IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v12y2021i1d10.1038_s41467-021-27323-3.html
   My bibliography  Save this article

Theta rhythmicity governs human behavior and hippocampal signals during memory-dependent tasks

Author

Listed:
  • Marije ter Wal

    (School of Psychology & Centre for Human Brain Health, University of Birmingham)

  • Juan Linde-Domingo

    (School of Psychology & Centre for Human Brain Health, University of Birmingham
    Max Planck Institute for Human Development)

  • Julia Lifanov

    (School of Psychology & Centre for Human Brain Health, University of Birmingham)

  • Frédéric Roux

    (School of Psychology & Centre for Human Brain Health, University of Birmingham)

  • Luca D. Kolibius

    (School of Psychology & Centre for Human Brain Health, University of Birmingham
    University of Glasgow)

  • Stephanie Gollwitzer

    (Universitätsklinikum Erlangen)

  • Johannes Lang

    (Universitätsklinikum Erlangen)

  • Hajo Hamer

    (Universitätsklinikum Erlangen)

  • David Rollings

    (Queen Elizabeth Hospital Birmingham)

  • Vijay Sawlani

    (Queen Elizabeth Hospital Birmingham)

  • Ramesh Chelvarajah

    (Queen Elizabeth Hospital Birmingham)

  • Bernhard Staresina

    (School of Psychology & Centre for Human Brain Health, University of Birmingham
    University of Oxford)

  • Simon Hanslmayr

    (School of Psychology & Centre for Human Brain Health, University of Birmingham
    University of Glasgow)

  • Maria Wimber

    (School of Psychology & Centre for Human Brain Health, University of Birmingham
    University of Glasgow)

Abstract

Memory formation and reinstatement are thought to lock to the hippocampal theta rhythm, predicting that encoding and retrieval processes appear rhythmic themselves. Here, we show that rhythmicity can be observed in behavioral responses from memory tasks, where participants indicate, using button presses, the timing of encoding and recall of cue-object associative memories. We find no evidence for rhythmicity in button presses for visual tasks using the same stimuli, or for questions about already retrieved objects. The oscillations for correctly remembered trials center in the slow theta frequency range (1-5 Hz). Using intracranial EEG recordings, we show that the memory task induces temporally extended phase consistency in hippocampal local field potentials at slow theta frequencies, but significantly more for remembered than forgotten trials, providing a potential mechanistic underpinning for the theta oscillations found in behavioral responses.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-27323-3
    DOI: 10.1038/s41467-021-27323-3
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-021-27323-3
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-021-27323-3?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. Julia Lifanov & Juan Linde-Domingo & Maria Wimber, 2021. "Feature-specific reaction times reveal a semanticisation of memories over time and with repeated remembering," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
    2. 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.
    3. Juan Linde-Domingo & Matthias S. Treder & Casper Kerrén & Maria Wimber, 2019. "Evidence that neural information flow is reversed between object perception and object reconstruction from memory," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    4. Laura Lee Colgin & Tobias Denninger & Marianne Fyhn & Torkel Hafting & Tora Bonnevie & Ole Jensen & May-Britt Moser & Edvard I. Moser, 2009. "Frequency of gamma oscillations routes flow of information in the hippocampus," Nature, Nature, vol. 462(7271), pages 353-357, November.
    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. Michael J. Kahana & Robert Sekuler & Jeremy B. Caplan & Matthew Kirschen & Joseph R. Madsen, 1999. "Human theta oscillations exhibit task dependence during virtual maze navigation," Nature, Nature, vol. 399(6738), pages 781-784, June.
    7. Berens, Philipp, 2009. "CircStat: A MATLAB Toolbox for Circular Statistics," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 31(i10).
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. 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.

    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. Chinnakkaruppan Adaikkan & Justin Joseph & Georgios Foustoukos & Jun Wang & Denis Polygalov & Roman Boehringer & Steven J. Middleton & Arthur J. Y. Huang & Li-Huei Tsai & Thomas J. McHugh, 2024. "Silencing CA1 pyramidal cells output reveals the role of feedback inhibition in hippocampal oscillations," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    2. 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.
    3. Vincent Douchamps & Matteo Volo & Alessandro Torcini & Demian Battaglia & Romain Goutagny, 2024. "Gamma oscillatory complexity conveys behavioral information in hippocampal networks," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    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. 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.
    6. Natalia Grion & Athena Akrami & Yangfang Zuo & Federico Stella & Mathew E Diamond, 2016. "Coherence between Rat Sensorimotor System and Hippocampus Is Enhanced during Tactile Discrimination," PLOS Biology, Public Library of Science, vol. 14(2), pages 1-26, February.
    7. Jennifer B Tennessen & Marla M Holt & Brianna M Wright & M Bradley Hanson & Candice K Emmons & Deborah A Giles & Jeffrey T Hogan & Sheila J Thornton & Volker B Deecke, 2023. "Divergent foraging strategies between populations of sympatric matrilineal killer whales," Behavioral Ecology, International Society for Behavioral Ecology, vol. 34(3), pages 373-386.
    8. Thomas Schreiner & Marit Petzka & Tobias Staudigl & Bernhard P. Staresina, 2023. "Respiration modulates sleep oscillations and memory reactivation in humans," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    9. Pengcheng Zhou & Shawn D Burton & Adam C Snyder & Matthew A Smith & Nathaniel N Urban & Robert E Kass, 2015. "Establishing a Statistical Link between Network Oscillations and Neural Synchrony," PLOS Computational Biology, Public Library of Science, vol. 11(10), pages 1-25, October.
    10. 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.
    11. Thomas Schreiner & Elisabeth Kaufmann & Soheyl Noachtar & Jan-Hinnerk Mehrkens & Tobias Staudigl, 2022. "The human thalamus orchestrates neocortical oscillations during NREM sleep," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    12. Mojtaba Chehelcheraghi & Cees van Leeuwen & Erik Steur & Chie Nakatani, 2017. "A neural mass model of cross frequency coupling," PLOS ONE, Public Library of Science, vol. 12(4), pages 1-19, April.
    13. Arthur Pewsey & Eduardo García-Portugués, 2021. "Recent advances in directional statistics," TEST: An Official Journal of the Spanish Society of Statistics and Operations Research, Springer;Sociedad de Estadística e Investigación Operativa, vol. 30(1), pages 1-58, March.
    14. César Henrique Mattos Pires & Felipe M. Pimenta & Carla A. D'Aquino & Osvaldo R. Saavedra & Xuerui Mao & Arcilan T. Assireu, 2020. "Coastal Wind Power in Southern Santa Catarina, Brazil," Energies, MDPI, vol. 13(19), pages 1-23, October.
    15. Alexis T Baria & Brian Maniscalco & Biyu J He, 2017. "Initial-state-dependent, robust, transient neural dynamics encode conscious visual perception," PLOS Computational Biology, Public Library of Science, vol. 13(11), pages 1-29, November.
    16. Matthijs J. Warrens & Bunga C. Pratiwi, 2016. "Kappa Coefficients for Circular Classifications," Journal of Classification, Springer;The Classification Society, vol. 33(3), pages 507-522, October.
    17. 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.
    18. Dhanya Parameshwaran & Upinder S Bhalla, 2013. "Theta Frequency Background Tunes Transmission but Not Summation of Spiking Responses," PLOS ONE, Public Library of Science, vol. 8(1), pages 1-12, January.
    19. Lombard, F. & Hawkins, Douglas M. & Potgieter, Cornelis J., 2017. "Sequential rank CUSUM charts for angular data," Computational Statistics & Data Analysis, Elsevier, vol. 105(C), pages 268-279.
    20. Masataka Sawayama & Shin'ya Nishida, 2018. "Material and shape perception based on two types of intensity gradient information," PLOS Computational Biology, Public Library of Science, vol. 14(4), pages 1-40, April.

    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:12:y:2021:i:1:d:10.1038_s41467-021-27323-3. 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.