Human deep sleep facilitates faster cerebrospinal fluid dynamics linked to brain oscillations for sleep homeostasis and memory

Abstract

How sleep maintains our healthy brain function has remained one of the biggest mysteries in neuroscience, medical settings, and daily lives. While cerebrospinal fluid (CSF) during sleep have been implicated in metabolic waste reduction in animals, how CSF dynamics are driven in the healthy human brain during deep sleep remains elusive. A myriad of research has shown that crucial cognitive processing manifests in slow wave and rapid-eye movement (REM) sleep, suggesting that a key to maintaining brain functions lies in deep sleep. By leveraging a simultaneous sparse-fMRI and polysomnography method, we demonstrate that deep sleep-specific faster CSF dynamics are associated with spontaneous brain oscillations in healthy young human participants. Slow waves and sleep spindles during slow-wave sleep and rapid eye movements and sawtooth waves during rapid eye movement (REM) sleep are tightly linked to low-amplitude faster CSF fluctuations. In contrast, slow waves during light sleep and arousals produced large but slower CSF signal changes. Furthermore, CSF signals are significantly faster in frequency during deep than light sleep. These brain oscillations during light and deep sleep recruited essentially different brain networks, with deep sleep involving memory and homeostatic circuits. Thus, human deep sleep has a unique way of enabling faster CSF dynamics that are distinctive from arousal mechanisms. Significance StatementSleep is indispensable to our life, but its functions remain a significant mystery in the field of neuroscience. One of the most enigmatic issues in sleep is whether and how sleep regulates the CSF. The present study demonstrates deep sleep-specific faster CSF dynamics time locked to sleep brain oscillations in healthy young human participants. Slow waves and sleep spindles during slow-wave sleep and rapid eye movements and sawtooth waves during REM sleep are tightly linked to CSF fluctuations, contributing to faster CSF signals. Our results consistently demonstrate that human deep sleep has a unique way of enabling faster CSF dynamics that are distinctive from arousal mechanisms.