Evolutionary shaping of human brain dynamics
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 WU-Minn Human Connectome Project: An overviewhttps://doi.org/10.1016/j.neuroimage.2013.05.041.
-
A macaque connectome for large-scale network simulations in TheVirtualBrainhttps://doi.org/10.1038/s41597-019-0129-z.
-
Open access resource for cellular-resolution analyses of corticocortical connectivity in the marmoset monkeyhttps://doi.org/10.1038/s41467-020-14858-0.
Article and author information
Author details
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
-
- 2,165
- views
-
- 394
- downloads
-
- 7
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
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)
Further reading
-
- Developmental Biology
- Neuroscience
During development axons undergo long-distance migrations as instructed by guidance molecules and their receptors, such as UNC-6/Netrin and UNC-40/DCC. Guidance cues act through long-range diffusive gradients (chemotaxis) or local adhesion (haptotaxis). However, how these discrete modes of action guide axons in vivo is poorly understood. Using time-lapse imaging of axon guidance in C. elegans, we demonstrate that UNC-6 and UNC-40 are required for local adhesion to an intermediate target and subsequent directional growth. Exogenous membrane-tethered UNC-6 is sufficient to mediate adhesion but not directional growth, demonstrating the separability of haptotaxis and chemotaxis. This conclusion is further supported by the endogenous UNC-6 distribution along the axon’s route. The intermediate and final targets are enriched in UNC-6 and separated by a ventrodorsal UNC-6 gradient. Continuous growth through the gradient requires UNC-40, which recruits UNC-6 to the growth cone tip. Overall, these data suggest that UNC-6 stimulates stepwise haptotaxis and chemotaxis in vivo.
-
- Neuroscience
Brain states fluctuate between exploratory and consummatory phases of behavior. These state changes affect both internal computation and the organism’s responses to sensory inputs. Understanding neuronal mechanisms supporting exploratory and consummatory states and their switching requires experimental control of behavioral shifts and collecting sufficient amounts of brain data. To achieve this goal, we developed the ThermoMaze, which exploits the animal’s natural warmth-seeking homeostatic behavior. By decreasing the floor temperature and selectively heating unmarked areas, we observed that mice avoided the aversive state by exploring the maze and finding the warm spot. In its design, the ThermoMaze is analogous to the widely used water maze but without the inconvenience of a wet environment and, therefore, allows the collection of physiological data in many trials. We combined the ThermoMaze with electrophysiology recording, and report that spiking activity of hippocampal CA1 neurons during sharp-wave ripple events encode the position of mice. Thus, place-specific firing is not confined to locomotion and associated theta oscillations but persist during waking immobility and sleep at the same location. The ThermoMaze will allow for detailed studies of brain correlates of immobility, preparatory–consummatory transitions, and open new options for studying behavior-mediated temperature homeostasis.