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Evidence for increased parallel information transmission in human brain networks compared to macaques and male mice

Author

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  • Alessandra Griffa

    (Lausanne University Hospital and University of Lausanne
    École Polytechnique Fédérale De Lausanne (EPFL)
    University of Geneva)

  • Mathieu Mach

    (École Polytechnique Fédérale De Lausanne (EPFL))

  • Julien Dedelley

    (École Polytechnique Fédérale De Lausanne (EPFL))

  • Daniel Gutierrez-Barragan

    (Functional Neuroimaging Laboratory, Center for Neuroscience and Cognitive systems, Istituto Italiano di Tecnologia)

  • Alessandro Gozzi

    (Functional Neuroimaging Laboratory, Center for Neuroscience and Cognitive systems, Istituto Italiano di Tecnologia)

  • Gilles Allali

    (Lausanne University Hospital and University of Lausanne)

  • Joanes Grandjean

    (Radboud University Medical Center
    Radboud University Medical Center)

  • Dimitri Ville

    (École Polytechnique Fédérale De Lausanne (EPFL)
    University of Geneva)

  • Enrico Amico

    (École Polytechnique Fédérale De Lausanne (EPFL)
    University of Geneva)

Abstract

Brain communication, defined as information transmission through white-matter connections, is at the foundation of the brain’s computational capacities that subtend almost all aspects of behavior: from sensory perception shared across mammalian species, to complex cognitive functions in humans. How did communication strategies in macroscale brain networks adapt across evolution to accomplish increasingly complex functions? By applying a graph- and information-theory approach to assess information-related pathways in male mouse, macaque and human brains, we show a brain communication gap between selective information transmission in non-human mammals, where brain regions share information through single polysynaptic pathways, and parallel information transmission in humans, where regions share information through multiple parallel pathways. In humans, parallel transmission acts as a major connector between unimodal and transmodal systems. The layout of information-related pathways is unique to individuals across different mammalian species, pointing at the individual-level specificity of information routing architecture. Our work provides evidence that different communication patterns are tied to the evolution of mammalian brain networks.

Suggested Citation

  • Alessandra Griffa & Mathieu Mach & Julien Dedelley & Daniel Gutierrez-Barragan & Alessandro Gozzi & Gilles Allali & Joanes Grandjean & Dimitri Ville & Enrico Amico, 2023. "Evidence for increased parallel information transmission in human brain networks compared to macaques and male mice," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43971-z
    DOI: 10.1038/s41467-023-43971-z
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    1. Andrea I. Luppi & Michael M. Craig & Ioannis Pappas & Paola Finoia & Guy B. Williams & Judith Allanson & John D. Pickard & Adrian M. Owen & Lorina Naci & David K. Menon & Emmanuel A. Stamatakis, 2019. "Consciousness-specific dynamic interactions of brain integration and functional diversity," Nature Communications, Nature, vol. 10(1), pages 1-12, December.
    2. Maria Giulia Preti & Dimitri Van De Ville, 2019. "Decoupling of brain function from structure reveals regional behavioral specialization in humans," Nature Communications, Nature, vol. 10(1), pages 1-7, December.
    3. 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.
    4. Jin Y. Yen, 1971. "Finding the K Shortest Loopless Paths in a Network," Management Science, INFORMS, vol. 17(11), pages 712-716, July.
    5. J. L. Vincent & G. H. Patel & M. D. Fox & A. Z. Snyder & J. T. Baker & D. C. Van Essen & J. M. Zempel & L. H. Snyder & M. Corbetta & M. E. Raichle, 2007. "Intrinsic functional architecture in the anaesthetized monkey brain," Nature, Nature, vol. 447(7140), pages 83-86, May.
    6. Casey Paquola & Reinder Vos De Wael & Konrad Wagstyl & Richard A I Bethlehem & Seok-Jun Hong & Jakob Seidlitz & Edward T Bullmore & Alan C Evans & Bratislav Misic & Daniel S Margulies & Jonathan Small, 2019. "Microstructural and functional gradients are increasingly dissociated in transmodal cortices," PLOS Biology, Public Library of Science, vol. 17(5), pages 1-28, May.
    7. Seung Wook Oh & Julie A. Harris & Lydia Ng & Brent Winslow & Nicholas Cain & Stefan Mihalas & Quanxin Wang & Chris Lau & Leonard Kuan & Alex M. Henry & Marty T. Mortrud & Benjamin Ouellette & Thuc Ngh, 2014. "A mesoscale connectome of the mouse brain," Nature, Nature, vol. 508(7495), pages 207-214, April.
    8. Marcus Kaiser & Claus C Hilgetag, 2006. "Nonoptimal Component Placement, but Short Processing Paths, due to Long-Distance Projections in Neural Systems," PLOS Computational Biology, Public Library of Science, vol. 2(7), pages 1-11, July.
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    1. Daniel Gutierrez-Barragan & Julian S. B. Ramirez & Stefano Panzeri & Ting Xu & Alessandro Gozzi, 2024. "Evolutionarily conserved fMRI network dynamics in the mouse, macaque, and human brain," Nature Communications, Nature, vol. 15(1), pages 1-16, December.

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