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Theta phase precession supports memory formation and retrieval of naturalistic experience in humans

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Listed:
  • Jie Zheng

    (Cedars-Sinai Medical Center
    University of California, Davis
    University of California, Davis
    Harvard Medical School)

  • Mar Yebra

    (Cedars-Sinai Medical Center)

  • Andrea G. P. Schjetnan

    (University of Toronto)

  • Kramay Patel

    (University of Toronto)

  • Chaim N. Katz

    (University of Toronto)

  • Michael Kyzar

    (Cedars-Sinai Medical Center)

  • Clayton P. Mosher

    (Cedars-Sinai Medical Center)

  • Suneil K. Kalia

    (University of Toronto)

  • Jeffrey M. Chung

    (Cedars-Sinai Medical Center)

  • Chrystal M. Reed

    (Cedars-Sinai Medical Center)

  • Taufik A. Valiante

    (University of Toronto)

  • Adam N. Mamelak

    (Cedars-Sinai Medical Center)

  • Gabriel Kreiman

    (Harvard Medical School
    Harvard University)

  • Ueli Rutishauser

    (Cedars-Sinai Medical Center
    Cedars-Sinai Medical Center
    Cedars-Sinai Medical Center
    California Institute of Technology)

Abstract

Associating different aspects of experience with discrete events is critical for human memory. A potential mechanism for linking memory components is phase precession, during which neurons fire progressively earlier in time relative to theta oscillations. However, no direct link between phase precession and memory has been established. Here we recorded single-neuron activity and local field potentials in the human medial temporal lobe while participants (n = 22) encoded and retrieved memories of movie clips. Bouts of theta and phase precession occurred following cognitive boundaries during movie watching and following stimulus onsets during memory retrieval. Phase precession was dynamic, with different neurons exhibiting precession in different task periods. Phase precession strength provided information about memory encoding and retrieval success that was complementary with firing rates. These data provide direct neural evidence for a functional role of phase precession in human episodic memory.

Suggested Citation

  • Jie Zheng & Mar Yebra & Andrea G. P. Schjetnan & Kramay Patel & Chaim N. Katz & Michael Kyzar & Clayton P. Mosher & Suneil K. Kalia & Jeffrey M. Chung & Chrystal M. Reed & Taufik A. Valiante & Adam N., 2024. "Theta phase precession supports memory formation and retrieval of naturalistic experience in humans," Nature Human Behaviour, Nature, vol. 8(12), pages 2423-2436, December.
    • Handle: RePEc:nat:nathum:v:8:y:2024:i:12:d:10.1038_s41562-024-01983-9
    DOI: 10.1038/s41562-024-01983-9
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    References listed on IDEAS

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    1. M. R. Mehta & A. K. Lee & M. A. Wilson, 2002. "Role of experience and oscillations in transforming a rate code into a temporal code," Nature, Nature, vol. 417(6890), pages 741-746, June.
    2. Kenneth D. Harris & Darrell A. Henze & Hajime Hirase & Xavier Leinekugel & George Dragoi & Andras Czurkó & György Buzsáki, 2002. "Spike train dynamics predicts theta-related phase precession in hippocampal pyramidal cells," Nature, Nature, vol. 417(6890), pages 738-741, June.
    3. Dmitriy Aronov & Rhino Nevers & David W. Tank, 2017. "Mapping of a non-spatial dimension by the hippocampal–entorhinal circuit," Nature, Nature, vol. 543(7647), pages 719-722, March.
    4. Nathaniel J. Killian & Michael J. Jutras & Elizabeth A. Buffalo, 2012. "A map of visual space in the primate entorhinal cortex," Nature, Nature, vol. 491(7426), pages 761-764, November.
    5. John Huxter & Neil Burgess & John O'Keefe, 2003. "Independent rate and temporal coding in hippocampal pyramidal cells," Nature, Nature, vol. 425(6960), pages 828-832, October.
    6. Leila Reddy & Matthew W. Self & Benedikt Zoefel & Marlène Poncet & Jessy K. Possel & Judith C. Peters & Johannes C. Baayen & Sander Idema & Rufin VanRullen & Pieter R. Roelfsema, 2021. "Theta-phase dependent neuronal coding during sequence learning in human single neurons," Nature Communications, Nature, vol. 12(1), pages 1-9, December.
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