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.
Highlights
Brain tissue contains almost no connective tissue, this enabling pressure waves to initiate long-distance brain pulsations
Brain pulsations are induced by vasomotion, respiration, and the cardiac cycle
Sleep strikingly increases spectral power and decreases spectral entropy of brain pulsations, especially for the very low frequency vasomotor waves
Spectral entropy of brain pulsations detected by MREG is a sensitive measure of vigilance, resembling the corresponding entropy changes detected by scalp EEG
Competing Interest Statement
Oura Health Ltd.'s provided the surveillance Oura rings for the study.
List of Abbreviations
- AASM
- American Academy of Sleep Medicine,
- AFNI
- analysis of functional neuroimaging software toolbox,
- AUC
- area under curve,
- A1-A2
- awake scan 1-2,
- BCG
- ballistocardiographic,
- BOLD
- blood oxygen level dependent,
- CANTAB
- Cambridge Neuropsychological Test Automated Battery,
- CO2
- carbon dioxide,
- CSF
- cerebrospinal fluid,
- DC
- direct current,
- df
- degrees of freedom,
- EC
- eyes closed scan,
- EEG
- electroencephalography,
- EGI
- Electrical Geodesics,
- FA
- flip angle,
- FFT
- fast Fourier transform,
- fMRI
- functional magnetic resonance imaging,
- FMRIB
- functional magnetic resonance imaging of the brain,
- FOV
- field of view,
- FSL
- FMRIB software library,
- FWE
- family wise error,
- MATLAB
- matrix laboratory software,
- MCFLIRT
- motion correction using FMRIB’s linear image registration tool,
- MNI
- Montreal Neurological Institute,
- MPRAGE
- magnetization prepared rapid gradient echo,
- MREG
- magnetic resonance encephalography,
- light sleep
- N1,
- intermediate sleep with sleep spindles and/or K-complexes
- N2,
- slow wave sleep
- N3,
- NREM
- non-rapid eye movement,
- OFNI
- Oulu functional neuroimaging group,
- PAL
- paired-associate learning,
- sleep with rapid eye movements
- REM,
- ROC
- receiver operating curve,
- ROI
- region of interest,
- RTI
- reaction time,
- S1–S4
- sleep scans 1-4,
- SE
- spectral entropy,
- SpO2
- fingertip oxygen partial saturation,
- TE
- echo time,
- TFCE
- threshold-free cluster enhancement,
- TR
- repetition time,
- VLF 0.008 - 0.1 Hz
- very low frequency.