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Acetylcholine modulates the temporal dynamics of human theta oscillations during memory

Author

Listed:
  • Tamara Gedankien

    (Columbia University)

  • Ryan Joseph Tan

    (University of Texas Southwestern)

  • Salman Ehtesham Qasim

    (Icahn School of Medicine at Mount Sinai)

  • Haley Moore

    (University of Texas Southwestern)

  • David McDonagh

    (University of Texas Southwestern)

  • Joshua Jacobs

    (Columbia University
    Columbia University)

  • Bradley Lega

    (University of Texas Southwestern)

Abstract

The cholinergic system is essential for memory. While degradation of cholinergic pathways characterizes memory-related disorders such as Alzheimer’s disease, the neurophysiological mechanisms linking the cholinergic system to human memory remain unknown. Here, combining intracranial brain recordings with pharmacological manipulation, we describe the neurophysiological effects of a cholinergic blocker, scopolamine, on the human hippocampal formation during episodic memory. We found that the memory impairment caused by scopolamine was coupled to disruptions of both the amplitude and phase alignment of theta oscillations (2–10 Hz) during encoding. Across individuals, the severity of theta phase disruption correlated with the magnitude of memory impairment. Further, cholinergic blockade disrupted connectivity within the hippocampal formation. Our results indicate that cholinergic circuits support memory by coordinating the temporal dynamics of theta oscillations across the hippocampal formation. These findings expand our mechanistic understanding of the neurophysiology of human memory and offer insights into potential treatments for memory-related disorders.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41025-y
    DOI: 10.1038/s41467-023-41025-y
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    References listed on IDEAS

    as
    1. Gray Umbach & Ryan Tan & Joshua Jacobs & Brad E. Pfeiffer & Bradley Lega, 2022. "Flexibility of functional neuronal assemblies supports human memory," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    2. 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.
    3. Ueli Rutishauser & Ian B. Ross & Adam N. Mamelak & Erin M. Schuman, 2010. "Human memory strength is predicted by theta-frequency phase-locking of single neurons," Nature, Nature, vol. 464(7290), pages 903-907, April.
    4. Soraya L. S. Dunn & Stephen M. Town & Jennifer K. Bizley & Daniel Bendor, 2022. "Behaviourally modulated hippocampal theta oscillations in the ferret persist during both locomotion and immobility," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    5. Marije ter Wal & Juan Linde-Domingo & Julia Lifanov & Frédéric Roux & Luca D. Kolibius & Stephanie Gollwitzer & Johannes Lang & Hajo Hamer & David Rollings & Vijay Sawlani & Ramesh Chelvarajah & Bernh, 2021. "Theta rhythmicity governs human behavior and hippocampal signals during memory-dependent tasks," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    6. Abhinav Goyal & Jonathan Miller & Salman E. Qasim & Andrew J. Watrous & Honghui Zhang & Joel M. Stein & Cory S. Inman & Robert E. Gross & Jon T. Willie & Bradley Lega & Jui-Jui Lin & Ashwini Sharan & , 2020. "Functionally distinct high and low theta oscillations in the human hippocampus," Nature Communications, Nature, vol. 11(1), pages 1-10, December.
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