Evolutionary shaping of human brain dynamics

Abstract
Data availability
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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

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Article and author information

Author details

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.

"This ORCID iD identifies the author of this article:" 0000-0002-2461-2760
James K Rilling

Department of Anthropology, Emory University, Atlanta, United States

Competing interests
The authors declare that no competing interests exist.
James A Roberts

QIMR Berghofer Medical Research Institute, Queensland, Australia

Competing interests
The authors declare that no competing interests exist.
Martijn van den Heuvel,

Department of Complex Traits Genetics, Vrije Universiteit Amsterdam, Amsterdam, Netherlands

Competing interests
The authors declare that no competing interests exist.
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.

"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

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.