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Hippocampal ensembles represent sequential relationships among an extended sequence of nonspatial events

Author

Listed:
  • Babak Shahbaba

    (University of California
    University of California
    University of California)

  • Lingge Li

    (University of California
    University of California)

  • Forest Agostinelli

    (University of California
    University of California
    University of South Carolina)

  • Mansi Saraf

    (University of California
    University of California)

  • Keiland W. Cooper

    (University of California
    University of California)

  • Derenik Haghverdian

    (University of California)

  • Gabriel A. Elias

    (University of California
    University of California)

  • Pierre Baldi

    (University of California
    University of California)

  • Norbert J. Fortin

    (University of California
    University of California
    University of California)

Abstract

The hippocampus is critical to the temporal organization of our experiences. Although this fundamental capacity is conserved across modalities and species, its underlying neuronal mechanisms remain unclear. Here we recorded hippocampal activity as rats remembered an extended sequence of nonspatial events unfolding over several seconds, as in daily life episodes in humans. We then developed statistical machine learning methods to analyze the ensemble activity and discovered forms of sequential organization and coding important for order memory judgments. Specifically, we found that hippocampal ensembles provide significant temporal coding throughout nonspatial event sequences, differentiate distinct types of task-critical information sequentially within events, and exhibit theta-associated reactivation of the sequential relationships among events. We also demonstrate that nonspatial event representations are sequentially organized within individual theta cycles and precess across successive cycles. These findings suggest a fundamental function of the hippocampal network is to encode, preserve, and predict the sequential order of experiences.

Suggested Citation

  • Babak Shahbaba & Lingge Li & Forest Agostinelli & Mansi Saraf & Keiland W. Cooper & Derenik Haghverdian & Gabriel A. Elias & Pierre Baldi & Norbert J. Fortin, 2022. "Hippocampal ensembles represent sequential relationships among an extended sequence of nonspatial events," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-28057-6
    DOI: 10.1038/s41467-022-28057-6
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    References listed on IDEAS

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    1. Albert Tsao & Jørgen Sugar & Li Lu & Cheng Wang & James J. Knierim & May-Britt Moser & Edvard I. Moser, 2018. "Integrating time from experience in the lateral entorhinal cortex," Nature, Nature, vol. 561(7721), pages 57-62, September.
    2. Chenguang Zheng & Ernie Hwaun & Carlos A. Loza & Laura Lee Colgin, 2021. "Hippocampal place cell sequences differ during correct and error trials in a spatial memory task," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    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.
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    Cited by:

    1. Huixin Lin & Jingfeng Zhou, 2024. "Hippocampal and orbitofrontal neurons contribute to complementary aspects of associative structure," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    2. Maanasa Jayachandran & Tatiana D. Viena & Andy Garcia & Abdiel Vasallo Veliz & Sofia Leyva & Valentina Roldan & Robert P. Vertes & Timothy A. Allen, 2023. "Nucleus reuniens transiently synchronizes memory networks at beta frequencies," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    3. Kevin K. Sit & Michael J. Goard, 2023. "Coregistration of heading to visual cues in retrosplenial cortex," Nature Communications, Nature, vol. 14(1), pages 1-15, December.

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