1. Neuroscience

Intrinsic timescales as an organizational principle of neural processing across the whole rhesus macaque brain

  1. Ana MG Manea  Is a corresponding author
  2. Anna Zilverstand
  3. Kamil Ugurbil
  4. Sarah Heilbronner
  5. Jan Zimmermann
  1. University of Minnesota, United States
https://doi.org/10.7554/eLife.75540
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  1. Ana MG Manea
  2. Anna Zilverstand
  3. Kamil Ugurbil
  4. Sarah Heilbronner
  5. Jan Zimmermann
(2022)
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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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

The following data sets were generated

Article and author information

Author details

  1. Ana MG Manea

    Department of Neuroscience, University of Minnesota, Minneapolis, United States
    For correspondence
    manea006@umn.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4786-9657

  2. Anna Zilverstand

    Department of Psychiatry and Behavioral Sciences, University of Minnesota, Minneapolis, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4889-9700

  3. Kamil Ugurbil

    Center for Magnetic Resonance Research, University of Minnesota, Minneapolis, United States
    Competing interests
    The authors declare that no competing interests exist.

  4. Sarah Heilbronner

    Department of Neuroscience, University of Minnesota, Minneapolis, United States
    Competing interests
    The authors declare that no competing interests exist.

  5. Jan Zimmermann

    Department of Neuroscience, University of Minnesota, Minneapolis, United States
    Competing interests
    The authors declare that no competing interests exist.

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

  1. 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

  1. Preprint posted: October 7, 2021 (view preprint)
  2. Received: November 13, 2021
  3. Accepted: February 28, 2022
  4. Accepted Manuscript published: March 2, 2022 (version 1)
  5. 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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  1. Ana MG Manea
  2. Anna Zilverstand
  3. Kamil Ugurbil
  4. Sarah Heilbronner
  5. Jan Zimmermann
(2022)
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

Share this article

https://doi.org/10.7554/eLife.75540

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