Effect of sleep deprivation and NREM sleep stage on physiological brain pulsations

Heta Helakari; Matti Järvelä; Tommi Väyrynen; Johanna Tuunanen; Johanna Piispala; Mika Kallio; Seyed Mohsen Ebrahimi; Valter Poltojainen; Janne Kananen; Ahmed Elabasy; Niko Huotari; Lauri Raitamaa; Timo Tuovinen; Vesa Korhonen; Maiken Nedergaard; Vesa Kiviniemi

doi:10.3389/fnins.2023.1275184

Effect of sleep deprivation and NREM sleep stage on physiological brain pulsations

Front Neurosci. 2023 Dec 1:17:1275184. doi: 10.3389/fnins.2023.1275184. eCollection 2023.

Authors

Heta Helakari^{1

2}, Matti Järvelä^{1

2}, Tommi Väyrynen^{1

2}, Johanna Tuunanen^{1

2}, Johanna Piispala³, Mika Kallio³, Seyed Mohsen Ebrahimi^{1

2}, Valter Poltojainen^{1

2}, Janne Kananen^{1

2

3}, Ahmed Elabasy^{1

2}, Niko Huotari^{1

2}, Lauri Raitamaa^{1

2}, Timo Tuovinen^{1

2}, Vesa Korhonen^{1

2}, Maiken Nedergaard^{4

5}, Vesa Kiviniemi^{1

2}

Affiliations

¹ Oulu Functional Neuroimaging (OFNI), Department of Diagnostic Radiology, Oulu University Hospital, Oulu, Finland.
² Research Unit of Health Sciences and Technology, Faculty of Medicine, University of Oulu, Oulu, Finland.
³ Clinical Neurophysiology, Oulu University Hospital, Oulu, Finland.
⁴ Center of Translational Neuromedicine, University of Copenhagen, Copenhagen, Denmark.
⁵ Center of Translational Neuromedicine, University of Rochester, Rochester, NY, United States.

Abstract

Introduction: Sleep increases brain fluid transport and the power of pulsations driving the fluids. We investigated how sleep deprivation or electrophysiologically different stages of non-rapid-eye-movement (NREM) sleep affect the human brain pulsations.

Methods: Fast functional magnetic resonance imaging (fMRI) was performed in healthy subjects (n = 23) with synchronous electroencephalography (EEG), that was used to verify arousal states (awake, N1 and N2 sleep). Cardiorespiratory rates were verified with physiological monitoring. Spectral power analysis assessed the strength, and spectral entropy assessed the stability of the pulsations.

Results: In N1 sleep, the power of vasomotor (VLF < 0.1 Hz), but not cardiorespiratory pulsations, intensified after sleep deprived vs. non-sleep deprived subjects. The power of all three pulsations increased as a function of arousal state (N2 > N1 > awake) encompassing brain tissue in both sleep stages, but extra-axial CSF spaces only in N2 sleep. Spectral entropy of full band and respiratory pulsations decreased most in N2 sleep stage, while cardiac spectral entropy increased in ventricles.

Discussion: In summary, the sleep deprivation and sleep depth, both increase the power and harmonize the spectral content of human brain pulsations.

Keywords: fluid transport; glymphatic; homeostasis; non-REM sleep; sleep pressure.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work was supported by Uniogs/MRC Oulu DP-grant (HH and JK), Emil Aaltonen Foundation (HH and MJ), Pohjois-Suomen Terveydenhuollon tukisäätiö (HH and VKo), The EU Joint Programme – Neurodegenerative Disease Research 2022–120 (VKi), Jane and Aatos Erkko Foundation grants I and 210043 (VKi), Academy of Finland TERVA grants I-II 314497, 335720 (VKi), Academy of Finland Grant 275342, 338599 (VKi), Valtion tutkimusrahoitus grants from Oulu University hospital (VKi, VKo), Orion Research Foundation sr (JK, TT, and MJ), Medical Research Center Oulu grant (JK), Maire Taponen Foundation sr (JK), Finnish Brain Foundation sr (JK and Vki), Instrumentarium Science Foundation sr (JK), The University of Oulu Scholarship Foundation (JK), The Finnish Medical Foundation (VKi, JK, TT, and MJ).