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

Author

Listed:
  • Beverly Setzer

    (Boston University
    Boston University)

  • Nina E. Fultz

    (Boston University
    Massachusetts General Hospital)

  • Daniel E. P. Gomez

    (Boston University
    Massachusetts General Hospital
    Harvard Medical School)

  • Stephanie D. Williams

    (Boston University)

  • Giorgio Bonmassar

    (Massachusetts General Hospital
    Harvard Medical School)

  • Jonathan R. Polimeni

    (Massachusetts General Hospital
    Harvard Medical School
    Massachusetts Institute of Technology)

  • Laura D. Lewis

    (Boston University
    Massachusetts General Hospital)

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.

Suggested Citation

  • Beverly Setzer & Nina E. Fultz & Daniel E. P. Gomez & Stephanie D. Williams & Giorgio Bonmassar & Jonathan R. Polimeni & Laura D. Lewis, 2022. "A temporal sequence of thalamic activity unfolds at transitions in behavioral arousal state," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-33010-8
    DOI: 10.1038/s41467-022-33010-8
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    References listed on IDEAS

    as
    1. Franz Weber & Yang Dan, 2016. "Circuit-based interrogation of sleep control," Nature, Nature, vol. 538(7623), pages 51-59, October.
    2. Michael J Prerau & Katie E Hartnack & Gabriel Obregon-Henao & Aaron Sampson & Margaret Merlino & Karen Gannon & Matt T Bianchi & Jeffrey M Ellenbogen & Patrick L Purdon, 2014. "Tracking the Sleep Onset Process: An Empirical Model of Behavioral and Physiological Dynamics," PLOS Computational Biology, Public Library of Science, vol. 10(10), pages 1-19, October.
    3. Eliana Vassena & James Deraeve & William H. Alexander, 2020. "Surprise, value and control in anterior cingulate cortex during speeded decision-making," Nature Human Behaviour, Nature, vol. 4(4), pages 412-422, April.
    4. Xiao Liu & Jacco A. de Zwart & Marieke L. Schölvinck & Catie Chang & Frank Q. Ye & David A. Leopold & Jeff H. Duyn, 2018. "Subcortical evidence for a contribution of arousal to fMRI studies of brain activity," Nature Communications, Nature, vol. 9(1), pages 1-10, December.
    5. Sakiko Honjoh & Shuntaro Sasai & Shannon S Schiereck & Hirotaka Nagai & Giulio Tononi & Chiara Cirelli, 2018. "Regulation of cortical activity and arousal by the matrix cells of the ventromedial thalamic nucleus," Nature Communications, Nature, vol. 9(1), pages 1-14, December.
    6. Michael J. Hawrylycz & Ed S. Lein & Angela L. Guillozet-Bongaarts & Elaine H. Shen & Lydia Ng & Jeremy A. Miller & Louie N. van de Lagemaat & Kimberly A. Smith & Amanda Ebbert & Zackery L. Riley & Chr, 2012. "An anatomically comprehensive atlas of the adult human brain transcriptome," Nature, Nature, vol. 489(7416), pages 391-399, September.
    7. N. D. Schiff & J. T. Giacino & K. Kalmar & J. D. Victor & K. Baker & M. Gerber & B. Fritz & B. Eisenberg & J. O’Connor & E. J. Kobylarz & S. Farris & A. Machado & C. McCagg & F. Plum & J. J. Fins & A., 2007. "Behavioural improvements with thalamic stimulation after severe traumatic brain injury," Nature, Nature, vol. 448(7153), pages 600-603, August.
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