IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-42465-2.html
   My bibliography  Save this article

Neuronal connected burst cascades bridge macroscale adaptive signatures across arousal states

Author

Listed:
  • Brandon R. Munn

    (The University of Sydney
    University of Sydney
    The University of Sydney)

  • Eli J. Müller

    (The University of Sydney
    University of Sydney
    The University of Sydney)

  • Vicente Medel

    (The University of Sydney
    Universidad Adolfo Ibañez)

  • Sharon L. Naismith

    (The University of Sydney
    The University of Sydney)

  • Joseph T. Lizier

    (The University of Sydney
    The University of Sydney)

  • Robert D. Sanders

    (Royal Prince Alfred Hospital
    The University of Sydney)

  • James M. Shine

    (The University of Sydney
    University of Sydney
    The University of Sydney)

Abstract

The human brain displays a rich repertoire of states that emerge from the microscopic interactions of cortical and subcortical neurons. Difficulties inherent within large-scale simultaneous neuronal recording limit our ability to link biophysical processes at the microscale to emergent macroscopic brain states. Here we introduce a microscale biophysical network model of layer-5 pyramidal neurons that display graded coarse-sampled dynamics matching those observed in macroscale electrophysiological recordings from macaques and humans. We invert our model to identify the neuronal spike and burst dynamics that differentiate unconscious, dreaming, and awake arousal states and provide insights into their functional signatures. We further show that neuromodulatory arousal can mediate different modes of neuronal dynamics around a low-dimensional energy landscape, which in turn changes the response of the model to external stimuli. Our results highlight the promise of multiscale modelling to bridge theories of consciousness across spatiotemporal scales.

Suggested Citation

  • Brandon R. Munn & Eli J. Müller & Vicente Medel & Sharon L. Naismith & Joseph T. Lizier & Robert D. Sanders & James M. Shine, 2023. "Neuronal connected burst cascades bridge macroscale adaptive signatures across arousal states," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-42465-2
    DOI: 10.1038/s41467-023-42465-2
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-42465-2
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-42465-2?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. Matthew E. Larkum & J. Julius Zhu & Bert Sakmann, 1999. "A new cellular mechanism for coupling inputs arriving at different cortical layers," Nature, Nature, vol. 398(6725), pages 338-341, March.
    2. Masafumi Oizumi & Shun-ichi Amari & Toru Yanagawa & Naotaka Fujii & Naotsugu Tsuchiya, 2016. "Measuring Integrated Information from the Decoding Perspective," PLOS Computational Biology, Public Library of Science, vol. 12(1), pages 1-18, January.
    3. Joshua H. Siegle & Xiaoxuan Jia & Séverine Durand & Sam Gale & Corbett Bennett & Nile Graddis & Greggory Heller & Tamina K. Ramirez & Hannah Choi & Jennifer A. Luviano & Peter A. Groblewski & Ruweida , 2021. "Survey of spiking in the mouse visual system reveals functional hierarchy," Nature, Nature, vol. 592(7852), pages 86-92, April.
    4. Shree Hari Gautam & Thanh T Hoang & Kylie McClanahan & Stephen K Grady & Woodrow L Shew, 2015. "Maximizing Sensory Dynamic Range by Tuning the Cortical State to Criticality," PLOS Computational Biology, Public Library of Science, vol. 11(12), pages 1-15, December.
    5. Nikos K. Logothetis, 2008. "What we can do and what we cannot do with fMRI," Nature, Nature, vol. 453(7197), pages 869-878, June.
    6. Brandon R. Munn & Eli J. Müller & Gabriel Wainstein & James M. Shine, 2021. "The ascending arousal system shapes neural dynamics to mediate awareness of cognitive states," Nature Communications, Nature, vol. 12(1), pages 1-9, December.
    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. 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.
    2. Rita Gil & Mafalda Valente & Noam Shemesh, 2024. "Rat superior colliculus encodes the transition between static and dynamic vision modes," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    3. Thomas F Varley & Olaf Sporns & Aina Puce & John Beggs, 2020. "Differential effects of propofol and ketamine on critical brain dynamics," PLOS Computational Biology, Public Library of Science, vol. 16(12), pages 1-29, December.
    4. Matteo Farinella & Daniel T Ruedt & Padraig Gleeson & Frederic Lanore & R Angus Silver, 2014. "Glutamate-Bound NMDARs Arising from In Vivo-like Network Activity Extend Spatio-temporal Integration in a L5 Cortical Pyramidal Cell Model," PLOS Computational Biology, Public Library of Science, vol. 10(4), pages 1-21, April.
    5. Jan C. Frankowski & Alexa Tierno & Shreya Pavani & Quincy Cao & David C. Lyon & Robert F. Hunt, 2022. "Brain-wide reconstruction of inhibitory circuits after traumatic brain injury," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    6. Oren Amsalem & Hidehiko Inagaki & Jianing Yu & Karel Svoboda & Ran Darshan, 2024. "Sub-threshold neuronal activity and the dynamical regime of cerebral cortex," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    7. Arjun A. Bhaskaran & Théo Gauvrit & Yukti Vyas & Guillaume Bony & Melanie Ginger & Andreas Frick, 2023. "Endogenous noise of neocortical neurons correlates with atypical sensory response variability in the Fmr1−/y mouse model of autism," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    8. Adam R. Pines & Bart Larsen & Zaixu Cui & Valerie J. Sydnor & Maxwell A. Bertolero & Azeez Adebimpe & Aaron F. Alexander-Bloch & Christos Davatzikos & Damien A. Fair & Ruben C. Gur & Raquel E. Gur & H, 2022. "Dissociable multi-scale patterns of development in personalized brain networks," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    9. repec:hum:wpaper:sfb649dp2014-036 is not listed on IDEAS
    10. Alejandro Morán & Miguel C Soriano, 2018. "Improving the quality of a collective signal in a consumer EEG headset," PLOS ONE, Public Library of Science, vol. 13(5), pages 1-21, May.
    11. Adam S. Tuzolele Mbuku, 2024. "Evolution of the concept of Homo Economicus in light of advances in Neuroeconomics: towards a more realistic model of economic decision-making [Evolution du concept de l'Homo Economicus à la lumièr," Post-Print hal-04564775, HAL.
    12. Giuseppe Chindemi & Marwan Abdellah & Oren Amsalem & Ruth Benavides-Piccione & Vincent Delattre & Michael Doron & András Ecker & Aurélien T. Jaquier & James King & Pramod Kumbhar & Caitlin Monney & Ro, 2022. "A calcium-based plasticity model for predicting long-term potentiation and depression in the neocortex," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    13. Pérez-Centeno, Victor, 2018. "Brain-driven entrepreneurship research: Expanded review and research agenda towards entrepreneurial enhancement," Working Papers 02/18, Institut für Mittelstandsforschung (IfM) Bonn.
    14. Olsen, Carmen & Gold, Anna, 2018. "Future research directions at the intersection between cognitive neuroscience research and auditors’ professional skepticism," Journal of Accounting Literature, Elsevier, vol. 41(C), pages 127-141.
    15. David Engel & Thomas W Malone, 2018. "Integrated information as a metric for group interaction," PLOS ONE, Public Library of Science, vol. 13(10), pages 1-19, October.
    16. Antonio J. Ibáñez-Molina & Sergio Iglesias-Parro, 2018. "A Comparison between Theoretical and Experimental Measures of Consciousness as Integrated Information in an Anatomically Based Network of Coupled Oscillators," Complexity, Hindawi, vol. 2018, pages 1-8, April.
    17. Ziqi Gao & Chenran Jiang & Jiawen Zhang & Xiaosen Jiang & Lanqing Li & Peilin Zhao & Huanming Yang & Yong Huang & Jia Li, 2023. "Hierarchical graph learning for protein–protein interaction," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    18. Edward A. B. Horrocks & Fabio R. Rodrigues & Aman B. Saleem, 2024. "Flexible neural population dynamics govern the speed and stability of sensory encoding in mouse visual cortex," Nature Communications, Nature, vol. 15(1), pages 1-23, December.
    19. Takayuki Niizato & Kotaro Sakamoto & Yoh-ichi Mototake & Hisashi Murakami & Takenori Tomaru & Tomotaro Hoshika & Toshiki Fukushima, 2020. "Finding continuity and discontinuity in fish schools via integrated information theory," PLOS ONE, Public Library of Science, vol. 15(2), pages 1-29, February.
    20. Eleonora Maggioni & Jorge Arrubla & Tracy Warbrick & Jürgen Dammers & Anna M Bianchi & Gianluigi Reni & Michela Tosetti & Irene Neuner & N Jon Shah, 2014. "Removal of Pulse Artefact from EEG Data Recorded in MR Environment at 3T. Setting of ICA Parameters for Marking Artefactual Components: Application to Resting-State Data," PLOS ONE, Public Library of Science, vol. 9(11), pages 1-15, November.
    21. Daniella Laureiro-Martínez & Stefano Brusoni & Nicola Canessa & Maurizio Zollo, 2015. "Understanding the exploration–exploitation dilemma: An fMRI study of attention control and decision-making performance," Strategic Management Journal, Wiley Blackwell, vol. 36(3), pages 319-338, March.

    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_s41467-023-42465-2. 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.