Navigable maps of structural brain networks across species

PLoS Comput Biol. 2020 Feb 3;16(2):e1007584. doi: 10.1371/journal.pcbi.1007584. eCollection 2020 Feb.

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Algorithms
  • Animals
  • Brain / anatomy & histology
  • Brain / physiology
  • Brain Mapping / methods*
  • Connectome*
  • Humans
  • Models, Neurological
  • Species Specificity

Grants and funding

We acknowledge financial support by the Sentinelle Nord project from the Canada First Research Excellence Fund (AA; sentinellenord.ulaval.ca; cfref-apogee.gc.ca), the Natural Sciences and Engineering Research Council of Canada (AA; Project 2019-05183; nserc-crsng.gc.ca), the Spanish "Juan de la Cierva-incorporación’" program (AA; Project IJCI-2016-30193; ciencia.gob.es), the James S. McDonnell Foundation Scholar Award in Complex System (MAS, grant number 220020363, jsmf.org), the Ministerio de Economía y Empresa (MAS; project FIS2016-76830-C2-2-P; mineco.gob.es), and the Ayudas Fundación BBVA a Equipos de Investigación Científica 2017 (MAS; project: Mapping Big Data Systems: embedding large complex networks in low-dimensional hidden metric spaces; fbbva.es). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.