Evolutionary shaping of human brain dynamics

  1. James C Pang  Is a corresponding author
  2. James K Rilling
  3. James A Roberts
  4. Martijn van den Heuvel,
  5. Luca Cocchi  Is a corresponding author
  1. Monash University, Australia
  2. Emory University, United States
  3. QIMR Berghofer Medical Research Institute, Australia
  4. Vrije Universiteit Amsterdam, Netherlands

Abstract

The human brain is distinct from those of other species in terms of size, organization, and connectivity. How do structural evolutionary differences drive patterns of neural activity enabling brain function? Here, we combine brain imaging and biophysical modeling to show that the anatomical wiring of the human brain distinctly shapes neural dynamics. This shaping is characterized by a narrower distribution of dynamic ranges across brain regions compared with that of chimpanzees, our closest living primate relatives. We find that such a narrow dynamic range distribution supports faster integration between regions, particularly in transmodal systems. Conversely, a broad dynamic range distribution as seen in chimpanzees facilitates brain processes relying more on neural interactions within specialized local brain systems. These findings suggest that human brain dynamics have evolved to foster rapid associative processes in service of complex cognitive functions and behavior.

Data availability

All source data and MATLAB codes to perform sample simulations, analyze results, and generate the main and supplementary figures of this study are openly available at https://github.com/jchrispang/evolution-brain-tuning.

The following previously published data sets were used

Article and author information

Author details

  1. James C Pang

    Turner Institute for Brain and Mental Health, Monash University, Clayton, Australia
    For correspondence
    James.Pang1@monash.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2461-2760
  2. James K Rilling

    Department of Anthropology, Emory University, Atlanta, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. James A Roberts

    QIMR Berghofer Medical Research Institute, Queensland, Australia
    Competing interests
    The authors declare that no competing interests exist.
  4. Martijn van den Heuvel,

    Department of Complex Traits Genetics, Vrije Universiteit Amsterdam, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  5. Luca Cocchi

    Systems Neuroscience Group, QIMR Berghofer Medical Research Institute, Brisbane, Australia
    For correspondence
    Luca.Cocchi@qimrberghofer.edu.au
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3651-2676

Funding

National Health and Medical Research Council (11144936)

  • James A Roberts

National Health and Medical Research Council (1145168)

  • James A Roberts

Netherlands Organization for Scientific Research (ALWOP.179)

  • Martijn van den Heuvel,

Netherlands Organization for Scientific Research (VIDI (452-16-015))

  • Martijn van den Heuvel,

European Research Council (Consolidator grant 101001062)

  • Martijn van den Heuvel,

National Health and Medical Research Council (1138711)

  • Luca Cocchi

National Health and Medical Research Council (2001283)

  • Luca Cocchi

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Claus Hilgetag

Ethics

Animal experimentation: All data were taken from previously published studies and were approved by the respective oversighting ethics committees. Procedures were carried out in accordance with protocols approved by the Yerkes National Primate Research Center and the Emory University Institutional Animal Care and Use Committee (YER-2001206).

Human subjects: All data were taken from previously published studies and were approved by the respective oversighting ethics committees. Procedures were carried out in accordance with protocols approved by the Yerkes National Primate Research Center and the Emory University Institutional Animal Care and Use Committee (YER-2001206). All humans were recruited as healthy volunteers with no known neurological conditions and provided informed consent (IRB00000028).

Version history

  1. Received: May 27, 2022
  2. Preprint posted: June 8, 2022 (view preprint)
  3. Accepted: October 21, 2022
  4. Accepted Manuscript published: October 26, 2022 (version 1)
  5. Version of Record published: November 14, 2022 (version 2)

Copyright

© 2022, Pang et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. James C Pang
  2. James K Rilling
  3. James A Roberts
  4. Martijn van den Heuvel,
  5. Luca Cocchi
(2022)
Evolutionary shaping of human brain dynamics
eLife 11:e80627.
https://doi.org/10.7554/eLife.80627

Share this article

https://doi.org/10.7554/eLife.80627

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