IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-37352-9.html
   My bibliography  Save this article

Sleep fMRI with simultaneous electrophysiology at 9.4 T in male mice

Author

Listed:
  • Yalin Yu

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Yue Qiu

    (Fudan University)

  • Gen Li

    (Peking University)

  • Kaiwei Zhang

    (Chinese Academy of Sciences)

  • Binshi Bo

    (Chinese Academy of Sciences)

  • Mengchao Pei

    (Chinese Academy of Sciences)

  • Jingjing Ye

    (ShanghaiTech University)

  • Garth J. Thompson

    (ShanghaiTech University)

  • Jing Cang

    (Fudan University)

  • Fang Fang

    (Fudan University
    The Central Hospital of Xuhui District)

  • Yanqiu Feng

    (Southern Medical University)

  • Xiaojie Duan

    (Peking University)

  • Chuanjun Tong

    (Chinese Academy of Sciences
    Southern Medical University)

  • Zhifeng Liang

    (Chinese Academy of Sciences
    Shanghai Center for Brain Science and Brain-Inspired Intelligence Technology)

Abstract

Sleep is ubiquitous and essential, but its mechanisms remain unclear. Studies in animals and humans have provided insights of sleep at vastly different spatiotemporal scales. However, challenges remain to integrate local and global information of sleep. Therefore, we developed sleep fMRI based on simultaneous electrophysiology at 9.4 T in male mice. Optimized un-anesthetized mouse fMRI setup allowed manifestation of NREM and REM sleep, and a large sleep fMRI dataset was collected and openly accessible. State dependent global patterns were revealed, and state transitions were found to be global, asymmetrical and sequential, which can be predicted up to 17.8 s using LSTM models. Importantly, sleep fMRI with hippocampal recording revealed potentiated sharp-wave ripple triggered global patterns during NREM than awake state, potentially attributable to co-occurrence of spindle events. To conclude, we established mouse sleep fMRI with simultaneous electrophysiology, and demonstrated its capability by revealing global dynamics of state transitions and neural events.

Suggested Citation

  • Yalin Yu & Yue Qiu & Gen Li & Kaiwei Zhang & Binshi Bo & Mengchao Pei & Jingjing Ye & Garth J. Thompson & Jing Cang & Fang Fang & Yanqiu Feng & Xiaojie Duan & Chuanjun Tong & Zhifeng Liang, 2023. "Sleep fMRI with simultaneous electrophysiology at 9.4 T in male mice," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37352-9
    DOI: 10.1038/s41467-023-37352-9
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-37352-9
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-37352-9?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Franz Weber & Shinjae Chung & Kevin T. Beier & Min Xu & Liqun Luo & Yang Dan, 2015. "Control of REM sleep by ventral medulla GABAergic neurons," Nature, Nature, vol. 526(7573), pages 435-438, October.
    2. Ziyue Wang & Xiang Fei & Xiaotong Liu & Yanjie Wang & Yue Hu & Wanling Peng & Ying-wei Wang & Siyu Zhang & Min Xu, 2022. "REM sleep is associated with distinct global cortical dynamics and controlled by occipital cortex," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    3. Chuanjun Tong & Cirong Liu & Kaiwei Zhang & Binshi Bo & Ying Xia & Hao Yang & Yanqiu Feng & Zhifeng Liang, 2022. "Multimodal analysis demonstrating the shaping of functional gradients in the marmoset brain," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    4. Siyuan Zhao & Gen Li & Chuanjun Tong & Wenjing Chen & Puxin Wang & Jiankun Dai & Xuefeng Fu & Zheng Xu & Xiaojun Liu & Linlin Lu & Zhifeng Liang & Xiaojie Duan, 2020. "Full activation pattern mapping by simultaneous deep brain stimulation and fMRI with graphene fiber electrodes," Nature Communications, Nature, vol. 11(1), pages 1-12, December.
    5. Franz Weber & Yang Dan, 2016. "Circuit-based interrogation of sleep control," Nature, Nature, vol. 538(7623), pages 51-59, October.
    6. N. K. Logothetis & O. Eschenko & Y. Murayama & M. Augath & T. Steudel & H. C. Evrard & M. Besserve & A. Oeltermann, 2012. "Hippocampal–cortical interaction during periods of subcortical silence," Nature, Nature, vol. 491(7425), pages 547-553, November.
    7. Franz Weber & Johnny Phong Hoang Do & Shinjae Chung & Kevin T. Beier & Mike Bikov & Mohammad Saffari Doost & Yang Dan, 2018. "Regulation of REM and Non-REM Sleep by Periaqueductal GABAergic Neurons," Nature Communications, Nature, vol. 9(1), pages 1-13, December.
    8. Xiao Liu & Jacco A. de Zwart & Marieke L. Schölvinck & Catie Chang & Frank Q. Ye & David A. Leopold & Jeff H. Duyn, 2018. "Subcortical evidence for a contribution of arousal to fMRI studies of brain activity," Nature Communications, Nature, vol. 9(1), pages 1-10, December.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Gianina Ungurean & Mehdi Behroozi & Leonard Böger & Xavier Helluy & Paul-Antoine Libourel & Onur Güntürkün & Niels C. Rattenborg, 2023. "Wide-spread brain activation and reduced CSF flow during avian REM sleep," Nature Communications, Nature, vol. 14(1), pages 1-12, December.

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Ya-Nan Zhao & Jian-Bo Jiang & Shi-Yuan Tao & Yang Zhang & Ze-Ka Chen & Wei-Min Qu & Zhi-Li Huang & Su-Rong Yang, 2022. "GABAergic neurons in the rostromedial tegmental nucleus are essential for rapid eye movement sleep suppression," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    2. Beverly Setzer & Nina E. Fultz & Daniel E. P. Gomez & Stephanie D. Williams & Giorgio Bonmassar & Jonathan R. Polimeni & Laura D. Lewis, 2022. "A temporal sequence of thalamic activity unfolds at transitions in behavioral arousal state," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    3. Sasa Teng & Fenghua Zhen & Li Wang & Jose Canovas Schalchli & Jane Simko & Xinyue Chen & Hao Jin & Christopher D. Makinson & Yueqing Peng, 2022. "Control of non-REM sleep by ventrolateral medulla glutamatergic neurons projecting to the preoptic area," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    4. Feng Han & Xufu Liu & Richard B. Mailman & Xuemei Huang & Xiao Liu, 2023. "Resting-state global brain activity affects early β-amyloid accumulation in default mode network," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    5. Dominik P. Koller & Michael Schirner & Petra Ritter, 2024. "Human connectome topology directs cortical traveling waves and shapes frequency gradients," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    6. Hong Yu & Xinkuan Xiang & Zongming Chen & Xu Wang & Jiaqi Dai & Xinxin Wang & Pengcheng Huang & Zheng-dong Zhao & Wei L. Shen & Haohong Li, 2021. "Periaqueductal gray neurons encode the sequential motor program in hunting behavior of mice," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    7. Anli A. Liu & Simon Henin & Saman Abbaspoor & Anatol Bragin & Elizabeth A. Buffalo & Jordan S. Farrell & David J. Foster & Loren M. Frank & Tamara Gedankien & Jean Gotman & Jennifer A. Guidera & Kari , 2022. "A consensus statement on detection of hippocampal sharp wave ripples and differentiation from other fast oscillations," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    8. Qiang Liu & Benjamin J. Bell & Dong Won Kim & Sang Soo Lee & Mehmet F. Keles & Qili Liu & Ian D. Blum & Annette A. Wang & Elijah J. Blank & Jiali Xiong & Joseph L. Bedont & Anna J. Chang & Habon Issa , 2023. "A clock-dependent brake for rhythmic arousal in the dorsomedial hypothalamus," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    9. Rodrigo Ordoñez Sierra & Lizeth Katherine Pedraza & Lívia Barcsai & Andrea Pejin & Qun Li & Gábor Kozák & Yuichi Takeuchi & Anett J. Nagy & Magor L. Lőrincz & Orrin Devinsky & György Buzsáki & Antal B, 2023. "Closed-loop brain stimulation augments fear extinction in male rats," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    10. Federico Rocchi & Carola Canella & Shahryar Noei & Daniel Gutierrez-Barragan & Ludovico Coletta & Alberto Galbusera & Alexia Stuefer & Stefano Vassanelli & Massimo Pasqualetti & Giuliano Iurilli & Ste, 2022. "Increased fMRI connectivity upon chemogenetic inhibition of the mouse prefrontal cortex," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    11. Yao Fei & Qihang Wu & Shijie Zhao & Kun Song & Junwei Han & Cirong Liu, 2024. "Diverse and asymmetric patterns of single-neuron projectome in regulating interhemispheric connectivity," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    12. Chuanjun Tong & Cirong Liu & Kaiwei Zhang & Binshi Bo & Ying Xia & Hao Yang & Yanqiu Feng & Zhifeng Liang, 2022. "Multimodal analysis demonstrating the shaping of functional gradients in the marmoset brain," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    13. Ziyue Wang & Xiang Fei & Xiaotong Liu & Yanjie Wang & Yue Hu & Wanling Peng & Ying-wei Wang & Siyu Zhang & Min Xu, 2022. "REM sleep is associated with distinct global cortical dynamics and controlled by occipital cortex," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    14. Xunda Wang & Alex T. L. Leong & Shawn Z. K. Tan & Eddie C. Wong & Yilong Liu & Lee-Wei Lim & Ed X. Wu, 2023. "Functional MRI reveals brain-wide actions of thalamically-initiated oscillatory activities on associative memory consolidation," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    15. HaoRan Chang & Ingrid M. Esteves & Adam R. Neumann & Majid H. Mohajerani & Bruce L. McNaughton, 2023. "Cortical reactivation of spatial and non-spatial features coordinates with hippocampus to form a memory dialogue," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    16. Jie Xia & Cirong Liu & Jiao Li & Yao Meng & Siqi Yang & Huafu Chen & Wei Liao, 2024. "Decomposing cortical activity through neuronal tracing connectome-eigenmodes in marmosets," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    17. Haoxin Zhang & Ivan Skelin & Shiting Ma & Michelle Paff & Lilit Mnatsakanyan & Michael A. Yassa & Robert T. Knight & Jack J. Lin, 2024. "Awake ripples enhance emotional memory encoding in the human brain," Nature Communications, Nature, vol. 15(1), pages 1-13, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37352-9. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.