Cited by 215Functional Brain Connectivity StudiesAdvanced Neuroimaging Techniques and ApplicationsAdvanced MRI Techniques and Applications

Relating structure and function in the human brain: relative contributions of anatomy, stationary dynamics, and non-stationarities

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Messé, Arnaud, Rudrauf, David, Benali, Habib, Marrelec, Guillaume·2014·PLoS Computational Biology

Abstract

Investigating the relationship between brain structure and function is a central endeavor for neuroscience research. Yet, the mechanisms shaping this relationship largely remain to be elucidated and are highly debated. In particular, the existence and relative contributions of anatomical constraints and dynamical physiological mechanisms of different types remain to be established. We addressed this issue by systematically comparing functional connectivity (FC) from resting-state functional magnetic resonance imaging data with simulations from increasingly complex computational models, and by manipulating anatomical connectivity obtained from fiber tractography based on diffusion-weighted imaging. We hypothesized that FC reflects the interplay of at least three types of components: (i) a backbone of anatomical connectivity, (ii) a stationary dynamical regime directly driven by the underlying anatomy, and (iii) other stationary and non-stationary dynamics not directly related to the anatomy. We showed that anatomical connectivity alone accounts for up to 15% of FC variance; that there is a stationary regime accounting for up to an additional 20% of variance and that this regime can be associated to a stationary FC; that a simple stationary model of FC better explains FC than more complex models; and that there is a large remaining variance (around 65%), which must contain the non-stationarities of FC evidenced in the literature. We also show that homotopic connections across cerebral hemispheres, which are typically improperly estimated, play a strong role in shaping all aspects of FC, notably indirect connections and the topographic organization of brain networks.

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  • Interregional functional connectivity arises from anatomical projection strengths, correlated gene expression, and synaptic receptor densities.

    “Interregional FC arises from anatomical projection strengths (Messe et al., 2014; Shen et al., 2012), correlated gene expression (Richiardi et al., 2015), and synaptic receptor densities (Turk et al., 2016; van den Heuvel et al., 2016b)”
  • Both highly parameterized simulations and sparser analytic predictions of FC appear comparably effective.

    “Models can involve highly parameterized simulations of regional activity (Hansen et al., 2015; Messe et al., 2014; Sanz-Leon et al., 2015), or sparser analytic predictions of FC using graph metrics of mutual communication (Goni et al., 2014; Grayson et al., 2016) (although, both approaches appear to be comparably effective; see Figure 1D).”
  • Even the best-performing SC-FC models generally account for less than 50% of the variance in FC across the brain in both humans and non-human primates.

    “Even the best-performing SC-FC models generally account for less than 50% of the variance in FC across the brain in both humans and non-human primates (Grayson et al., 2016; Messe et al., 2014; Misic et al., 2015).”

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Authors
Messé, A., Rudrauf, D., Benali, H., & Marrelec, G.
Affiliations
Inserm (FR)
Corresponding author
Messé, Arnaud
Venue
PLoS Computational Biology
Published
2014-03-20
Volume
10
Issue
3
Pages
e1003530
ISSN
  • 1553-734X (ISSN-L)
  • 1553-7358
OpenAlex
W2022159725
Cited by
215
References
57
Citations by year
2026: 4 · 2025: 12 · 2024: 11 · 2023: 12 · 2022: 19 · 2021: 23 · 2020: 25 · 2019: 17 · 2018: 24 · 2017: 22 · 2016: 17 · 2015: 22 · 2014: 7
FWCI
12.64
Type
journal article
Language
en
Open access
Locations
  • PLoS Computational Biology (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • HAL (submittedVersion, cc-by)
  • RePEc: Research Papers in Economics (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
Funders
  • Princeton University
  • Universitat Pompeu Fabra
  • Institut National de la Santé et de la Recherche Médicale
  • Université de Lausanne
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
  • Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced Neuroimaging Techniques and Applications
  • Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced MRI Techniques and Applications
Keywords
structure-function relationship, functional connectivity, resting-state fMRI, structural connectivity, non-stationary dynamics, fiber tractography, interhemispheric connections, indirect connections, diffusion-weighted imaging
MeSH terms
Adult, Brain, Brain Mapping, Computer Simulation, Female, Hemodynamics, Humans, Magnetic Resonance Imaging, Male, Models, Neurological, Nerve Net, Neural Pathways, Reproducibility of Results, Diffusion Magnetic Resonance Imaging, Young Adult

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