Elsevier

Psychoneuroendocrinology

Volume 35, Issue 7, August 2010, Pages 977-986
Psychoneuroendocrinology

Socially evaluated cold pressor stress after instrumental learning favors habits over goal-directed action

https://doi.org/10.1016/j.psyneuen.2009.12.010Get rights and content

Summary

Instrumental action can be controlled by two anatomically and functionally distinct systems: a goal-directed system that learns action–outcome associations and a habit system that learns stimulus–response associations without any link to the incentive value of the outcome. Recent evidence indicates that stress before learning modulates these two systems in favor of habitual control. Here, we examined the impact of a stress exposure after learning on instrumental performance. Participants learned to choose two instrumental actions that were associated with the delivery of different food rewards. After learning, one of these food rewards was devalued as participants were saturated with that food. Before being re-exposed to the instrumental actions in extinction, participants were subjected to the socially evaluated cold pressor test or a control procedure. Controls but not stressed participants reduced responding to the action associated with the devalued outcome. That is, acute stress before extinction testing abolished sensitivity of performance to outcome devaluation. Cortisol responses to stress correlated significantly with habitual performance. These findings show that stress induced by the socially evaluated cold pressor test can make behavior habitual without affecting processes involved in learning.

Introduction

Instrumental action can be controlled by two distinct processes: a goal-directed process that involves learning of associations between actions and the incentive value of an outcome (action–outcome learning), and a habit learning process that involves learning associations between contexts or stimuli and responses (stimulus–response learning) (Dickinson, 1985, Dickinson and Balleine, 1994). At a neural level, goal-directed and habitual processes are supported by distinct brain structures. Rodent studies indicated that goal-directed action relies on a neural network consisting of the medial prefrontal cortex, the dorsomedial striatum and the dorsomedial thalamus (Balleine and Dickinson, 1998, Corbit et al., 2003, Yin et al., 2005) whereas habits are mediated by the dorsolateral striatum (Yin et al., 2004, Yin et al., 2005). This dissociation has been confirmed in human neuroimaging and neuropsychological studies (Knowlton et al., 1996, Valentin et al., 2007, Tricomi et al., 2009).

Based on a large body of literature demonstrating that stress, i.e. the real or perceived threat of an individual's homeostasis (McEwen, 2000), and the glucocorticoid stress hormones (cortisol in humans) modulate learning and memory processes (de Quervain et al., 1998, Buchanan et al., 2006, Payne et al., 2007); for reviews see (Roozendaal et al., 2009, Wolf, 2009), we asked in a recent study whether stress affects the use of goal-directed and habit systems in instrumental learning (Schwabe and Wolf, 2009). In this previous study, we used a devaluation paradigm (Balleine and Dickinson, 1998) and found that acute stress before learning rendered participants’ action insensitive to changes in the value of the action goal. In other words: stress before learning made participants’ behavior habitual.

While these findings provided the first demonstration of a stress-induced modulation of goal-directed and habitual systems in instrumental action, this study did not address which processes were influenced by stress. Stress preceded both learning and extinction testing and cortisol levels were still elevated after training (i.e. before extinction testing). Therefore, it remained unclear whether stress affected processes involved in either acquisition (e.g. attention, initial encoding) or performance (e.g. memory retrieval, response inhibition). If stress exerted its effect mainly on acquisition processes, then instrumental behavior should remain unaffected by a stress exposure after learning. If, however, stress affected primarily performance, then we should see the impairment in the goal-directedness of behavior also when subjects are stressed before extinction testing.

In the present experiment, we examined whether acute stress favors habits over goal-directed action when it is administered before the extinction test. Participants were first trained in two instrumental actions leading with a high probability to two distinct food outcomes. After training, we devalued selectively one of the two food outcomes by inviting subjects to eat that food to satiety. Then, participants were exposed to an acute, brief stressor (hand in ice water and social evaluation in the socially evaluated cold pressor test, SECPT) or a non-stressful control condition, before they were tested in the two instrumental actions in extinction. Goal-directed behavior is expressed by a decrease in the frequency of the action associated with the devalued outcome, i.e. the food eaten to satiety.

Section snippets

Participants and design

Sixty-eight students of the Ruhr-University Bochum (34 men, 34 women) between 18 and 32 years of age (M ± SEM: 23.4 ± 0.3 years) and with a body-mass-index between 19 and 28 kg/m2 (22.6 ± 0.3 kg/m2) participated in this study. The following exclusion criteria were checked in a standardized interview: any medical condition, current or lifetime psychopathology, use of medication, drug abuse, smoking, any food intolerance as well as current or planned diet. Women taking oral contraceptives were excluded

Instrumental learning

As training proceeded, subjects preferred increasingly the high probability actions associated with the food rewards (i.e. the non-devalued and the subsequently devalued foods) over their low probability counterparts (Fig. 2). However, participants did not favor the high probability action in the neutral trials indicating that they were indifferent as to whether they received the effectively neutral outcome or not. This conclusion was supported by a group (SECPT vs. control) × sex (men vs. women) ×

Discussion

Here, we studied the impact of acute SECPT stress after learning on goal-directed and habitual instrumental performance. SECPT stress administered before extinction testing rendered subjects’ instrumental actions insensitive to changes in the value of the action goal and stress-induced cortisol elevations were associated with the selection of devalued instrumental actions. That is, acute SECPT stress impaired the goal-directedness of behavior and promoted habitual performance. Interestingly,

Contributors

Lars Schwabe is the lead author. He contributed to the design of the study, analyzed the data and wrote the manuscript. Oliver Wolf contributed to the design of the study. Both authors contributed to and have approved the final version of the manuscript.

Role of funding sources

Funding for this study was provided by the German Research Foundation (DFG, grant SCHW 1357/2-1); the DFG had no further role in study design; in the collection, analysis and interpretation of data; in the writing of the report; and in the decision to submit the paper for publication.

Conflict of interest

Both authors report no conflict of interest.

Acknowledgements

This work was supported by DFG grant SCHW 1357/2-1. We thank Karla Lücking and Florian Watzlawik for assistance during data collection. We gratefully acknowledge the technical assistance of Tobias Otto.

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