Poster No:
2576
Submission Type:
Abstract Submission
Authors:
Makoto Uji1, Xuemei Li1, An Saotome1,2, Ryosuke Katsumata1,3, Chisato Suzuki1, Kenichi Ueno1, Sayaka Aritake1,2, Masako Tamaki1,4
Institutions:
1RIKEN Center for Brain Science, Wako, Japan, 2Saitama Prefectural University, Saitama, Japan, 3Chiba University, Chiba, Japan, 4RIKEN Cluster for Pioneering Research, Wako, Japan
First Author:
Makoto Uji
RIKEN Center for Brain Science
Wako, Japan
Co-Author(s):
Xuemei Li
RIKEN Center for Brain Science
Wako, Japan
An Saotome
RIKEN Center for Brain Science|Saitama Prefectural University
Wako, Japan|Saitama, Japan
Ryosuke Katsumata
RIKEN Center for Brain Science|Chiba University
Wako, Japan|Chiba, Japan
Sayaka Aritake
RIKEN Center for Brain Science|Saitama Prefectural University
Wako, Japan|Saitama, Japan
Masako Tamaki
RIKEN Center for Brain Science|RIKEN Cluster for Pioneering Research
Wako, Japan|Wako, Japan
Introduction:
While cerebrospinal fluid (CSF) dynamics during sleep have recently been implicated in cleansing metabolic waste products in animals [1], how CSF is modulated with neural activities and events during deep NREM and REM sleep in humans [2] remains unclear. Previous studies in human subjects have shown that CSF fluctuations during light NREM sleep are coupled with K-complexes, a type of slow oscillations typically associated with arousals [3,4]. CSF during REM sleep has never been investigated in animals or humans. Does an arousal mechanism solely contribute to CSF dynamics or are any sleep-specific neural processes also linked to fluid changes during NREM and REM sleep? Our recent data revealed that deep NREM and REM sleep involved faster frequency components (0.06-0.12Hz and >0.12Hz) in CSF signals (Fig.1) [5], suggesting that abundant brain oscillations and events during deep stable sleep may play a crucial role in CSF dynamics and a waste clearance mechanism. In the present study we investigate whether sleep-specific brain oscillations and events during stable NREM and REM sleep are in fact associated with CSF dynamics in human subjects.
Methods:
25 healthy subjects (15 females, mean 23.6±4.8 years old) participated in two 90-min early afternoon naps with polysomnography (PSG) in a 3T Siemens Prisma MRI scanner. MRI data were acquired using a sparse GE-EPI sequence (TR/TE=3000/30ms, FA=85°, Multiband=3, 42 transverse slices, voxel size = 3x3x3mm3, 1800 volumes, B1+RMS=0.5μT, MR acquisition time=0.9s, quiet period=2.1s) [6]. An anatomical image, respiration and heartbeat signals were also acquired. PSG data were corrected for gradient and pulse artefacts [7]. Sleep stages were scored into wakefulness (stage W), NREM sleep stages 1-3 (N1-N3), and REM sleep. Events during sleep, including sleep spindles, slow-oscillations, rapid eye movements (REMs), and sawtooth waves were detected. Epochs containing arousals or motion artifacts were removed from further analyses. MRI data were denoised using cardiac and respiration, motion corrected, normalized, and averaged across all voxels in the lateral ventricles as CSF signals. CSF signals (0 to 30s) were baseline corrected (-9 to 0s) to investigate CSF changes for each sleep event.
Results:
The average sleep duration was 69.6±20.7 min and the proportion of each stage was 22.5%, 28.6%, 34.3%, 12.3%, and 2.4% for stages W, N1, N2, N3, and REM sleep, respectively. The interval of each sleep event showed that slow oscillations occurred every 43s during N2 and 6s during N3. Sleep spindles occurred every 5-6s during N2 and N3. REMs and sawtooth waves occurred every 8s during REM sleep (Fig.2). These intervals corresponded to frequency profiles in the CSF signals that we previously reported (faster frequency components, [5]). We next found that a large CSF fluctuation was induced at 8s after the onset of slow oscillations detected from N2. Slow oscillations during N3, which occurred more abundantly than N2, accompanied a smaller CSF peak at 5.5s after the onset (Fig.2A1). Additionally, sleep spindles also induced CSF fluctuation at 3-4s after the onset, lasting for about 20s (Fig.2A2). We further found that REM events and sawtooth waves during REM sleep coupled to CSF fluctuations, inducing fluctuations at 20s after the onset of the events (Fig.2A3).
Conclusions:
Our results demonstrate that sleep brain oscillations and events, such as slow oscillations and spindles during NREM sleep, and REMs and sawtooth waves during REM sleep, are indeed coupled to CSF signal fluctuations. This study reveals CSF signals are dynamically varied across different sleep depths and that CSF signal changes are coordinated with sleep-specific neural activities. These brain oscillations and events during deep NREM and REM sleep, associated with neural plasticity processes, may also play an essential role in a waste clearance mechanism for healthy brain functions in humans.
Novel Imaging Acquisition Methods:
EEG
Multi-Modal Imaging 2
Non-BOLD fMRI
Perception, Attention and Motor Behavior:
Sleep and Wakefulness 1
Physiology, Metabolism and Neurotransmission :
Neurophysiology of Imaging Signals
Keywords:
Cerebro Spinal Fluid (CSF)
Electroencephaolography (EEG)
FUNCTIONAL MRI
MRI
Sleep
Other - EEG-fMRI
1|2Indicates the priority used for review
Provide references using author date format
References
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[2] Uji, M., Tamaki, M. (2023). Sleep, learning, and memory in human research using noninvasive neuroimaging techniques. Neuroscience Research. https://doi.org/10.1016/j.neures.2022.12.013
[3] Fultz, N.E., Bonmassar, G., Setsompop, K., Stickgold, R.A., Rosen, B.R., Polimeni, J.R., & Lewis, L.D. (2019). Coupled electrophysiological, hemodynamic, and cerebrospinal fluid oscillations in human sleep. Science, 366(6465), 628-631. https://doi.org/10.1126/science.aax5440
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[5] Uji, M., Li, X., Saotome, A., Katsumata, R., Aritake, S., Suzuki, C., Ueno, K., M. Tamaki, M. (2023). Cerebrospinal fluid dynamics during NREM and REM sleep by a simultaneous sparse-fMRI and EEG method. OHBM 2023 in Montreal, Canada.
[6] Uji, M., Wilson, R., Francis, S.T., Mullinger, K.J., & Mayhew, S.D. (2018). Exploring the advantages of multiband fMRI with simultaneous EEG to investigate coupling between gamma frequency neural activity and the BOLD response in humans. Human Brain Mapping, 39(4), 1673-1687. https://doi.org/10.1002/hbm.23943
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