A model of hippocampal replay driven by experience and environmental structure facilitates spatial learning

  1. Nicolas Diekmann
  2. Sen Cheng  Is a corresponding author
  1. Ruhr University Bochum, Germany

Abstract

Replay of neuronal sequences in the hippocampus during resting states and sleep play an important role in learning and memory consolidation. Consistent with these functions, replay sequences have been shown to obey current spatial constraints. Nevertheless, replay does not necessarily reflect previous behavior and can construct never-experienced sequences. Here we propose a stochastic replay mechanism that prioritizes experiences based on three variables: 1. Experience strength, 2. experience similarity, and 3. inhibition of return. Using this prioritized replay mechanism to train reinforcement learning agents leads to far better performance than using random replay. Its performance is close to the state-of-the-art, but computationally intensive, algorithm by Mattar & Daw (2018). Importantly, our model reproduces diverse types of replay because of the stochasticity of the replay mechanism and experience-dependent differences between the three variables. In conclusion, a unified replay mechanism generates diverse replay statistics and is efficient in driving spatial learning.

Data availability

The current manuscript is a computational study, so no data have been generated for this manuscript. Modelling code has been made publicly available at https://github.com/sencheng/-Mechanisms-and-Functions-of-Hippocampal-Replay.

Article and author information

Author details

  1. Nicolas Diekmann

    Faculty of Computer Science, Ruhr University Bochum, Bochum, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3638-7617
  2. Sen Cheng

    Faculty of Computer Science, Ruhr University Bochum, Bochum, Germany
    For correspondence
    sen.cheng@rub.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6719-8029

Funding

Deutsche Forschungsgemeinschaft (419037518 - FOR 2812 P2)

  • Sen Cheng

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

© 2023, Diekmann & Cheng

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 2,774
    views
  • 343
    downloads
  • 8
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Nicolas Diekmann
  2. Sen Cheng
(2023)
A model of hippocampal replay driven by experience and environmental structure facilitates spatial learning
eLife 12:e82301.
https://doi.org/10.7554/eLife.82301

Share this article

https://doi.org/10.7554/eLife.82301

Further reading

    1. Neuroscience
    Jacob A Miller
    Insight

    When navigating environments with changing rules, human brain circuits flexibly adapt how and where we retain information to help us achieve our immediate goals.

    1. Neuroscience
    Franziska Auer, Katherine Nardone ... David Schoppik
    Research Article

    Cerebellar dysfunction leads to postural instability. Recent work in freely moving rodents has transformed investigations of cerebellar contributions to posture. However, the combined complexity of terrestrial locomotion and the rodent cerebellum motivate new approaches to perturb cerebellar function in simpler vertebrates. Here, we adapted a validated chemogenetic tool (TRPV1/capsaicin) to describe the role of Purkinje cells — the output neurons of the cerebellar cortex — as larval zebrafish swam freely in depth. We achieved both bidirectional control (activation and ablation) of Purkinje cells while performing quantitative high-throughput assessment of posture and locomotion. Activation modified postural control in the pitch (nose-up/nose-down) axis. Similarly, ablations disrupted pitch-axis posture and fin-body coordination responsible for climbs. Postural disruption was more widespread in older larvae, offering a window into emergent roles for the developing cerebellum in the control of posture. Finally, we found that activity in Purkinje cells could individually and collectively encode tilt direction, a key feature of postural control neurons. Our findings delineate an expected role for the cerebellum in postural control and vestibular sensation in larval zebrafish, establishing the validity of TRPV1/capsaicin-mediated perturbations in a simple, genetically tractable vertebrate. Moreover, by comparing the contributions of Purkinje cell ablations to posture in time, we uncover signatures of emerging cerebellar control of posture across early development. This work takes a major step towards understanding an ancestral role of the cerebellum in regulating postural maturation.