IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-53293-3.html
   My bibliography  Save this article

The brain hierarchically represents the past and future during multistep anticipation

Author

Listed:
  • Hannah Tarder-Stoll

    (Columbia University
    Baycrest Health Sciences)

  • Christopher Baldassano

    (Columbia University)

  • Mariam Aly

    (Columbia University
    University of California, Berkeley)

Abstract

Memory for temporal structure enables both planning of future events and retrospection of past events. We investigated how the brain flexibly represents extended temporal sequences into the past and future during anticipation. Participants learned sequences of environments in immersive virtual reality. Pairs of sequences had the same environments in a different order, enabling context-specific learning. During fMRI, participants anticipated upcoming environments multiple steps into the future in a given sequence. Temporal structure was represented in the hippocampus and across higher-order visual regions (1) bidirectionally, with graded representations into the past and future and (2) hierarchically, with further events into the past and future represented in successively more anterior brain regions. In hippocampus, these bidirectional representations were context-specific, and suppression of far-away environments predicted response time costs in anticipation. Together, this work sheds light on how we flexibly represent sequential structure to enable planning over multiple timescales.

Suggested Citation

  • Hannah Tarder-Stoll & Christopher Baldassano & Mariam Aly, 2024. "The brain hierarchically represents the past and future during multistep anticipation," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-53293-3
    DOI: 10.1038/s41467-024-53293-3
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-53293-3
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-53293-3?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. Fraser Aitken & Peter Kok, 2022. "Hippocampal representations switch from errors to predictions during acquisition of predictive associations," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    2. 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.
    3. G. Elliott Wimmer & Christian Büchel, 2019. "Learning of distant state predictions by the orbitofrontal cortex in humans," Nature Communications, Nature, vol. 10(1), pages 1-11, December.
    4. Adam Steel & Madeleine M. Billings & Edward H. Silson & Caroline E. Robertson, 2021. "A network linking scene perception and spatial memory systems in posterior cerebral cortex," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    5. Arno Klein & Satrajit S Ghosh & Forrest S Bao & Joachim Giard & Yrjö Häme & Eliezer Stavsky & Noah Lee & Brian Rossa & Martin Reuter & Elias Chaibub Neto & Anisha Keshavan, 2017. "Mindboggling morphometry of human brains," PLOS Computational Biology, Public Library of Science, vol. 13(2), pages 1-40, February.
    6. David J. Foster & Matthew A. Wilson, 2006. "Reverse replay of behavioural sequences in hippocampal place cells during the awake state," Nature, Nature, vol. 440(7084), pages 680-683, March.
    7. Adam Steel & Madeleine M. Billings & Edward H. Silson & Caroline E. Robertson, 2021. "Publisher Correction: A network linking scene perception and spatial memory systems in posterior cerebral cortex," Nature Communications, Nature, vol. 12(1), pages 1-1, December.
    8. Alison Montagrin & Denise E. Croote & Maria Giulia Preti & Liron Lerman & Mark G. Baxter & Daniela Schiller, 2024. "The hippocampus dissociates present from past and future goals," Nature Communications, Nature, vol. 15(1), pages 1-13, 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. Wilma A. Bainbridge & Chris I. Baker, 2022. "Multidimensional memory topography in the medial parietal cortex identified from neuroimaging of thousands of daily memory videos," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    2. Nir Moneta & Mona M. Garvert & Hauke R. Heekeren & Nicolas W. Schuck, 2023. "Task state representations in vmPFC mediate relevant and irrelevant value signals and their behavioral influence," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    3. Qi Huang & Zhibing Xiao & Qianqian Yu & Yuejia Luo & Jiahua Xu & Yukun Qu & Raymond Dolan & Timothy Behrens & Yunzhe Liu, 2024. "Replay-triggered brain-wide activation in humans," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    4. Serra E. Favila & Brice A. Kuhl & Jonathan Winawer, 2022. "Perception and memory have distinct spatial tuning properties in human visual cortex," Nature Communications, Nature, vol. 13(1), pages 1-21, December.
    5. Jeongho Park & Edward Soucy & Jennifer Segawa & Ross Mair & Talia Konkle, 2024. "Immersive scene representation in human visual cortex with ultra-wide-angle neuroimaging," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    6. 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.
    7. Jacob Tanner & Joshua Faskowitz & Andreia Sofia Teixeira & Caio Seguin & Ludovico Coletta & Alessandro Gozzi & Bratislav Mišić & Richard F. Betzel, 2024. "A multi-modal, asymmetric, weighted, and signed description of anatomical connectivity," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    8. Usman Farooq & George Dragoi, 2024. "Experience of Euclidean geometry sculpts the development and dynamics of rodent hippocampal sequential cell assemblies," Nature Communications, Nature, vol. 15(1), pages 1-24, December.
    9. Chaogan Yan & Dongqiang Liu & Yong He & Qihong Zou & Chaozhe Zhu & Xinian Zuo & Xiangyu Long & Yufeng Zang, 2009. "Spontaneous Brain Activity in the Default Mode Network Is Sensitive to Different Resting-State Conditions with Limited Cognitive Load," PLOS ONE, Public Library of Science, vol. 4(5), pages 1-11, May.
    10. Zachariah M. Reagh & Charan Ranganath, 2023. "Flexible reuse of cortico-hippocampal representations during encoding and recall of naturalistic events," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    11. 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.
    12. 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.
    13. 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.
    14. 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.
    15. 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.
    16. 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.
    17. Evan M. Russek & Rani Moran & Yunzhe Liu & Raymond J. Dolan & Quentin J. M. Huys, 2024. "Heuristics in risky decision-making relate to preferential representation of information," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    18. Demetrio Ferro & Tyler Cash-Padgett & Maya Zhe Wang & Benjamin Y. Hayden & Rubén Moreno-Bote, 2024. "Gaze-centered gating, reactivation, and reevaluation of economic value in orbitofrontal cortex," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    19. Buddhika Bellana & Abhijit Mahabal & Christopher J. Honey, 2022. "Narrative thinking lingers in spontaneous thought," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    20. Alpha Renner & Forrest Sheldon & Anatoly Zlotnik & Louis Tao & Andrew Sornborger, 2024. "The backpropagation algorithm implemented on spiking neuromorphic hardware," Nature Communications, Nature, vol. 15(1), pages 1-14, 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_s41467-024-53293-3. 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.