleep behavior disorder. Sleep Med. 2009;10:174–81.

    Article  PubMed  Google Scholar 

  33. Manni R, Terzaghi M, Glorioso M. Motor-behavioral episodes in REM sleep behavior disorder and phasic events during REM sleep. Sleep. 2009;32:241–5.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Leclair-Visonneau L, Oudiette D, Gaymard B, Leu-Semenescu S, Arnulf I. Do the eyes scan dream images during rapid eye movement sleep? Evidence from the rapid eye movement sleep behaviour disorder model. Brain. 2010;133:1737–46.

    Article  PubMed  Google Scholar 

  35. Mahowald MW, Schenck CH. REM sleep parasomnias. In: Kryger MH, Roth T, Dement WC, editors. Principles and practice of sleep medicine: Fifth edition. Amsterdam: Elsevier; 2010. p. 1083–97.

Download references

Acknowledgements

We would like to thank Drs. Eiji Yoshioka, Kaoru Takakusaki, and Shigeru Chiba for their valuable advice. We also appreciate Ms. Yui Kurosu and Ms. Yumiko Nakao for providing excellent technical support in the VPSG analysis.

Author information

Authors and Affiliations

  1. Department of Psychiatry, School of Medicine, Asahikawa Medical University, Midorigaoka Higashi 2-1-1-1, Asahikawa, Hokkaido, 078-8510, Japan

    Mondo Yoshizawa, Yoshiyuki Tamura, Asami Yasuda-Ohata, Shinsuke Yoshihara, Hideki Takasaki & Sadayuki Hashioka

Authors
  1. Mondo Yoshizawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yoshiyuki Tamura
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Asami Yasuda-Ohata
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shinsuke Yoshihara
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hideki Takasaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Sadayuki Hashioka
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sadayuki Hashioka.

Ethics declarations

Conflict of interest

The authors declare no conflicts of interest associated with this manuscript.

Additional information

Publisher's Note

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

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yoshizawa, M., Tamura, Y., Yasuda-Ohata, A. et al. Video polysomnographic analysis of elevated EMG activity and rapid eye movements before abnormal behaviors in REM sleep behavior disorder. Sleep Biol. Rhythms 21, 455–460 (2023). https://doi.org/10.1007/s41105-023-00472-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s41105-023-00472-2

Keywords

Search

Navigation