Coupled electrophysiological, hemodynamic, and cerebrospinal fluid oscillations in human sleep

By Nina E. Fultz, G. Bonmassar, Kawin Setsompop, Robert Stickgold, Bruce R. Rosen, J. Polimeni, Laura D. Lewis. Science, 2019

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Fluid dynamics during sleep During non–rapid eye movement sleep, low-frequency oscillations in neural activity support memory consolidation and neuronal computation. Sleep is also associated with increased interstitial fluid volume and clearance of metabolic waste products. It is unknown why these processes co-occur and how they are related. Fultz et al. simultaneously measured electrophysiological, hemodynamic, and flow signals in the human brain (see the Perspective by Grubb and Lauritzen). Large oscillations of fluid inflow to the brain appeared during sleep and were tightly coupled to functional magnetic resonance imaging signals and entrained to electroencephalogram slow waves. Slow oscillatory neuronal activity thus leads to oscillations in blood volume, drawing cerebrospinal fluid into and out of the brain. Science, this issue p. 628; see also p. 572 Slow EEG waves that define non-REM sleep are a mechanistic driver of the increased waste clearance that occurs during sleep. Sleep is essential for both cognition and maintenance of healthy brain function. Slow waves in neural activity contribute to memory consolidation, whereas cerebrospinal fluid (CSF) clears metabolic waste products from the brain. Whether these two processes are related is not known. We used accelerated neuroimaging to measure physiological and neural dynamics in the human brain. We discovered a coherent pattern of oscillating electrophysiological, hemodynamic, and CSF dynamics that appears during non–rapid eye movement sleep. Neural slow waves are followed by hemodynamic oscillations, which in turn are coupled to CSF flow. These results demonstrate that the sleeping brain exhibits waves of CSF flow on a macroscopic scale, and these CSF dynamics are interlinked with neural and hemodynamic rhythms.

Subfields: Cognitive Neuroscience, Endocrine and Autonomic Systems, Pediatrics, Perinatology and Child Health

View Paper: https://www.semanticscholar.org/paper/910055abc371a34530798209ef0a302b04d349cb

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