IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-38972-x.html
   My bibliography  Save this article

Hierarchical fluctuation shapes a dynamic flow linked to states of consciousness

Author

Listed:
  • Ang Li

    (Chinese Academy of Sciences)

  • Haiyang Liu

    (Capital Medical University
    Qinghai Provincial Traffic Hospital)

  • Xu Lei

    (Southwest University
    Ministry of Education)

  • Yini He

    (Beijing Normal University)

  • Qian Wu

    (Beijing Normal University
    Beijing Normal University)

  • Yan Yan

    (Chinese Academy of Sciences)

  • Xin Zhou

    (Beijing Normal University)

  • Xiaohan Tian

    (Beijing Normal University)

  • Yingjie Peng

    (Chinese Academy of Sciences)

  • Shangzheng Huang

    (Chinese Academy of Sciences)

  • Kaixin Li

    (Chinese Academy of Sciences)

  • Meng Wang

    (Beijing Normal University)

  • Yuqing Sun

    (Beijing Normal University)

  • Hao Yan

    (Peking University Sixth Hospital/Institute of Mental Health
    National Clinical Research Center for Mental Disorders (Peking University Sixth Hospital))

  • Cheng Zhang

    (Peking University First Hospital)

  • Sheng He

    (Chinese Academy of Sciences)

  • Ruquan Han

    (Capital Medical University)

  • Xiaoqun Wang

    (Chinese Academy of Sciences
    Beijing Normal University
    Beijing Normal University
    Beijing Normal University)

  • Bing Liu

    (Beijing Normal University
    Beijing Normal University
    Chinese Institute for Brain Research)

Abstract

Consciousness arises from the spatiotemporal neural dynamics, however, its relationship with neural flexibility and regional specialization remains elusive. We identified a consciousness-related signature marked by shifting spontaneous fluctuations along a unimodal-transmodal cortical axis. This simple signature is sensitive to altered states of consciousness in single individuals, exhibiting abnormal elevation under psychedelics and in psychosis. The hierarchical dynamic reflects brain state changes in global integration and connectome diversity under task-free conditions. Quasi-periodic pattern detection revealed that hierarchical heterogeneity as spatiotemporally propagating waves linking to arousal. A similar pattern can be observed in macaque electrocorticography. Furthermore, the spatial distribution of principal cortical gradient preferentially recapitulated the genetic transcription levels of the histaminergic system and that of the functional connectome mapping of the tuberomammillary nucleus, which promotes wakefulness. Combining behavioral, neuroimaging, electrophysiological, and transcriptomic evidence, we propose that global consciousness is supported by efficient hierarchical processing constrained along a low-dimensional macroscale gradient.

Suggested Citation

  • Ang Li & Haiyang Liu & Xu Lei & Yini He & Qian Wu & Yan Yan & Xin Zhou & Xiaohan Tian & Yingjie Peng & Shangzheng Huang & Kaixin Li & Meng Wang & Yuqing Sun & Hao Yan & Cheng Zhang & Sheng He & Ruquan, 2023. "Hierarchical fluctuation shapes a dynamic flow linked to states of consciousness," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38972-x
    DOI: 10.1038/s41467-023-38972-x
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-38972-x
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-38972-x?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. Seok-Jun Hong & Reinder Vos de Wael & Richard A. I. Bethlehem & Sara Lariviere & Casey Paquola & Sofie L. Valk & Michael P. Milham & Adriana Di Martino & Daniel S. Margulies & Jonathan Smallwood & Bor, 2019. "Atypical functional connectome hierarchy in autism," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    2. Michael J. Hawrylycz & Ed S. Lein & Angela L. Guillozet-Bongaarts & Elaine H. Shen & Lydia Ng & Jeremy A. Miller & Louie N. van de Lagemaat & Kimberly A. Smith & Amanda Ebbert & Zackery L. Riley & Chr, 2012. "An anatomically comprehensive atlas of the adult human brain transcriptome," Nature, Nature, vol. 489(7416), pages 391-399, September.
    3. Russell A. Poldrack & Timothy O. Laumann & Oluwasanmi Koyejo & Brenda Gregory & Ashleigh Hover & Mei-Yen Chen & Krzysztof J. Gorgolewski & Jeffrey Luci & Sung Jun Joo & Ryan L. Boyd & Scott Hunicke-Sm, 2015. "Long-term neural and physiological phenotyping of a single human," Nature Communications, Nature, vol. 6(1), pages 1-15, December.
    4. Andrea I. Luppi & Michael M. Craig & Ioannis Pappas & Paola Finoia & Guy B. Williams & Judith Allanson & John D. Pickard & Adrian M. Owen & Lorina Naci & David K. Menon & Emmanuel A. Stamatakis, 2019. "Consciousness-specific dynamic interactions of brain integration and functional diversity," Nature Communications, Nature, vol. 10(1), pages 1-12, December.
    5. Anandamohan Ghosh & Y Rho & A R McIntosh & R Kötter & V K Jirsa, 2008. "Noise during Rest Enables the Exploration of the Brain's Dynamic Repertoire," PLOS Computational Biology, Public Library of Science, vol. 4(10), pages 1-12, October.
    6. Kevin M. Anderson & Meghan A. Collins & Rowena Chin & Tian Ge & Monica D. Rosenberg & Avram J. Holmes, 2020. "Transcriptional and imaging-genetic association of cortical interneurons, brain function, and schizophrenia risk," Nature Communications, Nature, vol. 11(1), pages 1-15, December.
    7. Itay Yaron & Lucia Melloni & Michael Pitts & Liad Mudrik, 2022. "The ConTraSt database for analysing and comparing empirical studies of consciousness theories," Nature Human Behaviour, Nature, vol. 6(4), pages 593-604, April.
    8. Gustavo Deco & Diego Vidaurre & Morten L. Kringelbach, 2021. "Revisiting the global workspace orchestrating the hierarchical organization of the human brain," Nature Human Behaviour, Nature, vol. 5(4), pages 497-511, April.
    Full references (including those not matched with items on IDEAS)

    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. Xiaolu Kong & Ru Kong & Csaba Orban & Peng Wang & Shaoshi Zhang & Kevin Anderson & Avram Holmes & John D. Murray & Gustavo Deco & Martijn Heuvel & B. T. Thomas Yeo, 2021. "Sensory-motor cortices shape functional connectivity dynamics in the human brain," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    2. Stefano Berto & Alex H. Treacher & Emre Caglayan & Danni Luo & Jillian R. Haney & Michael J. Gandal & Daniel H. Geschwind & Albert A. Montillo & Genevieve Konopka, 2022. "Association between resting-state functional brain connectivity and gene expression is altered in autism spectrum disorder," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    3. Junjiao Feng & Liang Zhang & Chunhui Chen & Jintao Sheng & Zhifang Ye & Kanyin Feng & Jing Liu & Ying Cai & Bi Zhu & Zhaoxia Yu & Chuansheng Chen & Qi Dong & Gui Xue, 2022. "A cognitive neurogenetic approach to uncovering the structure of executive functions," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    4. Sungyong Um & Bin Zhang & Sunil Wattal & Youngjin Yoo, 2023. "Software Components and Product Variety in a Platform Ecosystem: A Dynamic Network Analysis of WordPress," Information Systems Research, INFORMS, vol. 34(4), pages 1339-1374, December.
    5. Alessandra Griffa & Mathieu Mach & Julien Dedelley & Daniel Gutierrez-Barragan & Alessandro Gozzi & Gilles Allali & Joanes Grandjean & Dimitri Ville & Enrico Amico, 2023. "Evidence for increased parallel information transmission in human brain networks compared to macaques and male mice," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    6. Tatsuya Osaki & Tomoya Duenki & Siu Yu A. Chow & Yasuhiro Ikegami & Romain Beaubois & Timothée Levi & Nao Nakagawa-Tamagawa & Yoji Hirano & Yoshiho Ikeuchi, 2024. "Complex activity and short-term plasticity of human cerebral organoids reciprocally connected with axons," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    7. Tingting Bo & Jie Li & Ganlu Hu & Ge Zhang & Wei Wang & Qian Lv & Shaoling Zhao & Junjie Ma & Meng Qin & Xiaohui Yao & Meiyun Wang & Guang-Zhong Wang & Zheng Wang, 2023. "Brain-wide and cell-specific transcriptomic insights into MRI-derived cortical morphology in macaque monkeys," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    8. Sofie L. Valk & Ting Xu & Casey Paquola & Bo-yong Park & Richard A. I. Bethlehem & Reinder Vos de Wael & Jessica Royer & Shahrzad Kharabian Masouleh & Şeyma Bayrak & Peter Kochunov & B. T. Thomas Yeo , 2022. "Genetic and phylogenetic uncoupling of structure and function in human transmodal cortex," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    9. Vincent Bazinet & Justine Y. Hansen & Reinder Vos de Wael & Boris C. Bernhardt & Martijn P. Heuvel & Bratislav Misic, 2023. "Assortative mixing in micro-architecturally annotated brain connectomes," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    10. Lynne Krohn & Karl Heilbron & Cornelis Blauwendraat & Regina H. Reynolds & Eric Yu & Konstantin Senkevich & Uladzislau Rudakou & Mehrdad A. Estiar & Emil K. Gustavsson & Kajsa Brolin & Jennifer A. Rus, 2022. "Genome-wide association study of REM sleep behavior disorder identifies polygenic risk and brain expression effects," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    11. Ada J. S. Chan & Worrawat Engchuan & Miriam S. Reuter & Zhuozhi Wang & Bhooma Thiruvahindrapuram & Brett Trost & Thomas Nalpathamkalam & Carol Negrijn & Sylvia Lamoureux & Giovanna Pellecchia & Rohan , 2022. "Genome-wide rare variant score associates with morphological subtypes of autism spectrum disorder," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    12. Thomas S. Wingo & Yue Liu & Ekaterina S. Gerasimov & Selina M. Vattathil & Meghan E. Wynne & Jiaqi Liu & Adriana Lori & Victor Faundez & David A. Bennett & Nicholas T. Seyfried & Allan I. Levey & Aliz, 2022. "Shared mechanisms across the major psychiatric and neurodegenerative diseases," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    13. Max Lam & Chia-Yen Chen & W. David Hill & Charley Xia & Ruoyu Tian & Daniel F. Levey & Joel Gelernter & Murray B. Stein & Alexander S. Hatoum & Hailiang Huang & Anil K. Malhotra & Heiko Runz & Tian Ge, 2022. "Collective genomic segments with differential pleiotropic patterns between cognitive dimensions and psychopathology," Nature Communications, Nature, vol. 13(1), pages 1-22, December.
    14. Xinyuan Liang & Lianglong Sun & Xuhong Liao & Tianyuan Lei & Mingrui Xia & Dingna Duan & Zilong Zeng & Qiongling Li & Zhilei Xu & Weiwei Men & Yanpei Wang & Shuping Tan & Jia-Hong Gao & Shaozheng Qin , 2024. "Structural connectome architecture shapes the maturation of cortical morphology from childhood to adolescence," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    15. Lisa-Marie Appel & Vedran Franke & Melania Bruno & Irina Grishkovskaya & Aiste Kasiliauskaite & Tanja Kaufmann & Ursula E. Schoeberl & Martin G. Puchinger & Sebastian Kostrhon & Carmen Ebenwaldner & M, 2021. "PHF3 regulates neuronal gene expression through the Pol II CTD reader domain SPOC," Nature Communications, Nature, vol. 12(1), pages 1-24, December.
    16. Jun Ding & Jian Ji & Zachary Rabow & Tong Shen & Jacob Folz & Christopher R. Brydges & Sili Fan & Xinchen Lu & Sajjan Mehta & Megan R. Showalter & Ying Zhang & Renee Araiza & Lynette R. Bower & K. C. , 2021. "A metabolome atlas of the aging mouse brain," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    17. Justine Y. Hansen & Golia Shafiei & Jacob W. Vogel & Kelly Smart & Carrie E. Bearden & Martine Hoogman & Barbara Franke & Daan Rooij & Jan Buitelaar & Carrie R. McDonald & Sanjay M. Sisodiya & Lianne , 2022. "Local molecular and global connectomic contributions to cross-disorder cortical abnormalities," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    18. Klaas Enno Stephan & Anthony Randal McIntosh & Claus C Hilgetag, 2010. "In Memoriam: Rolf Kötter (1961–2010)," PLOS Computational Biology, Public Library of Science, vol. 6(10), pages 1-3, October.
    19. 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.
    20. Minji Lee & Leandro R. D. Sanz & Alice Barra & Audrey Wolff & Jaakko O. Nieminen & Melanie Boly & Mario Rosanova & Silvia Casarotto & Olivier Bodart & Jitka Annen & Aurore Thibaut & Rajanikant Panda &, 2022. "Quantifying arousal and awareness in altered states of consciousness using interpretable deep learning," Nature Communications, Nature, vol. 13(1), pages 1-14, 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_s41467-023-38972-x. 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.