The structural connectome constrains fast brain dynamics

  1. Pierpaolo Sorrentino  Is a corresponding author
  2. Caio Seguin
  3. Rosaria Rucco
  4. Marianna Liparoti
  5. Emahnuel Troisi Lopez
  6. Simona Bonavita
  7. Mario Quarantelli MD
  8. Giuseppe Sorrentino
  9. Viktor Jirsa
  10. Andrew Zalesky
  1. Aix-Marseille University, France
  2. University of Melbourne, Australia
  3. University of Naples 'Parthenope', Italy
  4. Parthenope University of Naples, Italy
  5. University of Campania Luigi Vanvitelli, Italy
  6. National Research Council, Italy
  7. Aix-Marseille Université, France
  8. The University of Melbourne, Australia

Abstract

Brain activity during rest displays complex, rapidly evolving patterns in space and time. Structural connections comprising the human connectome are hypothesized to impose constraints on the dynamics of this activity. Here, we use magnetoencephalography (MEG) to quantify the extent to which fast neural dynamics in the human brain are constrained by structural connections inferred from diffusion MRI tractography. We characterize the spatio-temporal unfolding of whole-brain activity at the millisecond scale from source-reconstructed MEG data, estimating the probability that any two brain regions will significantly deviate from baseline activity in consecutive time epochs. We find that the structural connectome relates to, and likely affects, the rapid spreading of neuronal avalanches, evidenced by a significant association between these transition probabilities and structural connectivity strengths (r=0.37, <0.0001). This finding opens new avenues to study the relationship between brain structure and neural dynamics.

Data availability

The MEG data and the reconstructed avalanches are available upon request to the corresponding author (Pierpaolo Sorrentino), conditional on appropriate ethics approval at the local site. The availability of the data was not previously included in the ethical approval, and therefore data cannot be shared directly. In case data are requested, the corresponding author will request an amendment to the local ethical committee. Conditional to approval, the data will be made available. The Matlab code is available at https://github.com/pierpaolosorrentino/Transition-Matrices-

Article and author information

Author details

  1. Pierpaolo Sorrentino

    Institut de Neurosciences des Systèmes, Aix-Marseille University, Marseille, France
    For correspondence
    pierpaolo.SORRENTINO@univ-amu.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9556-9800
  2. Caio Seguin

    University of Melbourne, Melbourne, Australia
    Competing interests
    The authors declare that no competing interests exist.
  3. Rosaria Rucco

    Department of Motor Sciences and Wellness, University of Naples 'Parthenope', Naples, Italy
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0943-131X
  4. Marianna Liparoti

    scienze motorie, Parthenope University of Naples, Naples, Italy
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2192-6841
  5. Emahnuel Troisi Lopez

    scienze motorie, Parthenope University of Naples, Naples, Italy
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0220-2672
  6. Simona Bonavita

    Neurology Unit, University of Campania Luigi Vanvitelli, Naples, Italy
    Competing interests
    The authors declare that no competing interests exist.
  7. Mario Quarantelli MD

    Biostructure and Bioimaging Institute, National Research Council, Naples, Italy
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7836-454X
  8. Giuseppe Sorrentino

    Department of Motor Science and Wellness, University of Naples 'Parthenope', Naples, Italy
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0800-2433
  9. Viktor Jirsa

    Institut de Neurosciences des Systèmes, Aix-Marseille Université, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8251-8860
  10. Andrew Zalesky

    Melbourne Neuropsychiatry Centre, The University of Melbourne, Melbourne, Australia
    Competing interests
    The authors declare that no competing interests exist.

Funding

No external funding was received for this work.

Ethics

Human subjects: All participants gave written informed consent. The study complied with the declaration of Helsinki and was approved by the local Ethics Committee (Prot.n.93C.E./Reg. n.14-17OSS).

Reviewing Editor

  1. Diego Vidaurre

Publication history

  1. Preprint posted: November 25, 2020 (view preprint)
  2. Received: February 9, 2021
  3. Accepted: July 7, 2021
  4. Accepted Manuscript published: July 9, 2021 (version 1)
  5. Accepted Manuscript updated: July 13, 2021 (version 2)
  6. Version of Record published: July 21, 2021 (version 3)

Copyright

© 2021, Sorrentino 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. Pierpaolo Sorrentino
  2. Caio Seguin
  3. Rosaria Rucco
  4. Marianna Liparoti
  5. Emahnuel Troisi Lopez
  6. Simona Bonavita
  7. Mario Quarantelli MD
  8. Giuseppe Sorrentino
  9. Viktor Jirsa
  10. Andrew Zalesky
(2021)
The structural connectome constrains fast brain dynamics
eLife 10:e67400.
https://doi.org/10.7554/eLife.67400

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