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Sleep pressure propels cerebrovascular oscillations while sleep intensity correlates with respiration- and cardiac-driven brain pulsations

Ulv Larsen, S. M.; Holst, S. C.; Olsen, A. S.; Ozenne, B.; Zilstorff, D. B.; Brendstrup-Brix, K.; Weikop, P.; Pleinert, S.; Kiviniemi, V.; Jennum, P. J.; Nedergaard, M.; Knudsen, G. M.

2024-10-17 neurology
10.1101/2024.10.16.24315580 medRxiv
Show abstract

The waste-clearing flow of cerebrospinal fluid through the brain is driven by cerebrovascular, respiratory, and cardiac forces and is thought to be regulated by homeostatic sleep mechanisms. In a circadian-controlled sleep and sleep deprivation study, we investigated how heightened sleep pressure and slow-wave-rich sleep affect physiological brain oscillations in humans, as measured with accelerated neuroimaging. Our study also included a randomised, double-blind, placebo-controlled, cross-over administration of the adrenergic antagonist carvedilol, which allowed us to examine the effect of modulating cerebrovascular pulsatility. We report that sleep deprivation increases low frequency brain oscillations (LFOs) more than sleep does, with LFOs during sleep correlating with cognitive measures of sleep pressure. Conversely, slow-wave-rich NREM sleep (stages N2 and N3) enhances respiration- and cardiac-driven brain pulsations - particularly within grey and white matter. The strength of these brain pulsations escalates with sleep depth (N3 > N2) and correlates with EEG delta power. Carvedilol dampens LFOs, supporting that these reflect cerebrovascular oscillations. Altogether, our findings indicate that sleep pressure promotes cerebrovascular oscillations, while sleep slow waves synchronise with respiration- and cardiac-driven brain pulsations. Graphical Abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=77 SRC="FIGDIR/small/24315580v1_ufig1.gif" ALT="Figure 1"> View larger version (35K): org.highwire.dtl.DTLVardef@34757dorg.highwire.dtl.DTLVardef@d9f32org.highwire.dtl.DTLVardef@4eaa6borg.highwire.dtl.DTLVardef@966865_HPS_FORMAT_FIGEXP M_FIG C_FIG

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