One-shot learning and behavioral eligibility traces in sequential decision making

  1. Marco P Lehmann  Is a corresponding author
  2. He A Xu
  3. Vasiliki Liakoni
  4. Michael H Herzog
  5. Wulfram Gerstner
  6. Kerstin Preuschoff
  1. École Polytechnique Fédérale de Lausanne, Switzerland
  2. University of Geneva, Switzerland

Abstract

In many daily tasks we make multiple decisions before reaching a goal. In order to learn such sequences of decisions, a mechanism to link earlier actions to later reward is necessary. Reinforcement learning theory suggests two classes of algorithms solving this credit assignment problem: In classic temporal-difference learning, earlier actions receive reward information only after multiple repetitions of the task, whereas models with eligibility traces reinforce entire sequences of actions from a single experience (one-shot). Here we show one-shot learning of sequences. We developed a novel paradigm to directly observe which actions and states along a multi-step sequence are reinforced after a single reward. By focusing our analysis on those states for which RL with and without eligibility trace make qualitatively distinct predictions, we find direct behavioral (choice probability) and physiological (pupil dilation) signatures of reinforcement learning with eligibility trace across multiple sensory modalities.

Data availability

The datasets generated during the current study are available on Dryad, at the following address https://dx.doi.org/10.5061/dryad.j7h6f69

The following data sets were generated

Article and author information

Author details

  1. Marco P Lehmann

    School of Life Sciences, École Polytechnique Fédérale de Lausanne, Lausanne, Switzerland
    For correspondence
    marco.lehmann@alumni.epfl.ch
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5274-144X
  2. He A Xu

    School of Life Sciences, École Polytechnique Fédérale de Lausanne, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  3. Vasiliki Liakoni

    School of Life Sciences, École Polytechnique Fédérale de Lausanne, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  4. Michael H Herzog

    School of Life Sciences, École Polytechnique Fédérale de Lausanne, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  5. Wulfram Gerstner

    School of Life Sciences, École Polytechnique Fédérale de Lausanne, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  6. Kerstin Preuschoff

    Swiss Center for Affective Sciences, University of Geneva, Genève, Switzerland
    Competing interests
    The authors declare that no competing interests exist.

Funding

Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (CRSII2 147636 (Sinergia))

  • Marco P Lehmann
  • He A Xu
  • Vasiliki Liakoni
  • Michael H Herzog
  • Wulfram Gerstner
  • Kerstin Preuschoff

Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (CRSII2 200020 165538)

  • Marco P Lehmann
  • Vasiliki Liakoni
  • Wulfram Gerstner

Horizon 2020 Framework Programme (Human Brain Project (SGA2) 785907)

  • Michael H Herzog
  • Wulfram Gerstner

H2020 European Research Council (268 689 MultiRules)

  • Wulfram Gerstner

Horizon 2020 Framework Programme (Human Brain Project (SGA1) 720270)

  • Michael H Herzog
  • Wulfram Gerstner

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

Ethics

Human subjects: Experiments were conducted in accordance with the Helsinki declaration and approved by the ethics commission of the Canton de Vaud (164/14 Titre: Aspects fondamentaux de la reconnaissance des objets : protocole général). All participants were informed about the general purpose of the experiment and provided written, informed consent. They were told that they could quit the experiment at any time they wish.

Copyright

© 2019, Lehmann et al.

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

  • 2,951
    views
  • 420
    downloads
  • 15
    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. Marco P Lehmann
  2. He A Xu
  3. Vasiliki Liakoni
  4. Michael H Herzog
  5. Wulfram Gerstner
  6. Kerstin Preuschoff
(2019)
One-shot learning and behavioral eligibility traces in sequential decision making
eLife 8:e47463.
https://doi.org/10.7554/eLife.47463

Share this article

https://doi.org/10.7554/eLife.47463

Further reading

    1. Neuroscience
    Brian C Ruyle, Sarah Masud ... Jose A Morón
    Research Article

    Millions of Americans suffering from Opioid Use Disorders face a high risk of fatal overdose due to opioid-induced respiratory depression (OIRD). Fentanyl, a powerful synthetic opioid, is a major contributor to the rising rates of overdose deaths. Reversing fentanyl overdoses has proved challenging due to its high potency and the rapid onset of OIRD. We assessed the contributions of central and peripheral mu opioid receptors (MORs) in mediating fentanyl-induced physiological responses. The peripherally restricted MOR antagonist naloxone methiodide (NLXM) both prevented and reversed OIRD to a degree comparable to that of naloxone (NLX), indicating substantial involvement of peripheral MORs to OIRD. Interestingly, NLXM-mediated OIRD reversal did not produce aversive behaviors observed after NLX. We show that neurons in the nucleus of the solitary tract (nTS), the first central synapse of peripheral afferents, exhibit a biphasic activity profile following fentanyl exposure. NLXM pretreatment attenuates this activity, suggesting that these responses are mediated by peripheral MORs. Together, these findings establish a critical role for peripheral MORs, including ascending inputs to the nTS, as sites of dysfunction during OIRD. Furthermore, selective peripheral MOR antagonism could be a promising therapeutic strategy for managing OIRD by sparing CNS-driven acute opioid-associated withdrawal and aversion observed after NLX.

    1. Neuroscience
    David C Williams, Amanda Chu ... Michael A McDannald
    Research Advance Updated

    Recognizing and responding to threat cues is essential to survival. Freezing is a predominant threat behavior in rats. We have recently shown that a threat cue can organize diverse behaviors beyond freezing, including locomotion (Chu et al., 2024). However, that experimental design was complex, required many sessions, and had rats receive many foot shock presentations. Moreover, the findings were descriptive. Here, we gave female and male Long Evans rats cue light illumination paired or unpaired with foot shock (eight total) in a conditioned suppression setting using a range of shock intensities (0.15, 0.25, 0.35, or 0.50 mA). We found that conditioned suppression was only observed at higher foot shock intensities (0.35 mA and 0.50 mA). We constructed comprehensive temporal ethograms by scoring 22,272 frames across 12 behavior categories in 200-ms intervals around cue light illumination. The 0.50 mA and 0.35 mA shock-paired visual cues suppressed reward seeking, rearing, and scaling, as well as light-directed rearing and light-directed scaling. These shock-paired visual cues further elicited locomotion and freezing. Linear discriminant analyses showed that ethogram data could accurately classify rats into paired and unpaired groups. Using complete ethogram data produced superior classification compared to behavior subsets, including an immobility subset featuring freezing. The results demonstrate diverse threat behaviors – in a short and simple procedure – containing sufficient information to distinguish the visual fear conditioning status of individual rats.