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Hippocampal firing fields anchored to a moving object predict homing direction during path-integration-based behavior

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  • Maryam Najafian Jazi

    (Medical Faculty of Heidelberg University and German Cancer Research Center)

  • Adrian Tymorek

    (Medical Faculty of Heidelberg University and German Cancer Research Center)

  • Ting-Yun Yen

    (Medical Faculty of Heidelberg University and German Cancer Research Center)

  • Felix Jose Kavarayil

    (Medical Faculty of Heidelberg University and German Cancer Research Center)

  • Moritz Stingl

    (Medical Faculty of Heidelberg University and German Cancer Research Center)

  • Sherman Richard Chau

    (Medical Faculty of Heidelberg University and German Cancer Research Center)

  • Benay Baskurt

    (Medical Faculty of Heidelberg University and German Cancer Research Center)

  • Celia García Vilela

    (Medical Faculty of Heidelberg University and German Cancer Research Center)

  • Kevin Allen

    (Medical Faculty of Heidelberg University and German Cancer Research Center)

Abstract

Homing based on path integration (H-PI) is a form of navigation in which an animal uses self-motion cues to keep track of its position and return to a starting point. Despite evidence for a role of the hippocampus in homing behavior, the hippocampal spatial representations associated with H-PI are largely unknown. Here we developed a homing task (AutoPI task) that required a mouse to find a randomly placed lever on an arena before returning to its home base. Recordings from the CA1 area in male mice showed that hippocampal neurons remap between random foraging and AutoPI task, between trials in light and dark conditions, and between search and homing behavior. During the AutoPI task, approximately 25% of the firing fields were anchored to the lever position. The activity of 24% of the cells with a lever-anchored field predicted the homing direction of the animal on each trial. Our results demonstrate that the activity of hippocampal neurons with object-anchored firing fields predicts homing behavior.

Suggested Citation

  • Maryam Najafian Jazi & Adrian Tymorek & Ting-Yun Yen & Felix Jose Kavarayil & Moritz Stingl & Sherman Richard Chau & Benay Baskurt & Celia García Vilela & Kevin Allen, 2023. "Hippocampal firing fields anchored to a moving object predict homing direction during path-integration-based behavior," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-42642-3
    DOI: 10.1038/s41467-023-42642-3
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    1. Johnson Ying & Alexandra T. Keinath & Raphael Lavoie & Erika Vigneault & Salah El Mestikawy & Mark P. Brandon, 2022. "Disruption of the grid cell network in a mouse model of early Alzheimer’s disease," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    2. Øyvind Arne Høydal & Emilie Ranheim Skytøen & Sebastian Ola Andersson & May-Britt Moser & Edvard I. Moser, 2019. "Object-vector coding in the medial entorhinal cortex," Nature, Nature, vol. 568(7752), pages 400-404, April.
    3. Matthias Stangl & Ingmar Kanitscheider & Martin Riemer & Ila Fiete & Thomas Wolbers, 2020. "Sources of path integration error in young and aging humans," Nature Communications, Nature, vol. 11(1), pages 1-15, December.
    4. Ravikrishnan P. Jayakumar & Manu S. Madhav & Francesco Savelli & Hugh T. Blair & Noah J. Cowan & James J. Knierim, 2019. "Recalibration of path integration in hippocampal place cells," Nature, Nature, vol. 566(7745), pages 533-537, February.
    5. Torkel Hafting & Marianne Fyhn & Sturla Molden & May-Britt Moser & Edvard I. Moser, 2005. "Microstructure of a spatial map in the entorhinal cortex," Nature, Nature, vol. 436(7052), pages 801-806, August.
    6. Emma R. Wood & Paul A. Dudchenko & Howard Eichenbaum, 1999. "The global record of memory in hippocampal neuronal activity," Nature, Nature, vol. 397(6720), pages 613-616, February.
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