A temporal sequence of thalamic activity unfolds at transitions in behavioral arousal state

Awakening from sleep reflects a profound transformation in neural activity and behavior. The thalamus is a key controller of arousal state, but whether its diverse nuclei exhibit coordinated or distinct activity at transitions in behavioral arousal state is unknown. Using fast fMRI at ultra-high fie...

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Published inNature communications Vol. 13; no. 1; pp. 5442 - 15
Main Authors Setzer, Beverly, Fultz, Nina E., Gomez, Daniel E. P., Williams, Stephanie D., Bonmassar, Giorgio, Polimeni, Jonathan R., Lewis, Laura D.
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 16.09.2022
Nature Publishing Group
Nature Portfolio
Subjects
59/36
59/57
631/378/1385/1877
631/378/2649
9/26
Arousal
Arousal - physiology
Behavior
Brain
Brain - diagnostic imaging
Brain mapping
Cortex (cingulate)
Deactivation
Functional magnetic resonance imaging
Humanities and Social Sciences
Humans
multidisciplinary
Nuclei
Science
Science (multidisciplinary)
Sleep
Sleep and wakefulness
Temporal lobe
Thalamic nuclei
Thalamic Nuclei - diagnostic imaging
Thalamic Nuclei - physiology
Thalamus
Thalamus - diagnostic imaging
Thalamus - physiology
Wakefulness
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Abstract Awakening from sleep reflects a profound transformation in neural activity and behavior. The thalamus is a key controller of arousal state, but whether its diverse nuclei exhibit coordinated or distinct activity at transitions in behavioral arousal state is unknown. Using fast fMRI at ultra-high field (7 Tesla), we measured sub-second activity across thalamocortical networks and within nine thalamic nuclei to delineate these dynamics during spontaneous transitions in behavioral arousal state. We discovered a stereotyped sequence of activity across thalamic nuclei and cingulate cortex that preceded behavioral arousal after a period of inactivity, followed by widespread deactivation. These thalamic dynamics were linked to whether participants subsequently fell back into unresponsiveness, with unified thalamic activation reflecting maintenance of behavior. These results provide an outline of the complex interactions across thalamocortical circuits that orchestrate behavioral arousal state transitions, and additionally, demonstrate that fast fMRI can resolve sub-second subcortical dynamics in the human brain. How the brain transitions between sleep and wakefulness is not well understood. Here, the authors discover that a sequence of activity unfolds across the thalamus before transitions from unresponsiveness to active behavior.
AbstractList Awakening from sleep reflects a profound transformation in neural activity and behavior. The thalamus is a key controller of arousal state, but whether its diverse nuclei exhibit coordinated or distinct activity at transitions in behavioral arousal state is unknown. Using fast fMRI at ultra-high field (7 Tesla), we measured sub-second activity across thalamocortical networks and within nine thalamic nuclei to delineate these dynamics during spontaneous transitions in behavioral arousal state. We discovered a stereotyped sequence of activity across thalamic nuclei and cingulate cortex that preceded behavioral arousal after a period of inactivity, followed by widespread deactivation. These thalamic dynamics were linked to whether participants subsequently fell back into unresponsiveness, with unified thalamic activation reflecting maintenance of behavior. These results provide an outline of the complex interactions across thalamocortical circuits that orchestrate behavioral arousal state transitions, and additionally, demonstrate that fast fMRI can resolve sub-second subcortical dynamics in the human brain.Awakening from sleep reflects a profound transformation in neural activity and behavior. The thalamus is a key controller of arousal state, but whether its diverse nuclei exhibit coordinated or distinct activity at transitions in behavioral arousal state is unknown. Using fast fMRI at ultra-high field (7 Tesla), we measured sub-second activity across thalamocortical networks and within nine thalamic nuclei to delineate these dynamics during spontaneous transitions in behavioral arousal state. We discovered a stereotyped sequence of activity across thalamic nuclei and cingulate cortex that preceded behavioral arousal after a period of inactivity, followed by widespread deactivation. These thalamic dynamics were linked to whether participants subsequently fell back into unresponsiveness, with unified thalamic activation reflecting maintenance of behavior. These results provide an outline of the complex interactions across thalamocortical circuits that orchestrate behavioral arousal state transitions, and additionally, demonstrate that fast fMRI can resolve sub-second subcortical dynamics in the human brain.
Awakening from sleep reflects a profound transformation in neural activity and behavior. The thalamus is a key controller of arousal state, but whether its diverse nuclei exhibit coordinated or distinct activity at transitions in behavioral arousal state is unknown. Using fast fMRI at ultra-high field (7 Tesla), we measured sub-second activity across thalamocortical networks and within nine thalamic nuclei to delineate these dynamics during spontaneous transitions in behavioral arousal state. We discovered a stereotyped sequence of activity across thalamic nuclei and cingulate cortex that preceded behavioral arousal after a period of inactivity, followed by widespread deactivation. These thalamic dynamics were linked to whether participants subsequently fell back into unresponsiveness, with unified thalamic activation reflecting maintenance of behavior. These results provide an outline of the complex interactions across thalamocortical circuits that orchestrate behavioral arousal state transitions, and additionally, demonstrate that fast fMRI can resolve sub-second subcortical dynamics in the human brain.
Awakening from sleep reflects a profound transformation in neural activity and behavior. The thalamus is a key controller of arousal state, but whether its diverse nuclei exhibit coordinated or distinct activity at transitions in behavioral arousal state is unknown. Using fast fMRI at ultra-high field (7 Tesla), we measured sub-second activity across thalamocortical networks and within nine thalamic nuclei to delineate these dynamics during spontaneous transitions in behavioral arousal state. We discovered a stereotyped sequence of activity across thalamic nuclei and cingulate cortex that preceded behavioral arousal after a period of inactivity, followed by widespread deactivation. These thalamic dynamics were linked to whether participants subsequently fell back into unresponsiveness, with unified thalamic activation reflecting maintenance of behavior. These results provide an outline of the complex interactions across thalamocortical circuits that orchestrate behavioral arousal state transitions, and additionally, demonstrate that fast fMRI can resolve sub-second subcortical dynamics in the human brain.How the brain transitions between sleep and wakefulness is not well understood. Here, the authors discover that a sequence of activity unfolds across the thalamus before transitions from unresponsiveness to active behavior.
Awakening from sleep reflects a profound transformation in neural activity and behavior. The thalamus is a key controller of arousal state, but whether its diverse nuclei exhibit coordinated or distinct activity at transitions in behavioral arousal state is unknown. Using fast fMRI at ultra-high field (7 Tesla), we measured sub-second activity across thalamocortical networks and within nine thalamic nuclei to delineate these dynamics during spontaneous transitions in behavioral arousal state. We discovered a stereotyped sequence of activity across thalamic nuclei and cingulate cortex that preceded behavioral arousal after a period of inactivity, followed by widespread deactivation. These thalamic dynamics were linked to whether participants subsequently fell back into unresponsiveness, with unified thalamic activation reflecting maintenance of behavior. These results provide an outline of the complex interactions across thalamocortical circuits that orchestrate behavioral arousal state transitions, and additionally, demonstrate that fast fMRI can resolve sub-second subcortical dynamics in the human brain. How the brain transitions between sleep and wakefulness is not well understood. Here, the authors discover that a sequence of activity unfolds across the thalamus before transitions from unresponsiveness to active behavior.
How the brain transitions between sleep and wakefulness is not well understood. Here, the authors discover that a sequence of activity unfolds across the thalamus before transitions from unresponsiveness to active behavior.
ArticleNumber 5442
Author Setzer, Beverly
Williams, Stephanie D.
Bonmassar, Giorgio
Fultz, Nina E.
Lewis, Laura D.
Polimeni, Jonathan R.
Gomez, Daniel E. P.
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  givenname: Laura D.
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  surname: Lewis
  fullname: Lewis, Laura D.
  email: ldlewis@bu.edu
  organization: Department of Biomedical Engineering, Boston University, Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital
BackLink https://www.ncbi.nlm.nih.gov/pubmed/36114170$$D View this record in MEDLINE/PubMed
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Snippet Awakening from sleep reflects a profound transformation in neural activity and behavior. The thalamus is a key controller of arousal state, but whether its...
How the brain transitions between sleep and wakefulness is not well understood. Here, the authors discover that a sequence of activity unfolds across the...
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SubjectTerms 59/36
59/57
631/378/1385/1877
631/378/2649
9/26
Arousal
Arousal - physiology
Behavior
Brain
Brain - diagnostic imaging
Brain mapping
Cortex (cingulate)
Deactivation
Functional magnetic resonance imaging
Humanities and Social Sciences
Humans
multidisciplinary
Nuclei
Science
Science (multidisciplinary)
Sleep
Sleep and wakefulness
Temporal lobe
Thalamic nuclei
Thalamic Nuclei - diagnostic imaging
Thalamic Nuclei - physiology
Thalamus
Thalamus - diagnostic imaging
Thalamus - physiology
Wakefulness
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Title A temporal sequence of thalamic activity unfolds at transitions in behavioral arousal state
URI https://link.springer.com/article/10.1038/s41467-022-33010-8
https://www.ncbi.nlm.nih.gov/pubmed/36114170
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https://pubmed.ncbi.nlm.nih.gov/PMC9481532
https://doaj.org/article/5b02c8fad5b3487b8393d553c377c71f
Volume 13
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