IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-54257-3.html
   My bibliography  Save this article

A hierarchical active inference model of spatial alternation tasks and the hippocampal-prefrontal circuit

Author

Listed:
  • Toon Van de Maele

    (Ghent University - imec
    VERSES Research Lab)

  • Bart Dhoedt

    (Ghent University - imec)

  • Tim Verbelen

    (VERSES Research Lab)

  • Giovanni Pezzulo

    (National Research Council)

Abstract

Cognitive problem-solving benefits from cognitive maps aiding navigation and planning. Physical space navigation involves hippocampal (HC) allocentric codes, while abstract task space engages medial prefrontal cortex (mPFC) task-specific codes. Previous studies show that challenging tasks, like spatial alternation, require integrating these two types of maps. The disruption of the HC-mPFC circuit impairs performance. We propose a hierarchical active inference model clarifying how this circuit solves spatial interaction tasks by bridging physical and task-space maps. Simulations demonstrate that the model’s dual layers develop effective cognitive maps for physical and task space. The model solves spatial alternation tasks through reciprocal interactions between the two layers. Disrupting its communication impairs decision-making, which is consistent with empirical evidence. Additionally, the model adapts to switching between multiple alternation rules, providing a mechanistic explanation of how the HC-mPFC circuit supports spatial alternation tasks and the effects of disruption.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-54257-3
    DOI: 10.1038/s41467-024-54257-3
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-54257-3
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-54257-3?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. Stefano Recanatesi & Matthew Farrell & Guillaume Lajoie & Sophie Deneve & Mattia Rigotti & Eric Shea-Brown, 2021. "Predictive learning as a network mechanism for extracting low-dimensional latent space representations," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    2. 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.
    3. Hiroshi T. Ito & Sheng-Jia Zhang & Menno P. Witter & Edvard I. Moser & May-Britt Moser, 2015. "A prefrontal–thalamo–hippocampal circuit for goal-directed spatial navigation," Nature, Nature, vol. 522(7554), pages 50-55, June.
    4. Dileep George & Rajeev V. Rikhye & Nishad Gothoskar & J. Swaroop Guntupalli & Antoine Dedieu & Miguel Lázaro-Gredilla, 2021. "Clone-structured graph representations enable flexible learning and vicarious evaluation of cognitive maps," Nature Communications, Nature, vol. 12(1), pages 1-17, December.
    5. Francesco Donnarumma & Domenico Maisto & Giovanni Pezzulo, 2016. "Problem Solving as Probabilistic Inference with Subgoaling: Explaining Human Successes and Pitfalls in the Tower of Hanoi," PLOS Computational Biology, Public Library of Science, vol. 12(4), pages 1-30, April.
    6. Raunak Basu & Robert Gebauer & Tim Herfurth & Simon Kolb & Zahra Golipour & Tatjana Tchumatchenko & Hiroshi T. Ito, 2021. "The orbitofrontal cortex maps future navigational goals," Nature, Nature, vol. 599(7885), pages 449-452, November.
    7. 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.
    8. Takuya Isomura & Kiyoshi Kotani & Yasuhiko Jimbo & Karl J. Friston, 2023. "Experimental validation of the free-energy principle with in vitro neural networks," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    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. Will D Penny & Peter Zeidman & Neil Burgess, 2013. "Forward and Backward Inference in Spatial Cognition," PLOS Computational Biology, Public Library of Science, vol. 9(12), pages 1-22, December.
    2. Lukas Grossberger & Francesco P Battaglia & Martin Vinck, 2018. "Unsupervised clustering of temporal patterns in high-dimensional neuronal ensembles using a novel dissimilarity measure," PLOS Computational Biology, Public Library of Science, vol. 14(7), pages 1-34, July.
    3. Alexander Nitsch & Mona M. Garvert & Jacob L. S. Bellmund & Nicolas W. Schuck & Christian F. Doeller, 2024. "Grid-like entorhinal representation of an abstract value space during prospective decision making," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    4. Jordan Crivelli-Decker & Alex Clarke & Seongmin A. Park & Derek J. Huffman & Erie D. Boorman & Charan Ranganath, 2023. "Goal-oriented representations in the human hippocampus during planning and navigation," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    5. Hannah Muysers & Hung-Ling Chen & Johannes Hahn & Shani Folschweiller & Torfi Sigurdsson & Jonas-Frederic Sauer & Marlene Bartos, 2024. "A persistent prefrontal reference frame across time and task rules," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    6. 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.
    7. J Matthew Mahoney & Ali S Titiz & Amanda E Hernan & Rod C Scott, 2016. "Short-Range Temporal Interactions in Sleep; Hippocampal Spike Avalanches Support a Large Milieu of Sequential Activity Including Replay," PLOS ONE, Public Library of Science, vol. 11(2), pages 1-25, February.
    8. 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.
    9. 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.
    10. Marta Huelin Gorriz & Masahiro Takigawa & Daniel Bendor, 2023. "The role of experience in prioritizing hippocampal replay," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    11. 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.
    12. Li Zheng & Zhiyao Gao & Andrew S. McAvan & Eve A. Isham & Arne D. Ekstrom, 2021. "Partially overlapping spatial environments trigger reinstatement in hippocampus and schema representations in prefrontal cortex," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    13. 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.
    14. Nicolas Cazin & Martin Llofriu Alonso & Pablo Scleidorovich Chiodi & Tatiana Pelc & Bruce Harland & Alfredo Weitzenfeld & Jean-Marc Fellous & Peter Ford Dominey, 2019. "Reservoir computing model of prefrontal cortex creates novel combinations of previous navigation sequences from hippocampal place-cell replay with spatial reward propagation," PLOS Computational Biology, Public Library of Science, vol. 15(7), pages 1-32, July.
    15. 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.
    16. 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.
    17. 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.
    18. 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.
    19. 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.
    20. 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.

    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:15:y:2024:i:1:d:10.1038_s41467-024-54257-3. 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.