Sleep-Induced Vasomotor Pulsation is a Driver of Cerebrospinal Fluid and Blood-Brain Barrier Dynamics in the Human Brain

Sleep is crucial for restoring and maintaining brain tissue homeostasis, primarily through enhanced transport of cerebrospinal fluid (CSF) solutes. Infra-slow (<0.1 Hz) vasomotion, CSF flow, and the electrical potential of blood-brain barrier (BBB) all increase during sleep. While these phenomena have been linked to CSF solute transport, there is little understanding of their interaction as potentials drivers of CSF flow. Therefore, we recorded these three signals in a group of healthy volunteers across sleep-wake states with simultaneous 10 Hz functional magnetic resonance imaging (fMRI) of blood oxygen level dependent (BOLD) contrast, direct current-coupled electroencephalography (DC-EEG), and functional near-infrared spectroscopy (fNIRS). We next investigated the directed coupling patterns between these linked processes according to phase transfer entropy (TE). In the awake state, the electrophysiological BBB potential and water fluctuations predicted vasomotor waves uniformly throughout the brain. In sleep state, results showed a reversal of the direction of this coupling in cerebral cortex, as vasomotor BOLD waves started predicting both CSF and BBB potential shifts. Our findings indicate that vasomotor waves become the primary driver of CSF hydrodynamics and BBB electrical potential in human brain during sleep.