IDEAS home Printed from https://ideas.repec.org/a/plo/pcbi00/1006807.html
   My bibliography  Save this article

Information integration in large brain networks

Author

Listed:
  • Daniel Toker
  • Friedrich T Sommer

Abstract

An outstanding problem in neuroscience is to understand how information is integrated across the many modules of the brain. While classic information-theoretic measures have transformed our understanding of feedforward information processing in the brain’s sensory periphery, comparable measures for information flow in the massively recurrent networks of the rest of the brain have been lacking. To address this, recent work in information theory has produced a sound measure of network-wide “integrated information”, which can be estimated from time-series data. But, a computational hurdle has stymied attempts to measure large-scale information integration in real brains. Specifically, the measurement of integrated information involves a combinatorial search for the informational “weakest link” of a network, a process whose computation time explodes super-exponentially with network size. Here, we show that spectral clustering, applied on the correlation matrix of time-series data, provides an approximate but robust solution to the search for the informational weakest link of large networks. This reduces the computation time for integrated information in large systems from longer than the lifespan of the universe to just minutes. We evaluate this solution in brain-like systems of coupled oscillators as well as in high-density electrocortigraphy data from two macaque monkeys, and show that the informational “weakest link” of the monkey cortex splits posterior sensory areas from anterior association areas. Finally, we use our solution to provide evidence in support of the long-standing hypothesis that information integration is maximized by networks with a high global efficiency, and that modular network structures promote the segregation of information.Author summary: Information theory has been key to our understanding of the feedforward pathways of the brain’s sensory periphery. But, traditional information-theoretic measures only quantify communication between pairs of transmitters and receivers, and have been of limited utility in decoding signals in the recurrent networks that dominate the rest of the brain. To address this shortcoming, a theoretically sound measure of information integration has recently been derived, which can quantify communication across an entire brain network. This measure could be pivotal in understanding recurrent brain networks. But, a computational hurdle has made it impossible to quantify this measure in real brains. We present an approximate but robust solution to this hurdle, and use our solution to test long-held assumptions about how brain networks might integrate information.

Suggested Citation

  • Daniel Toker & Friedrich T Sommer, 2019. "Information integration in large brain networks," PLOS Computational Biology, Public Library of Science, vol. 15(2), pages 1-26, February.
  • Handle: RePEc:plo:pcbi00:1006807
    DOI: 10.1371/journal.pcbi.1006807
    as

    Download full text from publisher

    File URL: https://journals.plos.org/ploscompbiol/article?id=10.1371/journal.pcbi.1006807
    Download Restriction: no

    File URL: https://journals.plos.org/ploscompbiol/article/file?id=10.1371/journal.pcbi.1006807&type=printable
    Download Restriction: no

    File URL: https://libkey.io/10.1371/journal.pcbi.1006807?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. Max Tegmark, 2016. "Improved Measures of Integrated Information," PLOS Computational Biology, Public Library of Science, vol. 12(11), pages 1-34, November.
    2. Masafumi Oizumi & Larissa Albantakis & Giulio Tononi, 2014. "From the Phenomenology to the Mechanisms of Consciousness: Integrated Information Theory 3.0," PLOS Computational Biology, Public Library of Science, vol. 10(5), pages 1-25, May.
    3. 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.
    4. Michael Wibral & Nicolae Pampu & Viola Priesemann & Felix Siebenhühner & Hannes Seiwert & Michael Lindner & Joseph T Lizier & Raul Vicente, 2013. "Measuring Information-Transfer Delays," PLOS ONE, Public Library of Science, vol. 8(2), pages 1-19, February.
    5. Adam B Barrett & Anil K Seth, 2011. "Practical Measures of Integrated Information for Time-Series Data," PLOS Computational Biology, Public Library of Science, vol. 7(1), pages 1-18, January.
    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. 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.
    2. 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.
    3. Max Tegmark, 2016. "Improved Measures of Integrated Information," PLOS Computational Biology, Public Library of Science, vol. 12(11), pages 1-34, November.
    4. 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.
    5. 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.
    6. Masafumi Oizumi & Larissa Albantakis & Giulio Tononi, 2014. "From the Phenomenology to the Mechanisms of Consciousness: Integrated Information Theory 3.0," PLOS Computational Biology, Public Library of Science, vol. 10(5), pages 1-25, May.
    7. Peter Gordon Roetzel, 2019. "Information overload in the information age: a review of the literature from business administration, business psychology, and related disciplines with a bibliometric approach and framework developmen," Business Research, Springer;German Academic Association for Business Research, vol. 12(2), pages 479-522, December.
    8. David L Gibbs & Ilya Shmulevich, 2017. "Solving the influence maximization problem reveals regulatory organization of the yeast cell cycle," PLOS Computational Biology, Public Library of Science, vol. 13(6), pages 1-19, June.
    9. Adam B Barrett & Michael Murphy & Marie-Aurélie Bruno & Quentin Noirhomme & Mélanie Boly & Steven Laureys & Anil K Seth, 2012. "Granger Causality Analysis of Steady-State Electroencephalographic Signals during Propofol-Induced Anaesthesia," PLOS ONE, Public Library of Science, vol. 7(1), pages 1-12, January.
    10. Sourabh Lahiri & Philippe Nghe & Sander J Tans & Martin Luc Rosinberg & David Lacoste, 2017. "Information-theoretic analysis of the directional influence between cellular processes," PLOS ONE, Public Library of Science, vol. 12(11), pages 1-26, November.
    11. Coulibaly, Saliya & Bessin, Florent & Clerc, Marcel G. & Mussot, Arnaud, 2022. "Precursors-driven machine learning prediction of chaotic extreme pulses in Kerr resonators," Chaos, Solitons & Fractals, Elsevier, vol. 160(C).
    12. Libor Pekař & Radek Matušů & Roman Prokop, 2017. "Gridding discretization-based multiple stability switching delay search algorithm: The movement of a human being on a controlled swaying bow," PLOS ONE, Public Library of Science, vol. 12(6), pages 1-23, June.
    13. Xiaogeng Wan & Lanxi Xu, 2018. "A study for multiscale information transfer measures based on conditional mutual information," PLOS ONE, Public Library of Science, vol. 13(12), pages 1-30, December.
    14. Soumya Banerjee, 2021. "Emergent rules of computation in the Universe lead to life and consciousness: a computational framework for consciousness," Interdisciplinary Description of Complex Systems - scientific journal, Croatian Interdisciplinary Society Provider Homepage: http://indecs.eu, vol. 19(1), pages 31-41.
    15. Soumya Banerjee, 2021. "Emergent rules of computation in the Universe lead to life and consciousness: a computational framework for consciousness," Interdisciplinary Description of Complex Systems - scientific journal, Croatian Interdisciplinary Society Provider Homepage: http://indecs.eu, vol. 19(1), pages 31-41.
    16. Valmir C. Barbosa, 2017. "Information Integration from Distributed Threshold-Based Interactions," Complexity, Hindawi, vol. 2017, pages 1-14, January.
    17. Shinya Ito & Fang-Chin Yeh & Emma Hiolski & Przemyslaw Rydygier & Deborah E Gunning & Pawel Hottowy & Nicholas Timme & Alan M Litke & John M Beggs, 2014. "Large-Scale, High-Resolution Multielectrode-Array Recording Depicts Functional Network Differences of Cortical and Hippocampal Cultures," PLOS ONE, Public Library of Science, vol. 9(8), pages 1-16, August.
    18. Nicholas Timme & Shinya Ito & Maxym Myroshnychenko & Fang-Chin Yeh & Emma Hiolski & Pawel Hottowy & John M Beggs, 2014. "Multiplex Networks of Cortical and Hippocampal Neurons Revealed at Different Timescales," PLOS ONE, Public Library of Science, vol. 9(12), pages 1-43, December.
    19. Leonidas Sandoval Junior & Asher Mullokandov & Dror Y. Kenett, 2015. "Dependency Relations among International Stock Market Indices," JRFM, MDPI, vol. 8(2), pages 1-39, May.
    20. Jeffrey A Edlund & Nicolas Chaumont & Arend Hintze & Christof Koch & Giulio Tononi & Christoph Adami, 2011. "Integrated Information Increases with Fitness in the Evolution of Animats," PLOS Computational Biology, Public Library of Science, vol. 7(10), pages 1-13, October.

    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:pcbi00:1006807. 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.