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What lies underneath: Precise classification of brain states using time-dependent topological structure of dynamics

Author

Listed:
  • Fernando Soler-Toscano
  • Javier A Galadí
  • Anira Escrichs
  • Yonatan Sanz Perl
  • Ane López-González
  • Jacobo D Sitt
  • Jitka Annen
  • Olivia Gosseries
  • Aurore Thibaut
  • Rajanikant Panda
  • Francisco J Esteban
  • Steven Laureys
  • Morten L Kringelbach
  • José A Langa
  • Gustavo Deco

Abstract

The self-organising global dynamics underlying brain states emerge from complex recursive nonlinear interactions between interconnected brain regions. Until now, most efforts of capturing the causal mechanistic generating principles have supposed underlying stationarity, being unable to describe the non-stationarity of brain dynamics, i.e. time-dependent changes. Here, we present a novel framework able to characterise brain states with high specificity, precisely by modelling the time-dependent dynamics. Through describing a topological structure associated to the brain state at each moment in time (its attractor or ‘information structure’), we are able to classify different brain states by using the statistics across time of these structures hitherto hidden in the neuroimaging dynamics. Proving the strong potential of this framework, we were able to classify resting-state BOLD fMRI signals from two classes of post-comatose patients (minimally conscious state and unresponsive wakefulness syndrome) compared with healthy controls with very high precision.Author summary: Brain states emerge through continuously evolving dynamics of brain networks. The usual way of modelling these dynamics is by using stationary systems: there is one structure (attractor) which is responsible of the brain dynamics. We adopt a different approach by characterising the brain activity through a landscape of informational structures (IS) changing in time. We use a model transformation procedure to produce these structures and look at several properties related to how the different brain networks interact not in the observed resting-state fMRI signal but in the information structure underlying it. These properties provide measures strongly related with relevant characteristics of conscious activity, such as metastability, information integration or synchronisation. The distribution of IS measures is studied for healthy controls (HC) and two groups of post-comatose patients with disorders of consciousness (DOC): minimally conscious state (MCS) and unresponsive wakefulness syndrome (UWS). Based on IS measures, machine learners classifiers identify the state of consciousness with an outstanding discrimination (precision of 95.6% por HC/DOC and 86.6% for MCS/UWS).

Suggested Citation

  • Fernando Soler-Toscano & Javier A Galadí & Anira Escrichs & Yonatan Sanz Perl & Ane López-González & Jacobo D Sitt & Jitka Annen & Olivia Gosseries & Aurore Thibaut & Rajanikant Panda & Francisco J Es, 2022. "What lies underneath: Precise classification of brain states using time-dependent topological structure of dynamics," PLOS Computational Biology, Public Library of Science, vol. 18(9), pages 1-20, September.
  • Handle: RePEc:plo:pcbi00:1010412
    DOI: 10.1371/journal.pcbi.1010412
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    References listed on IDEAS

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    1. 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.
    2. Galadí, J.A. & Soler-Toscano, F. & Langa, J.A., 2022. "Model transform and local parameters. Application to instantaneous attractors," Chaos, Solitons & Fractals, Elsevier, vol. 159(C).
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