IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-41025-y.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-41025-y
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-41025-y?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    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. 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.
    5. 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.
    6. 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.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. 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.
    2. Dominik P. Koller & Michael Schirner & Petra Ritter, 2024. "Human connectome topology directs cortical traveling waves and shapes frequency gradients," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    3. Guillaume Etter & Suzanne Veldt & Jisoo Choi & Sylvain Williams, 2023. "Optogenetic frequency scrambling of hippocampal theta oscillations dissociates working memory retrieval from hippocampal spatiotemporal codes," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    4. Manuela Costa & Diego Lozano-Soldevilla & Antonio Gil-Nagel & Rafael Toledano & Carina R. Oehrn & Lukas Kunz & Mar Yebra & Costantino Mendez-Bertolo & Lennart Stieglitz & Johannes Sarnthein & Nikolai , 2022. "Aversive memory formation in humans involves an amygdala-hippocampus phase code," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    5. Cui, Kai & Li, Xinxue & Li, Gang, 2023. "What kind of fiscal policies and natural resources efficiency promotes green economic growth? Evidence from regression analysis," Resources Policy, Elsevier, vol. 85(PB).
    6. 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.
    7. 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.
    8. 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.
    9. Lin Zhang & Beibei Sun & Fei Shu & Ying Huang, 2022. "Comparing paper level classifications across different methods and systems: an investigation of Nature publications," Scientometrics, Springer;Akadémiai Kiadó, vol. 127(12), pages 7633-7651, December.
    10. Eriselda Vrapi & Xhevdet Zekaj, 2015. "Importance of Video Aids’ Usage in Teaching and Learning Process of English Language Classes," European Journal of Interdisciplinary Studies Articles, Revistia Research and Publishing, vol. 1, September.
    11. Qin, Ying-Mei & Che, Yan-Qiu & Zhao, Jia, 2018. "Effects of degree distributions on signal propagation in noisy feedforward neural networks," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 512(C), pages 763-774.
    12. Serena Scarpelli & Chiara Bartolacci & Aurora D’Atri & Maurizio Gorgoni & Luigi De Gennaro, 2019. "Mental Sleep Activity and Disturbing Dreams in the Lifespan," IJERPH, MDPI, vol. 16(19), pages 1-23, September.
    13. Yuxuan Li & Jesse K. Pazdera & Michael J. Kahana, 2024. "EEG decoders track memory dynamics," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    14. 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.
    15. 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.
    16. Weiwei Ding & Yuhong Zhang & Liya Huang, 2022. "Using a Novel Functional Brain Network Approach to Locate Important Nodes for Working Memory Tasks," IJERPH, MDPI, vol. 19(6), pages 1-14, March.
    17. Diego B. Piza & Benjamin W. Corrigan & Roberto A. Gulli & Sonia Carmo & A. Claudio Cuello & Lyle Muller & Julio Martinez-Trujillo, 2024. "Primacy of vision shapes behavioral strategies and neural substrates of spatial navigation in marmoset hippocampus," Nature Communications, Nature, vol. 15(1), pages 1-21, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41025-y. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.