Intrinsic timescales as an organizational principle of neural processing across the whole rhesus macaque brain
- University of Minnesota, United States
Abstract
Hierarchical temporal dynamics are a fundamental computational property of the brain; however, there are no whole-brain, noninvasive investigations into timescales of neural processing in animal models. To that end, we used the spatial resolution and sensitivity of ultrahigh field fMRI performed at 10.5 Tesla to probe timescales across the whole macaque brain. We uncovered within-species consistency between timescales estimated from fMRI and electrophysiology. Crucially, we extended existing electrophysiological hierarchies to whole brain topographies. Our results validate the complementary use of hemodynamic and electrophysiological intrinsic timescales, establishing a basis for future translational work. Further, with these results in hand, we were able to show that one facet of the high-dimensional functional connectivity topography of any region in the brain is closely related to hierarchical temporal dynamics. We demonstrated that intrinsic timescales are organized along spatial gradients that closely match functional connectivity gradient topographies across the whole brain. We conclude that intrinsic timescales are a unifying organizational principle of neural processing across the whole brain.
Data availability
The functional connectivity gradient maps and the timescale maps have been uploaded to figshare.Functional connectivity gradients: https://doi.org/10.6084/m9.figshare.19189331Intrinsic neural timescales: https://doi.org/10.6084/m9.figshare.19197026
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Resting-state functional connectivity gradients and intrinsic neural timescalesFigshare, 10.6084/m9.figshare.19189331.
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Resting-state functional connectivity gradients and intrinsic neural timescalesFigshare, 10.6084/m9.figshare.19197026.
Article and author information
Author details
Funding
NIH (P41 EB027061)
- Kamil Ugurbil
- Jan Zimmermann
NIH (R01 MH118257)
- Sarah Heilbronner
NIH (R56 EB031765)
- Jan Zimmermann
NIH (R01 MH128177)
- Jan Zimmermann
Digital Technologies Initiative
- Jan Zimmermann
Minnesota Institute of Robotics
- Jan Zimmermann
Young Investigator Awards from the Brain & Behavior Research Foundation
- Anna Zilverstand
- Sarah Heilbronner
NIH (P30DA048742)
- Anna Zilverstand
- Sarah Heilbronner
- Jan Zimmermann
UMN AIRP award
- Anna Zilverstand
- Sarah Heilbronner
- Jan Zimmermann
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Daeyeol Lee, Johns Hopkins University, United States
Ethics
Animal experimentation: Experimental procedures were carried out in accordance with the University of Minnesota Institutional Animal Care and Use Committee and the National Institute of Health standards for the care and use of nonhuman primates. Protocol IDs: 2005-38127A 2005-38135A 1911-37623A
Version history
- Preprint posted: October 7, 2021 (view preprint)
- Received: November 13, 2021
- Accepted: February 28, 2022
- Accepted Manuscript published: March 2, 2022 (version 1)
- Version of Record published: March 15, 2022 (version 2)
Copyright
© 2022, Manea 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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Intrinsic timescales as an organizational principle of neural processing across the whole rhesus macaque brain
eLife 11:e75540.
https://doi.org/10.7554/eLife.75540
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