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Human NREM Sleep Promotes Brain-Wide Vasomotor and Respiratory Pulsations

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. Cardi...

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Autores principales: Helakari, Heta, Korhonen, Vesa, Holst, Sebastian C., Piispala, Johanna, Kallio, Mika, Väyrynen, Tommi, Huotari, Niko, Raitamaa, Lauri, Tuunanen, Johanna, Kananen, Janne, Järvelä, Matti, Tuovinen, Timo, Raatikainen, Ville, Borchardt, Viola, Kinnunen, Hannu, Nedergaard, Maiken, Kiviniemi, Vesa
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Society for Neuroscience 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8944230/
https://www.ncbi.nlm.nih.gov/pubmed/35135852
http://dx.doi.org/10.1523/JNEUROSCI.0934-21.2022
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author Helakari, Heta
Korhonen, Vesa
Holst, Sebastian C.
Piispala, Johanna
Kallio, Mika
Väyrynen, Tommi
Huotari, Niko
Raitamaa, Lauri
Tuunanen, Johanna
Kananen, Janne
Järvelä, Matti
Tuovinen, Timo
Raatikainen, Ville
Borchardt, Viola
Kinnunen, Hannu
Nedergaard, Maiken
Kiviniemi, Vesa
author_facet Helakari, Heta
Korhonen, Vesa
Holst, Sebastian C.
Piispala, Johanna
Kallio, Mika
Väyrynen, Tommi
Huotari, Niko
Raitamaa, Lauri
Tuunanen, Johanna
Kananen, Janne
Järvelä, Matti
Tuovinen, Timo
Raatikainen, Ville
Borchardt, Viola
Kinnunen, Hannu
Nedergaard, Maiken
Kiviniemi, Vesa
author_sort Helakari, Heta
collection PubMed
description 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. SIGNIFICANCE STATEMENT We report that the spectral power of physiological brain pulsation mechanisms driven by vasomotor, respiration, and cardiac rhythms in human brain increase during sleep, extending previous observations of their association with glymphatic brain clearance during sleep in rodents. The magnitudes of increased pulsations follow the rank order of vasomotor greater than respiratory greater than cardiac pulsations, with correspondingly declining spatial extents. Spectral entropy, previously known as vigilance and as an anesthesia metric, decreased during NREM sleep compared with the awake state in very low and respiratory frequencies, indicating reduced signal complexity. An EEG slow oscillation power increase occurring in the early sleep phase (NREM 1–2) spatially overlapped with pulsation changes, indicating reciprocal mechanisms between those measures.
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spelling pubmed-89442302022-03-28 Human NREM Sleep Promotes Brain-Wide Vasomotor and Respiratory Pulsations Helakari, Heta Korhonen, Vesa Holst, Sebastian C. Piispala, Johanna Kallio, Mika Väyrynen, Tommi Huotari, Niko Raitamaa, Lauri Tuunanen, Johanna Kananen, Janne Järvelä, Matti Tuovinen, Timo Raatikainen, Ville Borchardt, Viola Kinnunen, Hannu Nedergaard, Maiken Kiviniemi, Vesa J Neurosci Research Articles 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. SIGNIFICANCE STATEMENT We report that the spectral power of physiological brain pulsation mechanisms driven by vasomotor, respiration, and cardiac rhythms in human brain increase during sleep, extending previous observations of their association with glymphatic brain clearance during sleep in rodents. The magnitudes of increased pulsations follow the rank order of vasomotor greater than respiratory greater than cardiac pulsations, with correspondingly declining spatial extents. Spectral entropy, previously known as vigilance and as an anesthesia metric, decreased during NREM sleep compared with the awake state in very low and respiratory frequencies, indicating reduced signal complexity. An EEG slow oscillation power increase occurring in the early sleep phase (NREM 1–2) spatially overlapped with pulsation changes, indicating reciprocal mechanisms between those measures. Society for Neuroscience 2022-03-23 /pmc/articles/PMC8944230/ /pubmed/35135852 http://dx.doi.org/10.1523/JNEUROSCI.0934-21.2022 Text en Copyright © 2022 Helakari et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Articles
Helakari, Heta
Korhonen, Vesa
Holst, Sebastian C.
Piispala, Johanna
Kallio, Mika
Väyrynen, Tommi
Huotari, Niko
Raitamaa, Lauri
Tuunanen, Johanna
Kananen, Janne
Järvelä, Matti
Tuovinen, Timo
Raatikainen, Ville
Borchardt, Viola
Kinnunen, Hannu
Nedergaard, Maiken
Kiviniemi, Vesa
Human NREM Sleep Promotes Brain-Wide Vasomotor and Respiratory Pulsations
title Human NREM Sleep Promotes Brain-Wide Vasomotor and Respiratory Pulsations
title_full Human NREM Sleep Promotes Brain-Wide Vasomotor and Respiratory Pulsations
title_fullStr Human NREM Sleep Promotes Brain-Wide Vasomotor and Respiratory Pulsations
title_full_unstemmed Human NREM Sleep Promotes Brain-Wide Vasomotor and Respiratory Pulsations
title_short Human NREM Sleep Promotes Brain-Wide Vasomotor and Respiratory Pulsations
title_sort human nrem sleep promotes brain-wide vasomotor and respiratory pulsations
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8944230/
https://www.ncbi.nlm.nih.gov/pubmed/35135852
http://dx.doi.org/10.1523/JNEUROSCI.0934-21.2022
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