Human deep sleep facilitates cerebrospinal fluid dynamics linked to spontaneous brain oscillations and neural events

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 has 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-functional MRI and polysomnography method, we demonstrate that deep sleep–specific CSF dynamics are associated with spontaneous brain oscillations in healthy young human participants. Slow waves and sleep spindles during slow-wave sleep are tightly linked to short-cycle, frequent, and moderate CSF fluctuations. In contrast, slow waves during light sleep and arousals produce slow, infrequent, and steep CSF signal changes. Rapid eye movements and sawtooth waves during REM sleep are also linked to CSF signal changes. Furthermore, CSF signals are significantly faster in frequency during deep than light sleep. These brain oscillations during light and deep sleep recruit essentially different brain networks, with deep sleep involving memory and homeostatic circuits. Thus, human deep sleep has a unique way of facilitating CSF dynamics that are distinctive from arousal mechanisms.