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Navigable maps of structural brain networks across species

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  • Antoine Allard
  • M Ángeles Serrano

Abstract

Connectomes are spatially embedded networks whose architecture has been shaped by physical constraints and communication needs throughout evolution. Using a decentralized navigation protocol, we investigate the relationship between the structure of the connectomes of different species and their spatial layout. As a navigation strategy, we use greedy routing where nearest neighbors, in terms of geometric distance, are visited. We measure the fraction of successful greedy paths and their length as compared to shortest paths in the topology of connectomes. In Euclidean space, we find a striking difference between the navigability properties of mammalian and non-mammalian species, which implies the inability of Euclidean distances to fully explain the structural organization of their connectomes. In contrast, we find that hyperbolic space, the effective geometry of complex networks, provides almost perfectly navigable maps of connectomes for all species, meaning that hyperbolic distances are exceptionally congruent with the structure of connectomes. Hyperbolic maps therefore offer a quantitative meaningful representation of connectomes that suggests a new cartography of the brain based on the combination of its connectivity with its effective geometry rather than on its anatomy only. Hyperbolic maps also provide a universal framework to study decentralized communication processes in connectomes of different species and at different scales on an equal footing.Author summary: Recent advances in network science include the discovery that complex networks have a hidden geometry and that this geometry is hyperbolic. Studying complex networks through the lens of their effective hyperbolic geometry has led to valuable insights on the organization of a variety of complex systems ranging from the Internet to the metabolism of E. coli and humans. In this paper, we show that this methodology can also be used to infer high-quality maps of connectomes, where brain regions are given coordinates in hyperbolic space such that the closer they are the more likely that they are connected. Additionally, we find that, even if Euclidean space is typically assumed as the natural geometry of the brain, distances in hyperbolic space offer a more accurate interpretation of the structure of connectomes, which suggests a new perspective for the mapping of the organization of the brain’s neuroanatomical regions.

Suggested Citation

  • Antoine Allard & M Ángeles Serrano, 2020. "Navigable maps of structural brain networks across species," PLOS Computational Biology, Public Library of Science, vol. 16(2), pages 1-20, February.
  • Handle: RePEc:plo:pcbi00:1007584
    DOI: 10.1371/journal.pcbi.1007584
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    References listed on IDEAS

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    Cited by:

    1. Robert Jankowski & Antoine Allard & Marián Boguñá & M. Ángeles Serrano, 2023. "The D-Mercator method for the multidimensional hyperbolic embedding of real networks," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    2. Farnaz Zamani Esfahlani & Joshua Faskowitz & Jonah Slack & Bratislav Mišić & Richard F. Betzel, 2022. "Local structure-function relationships in human brain networks across the lifespan," Nature Communications, Nature, vol. 13(1), pages 1-16, December.

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