University of Oulu

Helakari, H., Korhonen, V., Holst, S. C., Piispala, J., Kallio, M., Väyrynen, T., Huotari, N., Raitamaa, L., Tuunanen, J., Kananen, J., Järvelä, M., Tuovinen, T., Raatikainen, V., Borchardt, V., Kinnunen, H., Nedergaard, M., & Kiviniemi, V. (2022). Human nrem sleep promotes brain-wide vasomotor and respiratory pulsations. The Journal of Neuroscience, 42(12), 2503–2515. https://doi.org/10.1523/JNEUROSCI.0934-21.2022

Human NREM Sleep Promotes Brain-Wide Vasomotor and Respiratory Pulsations

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Author: Helakari, Heta1,2,3; Korhonen, Vesa1,2,3; Holst, Sebastian C.4;
Organizations: 1Oulu Functional Neuroimaging, Department of Diagnostic Radiology, Oulu University Hospital, 90220 Oulu, Finland
2Medical Imaging, Physics and Technology, Faculty of Medicine, University of Oulu, 90220 Oulu, Finland
3Medical Research Center, Oulu University Hospital, 90220 Oulu, Finland
4Neurobiology Research Unit, University of Copenhagen, 2200 Copenhagen, Denmark
5Clinical Neurophysiology, Oulu University Hospital, 90220 Oulu, Finland
6Oura Health, 90590 Oulu, Finland
7Center of Translational Neuromedicine, University of Copenhagen, 2200 Copenhagen, Denmark
8Center of Translational Neuromedicine, University of Rochester, Rochester, New York 14642
Format: article
Version: published version
Access: open
Online Access: PDF Full Text (PDF, 3.7 MB)
Persistent link: http://urn.fi/urn:nbn:fi-fe2022122173101
Language: English
Published: Society for Neuroscience, 2022
Publish Date: 2022-12-21
Description:

Abstract

The physiological underpinnings of the necessity of sleep remain uncertain. Recent evidence suggests that sleep increases the convection of cerebrospinal fluid (CSF) and promotes the export of interstitial solutes, thus providing a framework to explain why all vertebrate species require sleep. Cardiovascular, respiratory and vasomotor brain pulsations have each been shown to drive CSF flow along perivascular spaces, yet it is unknown how such pulsations may change during sleep in humans. To investigate these pulsation phenomena in relation to sleep, we simultaneously recorded fast fMRI, magnetic resonance encephalography (MREG), and electroencephalography (EEG) signals in a group of healthy volunteers. We quantified sleep-related changes in the signal frequency distributions by spectral entropy analysis and calculated the strength of the physiological (vasomotor, respiratory, and cardiac) brain pulsations by power sum analysis in 15 subjects (age 26.5 ± 4.2 years, 6 females). Finally, we identified spatial similarities between EEG slow oscillation (0.2–2 Hz) power and MREG pulsations. Compared with wakefulness, nonrapid eye movement (NREM) sleep was characterized by reduced spectral entropy and increased brain pulsation intensity. These effects were most pronounced in posterior brain areas for very low-frequency (≤0.1 Hz) vasomotor pulsations but were also evident brain-wide for respiratory pulsations, and to a lesser extent for cardiac brain pulsations. There was increased EEG slow oscillation power in brain regions spatially overlapping with those showing sleep-related MREG pulsation changes. We suggest that reduced spectral entropy and enhanced pulsation intensity are characteristic of NREM sleep. With our findings of increased power of slow oscillation, the present results support the proposition that sleep promotes fluid transport in human brain.

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Series: The Journal of neuroscience
ISSN: 0270-6474
ISSN-E: 1529-2401
ISSN-L: 0270-6474
Volume: 42
Issue: 12
Pages: 2503 - 2515
DOI: 10.1523/jneurosci.0934-21.2022
OADOI: https://oadoi.org/10.1523/jneurosci.0934-21.2022
Type of Publication: A1 Journal article – refereed
Field of Science: 3112 Neurosciences
3126 Surgery, anesthesiology, intensive care, radiology
Subjects:
Funding: This work was supported by Uniogs/Medical Research Center, Oulu, Doctoral Program Grant (H.H., J.K.), Pohjois-Suomen Terveydenhuollon tukisäätiö (H.H., V. Korhonen), Jane and Aatos Erkko Foundation (V. Kiviniemi), Academy of Finland and Aivosäätiö TERVA Grant 314497 (V. Kiviniemi), Academy of Finland Grant 275342 (V. Kiviniemi), the SalWe Research Program for Mind and Body (Finnish Funding Agency for Technology and Innovation, Grant No. 1104/10; V. Kiviniemi), Finnish Medical Foundation (V. Kiviniemi, J.K., T.T.), Finnish Neurological Foundation (V. Kiviniemi), KEVO grants from Oulu University Hospital (V. Kiviniemi), Orion Research Foundation (J.K., T.T.), Medical Research Center, Oulu (J.K., V.R.), Maire Taponen Foundation (J.K.), Finnish Brain Foundation (J.K., V. Kiviniemi), Instrumentarium Science Foundation (J.K.), and the University of Oulu Scholarship Foundation (J.K., V.R.).
Academy of Finland Grant Number: 314497
Detailed Information: 314497 (Academy of Finland Funding decision)
Copyright information: © 2022 Helakari et al. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
  https://creativecommons.org/licenses/by/4.0/