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Dynamic Functional Connectivity between Order and Randomness and its Evolution across the Human Adult Lifespan

View ORCID ProfileDemian Battaglia, Thomas Boudou, Enrique C. A. Hansen, Diego Lombardo, Sabrina Chettouf, Andreas Daffertshofer, Anthony R. McIntosh, Joelle Zimmermann, Petra Ritter, Viktor Jirsa
doi: https://doi.org/10.1101/107243
Demian Battaglia
Université Aix-Marseille, INSERM UMR 1106, Institut de Neurosciences des Systèmes, F-13005 Marseille, France
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  • ORCID record for Demian Battaglia
  • For correspondence: demian.battaglia@univ-amu.fr
Thomas Boudou
Université Aix-Marseille, INSERM UMR 1106, Institut de Neurosciences des Systèmes, F-13005 Marseille, FranceENSTA ParisTech, F-91762 Palaiseau, France
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Enrique C. A. Hansen
Université Aix-Marseille, INSERM UMR 1106, Institut de Neurosciences des Systèmes, F-13005 Marseille, FranceEcole Normale Supérieure, Section de Neurosciences, F-75005 Paris, France
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Diego Lombardo
Université Aix-Marseille, INSERM UMR 1106, Institut de Neurosciences des Systèmes, F-13005 Marseille, France
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Sabrina Chettouf
Brain Simulation Section, Department of Neurology, Charité Universitätsmedizin and Berlin Institute of Health, D-10117 Berlin, GermanyBernstein Center for Computational Neuroscience, D-10117 Berlin, GermanyFaculty of Behavioural and Movement Sciences, Vrije Universiteit Amsterdam, 1081 BT Amsterdam, The Netherlands
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Andreas Daffertshofer
Faculty of Behavioural and Movement Sciences, Vrije Universiteit Amsterdam, 1081 BT Amsterdam, The Netherlands
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Anthony R. McIntosh
Rotman Research Institute, Baycrest Centre, Toronto, Ontario, M6A 2E1, Canada
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Joelle Zimmermann
Brain Simulation Section, Department of Neurology, Charité Universitätsmedizin and Berlin Institute of Health, D-10117 Berlin, GermanyRotman Research Institute, Baycrest Centre, Toronto, Ontario, M6A 2E1, Canada
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Petra Ritter
Brain Simulation Section, Department of Neurology, Charité Universitätsmedizin and Berlin Institute of Health, D-10117 Berlin, GermanyBernstein Center for Computational Neuroscience, D-10117 Berlin, Germany
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Viktor Jirsa
Université Aix-Marseille, INSERM UMR 1106, Institut de Neurosciences des Systèmes, F-13005 Marseille, France
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  • Abstract
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Abstract

Functional Connectivity (FC) in resting-state or task conditions is not frozen but inherently dynamic. Yet, there is no consensus on whether fluctuations in FC resemble isolated transitions between discrete FC states rather than continuous changes. This quarrel hampered advancing the study of dynamic FC. This is unfortunate as the structure of fluctuations in FC can provide crucial information about developmental changes, aging, or progression of pathologies. We merge the two perspectives and consider dynamic FC as continuous network reconfiguration, including a stochastic exploration of the space of possible steady FC states. The statistical properties of this random walk deviate both from an “order-driven” dynamics, in which the mean FC is preserved, and from a “randomness-driven” scenario, in which fluctuations of FC remain uncorrelated over time. Instead, dynamic FC turns out to have a complex structure endowed with long-range sequential correlations giving rise to transient slowing and acceleration epochs in the continuous flow of reconfiguration. When applying our analysis to an fMRI dataset in healthy elderly, we find that the dynamic FC tends to slow down, becomes less complex and more random with increasing age. All these effects are strongly associated with age-related changes in cognitive performance.

Highlights

  • Dynamic Functional Connectivity (dFC) at rest and during cognitive task performs a “complex” (anomalous) random walk.

  • Speed of dFC slows down with aging.

  • Resting dFC replaces complexity by randomness with aging.

  • Task performance correlates with the speed and complexity of dFC.

Footnotes

  • ↵+ Shared last authorship

  • Other e-mail addresses: Thomas Boudou, thomas.boudou{at}ensta-paristech.fr, Enrique C. A. Hansen, hansen{at}biologie.ens.fr, Diego Lombardo, diego.lombardo{at}univ-amu.fr, Sabrina Chettouf, sabrina.chettouf{at}charite.de, Andreas Daffertshofer, a.daffertshofer{at}vu.nl, A. Randal McIntosh, rmcintosh{at}research.baycrest.org, Joelle Zimmermann, jzimmermann{at}research.baycrest.org, Petra Ritter, petra.ritter{at}charite.de, Viktor Jirsa, viktor.jirsa{at}univ-amu.fr

  • This version replaces a previous preprint submitted in 2017. All analyses had to be repeated following discovery of problems in preprocessing. All results were confirmed, but, meanwhile, our understanding of the methods had considerably progressed, leading to major changes in our presentation (also taking in account new analyses). This manuscript is thus the first of a fully new diptych containing a comprehensive presentation of our current vision of dFC as a random walk in FC space with complex spatiotemporal structure.

  • Abbreviations

    rs
    resting-state
    RSN
    resting-state network
    fMRI
    functional magnetic resonance imaging
    BOLD
    blood oxygen level dependent
    SC
    structural connectivity
    FC
    functional connectivity
    dFC
    dynamic functional connectivity
    DFA
    detrended fluctuation analysis
    MoCA
    Montreal Cognitive Assessment
    SO
    spectral overlap
  • Copyright 
    The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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    Posted January 17, 2020.
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    Dynamic Functional Connectivity between Order and Randomness and its Evolution across the Human Adult Lifespan
    Demian Battaglia, Thomas Boudou, Enrique C. A. Hansen, Diego Lombardo, Sabrina Chettouf, Andreas Daffertshofer, Anthony R. McIntosh, Joelle Zimmermann, Petra Ritter, Viktor Jirsa
    bioRxiv 107243; doi: https://doi.org/10.1101/107243
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    Dynamic Functional Connectivity between Order and Randomness and its Evolution across the Human Adult Lifespan
    Demian Battaglia, Thomas Boudou, Enrique C. A. Hansen, Diego Lombardo, Sabrina Chettouf, Andreas Daffertshofer, Anthony R. McIntosh, Joelle Zimmermann, Petra Ritter, Viktor Jirsa
    bioRxiv 107243; doi: https://doi.org/10.1101/107243

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