IDEAS home Printed from https://ideas.repec.org/a/plo/pcbi00/1007686.html
   My bibliography  Save this article

Cortical ignition dynamics is tightly linked to the core organisation of the human connectome

Author

Listed:
  • Samy Castro
  • Wael El-Deredy
  • Demian Battaglia
  • Patricio Orio

Abstract

The capability of cortical regions to flexibly sustain an “ignited” state of activity has been discussed in relation to conscious perception or hierarchical information processing. Here, we investigate how the intrinsic propensity of different regions to get ignited is determined by the specific topological organisation of the structural connectome. More specifically, we simulated the resting-state dynamics of mean-field whole-brain models and assessed how dynamic multistability and ignition differ between a reference model embedding a realistic human connectome, and alternative models based on a variety of randomised connectome ensembles. We found that the strength of global excitation needed to first trigger ignition in a subset of regions is substantially smaller for the model embedding the empirical human connectome. Furthermore, when increasing the strength of excitation, the propagation of ignition outside of this initial core–which is able to self-sustain its high activity–is way more gradual than for any of the randomised connectomes, allowing for graded control of the number of ignited regions. We explain both these assets in terms of the exceptional weighted core-shell organisation of the empirical connectome, speculating that this topology of human structural connectivity may be attuned to support enhanced ignition dynamics.Author summary: The activity of the cortex in mammals constantly fluctuates in relation to cognitive tasks, but also during rest. The ability of brain regions to display ignition, a fast transition from low to high activity is central for the emergence of conscious perception and decision making. Here, using a biophysically inspired model of cortical activity, we show how the structural organization of human cortex supports and constrains the rise of this ignited dynamics in spontaneous cortical activity. We found that the weighted core-shell organization of the human connectome allows for a uniquely graded ignition. This graded ignition implies a smooth control of the ignition in cortical areas tuned by the global excitability. The smooth control cannot be replicated by surrogate connectomes, even though they conserve key local or global network properties. Indeed, ignition in the human cortex is first triggered on the strongest and most densely interconnected cortical areas–the “ignition core”–, emerging at the lowest global excitability value compared to surrogate connectomes. Finally, we suggest developmental and evolutionary constraints of the mesoscale organization that support this enhanced ignition dynamics in cortical activity.

Suggested Citation

  • Samy Castro & Wael El-Deredy & Demian Battaglia & Patricio Orio, 2020. "Cortical ignition dynamics is tightly linked to the core organisation of the human connectome," PLOS Computational Biology, Public Library of Science, vol. 16(7), pages 1-23, July.
  • Handle: RePEc:plo:pcbi00:1007686
    DOI: 10.1371/journal.pcbi.1007686
    as

    Download full text from publisher

    File URL: https://journals.plos.org/ploscompbiol/article?id=10.1371/journal.pcbi.1007686
    Download Restriction: no

    File URL: https://journals.plos.org/ploscompbiol/article/file?id=10.1371/journal.pcbi.1007686&type=printable
    Download Restriction: no

    File URL: https://libkey.io/10.1371/journal.pcbi.1007686?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. Logan Harriger & Martijn P van den Heuvel & Olaf Sporns, 2012. "Rich Club Organization of Macaque Cerebral Cortex and Its Role in Network Communication," PLOS ONE, Public Library of Science, vol. 7(9), pages 1-13, September.
    2. Paul T E Cusack, 2020. "The Human Brain," Biomedical Journal of Scientific & Technical Research, Biomedical Research Network+, LLC, vol. 31(3), pages 24261-24266, October.
    3. Richard F. Betzel & John D. Medaglia & Danielle S. Bassett, 2018. "Diversity of meso-scale architecture in human and non-human connectomes," Nature Communications, Nature, vol. 9(1), pages 1-14, December.
    4. Christoph Kirst & Marc Timme & Demian Battaglia, 2016. "Dynamic information routing in complex networks," Nature Communications, Nature, vol. 7(1), pages 1-9, 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. Dominic Holland & Oleksandr Frei & Rahul Desikan & Chun-Chieh Fan & Alexey A Shadrin & Olav B Smeland & V S Sundar & Paul Thompson & Ole A Andreassen & Anders M Dale, 2020. "Beyond SNP heritability: Polygenicity and discoverability of phenotypes estimated with a univariate Gaussian mixture model," PLOS Genetics, Public Library of Science, vol. 16(5), pages 1-30, May.
    2. Julia Berezutskaya & Zachary V Freudenburg & Umut Güçlü & Marcel A J van Gerven & Nick F Ramsey, 2020. "Brain-optimized extraction of complex sound features that drive continuous auditory perception," PLOS Computational Biology, Public Library of Science, vol. 16(7), pages 1-34, July.
    3. Abigail B. Schneider & Bridget Leonard, 2022. "From anxiety to control: Mask‐wearing, perceived marketplace influence, and emotional well‐being during the COVID‐19 pandemic," Journal of Consumer Affairs, Wiley Blackwell, vol. 56(1), pages 97-119, March.
    4. Geonhui Lee & Woong Choi & Hanjin Jo & Wookhyun Park & Jaehyo Kim, 2020. "Analysis of motor control strategy for frontal and sagittal planes of circular tracking movements using visual feedback noise from velocity change and depth information," PLOS ONE, Public Library of Science, vol. 15(11), pages 1-22, November.
    5. Yoon, Jisung & Park, Jinseo & Yun, Jinhyuk & Jung, Woo-Sung, 2023. "Quantifying knowledge synchronization with the network-driven approach," Journal of Informetrics, Elsevier, vol. 17(4).
    6. Odelaisy León-Triana & Julián Pérez-Beteta & David Albillo & Ana Ortiz de Mendivil & Luis Pérez-Romasanta & Elisabet González-Del Portillo & Manuel Llorente & Natalia Carballo & Estanislao Arana & Víc, 2021. "Brain Metastasis Response to Stereotactic Radio Surgery: A Mathematical Approach," Mathematics, MDPI, vol. 9(7), pages 1-19, March.
    7. Mirren Charnley & Saba Islam & Guneet K. Bindra & Jeremy Engwirda & Julian Ratcliffe & Jiangtao Zhou & Raffaele Mezzenga & Mark D. Hulett & Kyunghoon Han & Joshua T. Berryman & Nicholas P. Reynolds, 2022. "Neurotoxic amyloidogenic peptides in the proteome of SARS-COV2: potential implications for neurological symptoms in COVID-19," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    8. Nguyen, Ha Trong & Brinkman, Sally & Le, Huong Thu & Zubrick, Stephen R. & Mitrou, Francis, 2022. "Gender differences in time allocation contribute to differences in developmental outcomes in children and adolescents," Economics of Education Review, Elsevier, vol. 89(C).
    9. Gregor Wolbring, 2022. "Auditing the ‘Social’ of Quantum Technologies: A Scoping Review," Societies, MDPI, vol. 12(2), pages 1-38, March.
    10. April R. Kriebel & Joshua D. Welch, 2022. "UINMF performs mosaic integration of single-cell multi-omic datasets using nonnegative matrix factorization," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    11. Boada, Júlia Pareto & Maestre, Begoña Román & Genís, Carme Torras, 2021. "The ethical issues of social assistive robotics: A critical literature review," Technology in Society, Elsevier, vol. 67(C).
    12. Hamed Nili & Alexander Walther & Arjen Alink & Nikolaus Kriegeskorte, 2020. "Inferring exemplar discriminability in brain representations," PLOS ONE, Public Library of Science, vol. 15(6), pages 1-28, June.
    13. Valtteri Arstila & Alexandra L Georgescu & Henri Pesonen & Daniel Lunn & Valdas Noreika & Christine M Falter-Wagner, 2020. "Event timing in human vision: Modulating factors and independent functions," PLOS ONE, Public Library of Science, vol. 15(8), pages 1-22, August.
    14. Don, Arjuna P.H. & Peters, James F. & Ramanna, Sheela & Tozzi, Arturo, 2021. "Quaternionic views of rs-fMRI hierarchical brain activation regions. Discovery of multilevel brain activation region intensities in rs-fMRI video frames," Chaos, Solitons & Fractals, Elsevier, vol. 152(C).
    15. Linzmajer, Marc & Hubert, Mirja & Hubert, Marco, 2021. "It’s about the process, not the result: An fMRI approach to explore the encoding of explicit and implicit price information," Journal of Economic Psychology, Elsevier, vol. 86(C).
    16. Natalie J Shook & Barış Sevi & Jerin Lee & Benjamin Oosterhoff & Holly N Fitzgerald, 2020. "Disease avoidance in the time of COVID-19: The behavioral immune system is associated with concern and preventative health behaviors," PLOS ONE, Public Library of Science, vol. 15(8), pages 1-15, August.
    17. Cristina Lázaro-Pérez & José Ángel Martínez-López & José Gómez-Galán, 2020. "Addictions in Spanish College Students in Confinement Times: Preventive and Social Perspective," Social Sciences, MDPI, vol. 9(11), pages 1-21, October.
    18. Yashika Arora & Pushpinder Walia & Mitsuhiro Hayashibe & Makii Muthalib & Shubhajit Roy Chowdhury & Stephane Perrey & Anirban Dutta, 2021. "Grey-box modeling and hypothesis testing of functional near-infrared spectroscopy-based cerebrovascular reactivity to anodal high-definition tDCS in healthy humans," PLOS Computational Biology, Public Library of Science, vol. 17(10), pages 1-38, October.
    19. Antoine Allard & M Ángeles Serrano, 2020. "Navigable maps of structural brain networks across species," PLOS Computational Biology, Public Library of Science, vol. 16(2), pages 1-20, February.
    20. Elvisa Drishti & Bresena Kopliku & Drini Imami, 2022. "Active political engagement, political patronage and local labour markets – The example of Shkoder," International Journal of Manpower, Emerald Group Publishing Limited, vol. 44(6), pages 1118-1142, April.

    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:plo:pcbi00:1007686. 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: ploscompbiol (email available below). General contact details of provider: https://journals.plos.org/ploscompbiol/ .

    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.