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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
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    References listed on IDEAS

    as
    1. Berens, Philipp, 2009. "CircStat: A MATLAB Toolbox for Circular Statistics," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 31(i10).
    2. 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.
    3. 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.
    4. 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.
    5. 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.
    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.
    7. 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.
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    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.

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