Stress diminishes outcome but enhances response representations during instrumental learning

  1. Jacqueline Katharina Meier
  2. Bernhard P Staresina
  3. Lars Schwabe  Is a corresponding author
  1. Universität Hamburg, Germany
  2. University of Birmingham, United Kingdom

Abstract

Stress may shift behavioural control from a goal-directed system that encodes action-outcome relationships, to a habitual system that learns stimulus-response associations. Although this shift to habits is highly relevant for stress-related psychopathologies, limitations of existing behavioural paradigms hinders research from answering the fundamental question of whether the stress-induced bias to habits is due to reduced outcome processing, or enhanced response processing at the time of stimulus presentation - or both. Here, we used EEG-based multivariate pattern analysis to decode neural outcome representations crucial for goal-directed control, as well as response representations during instrumental learning. We show that stress reduced outcome representations but enhanced response representations. Both were directly associated with a behavioural index of habitual responding. Furthermore, changes in outcome and response representations were uncorrelated, suggesting that these may reflect distinct processes. Our findings indicate that habitual behaviour under stress may be the result of both enhanced stimulus-response processing and diminished outcome processing.

Data availability

Data reported in this manuscript are available from the website: https://github.com/08122019/From-goal-directed-action-to-habit.

Article and author information

Author details

  1. Jacqueline Katharina Meier

    Department of Cognitive Psychology, Universität Hamburg, Hamburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Bernhard P Staresina

    Department of Experimental Psychology, University of Birmingham, Birmingham, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0558-9745
  3. Lars Schwabe

    Department of Cognitive Psychology, Universität Hamburg, Hamburg, Germany
    For correspondence
    lars.schwabe@uni-hamburg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4429-4373

Funding

Deutsche Forschungsgemeinschaft (SCHW1357/23-1)

  • Lars Schwabe

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

Ethics

Human subjects: All participants provided informed consent before participation in the experiment. The experiment was performed in line with the Declaration of Helsinki and approved by the ethics committee of the Faculty of Psychology and Human Movement Sciences at the Universität Hamburg (2018_197_Schwabe).

Copyright

© 2022, Meier 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

  • 1,425
    views
  • 309
    downloads
  • 14
    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. Jacqueline Katharina Meier
  2. Bernhard P Staresina
  3. Lars Schwabe
(2022)
Stress diminishes outcome but enhances response representations during instrumental learning
eLife 11:e67517.
https://doi.org/10.7554/eLife.67517

Share this article

https://doi.org/10.7554/eLife.67517

Further reading

    1. Neuroscience
    Sven Ohl, Martin Rolfs
    Research Article

    Detecting causal relations structures our perception of events in the world. Here, we determined for visual interactions whether generalized (i.e. feature-invariant) or specialized (i.e. feature-selective) visual routines underlie the perception of causality. To this end, we applied a visual adaptation protocol to assess the adaptability of specific features in classical launching events of simple geometric shapes. We asked observers to report whether they observed a launch or a pass in ambiguous test events (i.e. the overlap between two discs varied from trial to trial). After prolonged exposure to causal launch events (the adaptor) defined by a particular set of features (i.e. a particular motion direction, motion speed, or feature conjunction), observers were less likely to see causal launches in subsequent ambiguous test events than before adaptation. Crucially, adaptation was contingent on the causal impression in launches as demonstrated by a lack of adaptation in non-causal control events. We assessed whether this negative aftereffect transfers to test events with a new set of feature values that were not presented during adaptation. Processing in specialized (as opposed to generalized) visual routines predicts that the transfer of visual adaptation depends on the feature similarity of the adaptor and the test event. We show that the negative aftereffects do not transfer to unadapted launch directions but do transfer to launch events of different speeds. Finally, we used colored discs to assign distinct feature-based identities to the launching and the launched stimulus. We found that the adaptation transferred across colors if the test event had the same motion direction as the adaptor. In summary, visual adaptation allowed us to carve out a visual feature space underlying the perception of causality and revealed specialized visual routines that are tuned to a launch’s motion direction.

    1. Neuroscience
    Gergely F Turi, Sasa Teng ... Yueqing Peng
    Research Article

    Synchronous neuronal activity is organized into neuronal oscillations with various frequency and time domains across different brain areas and brain states. For example, hippocampal theta, gamma, and sharp wave oscillations are critical for memory formation and communication between hippocampal subareas and the cortex. In this study, we investigated the neuronal activity of the dentate gyrus (DG) with optical imaging tools during sleep-wake cycles in mice. We found that the activity of major glutamatergic cell populations in the DG is organized into infraslow oscillations (0.01–0.03 Hz) during NREM sleep. Although the DG is considered a sparsely active network during wakefulness, we found that 50% of granule cells and about 25% of mossy cells exhibit increased activity during NREM sleep, compared to that during wakefulness. Further experiments revealed that the infraslow oscillation in the DG was correlated with rhythmic serotonin release during sleep, which oscillates at the same frequency but in an opposite phase. Genetic manipulation of 5-HT receptors revealed that this neuromodulatory regulation is mediated by Htr1a receptors and the knockdown of these receptors leads to memory impairment. Together, our results provide novel mechanistic insights into how the 5-HT system can influence hippocampal activity patterns during sleep.