Cited by 115Complex Network Analysis TechniquesFunctional Brain Connectivity StudiesAdvanced Neuroimaging Techniques and Applications

A spectrum of routing strategies for brain networks

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Avena-Koenigsberger, Andrea, Yan, Xiaoran, Kolchinsky, Artemy, van den Heuvel, Martijn P., Hagmann, Patric, Sporns, Olaf·2019·PLOS Computational Biology

Abstract

Communication of signals among nodes in a complex network poses fundamental problems of efficiency and cost. Routing of messages along shortest paths requires global information about the topology, while spreading by diffusion, which operates according to local topological features, is informationally "cheap" but inefficient. We introduce a stochastic model for network communication that combines local and global information about the network topology to generate biased random walks on the network. The model generates a continuous spectrum of dynamics that converge onto shortest-path and random-walk (diffusion) communication processes at the limiting extremes. We implement the model on two cohorts of human connectome networks and investigate the effects of varying the global information bias on the network's communication cost. We identify routing strategies that approach a (highly efficient) shortest-path communication process with a relatively small global information bias on the system's dynamics. Moreover, we show that the cost of routing messages from and to hub nodes varies as a function of the global information bias driving the system's dynamics. Finally, we implement the model to identify individual subject differences from a communication dynamics point of view. The present framework departs from the classical shortest paths vs. diffusion dichotomy, unifying both models under a single family of dynamical processes that differ by the extent to which global information about the network topology influences the routing patterns of neural signals traversing the network.

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  • Identification of shortest paths demands individual regions to possess global knowledge of structural connectivity, which is unlikely in decentralized systems such as the brain.

    “However, algorithmically, the identification of shortest paths demands individual regions to possess global knowledge of structural connectivity, a requirement unlikely to be met in decentralized systems such as the brain (Avena-Koenigsberger et al., 2019; Goñi et al., 2014; Seguin et al., 2018).”

    From Quantitative mapping of the brain’s structural connectivity using diffusion MRI tractography: A review (2022) · cites this paper as Avena-Koenigsberger et al., 2019

    The Introduction says that routing along shortest paths relies on all elements having information about the network’s global topology. The Discussion, however, calls it an open question how a brain system gains that information and raises the possibility that it learns about its topology through feedback; it does not establish that the requirement is unlikely to be met. (LLM, conf=0.86)

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Authors
Avena-Koenigsberger, A., Yan, X., Kolchinsky, A., van den Heuvel, M. P., Hagmann, P., & Sporns, O.
Affiliations
  • Indiana University Bloomington (US)
  • Santa Fe Institute (US)
  • Centre Hospitalier Universitaire Vaudois (CH)
Venue
PLOS Computational Biology
Published
2019-03-08
Volume
15
Issue
3
Pages
e1006833
ISSN
  • 1553-734X (ISSN-L)
  • 1553-7358
OpenAlex
W2795327628
Cited by
115
References
4
Citations by year
2026: 1 · 2025: 14 · 2024: 17 · 2023: 17 · 2022: 11 · 2021: 24 · 2020: 28 · 2019: 3
FWCI
7.64
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)
  • VU Research Portal (publishedVersion, other-oa)
  • PubMed (publishedVersion)
  • SERVAL (Université de Lausanne) (publishedVersion, cc-by)
  • arXiv (Cornell University) (submittedVersion)
  • IRIS (submittedVersion, cc-by)
  • RePEc: Research Papers in Economics (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
  • IUScholarWorks Open (Indiana University) (submittedVersion)
  • Amsterdam UMC (VU Amsterdam) - Institutional Repository (submittedVersion, other-oa)
  • Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
  • arXiv (Cornell University)
Funders
  • Nederlandse Organisatie voor Wetenschappelijk Onderzoek (452-16-015, 1U54MH091657)
  • Fondation Leenaards
  • National Institutes of Health (1U54‐MH‐091657)
  • McDonnell Center for Systems Neuroscience (1U54MH091657)
  • NIH Blueprint for Neuroscience Research (1U54-MH-091657)
  • National Center for Complementary and Integrative Health (R01AT009036)
Topics
  • Physical Sciences › Physics and Astronomy › Statistical and Nonlinear Physics › Complex Network Analysis Techniques
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
  • Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced Neuroimaging Techniques and Applications
Keywords
brain networks, network routing, biased random walk, shortest path, diffusion, communication overhead, human connectome, network hubs, individual differences, network topology
MeSH terms
Brain Mapping, Communication, Humans, Models, Neurological, Stochastic Processes, Cohort Studies, Connectome

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