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

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 functional magneti...

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Main Authors: Ana MG Manea, Anna Zilverstand, Kamil Ugurbil, Sarah R Heilbronner, Jan Zimmermann
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2022-03-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/75540
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author Ana MG Manea
Anna Zilverstand
Kamil Ugurbil
Sarah R Heilbronner
Jan Zimmermann
author_facet Ana MG Manea
Anna Zilverstand
Kamil Ugurbil
Sarah R Heilbronner
Jan Zimmermann
author_sort Ana MG Manea
collection DOAJ
description 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 functional magnetic resonance imaging (fMRI) performed at 10.5 T 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 (FC) 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 FC gradient topographies across the whole brain. We conclude that intrinsic timescales are a unifying organizational principle of neural processing across the whole brain.
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spelling doaj.art-8b64964c2a9244ab847fd52079a41f362022-12-22T03:52:04ZengeLife Sciences Publications LtdeLife2050-084X2022-03-011110.7554/eLife.75540Intrinsic timescales as an organizational principle of neural processing across the whole rhesus macaque brainAna MG Manea0https://orcid.org/0000-0002-4786-9657Anna Zilverstand1https://orcid.org/0000-0002-4889-9700Kamil Ugurbil2Sarah R Heilbronner3Jan Zimmermann4Department of Neuroscience, University of Minnesota, Minneapolis, United States; Center for Magnetic Resonance Research, University of Minnesota, Minneapolis, United StatesDepartment of Psychiatry & Behavioral Sciences , University of Minnesota, Minneapolis, United States; Medical Discovery Team on Addiction, University of Minnesota, Minneapolis, United StatesCenter for Magnetic Resonance Research, University of Minnesota, Minneapolis, United States; Center for Neuroengineering, University of Minnesota, Minneapolis, United States; Department of Radiology, University of Minnesota, Minneapolis, United StatesDepartment of Neuroscience, University of Minnesota, Minneapolis, United States; Medical Discovery Team on Addiction, University of Minnesota, Minneapolis, United States; Center for Neuroengineering, University of Minnesota, Minneapolis, United StatesDepartment of Neuroscience, University of Minnesota, Minneapolis, United States; Center for Magnetic Resonance Research, University of Minnesota, Minneapolis, United States; Medical Discovery Team on Addiction, University of Minnesota, Minneapolis, United States; Center for Neuroengineering, University of Minnesota, Minneapolis, United States; Department of Biomedical Engineering, University of Minnesota, Minneapolis, United StatesHierarchical 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 functional magnetic resonance imaging (fMRI) performed at 10.5 T 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 (FC) 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 FC gradient topographies across the whole brain. We conclude that intrinsic timescales are a unifying organizational principle of neural processing across the whole brain.https://elifesciences.org/articles/75540neural timescalesfunctional connectivityfMRIultrahigh filedresting-statespontaneous activity
spellingShingle Ana MG Manea
Anna Zilverstand
Kamil Ugurbil
Sarah R Heilbronner
Jan Zimmermann
Intrinsic timescales as an organizational principle of neural processing across the whole rhesus macaque brain
eLife
neural timescales
functional connectivity
fMRI
ultrahigh filed
resting-state
spontaneous activity
title Intrinsic timescales as an organizational principle of neural processing across the whole rhesus macaque brain
title_full Intrinsic timescales as an organizational principle of neural processing across the whole rhesus macaque brain
title_fullStr Intrinsic timescales as an organizational principle of neural processing across the whole rhesus macaque brain
title_full_unstemmed Intrinsic timescales as an organizational principle of neural processing across the whole rhesus macaque brain
title_short Intrinsic timescales as an organizational principle of neural processing across the whole rhesus macaque brain
title_sort intrinsic timescales as an organizational principle of neural processing across the whole rhesus macaque brain
topic neural timescales
functional connectivity
fMRI
ultrahigh filed
resting-state
spontaneous activity
url https://elifesciences.org/articles/75540
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