Disruption in structural-functional network repertoire and time-resolved subcortical fronto-temporoparietal connectivity in disorders of consciousness

  1. Rajanikant Panda
  2. Aurore Thibaut
  3. Ane Lopez-Gonzalez
  4. Anira Escrichs
  5. Mohamed Ali Bahri
  6. Arjan Hillebrand
  7. Gustavo Deco
  8. Steven Laureys
  9. Olivia Gosseries
  10. Jitka Annen  Is a corresponding author
  11. Prejaas Tewarie  Is a corresponding author
  1. University of Liège, Belgium
  2. Universitat Pompeu Fabra, Spain
  3. Amsterdam University Medical Centers, Netherlands
  4. University of Nottingham, United Kingdom

Abstract

Understanding recovery of consciousness and elucidating its underlying mechanism is believed to be crucial in the field of basic neuroscience and medicine. Ideas such as the global neuronal workspace and the mesocircuit theory hypothesize that failure of recovery in conscious states coincide with loss of connectivity between subcortical and frontoparietal areas, a loss of the repertoire of functional networks states and metastable brain activation. We adopted a time-resolved functional connectivity framework to explore these ideas and assessed the repertoire of functional network states as a potential marker of consciousness and its potential ability to tell apart patients in the unresponsive wakefulness syndrome (UWS) and minimally conscious state (MCS). In addition, prediction of these functional network states by underlying hidden spatial patterns in the anatomical network, i.e. so-called eigenmodes, were supplemented as potential markers. By analysing time-resolved functional connectivity from functional MRI data, we demonstrated a reduction of metastability and functional network repertoire in UWS compared to MCS patients. This was expressed in terms of diminished dwell times and loss of nonstationarity in the default mode network and subcortical fronto-temporoparietal network in UWS compared to MCS patients. We further demonstrated that these findings co-occurred with a loss of dynamic interplay between structural eigenmodes and emerging time-resolved functional connectivity in UWS. These results are, amongst others, in support of the global neuronal workspace theory and the mesocircuit hypothesis, underpinning the role of time-resolved thalamo-cortical connections and metastability in the recovery of consciousness.

Data availability

Connectivity matrices will be made available open access through EBRAINS of the Human Brain Project.

The following previously published data sets were used

Article and author information

Author details

  1. Rajanikant Panda

    Coma Science Group, University of Liège, Liège, Belgium
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0960-4340
  2. Aurore Thibaut

    Coma Science Group, University of Liège, Liège, Belgium
    Competing interests
    The authors declare that no competing interests exist.
  3. Ane Lopez-Gonzalez

    Center for Brain and Cognition, Universitat Pompeu Fabra, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
  4. Anira Escrichs

    Coma Science Group, University of Liège, Liège, Belgium
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6482-9737
  5. Mohamed Ali Bahri

    GIGA-Cyclotron Research Centre-In Vivo Imaging, University of Liège, Liège, Belgium
    Competing interests
    The authors declare that no competing interests exist.
  6. Arjan Hillebrand

    Department of Clinical Neurophysiology, Amsterdam University Medical Centers, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8508-3532
  7. Gustavo Deco

    Center for Brain and Cognition, Universitat Pompeu Fabra, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
  8. Steven Laureys

    Coma Science Group, University of Liège, Liège, Belgium
    Competing interests
    The authors declare that no competing interests exist.
  9. Olivia Gosseries

    Coma Science Group, University of Liège, Liège, Belgium
    Competing interests
    The authors declare that no competing interests exist.
  10. Jitka Annen

    Coma Science Group, University of Liège, Liège, Belgium
    For correspondence
    jitka.annen@uliege.be
    Competing interests
    The authors declare that no competing interests exist.
  11. Prejaas Tewarie

    School of Physics, University of Nottingham, Nottingham, United Kingdom
    For correspondence
    prejaas.tewarie@nottingham.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3311-4990

Funding

Horizon 2020 Framework Programme (945539)

  • Ane Lopez-Gonzalez

Horizon 2020 Framework Programme (785907)

  • Gustavo Deco

Horizon 2020 Framework Programme (778234)

  • Olivia Gosseries

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Muireann Irish, University of Sydney, Australia

Ethics

Human subjects: Written informed consent was obtained from all healthy subjects and the legalrepresentative for DOC patients.

Version history

  1. Preprint posted: December 12, 2021 (view preprint)
  2. Received: January 31, 2022
  3. Accepted: August 1, 2022
  4. Accepted Manuscript published: August 2, 2022 (version 1)
  5. Version of Record published: August 17, 2022 (version 2)

Copyright

© 2022, Panda et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Rajanikant Panda
  2. Aurore Thibaut
  3. Ane Lopez-Gonzalez
  4. Anira Escrichs
  5. Mohamed Ali Bahri
  6. Arjan Hillebrand
  7. Gustavo Deco
  8. Steven Laureys
  9. Olivia Gosseries
  10. Jitka Annen
  11. Prejaas Tewarie
(2022)
Disruption in structural-functional network repertoire and time-resolved subcortical fronto-temporoparietal connectivity in disorders of consciousness
eLife 11:e77462.
https://doi.org/10.7554/eLife.77462

Share this article

https://doi.org/10.7554/eLife.77462

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