Sleep-specific changes in physiological brain pulsations

Helakari, H.; Korhonen, V.; Holst, S. C.; Piispala, J.; Kallio, M.; Vayrynen, T.; Huotari, N.; Raitamaa, L.; Kananen, J.; Jarvela, M.; Raatikainen, V.; Borchardt, V.; Kinnunen, H.; Nedergaard, M.; Kiviniemi, V.

doi:10.1101/2020.09.03.280479

bioRxiv · 10.1101/2020.09.03.280479

Sleep-specific changes in physiological brain pulsations

Helakari, H.·Korhonen, V.·Holst, S. C.·Piispala, J.·Kallio, M.·Vayrynen, T.·Huotari, N.·Raitamaa, L.·Kananen, J.·Jarvela, M.·Raatikainen, V.·Borchardt, V.·Kinnunen, H.·Nedergaard, M.·Kiviniemi, V.

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Abstract

Sleep is known to increase the convection of interstitial brain metabolites along with cerebrospinal fluid (CSF). We used ultrafast magnetic resonance encephalography (MREGBOLD) to quantify the effect of sleep on physiological (vasomotor, respiratory and cardiac) brain pulsations driving the CSF convection in humans. Transition to electroencephalography verified sleep occurred in conjunction with power increase and reduced spectral entropy (SE) of physiological brain pulsations. During sleep, the greatest increase in spectral power was in very-low frequency (VLF < 0.1 Hz) waves, followed by respiratory and cardiac brain pulsations. SE reduction coincided with decreased vigilance in awake state and could robustly (ROC 0.88, p < 0.001) differentiate between sleep vs. awake states, indicating the sensitivity of SE of the MREGBOLD signal as a marker for sleep level. In conclusion, the three physiological brain pulsation contribute to the sleep-associated increase in glymphatic CSF convective flow in an inverse frequency order. HighlightsO_LIBrain tissue contains almost no connective tissue, this enabling pressure waves to initiate long-distance brain pulsations C_LIO_LIBrain pulsations are induced by vasomotion, respiration, and the cardiac cycle C_LIO_LISleep strikingly increases spectral power and decreases spectral entropy of brain pulsations, especially for the very low frequency vasomotor waves C_LIO_LISpectral entropy of brain pulsations detected by MREG is a sensitive measure of vigilance, resembling the corresponding entropy changes detected by scalp EEG C_LI

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Helakari, H., Korhonen, V., Holst, S. C., Piispala, J., Kallio, M., Vayrynen, T., Huotari, N., Raitamaa, L., Kananen, J., Jarvela, M., Raatikainen, V., Borchardt, V., Kinnunen, H., Nedergaard, M., Kiviniemi, V.. 2020-09-03. Sleep-specific changes in physiological brain pulsations. https://doi.org/10.1101/2020.09.03.280479

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