Stress diminishes outcome but enhances response representations during instrumental learning

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Stress may shift behavioural control from a goal-directed system that encodes action-outcome relationships to a habit system that learns stimulus-response associations. Although this shift to habits is highly relevant for stress-related psychopathologies, limitations of existing behavioural paradigms hindered previous research to answer the fundamental question of whether the stress-induced bias to habits is due to impaired goal-directed or enhanced habitual processing (or both). Here, we leveraged EEG-based multivariate pattern analysis to decode neural outcome representations, crucial for goal-directed control, and response representations, essential for habitual responding, during instrumental learning. We show that stress reduces outcome representations but enhances response representations, both of which were directly associated with a behavioural index of habitual responding. Further, changes in outcome and response representations were uncorrelated, suggesting that these may reflect distinct processes. Our findings indicate that habit behaviour under stress is the result of both enhanced habitual and diminished goal-directed processing.

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  1. Reviewer #3 (Public Review):

    Meier et al. used electroencephalography (EEG) to test the mechanism underlying a well-known phenomenon where stress induces subjects to behave in a more habitual way during decision-making, as opposed to using a more deliberative goal-directed strategy. The authors tested two groups of human subjects who were randomly assigned to a stress manipulation or a similar control manipulation. These participants then carried out a reinforcement learning task where they had to choose between two alternative responses to a stimulus. On some blocks the value of one response would be 'devalued' such that the alternative action would be more appropriate. Participants who went through the stress manipulation were more likely to persist with an action that previously yielded a high reward outcome even when this response had been devalued - indicative of a failure in goal-directed decision-making. Critically, the authors associated responses and outcomes with stimuli that were decodable from EEG signals, making it possible to evaluate whether participants were prospectively considering the correct response or outcome prior to committing a response or receiving feedback. Meier et al. find that, over time, the stressed participants came to prospectively represent the coming response more and the outcome less, while the control group showed reduced prospective representation of the response. The degree of this change toward greater representation of responses versus outcomes across participants was also correlated with a more habit-based decision strategy in devaluation trials.

    Overall, this is a well-designed and sophisticated study that makes an important contribution to our understanding of the mechanism by which stress promotes more habit-like behavior, with broad implications for our understanding of how maladaptive behaviors might be formed in many clinical conditions. The conclusions are well supported by the data and confidence in the results is bolstered by several additional control measurements. However, I would have appreciated more effort to link this work to other related literature, as well as some more detail in some parts of the methods and additional control analyses to rule out alternative explanations for some of the main results of interest.

  2. Reviewer #2 (Public Review):

    A number of psychological states and traits have been demonstrated to render behavior under goal-directed or habitual control, stress being one of them. In this paper, using electroencephalography, the authors investigated the neural representations of stimulus, responses and outcomes in a task whose aim was to distinguish between the two types of behavioral control. By training a classifier to distinguish between neural signals related to the representations of instrumental responses and the outcomes produced by those responses, the authors found that during the last block of the experiment (after more extended training in the task), signals for outcome representations were weaker and response representations stronger in a stress-induced group compared to a control group. This is consistent with the idea that habits are performed when there is a stronger link between stimuli and responses that does not require a representation of the outcomes that follow from behavior. Although the methods of this paper are sound and the idea interesting and relevant for the current state of the art in habit research, it is not clear if the underlying theoretical contribution it should motivate is supported by the data produced by the experimental design employed by the authors.

  3. Reviewer #1 (Public Review):

    The authors used EEG-based multivariate pattern analysis and acute stress induction to assess the neural representations mediating a previously demonstrated influence of stress on the balance between goal-directed and habitual responding. They found that stress reduced neural outcome representations and enhanced response representations - results that are consistent with associative structures thought to mediate goal-directed and habitual response strategies, respectively. The study addresses an important and open question, and the combination of clinical, neural and behavioral assays is appealing. However, the interpretability, and thus impact, is threatened by an apparent lack of temporal synchrony between relevant measures, and by the potential effects of social feedback.

    Specifically, it is hard to understand how neural and behavioral devaluation differences between groups can be stress related given that they emerge at a point when differences in stress measures (e.g., cortisol) are no longer present. It seems more likely that, at the time when devaluation insensitivity became more pronounced in the stress group, this group was being released from stress, perhaps experiencing corollary fatigue or buoyancy.

    Another concern is that it is unclear whether the "Error" feedback screen was being employed during devaluation blocks. This is important, because most human psychology experiments use accuracy as the only incentive, and it appears to be a pretty effective motivator. Given that participants in the stress group had just been subjected to an aversive social stressor, they might have found the socially relevant error feedback more painful than the relatively minor response cost.

  4. Evaluation Summary:

    The authors used EEG-based multivariate pattern analysis and acute stress induction to assess the neural representations mediating a previously demonstrated influence of stress on the balance between goal-directed and habitual responding. While the results should be of interest to a wide range of neuroscientists, the temporal alignment of clinical, behavioral, and neural measures somewhat obscures the underlying causal mechanisms.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 agreed to share their name with the authors.)