IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-42642-3.html
   My bibliography  Save this article

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

Author

Listed:
  • 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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-42642-3
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-42642-3?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. 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.
    2. 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.
    3. 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.
    4. 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.
    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.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Taylor J. Malone & Nai-Wen Tien & Yan Ma & Lian Cui & Shangru Lyu & Garret Wang & Duc Nguyen & Kai Zhang & Maxym V. Myroshnychenko & Jean Tyan & Joshua A. Gordon & David A. Kupferschmidt & Yi Gu, 2024. "A consistent map in the medial entorhinal cortex supports spatial memory," Nature Communications, Nature, vol. 15(1), pages 1-22, December.
    2. Kyerl Park & Yoonsoo Yeo & Kisung Shin & Jeehyun Kwag, 2024. "Egocentric neural representation of geometric vertex in the retrosplenial cortex," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    3. Qiming Shao & Ligu Chen & Xiaowan Li & Miao Li & Hui Cui & Xiaoyue Li & Xinran Zhao & Yuying Shi & Qiang Sun & Kaiyue Yan & Guangfu Wang, 2024. "A non-canonical visual cortical-entorhinal pathway contributes to spatial navigation," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    4. Fabian Kessler & Julia Frankenstein & Constantin A. Rothkopf, 2024. "Human navigation strategies and their errors result from dynamic interactions of spatial uncertainties," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    5. Laurenz Muessig & Fabio Ribeiro Rodrigues & Tale L. Bjerknes & Benjamin W. Towse & Caswell Barry & Neil Burgess & Edvard I. Moser & May-Britt Moser & Francesca Cacucci & Thomas J. Wills, 2024. "Environment geometry alters subiculum boundary vector cell receptive fields in adulthood and early development," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    6. Simone Viganò & Rena Bayramova & Christian F. Doeller & Roberto Bottini, 2023. "Mental search of concepts is supported by egocentric vector representations and restructured grid maps," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    7. Isabella C. Wagner & Luise P. Graichen & Boryana Todorova & Andre Lüttig & David B. Omer & Matthias Stangl & Claus Lamm, 2023. "Entorhinal grid-like codes and time-locked network dynamics track others navigating through space," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    8. Noga Mosheiff & Haggai Agmon & Avraham Moriel & Yoram Burak, 2017. "An efficient coding theory for a dynamic trajectory predicts non-uniform allocation of entorhinal grid cells to modules," PLOS Computational Biology, Public Library of Science, vol. 13(6), pages 1-19, June.
    9. Saskia Kuliga & Martin Berwig & Martina Roes, 2021. "Wayfinding in People with Alzheimer’s Disease: Perspective Taking and Architectural Cognition—A Vision Paper on Future Dementia Care Research Opportunities," Sustainability, MDPI, vol. 13(3), pages 1-24, January.
    10. Balázs Ujfalussy & Tamás Kiss & Péter Érdi, 2009. "Parallel Computational Subunits in Dentate Granule Cells Generate Multiple Place Fields," PLOS Computational Biology, Public Library of Science, vol. 5(9), pages 1-16, September.
    11. Louis-Emmanuel Martinet & Denis Sheynikhovich & Karim Benchenane & Angelo Arleo, 2011. "Spatial Learning and Action Planning in a Prefrontal Cortical Network Model," PLOS Computational Biology, Public Library of Science, vol. 7(5), pages 1-21, May.
    12. Florian Raudies & Michael E Hasselmo, 2012. "Modeling Boundary Vector Cell Firing Given Optic Flow as a Cue," PLOS Computational Biology, Public Library of Science, vol. 8(6), pages 1-17, June.
    13. Avgar, Tal & Deardon, Rob & Fryxell, John M., 2013. "An empirically parameterized individual based model of animal movement, perception, and memory," Ecological Modelling, Elsevier, vol. 251(C), pages 158-172.
    14. Sabrina L. L. Maoz & Matthias Stangl & Uros Topalovic & Daniel Batista & Sonja Hiller & Zahra M. Aghajan & Barbara Knowlton & John Stern & Jean-Philippe Langevin & Itzhak Fried & Dawn Eliashiv & Nanth, 2023. "Dynamic neural representations of memory and space during human ambulatory navigation," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    15. Alexander Thomas Keinath, 2016. "The Preferred Directions of Conjunctive Grid X Head Direction Cells in the Medial Entorhinal Cortex Are Periodically Organized," PLOS ONE, Public Library of Science, vol. 11(3), pages 1-11, March.
    16. Toon Van de Maele & Bart Dhoedt & Tim Verbelen & Giovanni Pezzulo, 2024. "A hierarchical active inference model of spatial alternation tasks and the hippocampal-prefrontal circuit," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    17. Federica Sigismondi & Yangwen Xu & Mattia Silvestri & Roberto Bottini, 2024. "Altered grid-like coding in early blind people," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    18. Netto, Vinicius M. & Brigatti, Edgardo & Meirelles, João & Ribeiro, Fabiano L. & Pace, Bruno & Cacholas, Caio & Sanches, Patricia Mara, 2018. "Cities, from information to interaction," SocArXiv jgz5d, Center for Open Science.
    19. Davide Spalla & Alessandro Treves & Charlotte N. Boccara, 2022. "Angular and linear speed cells in the parahippocampal circuits," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    20. Carina Curto & Vladimir Itskov, 2008. "Cell Groups Reveal Structure of Stimulus Space," PLOS Computational Biology, Public Library of Science, vol. 4(10), pages 1-13, October.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-42642-3. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.