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Cortical structure of neural synchrony and information flow during transition from wakefulness to light non-rapid eye movement sleep

Joline M. Fan, Kiwamu Kudo, Parul Verma, Kamalini G. Ranasinghe, Hirofumi Morise, Anne M. Findlay, Keith Vossel, Heidi E. Kirsch, Ashish Raj, Andrew D. Krystal, Srikantan S. Nagarajan
doi: https://doi.org/10.1101/2022.03.09.483562
Joline M. Fan
1Department of Neurology, University of California San Francisco, San Francisco CA, USA
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  • For correspondence: joline.fan@ucsf.edu
Kiwamu Kudo
2Department of Radiology and Biomedical Imaging, University of California San Francisco, San Francisco, USA
3Medical Imaging Center, Ricoh Company, Ltd., Kanazawa, Japan
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Parul Verma
2Department of Radiology and Biomedical Imaging, University of California San Francisco, San Francisco, USA
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Kamalini G. Ranasinghe
1Department of Neurology, University of California San Francisco, San Francisco CA, USA
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Hirofumi Morise
2Department of Radiology and Biomedical Imaging, University of California San Francisco, San Francisco, USA
3Medical Imaging Center, Ricoh Company, Ltd., Kanazawa, Japan
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Anne M. Findlay
2Department of Radiology and Biomedical Imaging, University of California San Francisco, San Francisco, USA
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Keith Vossel
1Department of Neurology, University of California San Francisco, San Francisco CA, USA
5Mary S. Easton Center for Alzheimer’s Disease Research, Department of Neurology, David Geffen School of Medicine, University of California Los Angeles, Los Angeles, CA, USA
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Heidi E. Kirsch
1Department of Neurology, University of California San Francisco, San Francisco CA, USA
2Department of Radiology and Biomedical Imaging, University of California San Francisco, San Francisco, USA
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Ashish Raj
2Department of Radiology and Biomedical Imaging, University of California San Francisco, San Francisco, USA
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Andrew D. Krystal
4Department of Psychiatry, University of California San Francisco, San Francisco CA, USA
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Srikantan S. Nagarajan
2Department of Radiology and Biomedical Imaging, University of California San Francisco, San Francisco, USA
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ABSTRACT

Sleep is a highly stereotyped phenomenon, requiring robust spatial and temporal coordination of neural activity. How the brain coordinates neural activity with sleep onset can provide insight into the physiological functions subserved by sleep and pathologic phenomena associated with sleep onset. We quantified whole-brain network changes in synchrony and information flow during the transition from wake to non-rapid eye movement (NREM) sleep using magnetoencephalography imaging in healthy subjects. In addition, we performed computational modeling to infer excitatory and inhibitory properties of local neural activity. The sleep transition was identified to be encoded in spatially and temporally specific patterns of local and long-range neural synchrony. Patterns of information flow revealed that mesial frontal regions receive hierarchically organized inputs from broad cortical regions upon sleep onset. Finally, biophysical neural mass modeling demonstrated spatially heterogeneous properties of cortical excitation-to-inhibition from wake to NREM. Together, these findings reveal whole-brain corticocortical structure in the sleep-wake transition and demonstrate the orchestration of local and long-range, frequency-specific cortical interactions that are fundamental to sleep onset.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • This version includes updates to the text and nomenclature.

  • Abbreviations

    Amy
    amygdala
    CG
    cingulate gyrus
    FC
    functional connectivity
    FuG
    fusiform gyrus
    Hipp
    hippocampus
    IFG
    inferior frontal gyrus
    IPL
    inferior parietal lobule
    INS
    insula
    ITG
    inferior temporal gyrus
    IQR
    interquartile range
    LocC
    lateral occipital cortex
    MEG
    magnetoencephalography
    MFG
    middle frontal gyrus
    MTG
    middle temporal gyrus
    MVOcC
    medioventral occipital cortex
    NREM
    non-rapid eye movement
    N1
    stage 1 sleep (NREM)
    N2
    stage 2 sleep (NREM)
    OrG
    orbital frontal gyrus
    PCL
    paracentral lobule
    Pcun
    precuneus
    PhG
    parahippocampal gyrus
    PoG
    postcentral gyrus
    PrG
    precentral gyrus
    pSTS
    posterior superior temporal sulcus
    ROI
    region of interest
    SFG
    superior frontal gyrus
    SPL
    superior parietal lobule
    STG
    superior temporal gyrus
    W
    wake
  • Copyright 
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    Posted December 08, 2022.
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    Cortical structure of neural synchrony and information flow during transition from wakefulness to light non-rapid eye movement sleep
    Joline M. Fan, Kiwamu Kudo, Parul Verma, Kamalini G. Ranasinghe, Hirofumi Morise, Anne M. Findlay, Keith Vossel, Heidi E. Kirsch, Ashish Raj, Andrew D. Krystal, Srikantan S. Nagarajan
    bioRxiv 2022.03.09.483562; doi: https://doi.org/10.1101/2022.03.09.483562
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    Cortical structure of neural synchrony and information flow during transition from wakefulness to light non-rapid eye movement sleep
    Joline M. Fan, Kiwamu Kudo, Parul Verma, Kamalini G. Ranasinghe, Hirofumi Morise, Anne M. Findlay, Keith Vossel, Heidi E. Kirsch, Ashish Raj, Andrew D. Krystal, Srikantan S. Nagarajan
    bioRxiv 2022.03.09.483562; doi: https://doi.org/10.1101/2022.03.09.483562

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