Acute stress alters probabilistic reversal learning in healthy male adults
Behavioural adaptation is a fundamental cognitive ability, ensuring survival by allowing for flexible adjustment to changing environments. In laboratory settings, behavioural adaptation can be measured with reversal learning paradigms requiring agents to adjust reward learning to stimulus–action–out...
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Published in | The European journal of neuroscience Vol. 57; no. 5; pp. 824 - 839 |
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Main Authors | , , , , , , , |
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Language | English |
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Abstract | Behavioural adaptation is a fundamental cognitive ability, ensuring survival by allowing for flexible adjustment to changing environments. In laboratory settings, behavioural adaptation can be measured with reversal learning paradigms requiring agents to adjust reward learning to stimulus–action–outcome contingency changes. Stress is found to alter flexibility of reward learning, but effect directionality is mixed across studies. Here, we used model‐based functional MRI (fMRI) in a within‐subjects design to investigate the effect of acute psychosocial stress on flexible behavioural adaptation. Healthy male volunteers (n = 28) did a reversal learning task during fMRI in two sessions, once after the Trier Social Stress Test (TSST), a validated psychosocial stress induction method, and once after a control condition. Stress effects on choice behaviour were investigated using multilevel generalized linear models and computational models describing different learning processes that potentially generated the data. Computational models were fitted using a hierarchical Bayesian approach, and model‐derived reward prediction errors (RPE) were used as fMRI regressors. We found that acute psychosocial stress slightly increased correct response rates. Model comparison revealed that double‐update learning with altered choice temperature under stress best explained the observed behaviour. In the brain, model‐derived RPEs were correlated with BOLD signals in striatum and ventromedial prefrontal cortex (vmPFC). Striatal RPE signals for win trials were stronger during stress compared with the control condition. Our study suggests that acute psychosocial stress could enhance reversal learning and RPE brain responses in healthy male participants and provides a starting point to explore these effects further in a more diverse population.
In this study, we investigated the effect of acute psychosocial stress on flexible behavioural adaptation using a reversal learning task during fMRI scanning and after a Trier Social Stress Test in 28 healthy male participants. We found a small improving effect on task performance accuracy, which was best explained by Rescorla–Wagner double updating in our computational modelling approach. At the neural level, we saw that striatal reward prediction error signal for win trials was stronger during the stress compared with the control condition. |
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AbstractList | Behavioural adaptation is a fundamental cognitive ability, ensuring survival by allowing for flexible adjustment to changing environments. In laboratory settings, behavioural adaptation can be measured with reversal learning paradigms requiring agents to adjust reward learning to stimulus–action–outcome contingency changes. Stress is found to alter flexibility of reward learning, but effect directionality is mixed across studies. Here, we used model‐based functional MRI (fMRI) in a within‐subjects design to investigate the effect of acute psychosocial stress on flexible behavioural adaptation. Healthy male volunteers (n = 28) did a reversal learning task during fMRI in two sessions, once after the Trier Social Stress Test (TSST), a validated psychosocial stress induction method, and once after a control condition. Stress effects on choice behaviour were investigated using multilevel generalized linear models and computational models describing different learning processes that potentially generated the data. Computational models were fitted using a hierarchical Bayesian approach, and model‐derived reward prediction errors (RPE) were used as fMRI regressors. We found that acute psychosocial stress slightly increased correct response rates. Model comparison revealed that double‐update learning with altered choice temperature under stress best explained the observed behaviour. In the brain, model‐derived RPEs were correlated with BOLD signals in striatum and ventromedial prefrontal cortex (vmPFC). Striatal RPE signals for win trials were stronger during stress compared with the control condition. Our study suggests that acute psychosocial stress could enhance reversal learning and RPE brain responses in healthy male participants and provides a starting point to explore these effects further in a more diverse population.
In this study, we investigated the effect of acute psychosocial stress on flexible behavioural adaptation using a reversal learning task during fMRI scanning and after a Trier Social Stress Test in 28 healthy male participants. We found a small improving effect on task performance accuracy, which was best explained by Rescorla–Wagner double updating in our computational modelling approach. At the neural level, we saw that striatal reward prediction error signal for win trials was stronger during the stress compared with the control condition. Behavioural adaptation is a fundamental cognitive ability, ensuring survival by allowing for flexible adjustment to changing environments. In laboratory settings, behavioural adaptation can be measured with reversal learning paradigms requiring agents to adjust reward learning to stimulus–action–outcome contingency changes. Stress is found to alter flexibility of reward learning, but effect directionality is mixed across studies. Here, we used model‐based functional MRI (fMRI) in a within‐subjects design to investigate the effect of acute psychosocial stress on flexible behavioural adaptation. Healthy male volunteers (n = 28) did a reversal learning task during fMRI in two sessions, once after the Trier Social Stress Test (TSST), a validated psychosocial stress induction method, and once after a control condition. Stress effects on choice behaviour were investigated using multilevel generalized linear models and computational models describing different learning processes that potentially generated the data. Computational models were fitted using a hierarchical Bayesian approach, and model‐derived reward prediction errors (RPE) were used as fMRI regressors. We found that acute psychosocial stress slightly increased correct response rates. Model comparison revealed that double‐update learning with altered choice temperature under stress best explained the observed behaviour. In the brain, model‐derived RPEs were correlated with BOLD signals in striatum and ventromedial prefrontal cortex (vmPFC). Striatal RPE signals for win trials were stronger during stress compared with the control condition. Our study suggests that acute psychosocial stress could enhance reversal learning and RPE brain responses in healthy male participants and provides a starting point to explore these effects further in a more diverse population. Behavioural adaptation is a fundamental cognitive ability, ensuring survival by allowing for flexible adjustment to changing environments. In laboratory settings, behavioural adaptation can be measured with reversal learning paradigms requiring agents to adjust reward learning to stimulus–action–outcome contingency changes. Stress is found to alter flexibility of reward learning, but effect directionality is mixed across studies. Here, we used model‐based functional MRI (fMRI) in a within‐subjects design to investigate the effect of acute psychosocial stress on flexible behavioural adaptation. Healthy male volunteers ( n = 28) did a reversal learning task during fMRI in two sessions, once after the Trier Social Stress Test (TSST), a validated psychosocial stress induction method, and once after a control condition. Stress effects on choice behaviour were investigated using multilevel generalized linear models and computational models describing different learning processes that potentially generated the data. Computational models were fitted using a hierarchical Bayesian approach, and model‐derived reward prediction errors (RPE) were used as fMRI regressors. We found that acute psychosocial stress slightly increased correct response rates. Model comparison revealed that double‐update learning with altered choice temperature under stress best explained the observed behaviour. In the brain, model‐derived RPEs were correlated with BOLD signals in striatum and ventromedial prefrontal cortex (vmPFC). Striatal RPE signals for win trials were stronger during stress compared with the control condition. Our study suggests that acute psychosocial stress could enhance reversal learning and RPE brain responses in healthy male participants and provides a starting point to explore these effects further in a more diverse population. Behavioural adaptation is a fundamental cognitive ability, ensuring survival by allowing for flexible adjustment to changing environments. In laboratory settings, behavioural adaptation can be measured with reversal learning paradigms requiring agents to adjust reward learning to stimulus-action-outcome contingency changes. Stress is found to alter flexibility of reward learning, but effect directionality is mixed across studies. Here, we used model-based functional MRI (fMRI) in a within-subjects design to investigate the effect of acute psychosocial stress on flexible behavioural adaptation. Healthy male volunteers (n = 28) did a reversal learning task during fMRI in two sessions, once after the Trier Social Stress Test (TSST), a validated psychosocial stress induction method, and once after a control condition. Stress effects on choice behaviour were investigated using multilevel generalized linear models and computational models describing different learning processes that potentially generated the data. Computational models were fitted using a hierarchical Bayesian approach, and model-derived reward prediction errors (RPE) were used as fMRI regressors. We found that acute psychosocial stress slightly increased correct response rates. Model comparison revealed that double-update learning with altered choice temperature under stress best explained the observed behaviour. In the brain, model-derived RPEs were correlated with BOLD signals in striatum and ventromedial prefrontal cortex (vmPFC). Striatal RPE signals for win trials were stronger during stress compared with the control condition. Our study suggests that acute psychosocial stress could enhance reversal learning and RPE brain responses in healthy male participants and provides a starting point to explore these effects further in a more diverse population.Behavioural adaptation is a fundamental cognitive ability, ensuring survival by allowing for flexible adjustment to changing environments. In laboratory settings, behavioural adaptation can be measured with reversal learning paradigms requiring agents to adjust reward learning to stimulus-action-outcome contingency changes. Stress is found to alter flexibility of reward learning, but effect directionality is mixed across studies. Here, we used model-based functional MRI (fMRI) in a within-subjects design to investigate the effect of acute psychosocial stress on flexible behavioural adaptation. Healthy male volunteers (n = 28) did a reversal learning task during fMRI in two sessions, once after the Trier Social Stress Test (TSST), a validated psychosocial stress induction method, and once after a control condition. Stress effects on choice behaviour were investigated using multilevel generalized linear models and computational models describing different learning processes that potentially generated the data. Computational models were fitted using a hierarchical Bayesian approach, and model-derived reward prediction errors (RPE) were used as fMRI regressors. We found that acute psychosocial stress slightly increased correct response rates. Model comparison revealed that double-update learning with altered choice temperature under stress best explained the observed behaviour. In the brain, model-derived RPEs were correlated with BOLD signals in striatum and ventromedial prefrontal cortex (vmPFC). Striatal RPE signals for win trials were stronger during stress compared with the control condition. Our study suggests that acute psychosocial stress could enhance reversal learning and RPE brain responses in healthy male participants and provides a starting point to explore these effects further in a more diverse population. Behavioural adaptation is a fundamental cognitive ability, ensuring survival by allowing for flexible adjustment to changing environments. In laboratory settings, behavioural adaptation can be measured with reversal learning paradigms requiring agents to adjust reward learning to stimulus-action-outcome contingency changes. Stress is found to alter flexibility of reward learning, but effect directionality is mixed across studies. Here, we used model-based functional MRI (fMRI) in a within-subjects design to investigate the effect of acute psychosocial stress on flexible behavioural adaptation. Healthy male volunteers (n = 28) did a reversal learning task during fMRI in two sessions, once after the Trier Social Stress Test (TSST), a validated psychosocial stress induction method, and once after a control condition. Stress effects on choice behaviour were investigated using multilevel generalized linear models and computational models describing different learning processes that potentially generated the data. Computational models were fitted using a hierarchical Bayesian approach, and model-derived reward prediction errors (RPE) were used as fMRI regressors. We found that acute psychosocial stress slightly increased correct response rates. Model comparison revealed that double-update learning with altered choice temperature under stress best explained the observed behaviour. In the brain, model-derived RPEs were correlated with BOLD signals in striatum and ventromedial prefrontal cortex (vmPFC). Striatal RPE signals for win trials were stronger during stress compared with the control condition. Our study suggests that acute psychosocial stress could enhance reversal learning and RPE brain responses in healthy male participants and provides a starting point to explore these effects further in a more diverse population. |
Author | Luettgau, Lennart Wieland, Lara Schlagenhauf, Florian Panitz, Martin Ebrahimi, Claudia Sjoerds, Zsuzsika Katthagen, Teresa Heinz, Andreas |
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BackLink | https://www.ncbi.nlm.nih.gov/pubmed/36656136$$D View this record in MEDLINE/PubMed |
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Copyright | 2023 The Authors. published by Federation of European Neuroscience Societies and John Wiley & Sons Ltd. 2023 The Authors. European Journal of Neuroscience published by Federation of European Neuroscience Societies and John Wiley & Sons Ltd. 2023. This article is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. |
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Notes | Funding information This work was supported by the Rubicon award granted to ZS by the Netherlands Organization for Scientific Research (NWO; Rubicon 2014/05563/ALW), by the Einstein Center for Neurosciences (LW), and by the Heisenberg program from the German Research Foundation (Grant Number SCHL 1969/5‐1), as well as the Max Planck Society and grants from the German Research Foundation awarded to FS (DFG SCHL 1969/2‐2 as part of FOR1617 and SCHL1969/1‐2 and 402170461 as part of TRR265). Florian Schlagenhauf and Zsuzsika Sjoerds shared last authorship. Edited by: John Foxe ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 |
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SubjectTerms | Adult Bayes Theorem Bayesian analysis Brain - diagnostic imaging Brain mapping Choice learning Cognition - physiology Cognitive ability cognitive flexibility computational modelling Computational neuroscience decision‐making Functional magnetic resonance imaging Generalized linear models Humans Magnetic Resonance Imaging Male Mathematical models Neostriatum Prefrontal cortex Prefrontal Cortex - diagnostic imaging Reinforcement Reversal learning Reversal Learning - physiology Reward Social interactions TSST |
Title | Acute stress alters probabilistic reversal learning in healthy male adults |
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