Abstract
Rapid eye movement sleep (REMS) is a peculiar brain state combining the behavioral components of sleep and the electrophysiological profiles of wake. After decades of research our understanding of REMS still is precluded by the difficulty to observe its spontaneous dynamics and the lack of multimodal recording approaches to build comprehensive datasets. We used functional ultrasound (fUS) imaging concurrently with extracellular recordings of local field potentials (LFP) to reveal brain-wide spatiotemporal hemodynamics of single REMS episodes. We demonstrate for the first time the close association between global hyperemic events – largely outmatching wake levels in most brain regions – and local hippocampal theta (6–10 Hz) and fast gamma (80–110 Hz) events in the CA1 region. In particular, the power of fast gamma oscillations strongly correlated with the amplitude of subsequent vascular events. Our findings challenge our current understanding of neurovascular coupling and question the evolutionary benefit of such energy-demanding patterns in REMS function.
Highlights
Rapid eye movement sleep (REMS) is a peculiar brain state combining the behavioral components of sleep and the electrophysiological profiles of wake
Using a traditional sleep scoring procedure based on movement detection, neck electromyogram (EMG) and intra-hippocampal local field potentials (LFP), we were able to distinguish between four different states: quiet wake (QW), active wake (AW), non-REM sleep (NREMS), and REM sleep (REMS) [Fig. 1a]
The LFP patterns were strongly similar between AW and REM, as characterized by prominent peaks in the theta (6–10 Hz) and high-gamma (100–150 Hz) bands, low ripple content and high theta/delta ratio28 [Supplementary Fig. 1], we found that cerebral blood volume (CBV) profiles strongly differ between these two states, whereas QW and NREMS showed relatively low CBV levels
Summary
Rapid eye movement sleep (REMS) is a peculiar brain state combining the behavioral components of sleep and the electrophysiological profiles of wake. Previous work on hippocampal replay in rodents have established that sharp-wave ripples support memory consolidation processes by facilitating the transfer of newly formed memory traces in the hippocampus towards stable cortical sites during sleep[5,6] and that they are critical for spatial learning during the awake state[7] Most of these breakthroughs have focused on hippocampal recordings during slow-wave sleep (SWS), leaving rapid-eye-movement sleep (REMS) comparatively understudied and confining its putative role to dreaming and emotional processing[8]. Due to the transient nature of REMS and to the significant caveats associated with actual recording techniques, a simultaneous monitoring of electrographic and vascular events during spontaneous sleep has been very hard to achieve This results in an important lack of data regarding the activity of distributed networks during REMS and a poor understanding of the physiological function of its phasic events. We isolated precursors to VS in the theta (6–10 Hz) and high-gamma (70–110 Hz) bands of hippocampal LFP, and the intensity of each individual VS was best accounted for by the power of fast gamma, suggesting a strong association between local electrographic events and massive brain-wide vascular patterns
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