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Hippocampal place-cell sequences depict future paths to remembered goals

Author

Listed:
  • Brad E. Pfeiffer

    (Johns Hopkins University School Of Medicine)

  • David J. Foster

    (Johns Hopkins University School Of Medicine)

Abstract

Effective navigation requires planning extended routes to remembered goal locations. Hippocampal place cells have been proposed to have a role in navigational planning, but direct evidence has been lacking. Here we show that before goal-directed navigation in an open arena, the rat hippocampus generates brief sequences encoding spatial trajectories strongly biased to progress from the subject’s current location to a known goal location. These sequences predict immediate future behaviour, even in cases in which the specific combination of start and goal locations is novel. These results indicate that hippocampal sequence events characterized previously in linearly constrained environments as ‘replay’ are also capable of supporting a goal-directed, trajectory-finding mechanism, which identifies important places and relevant behavioural paths, at specific times when memory retrieval is required, and in a manner that could be used to control subsequent navigational behaviour.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:nature:v:497:y:2013:i:7447:d:10.1038_nature12112
    DOI: 10.1038/nature12112
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    1. Hefei Guan & Steven J. Middleton & Takafumi Inoue & Thomas J. McHugh, 2021. "Lateralization of CA1 assemblies in the absence of CA3 input," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
    2. 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.
    3. 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.
    4. Zhewei Zhang & Yuji K. Takahashi & Marlian Montesinos-Cartegena & Thorsten Kahnt & Angela J. Langdon & Geoffrey Schoenbaum, 2024. "Expectancy-related changes in firing of dopamine neurons depend on hippocampus," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    5. 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.
    6. 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.
    7. Hong Yu & Xinkuan Xiang & Zongming Chen & Xu Wang & Jiaqi Dai & Xinxin Wang & Pengcheng Huang & Zheng-dong Zhao & Wei L. Shen & Haohong Li, 2021. "Periaqueductal gray neurons encode the sequential motor program in hunting behavior of mice," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    8. 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.
    9. 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.
    10. 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.
    11. Guillaume Viejo & Thomas Cortier & Adrien Peyrache, 2018. "Brain-state invariant thalamo-cortical coordination revealed by non-linear encoders," PLOS Computational Biology, Public Library of Science, vol. 14(3), pages 1-25, March.
    12. 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.
    13. John Palmer & Adam Keane & Pulin Gong, 2017. "Learning and executing goal-directed choices by internally generated sequences in spiking neural circuits," PLOS Computational Biology, Public Library of Science, vol. 13(7), pages 1-23, July.
    14. Georgy Antonov & Christopher Gagne & Eran Eldar & Peter Dayan, 2022. "Optimism and pessimism in optimised replay," PLOS Computational Biology, Public Library of Science, vol. 18(1), pages 1-32, January.
    15. Trygve Solstad & Hosam N Yousif & Terrence J Sejnowski, 2014. "Place Cell Rate Remapping by CA3 Recurrent Collaterals," PLOS Computational Biology, Public Library of Science, vol. 10(6), pages 1-10, June.
    16. 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.
    17. 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.
    18. 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.
    19. Bahaaeddin Attaallah & Pierre Petitet & Rhea Zambellas & Sofia Toniolo & Maria Raquel Maio & Akke Ganse-Dumrath & Sarosh R. Irani & Sanjay G. Manohar & Masud Husain, 2024. "The role of the human hippocampus in decision-making under uncertainty," Nature Human Behaviour, Nature, vol. 8(7), pages 1366-1382, July.

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