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Widespread theta synchrony and high-frequency desynchronization underlies enhanced cognition

Author

Listed:
  • E. A. Solomon

    (University of Pennsylvania)

  • J. E. Kragel

    (University of Pennsylvania)

  • M. R. Sperling

    (Thomas Jefferson University Hospital)

  • A. Sharan

    (Thomas Jefferson University Hospital)

  • G. Worrell

    (Mayo Clinic)

  • M. Kucewicz

    (Mayo Clinic)

  • C. S. Inman

    (Emory School of Medicine)

  • B. Lega

    (University of Texas Southwestern)

  • K. A. Davis

    (Hospital of the University of Pennsylvania)

  • J. M. Stein

    (Hospital of the University of Pennsylvania)

  • B. C. Jobst

    (Dartmouth Medical Center)

  • K. A. Zaghloul

    (National Institutes of Health)

  • S. A. Sheth

    (Columbia University Medical Center)

  • D. S. Rizzuto

    (University of Pennsylvania)

  • M. J. Kahana

    (University of Pennsylvania)

Abstract

The idea that synchronous neural activity underlies cognition has driven an extensive body of research in human and animal neuroscience. Yet, insufficient data on intracranial electrical connectivity has precluded a direct test of this hypothesis in a whole-brain setting. Through the lens of memory encoding and retrieval processes, we construct whole-brain connectivity maps of fast gamma (30–100 Hz) and slow theta (3–8 Hz) spectral neural activity, based on data from 294 neurosurgical patients fitted with indwelling electrodes. Here we report that gamma networks desynchronize and theta networks synchronize during encoding and retrieval. Furthermore, for nearly all brain regions we studied, gamma power rises as that region desynchronizes with gamma activity elsewhere in the brain, establishing gamma as a largely asynchronous phenomenon. The abundant phenomenon of theta synchrony is positively correlated with a brain region’s gamma power, suggesting a predominant low-frequency mechanism for inter-regional communication.

Suggested Citation

  • E. A. Solomon & J. E. Kragel & M. R. Sperling & A. Sharan & G. Worrell & M. Kucewicz & C. S. Inman & B. Lega & K. A. Davis & J. M. Stein & B. C. Jobst & K. A. Zaghloul & S. A. Sheth & D. S. Rizzuto & , 2017. "Widespread theta synchrony and high-frequency desynchronization underlies enhanced cognition," Nature Communications, Nature, vol. 8(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:8:y:2017:i:1:d:10.1038_s41467-017-01763-2
    DOI: 10.1038/s41467-017-01763-2
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    Cited by:

    1. Antoine Collomb-Clerc & Maëlle C. M. Gueguen & Lorella Minotti & Philippe Kahane & Vincent Navarro & Fabrice Bartolomei & Romain Carron & Jean Regis & Stephan Chabardès & Stefano Palminteri & Julien B, 2023. "Human thalamic low-frequency oscillations correlate with expected value and outcomes during reinforcement learning," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    2. Elizabeth L. Johnson & Jack J. Lin & David King-Stephens & Peter B. Weber & Kenneth D. Laxer & Ignacio Saez & Fady Girgis & Mark D’Esposito & Robert T. Knight & David Badre, 2023. "A rapid theta network mechanism for flexible information encoding," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    3. Marie-Christin Fellner & Stephanie Gollwitzer & Stefan Rampp & Gernot Kreiselmeyr & Daniel Bush & Beate Diehl & Nikolai Axmacher & Hajo Hamer & Simon Hanslmayr, 2019. "Spectral fingerprints or spectral tilt? Evidence for distinct oscillatory signatures of memory formation," PLOS Biology, Public Library of Science, vol. 17(7), pages 1-30, July.
    4. Zsuzsanna Kocsis & Rick L. Jenison & Peter N. Taylor & Ryan M. Calmus & Bob McMurray & Ariane E. Rhone & McCall E. Sarrett & Carolina Deifelt Streese & Yukiko Kikuchi & Phillip E. Gander & Joel I. Ber, 2023. "Immediate neural impact and incomplete compensation after semantic hub disconnection," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    5. Yuxuan Li & Jesse K. Pazdera & Michael J. Kahana, 2024. "EEG decoders track memory dynamics," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    6. Tamara Gedankien & Ryan Joseph Tan & Salman Ehtesham Qasim & Haley Moore & David McDonagh & Joshua Jacobs & Bradley Lega, 2023. "Acetylcholine modulates the temporal dynamics of human theta oscillations during memory," Nature Communications, Nature, vol. 14(1), pages 1-13, December.

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