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.

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).

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.

Metrics

  • 2,053
    views
  • 375
    downloads
  • 7
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  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

Further reading

    1. Medicine
    2. Neuroscience
    LeYuan Gu, WeiHui Shao ... HongHai Zhang
    Research Article

    The advent of midazolam holds profound implications for modern clinical practice. The hypnotic and sedative effects of midazolam afford it broad clinical applicability. However, the specific mechanisms underlying the modulation of altered consciousness by midazolam remain elusive. Herein, using pharmacology, optogenetics, chemogenetics, fiber photometry, and gene knockdown, this in vivo research revealed the role of locus coeruleus (LC)-ventrolateral preoptic nucleus noradrenergic neural circuit in regulating midazolam-induced altered consciousness. This effect was mediated by α1 adrenergic receptors. Moreover, gamma-aminobutyric acid receptor type A (GABAA-R) represents a mechanistically crucial binding site in the LC for midazolam. These findings will provide novel insights into the neural circuit mechanisms underlying the recovery of consciousness after midazolam administration and will help guide the timing of clinical dosing and propose effective intervention targets for timely recovery from midazolam-induced loss of consciousness.

    1. Neuroscience
    Samyogita Hardikar, Bronte Mckeown ... Jonathan Smallwood
    Research Article

    Complex macro-scale patterns of brain activity that emerge during periods of wakeful rest provide insight into the organisation of neural function, how these differentiate individuals based on their traits, and the neural basis of different types of self-generated thoughts. Although brain activity during wakeful rest is valuable for understanding important features of human cognition, its unconstrained nature makes it difficult to disentangle neural features related to personality traits from those related to the thoughts occurring at rest. Our study builds on recent perspectives from work on ongoing conscious thought that highlight the interactions between three brain networks – ventral and dorsal attention networks, as well as the default mode network. We combined measures of personality with state-of-the-art indices of ongoing thoughts at rest and brain imaging analysis and explored whether this ‘tri-partite’ view can provide a framework within which to understand the contribution of states and traits to observed patterns of neural activity at rest. To capture macro-scale relationships between different brain systems, we calculated cortical gradients to describe brain organisation in a low-dimensional space. Our analysis established that for more introverted individuals, regions of the ventral attention network were functionally more aligned to regions of the somatomotor system and the default mode network. At the same time, a pattern of detailed self-generated thought was associated with a decoupling of regions of dorsal attention from regions in the default mode network. Our study, therefore, establishes that interactions between attention systems and the default mode network are important influences on ongoing thought at rest and highlights the value of integrating contemporary perspectives on conscious experience when understanding patterns of brain activity at rest.