IDEAS home Printed from https://ideas.repec.org/a/plo/pcbi00/1007584.html
   My bibliography  Save this article

Navigable maps of structural brain networks across species

Author

Listed:
  • 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
    as

    Download full text from publisher

    File URL: https://journals.plos.org/ploscompbiol/article?id=10.1371/journal.pcbi.1007584
    Download Restriction: no

    File URL: https://journals.plos.org/ploscompbiol/article/file?id=10.1371/journal.pcbi.1007584&type=printable
    Download Restriction: no

    File URL: https://libkey.io/10.1371/journal.pcbi.1007584?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Guillermo Garc'ia-P'erez & Mari'an Bogu~n'a & Antoine Allard & M. 'Angeles Serrano, 2015. "The hidden hyperbolic geometry of international trade: World Trade Atlas 1870-2013," Papers 1512.02233, arXiv.org, revised May 2016.
    2. Caio Seguin & Adeel Razi & Andrew Zalesky, 2019. "Inferring neural signalling directionality from undirected structural connectomes," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    3. Shin-ya Takemura & Arjun Bharioke & Zhiyuan Lu & Aljoscha Nern & Shiv Vitaladevuni & Patricia K. Rivlin & William T. Katz & Donald J. Olbris & Stephen M. Plaza & Philip Winston & Ting Zhao & Jane Anne, 2013. "A visual motion detection circuit suggested by Drosophila connectomics," Nature, Nature, vol. 500(7461), pages 175-181, August.
    4. Andrea Avena-Koenigsberger & Xiaoran Yan & Artemy Kolchinsky & Martijn P van den Heuvel & Patric Hagmann & Olaf Sporns, 2019. "A spectrum of routing strategies for brain networks," PLOS Computational Biology, Public Library of Science, vol. 15(3), pages 1-24, March.
    5. Marián Boguñá & Fragkiskos Papadopoulos & Dmitri Krioukov, 2010. "Sustaining the Internet with hyperbolic mapping," Nature Communications, Nature, vol. 1(1), pages 1-8, December.
    6. Moritz Helmstaedter & Kevin L. Briggman & Srinivas C. Turaga & Viren Jain & H. Sebastian Seung & Winfried Denk, 2013. "Connectomic reconstruction of the inner plexiform layer in the mouse retina," Nature, Nature, vol. 500(7461), pages 168-174, August.
    7. Logan Harriger & Martijn P van den Heuvel & Olaf Sporns, 2012. "Rich Club Organization of Macaque Cerebral Cortex and Its Role in Network Communication," PLOS ONE, Public Library of Science, vol. 7(9), pages 1-13, September.
    8. Ahn, Yong-Yeol & Jeong, Hawoong & Kim, Beom Jun, 2006. "Wiring cost in the organization of a biological neuronal network," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 367(C), pages 531-537.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    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.

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    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. Yuhan Chen & Shengjun Wang & Claus C Hilgetag & Changsong Zhou, 2017. "Features of spatial and functional segregation and integration of the primate connectome revealed by trade-off between wiring cost and efficiency," PLOS Computational Biology, Public Library of Science, vol. 13(9), pages 1-37, September.
    3. Saha, Papri & Sarkar, Debasish, 2022. "Allometric scaling of von Neumann entropy in animal connectomes and its evolutionary aspect," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 600(C).
    4. Inna Čábelková & Luboš Smutka & Svitlana Rotterova & Olesya Zhytna & Vít Kluger & David Mareš, 2022. "The Sustainability of International Trade: The Impact of Ongoing Military Conflicts, Infrastructure, Common Language, and Economic Wellbeing in Post-Soviet Region," Sustainability, MDPI, vol. 14(17), pages 1-14, August.
    5. Toufiq Parag & Anirban Chakraborty & Stephen Plaza & Louis Scheffer, 2015. "A Context-Aware Delayed Agglomeration Framework for Electron Microscopy Segmentation," PLOS ONE, Public Library of Science, vol. 10(5), pages 1-19, May.
    6. Samy Castro & Wael El-Deredy & Demian Battaglia & Patricio Orio, 2020. "Cortical ignition dynamics is tightly linked to the core organisation of the human connectome," PLOS Computational Biology, Public Library of Science, vol. 16(7), pages 1-23, July.
    7. Dai, Liang & Derudder, Ben & Liu, Xingjian, 2018. "Transport network backbone extraction: A comparison of techniques," Journal of Transport Geography, Elsevier, vol. 69(C), pages 271-281.
    8. Wang, Zuxi & Wu, Yao & Li, Qingguang & Jin, Fengdong & Xiong, Wei, 2016. "Link prediction based on hyperbolic mapping with community structure for complex networks," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 450(C), pages 609-623.
    9. Daniel Soudry & Suraj Keshri & Patrick Stinson & Min-hwan Oh & Garud Iyengar & Liam Paninski, 2015. "Efficient "Shotgun" Inference of Neural Connectivity from Highly Sub-sampled Activity Data," PLOS Computational Biology, Public Library of Science, vol. 11(10), pages 1-30, October.
    10. Jen-Chun Hsiang & Ning Shen & Florentina Soto & Daniel Kerschensteiner, 2024. "Distributed feature representations of natural stimuli across parallel retinal pathways," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    11. Shang, Ke-ke & Small, Michael & Yan, Wei-sheng, 2017. "Link direction for link prediction," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 469(C), pages 767-776.
    12. Badhwar, Rahul & Bagler, Ganesh, 2017. "A distance constrained synaptic plasticity model of C. elegans neuronal network," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 469(C), pages 313-322.
    13. Ma, Lili & Jiang, Xin & Wu, Kaiyuan & Zhang, Zhanli & Tang, Shaoting & Zheng, Zhiming, 2012. "Surveying network community structure in the hidden metric space," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 391(1), pages 371-378.
    14. Wang, Zuxi & Li, Qingguang & Xiong, Wei & Jin, Fengdong & Wu, Yao, 2016. "Fast community detection based on sector edge aggregation metric model in hyperbolic space," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 452(C), pages 178-191.
    15. repec:hal:spmain:info:hdl:2441/6h7io1v56e8k4qtht2cuvjcfa5 is not listed on IDEAS
    16. Wang, Zuxi & Li, Qingguang & Jin, Fengdong & Xiong, Wei & Wu, Yao, 2016. "Hyperbolic mapping of complex networks based on community information," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 455(C), pages 104-119.
    17. Huang, Wei & Chen, Shengyong & Wang, Wanliang, 2014. "Navigation in spatial networks: A survey," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 393(C), pages 132-154.
    18. Béatrice Dedinger & Paul Girard, 2018. "RICardo World Trade Web, 1834-1938," Post-Print hal-03619636, HAL.
    19. Maksim Kitsak & Alexander Ganin & Ahmed Elmokashfi & Hongzhu Cui & Daniel A. Eisenberg & David L. Alderson & Dmitry Korkin & Igor Linkov, 2023. "Finding shortest and nearly shortest path nodes in large substantially incomplete networks by hyperbolic mapping," Nature Communications, Nature, vol. 14(1), pages 1-9, December.
    20. Kelly B. Yancey & Matthew P. Yancey, 0. "Bipartite communities via spectral partitioning," Journal of Combinatorial Optimization, Springer, vol. 0, pages 1-34.
    21. Pawanesh & Charu Sharma & Niteesh Sahni, 2024. "Explaining Indian Stock Market through Geometry of Scale free Networks," Papers 2404.04710, arXiv.org, revised Oct 2024.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:plo:pcbi00:1007584. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: ploscompbiol (email available below). General contact details of provider: https://journals.plos.org/ploscompbiol/ .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.