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Hippocampal sharp-wave ripples correlate with periods of naturally occurring self-generated thoughts in humans

Author

Listed:
  • Takamitsu Iwata

    (Osaka University)

  • Takufumi Yanagisawa

    (Osaka University
    Osaka University)

  • Yuji Ikegaya

    (The University of Tokyo
    The University of Tokyo
    Center for Information and Neural Networks)

  • Jonathan Smallwood

    (Queen’s University)

  • Ryohei Fukuma

    (Osaka University
    Osaka University)

  • Satoru Oshino

    (Osaka University)

  • Naoki Tani

    (Osaka University)

  • Hui Ming Khoo

    (Osaka University)

  • Haruhiko Kishima

    (Osaka University)

Abstract

Core features of human cognition highlight the importance of the capacity to focus on information distinct from events in the here and now, such as mind wandering. However, the brain mechanisms that underpin these self-generated states remain unclear. An emerging hypothesis is that self-generated states depend on the process of memory replay, which is linked to sharp-wave ripples (SWRs), which are transient high-frequency oscillations originating in the hippocampus. Local field potentials were recorded from the hippocampus of 10 patients with epilepsy for up to 15 days, and experience sampling was used to describe their association with ongoing thought patterns. The SWR rates were higher during extended periods of time when participants’ ongoing thoughts were more vivid, less desirable, had more imaginable properties, and exhibited fewer correlations with an external task. These data suggest a role for SWR in the patterns of ongoing thoughts that humans experience in daily life.

Suggested Citation

  • Takamitsu Iwata & Takufumi Yanagisawa & Yuji Ikegaya & Jonathan Smallwood & Ryohei Fukuma & Satoru Oshino & Naoki Tani & Hui Ming Khoo & Haruhiko Kishima, 2024. "Hippocampal sharp-wave ripples correlate with periods of naturally occurring self-generated thoughts in humans," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-48367-1
    DOI: 10.1038/s41467-024-48367-1
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    References listed on IDEAS

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    1. Thomas Andrillon & Angus Burns & Teigane Mackay & Jennifer Windt & Naotsugu Tsuchiya, 2021. "Predicting lapses of attention with sleep-like slow waves," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    2. David G Jenkins & Pedro F Quintana-Ascencio, 2020. "A solution to minimum sample size for regressions," PLOS ONE, Public Library of Science, vol. 15(2), pages 1-15, February.
    3. A. Turnbull & H. T. Wang & C. Murphy & N. S. P. Ho & X. Wang & M. Sormaz & T. Karapanagiotidis & R. M. Leech & B. Bernhardt & D. S. Margulies & D. Vatansever & E. Jefferies & J. Smallwood, 2019. "Left dorsolateral prefrontal cortex supports context-dependent prioritisation of off-task thought," Nature Communications, Nature, vol. 10(1), pages 1-10, December.
    4. Brad E. Pfeiffer & David J. Foster, 2013. "Hippocampal place-cell sequences depict future paths to remembered goals," Nature, Nature, vol. 497(7447), pages 74-79, May.
    5. Anli A. Liu & Simon Henin & Saman Abbaspoor & Anatol Bragin & Elizabeth A. Buffalo & Jordan S. Farrell & David J. Foster & Loren M. Frank & Tamara Gedankien & Jean Gotman & Jennifer A. Guidera & Kari , 2022. "A consensus statement on detection of hippocampal sharp wave ripples and differentiation from other fast oscillations," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    6. David Tingley & Kathryn McClain & Ekin Kaya & Jordan Carpenter & György Buzsáki, 2021. "A metabolic function of the hippocampal sharp wave-ripple," Nature, Nature, vol. 597(7874), pages 82-86, September.
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