Human NREM Sleep Promotes Brain-Wide Vasomotor and Respiratory Pulsations
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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.
In: Journal of Neuroscience, Vol. 42, No. 12, 2022, p. 2503-2515.Research output: Contribution to journal › Journal article › Research › peer-review
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TY - JOUR
T1 - Human NREM Sleep Promotes Brain-Wide Vasomotor and Respiratory Pulsations
AU - Helakari, Heta
AU - Korhonen, Vesa
AU - Holst, Sebastian C.
AU - Piispala, Johanna
AU - Kallio, Mika
AU - Väyrynen, Tommi
AU - Huotari, Niko
AU - Raitamaa, Lauri
AU - Tuunanen, Johanna
AU - Kananen, Janne
AU - Järvelä, Matti
AU - Tuovinen, Timo
AU - Raatikainen, Ville
AU - Borchardt, Viola
AU - Kinnunen, Hannu
AU - Nedergaard, Maiken
AU - Kiviniemi, Vesa
N1 - Publisher Copyright: Copyright © 2022 Helakari et al.
PY - 2022
Y1 - 2022
N2 - 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.
AB - 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.
KW - brain pulsations
KW - fast fMRI
KW - glymphatic clearance
KW - sleep
KW - slow-wave EEG
KW - spectral power
U2 - 10.1523/JNEUROSCI.0934-21.2022
DO - 10.1523/JNEUROSCI.0934-21.2022
M3 - Journal article
C2 - 35135852
AN - SCOPUS:85128000248
VL - 42
SP - 2503
EP - 2515
JO - The Journal of neuroscience : the official journal of the Society for Neuroscience
JF - The Journal of neuroscience : the official journal of the Society for Neuroscience
SN - 0270-6474
IS - 12
ER -
ID: 342609204