Asymmetric effects of acute stress on cost and benefit learning

Stella D Voulgaropoulou; Fasya Fauzani; Janine Pfirrmann; Claudia Vingerhoets; Thérèse van Amelsvoort; Dennis Hernaus

doi:10.1016/j.psyneuen.2021.105646

Asymmetric effects of acute stress on cost and benefit learning

Stella D Voulgaropoulou^*, Fasya Fauzani, Janine Pfirrmann, Claudia Vingerhoets, Thérèse van Amelsvoort, Dennis Hernaus^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › Academic › peer-review

Abstract

BACKGROUND: Humans are continuously exposed to stressful challenges in everyday life. Such stressful events trigger a complex physiological reaction - the fight-or-flight response - that can hamper flexible decision-making and learning. Inspired by key neural and peripheral characteristics of the fight-or-flight response, here, we ask whether acute stress changes how humans learn about costs and benefits.

METHODS: Healthy adults were randomly exposed to an acute stress (age mean=23.48, 21/40 female) or no-stress control (age mean=23.80, 22/40 female) condition, after which they completed a reinforcement learning task in which they minimize cost (physical effort) and maximize benefits (monetary rewards). During the task pupillometry data were collected. A computational model of cost-benefit reinforcement learning was employed to investigate the effect of acute stress on cost and benefit learning and decision-making.

RESULTS: Acute stress improved learning to maximize rewards relative to minimizing physical effort (Condition-by-Trial Type interaction: F(1,78)= 6.53, p = 0.01, n2G= 0.04; reward > effort in stress condition: t(39) = 5.40, p < 0.01). Computational modelling revealed that asymmetric learning could be explained by changes in the learning rates of reward value and action cost [condition-by-learning rate (αR, αE) interaction: F(1,78)= 6.42, p = 0.01, n2G= 0.03; αE> αR in control condition: t(39) = -4.75, p < 0.001]. This process was associated with distinct alterations in pupil size fluctuations. Data and scripts are available (https://osf.io/ydv2q/).

CONCLUSIONS: Here we demonstrate that acute stress is associated with asymmetric learning about reward value versus action cost, thereby providing new insights into learning strategies under acute stress, which, depending on the context, may be maladaptive or beneficial. Our pupillometry and physiological results tentatively link asymmetric cost and benefit learning to stress-related changes in catecholamine activity.

Original language	English
Article number	105646
Number of pages	10
Journal	Psychoneuroendocrinology
Volume	138
Early online date	24 Dec 2021
DOIs	https://doi.org/10.1016/j.psyneuen.2021.105646
Publication status	Published - Apr 2022

Keywords

Acute stress
Reinforcement learning
Computational modelling
Costs and benefits
Reward
Effort
DOPAMINE NEURONS
REWARD
ADAPTATION
PREDICTION
NETWORKS
DYNAMICS
CORTISOL
BRAIN

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Cite this

@article{965c0e387d86453bbc07fd4e2ba8e805,

title = "Asymmetric effects of acute stress on cost and benefit learning",

abstract = "BACKGROUND: Humans are continuously exposed to stressful challenges in everyday life. Such stressful events trigger a complex physiological reaction - the fight-or-flight response - that can hamper flexible decision-making and learning. Inspired by key neural and peripheral characteristics of the fight-or-flight response, here, we ask whether acute stress changes how humans learn about costs and benefits.METHODS: Healthy adults were randomly exposed to an acute stress (age mean=23.48, 21/40 female) or no-stress control (age mean=23.80, 22/40 female) condition, after which they completed a reinforcement learning task in which they minimize cost (physical effort) and maximize benefits (monetary rewards). During the task pupillometry data were collected. A computational model of cost-benefit reinforcement learning was employed to investigate the effect of acute stress on cost and benefit learning and decision-making.RESULTS: Acute stress improved learning to maximize rewards relative to minimizing physical effort (Condition-by-Trial Type interaction: F(1,78)= 6.53, p = 0.01, n2G= 0.04; reward > effort in stress condition: t(39) = 5.40, p < 0.01). Computational modelling revealed that asymmetric learning could be explained by changes in the learning rates of reward value and action cost [condition-by-learning rate (αR, αE) interaction: F(1,78)= 6.42, p = 0.01, n2G= 0.03; αE> αR in control condition: t(39) = -4.75, p < 0.001]. This process was associated with distinct alterations in pupil size fluctuations. Data and scripts are available (https://osf.io/ydv2q/).CONCLUSIONS: Here we demonstrate that acute stress is associated with asymmetric learning about reward value versus action cost, thereby providing new insights into learning strategies under acute stress, which, depending on the context, may be maladaptive or beneficial. Our pupillometry and physiological results tentatively link asymmetric cost and benefit learning to stress-related changes in catecholamine activity.",

keywords = "Acute stress, Reinforcement learning, Computational modelling, Costs and benefits, Reward, Effort, DOPAMINE NEURONS, REWARD, ADAPTATION, PREDICTION, NETWORKS, DYNAMICS, CORTISOL, BRAIN",

author = "Voulgaropoulou, {Stella D} and Fasya Fauzani and Janine Pfirrmann and Claudia Vingerhoets and {van Amelsvoort}, Th{\'e}r{\`e}se and Dennis Hernaus",

note = "Funding Information: We are indebted to Drs. Conny Quaedflieg, Edwin S. Dalmaijer. and Ross D. Markello for advice on stress-induction procedures and paradigm development. We thank Dr. Michael Frank for advice on hierarchical computational modelling procedures. We thank Katya Brat-Matchett for involvement in participant recruitment and Truda Driessen for administrative support. D.H. has received financial compensation as a consultant for P1vital Products Ltd. These activities were unrelated to the work presented in this manuscript. The authors declare no competing interests. Publisher Copyright: {\textcopyright} 2022 The Authors",

year = "2022",

month = apr,

doi = "10.1016/j.psyneuen.2021.105646",

language = "English",

volume = "138",

journal = "Psychoneuroendocrinology",

issn = "0306-4530",

publisher = "Elsevier Science",

}

TY - JOUR

T1 - Asymmetric effects of acute stress on cost and benefit learning

AU - Voulgaropoulou, Stella D

AU - Fauzani, Fasya

AU - Pfirrmann, Janine

AU - Vingerhoets, Claudia

AU - van Amelsvoort, Thérèse

AU - Hernaus, Dennis

N1 - Funding Information: We are indebted to Drs. Conny Quaedflieg, Edwin S. Dalmaijer. and Ross D. Markello for advice on stress-induction procedures and paradigm development. We thank Dr. Michael Frank for advice on hierarchical computational modelling procedures. We thank Katya Brat-Matchett for involvement in participant recruitment and Truda Driessen for administrative support. D.H. has received financial compensation as a consultant for P1vital Products Ltd. These activities were unrelated to the work presented in this manuscript. The authors declare no competing interests. Publisher Copyright: © 2022 The Authors

PY - 2022/4

Y1 - 2022/4

N2 - BACKGROUND: Humans are continuously exposed to stressful challenges in everyday life. Such stressful events trigger a complex physiological reaction - the fight-or-flight response - that can hamper flexible decision-making and learning. Inspired by key neural and peripheral characteristics of the fight-or-flight response, here, we ask whether acute stress changes how humans learn about costs and benefits.METHODS: Healthy adults were randomly exposed to an acute stress (age mean=23.48, 21/40 female) or no-stress control (age mean=23.80, 22/40 female) condition, after which they completed a reinforcement learning task in which they minimize cost (physical effort) and maximize benefits (monetary rewards). During the task pupillometry data were collected. A computational model of cost-benefit reinforcement learning was employed to investigate the effect of acute stress on cost and benefit learning and decision-making.RESULTS: Acute stress improved learning to maximize rewards relative to minimizing physical effort (Condition-by-Trial Type interaction: F(1,78)= 6.53, p = 0.01, n2G= 0.04; reward > effort in stress condition: t(39) = 5.40, p < 0.01). Computational modelling revealed that asymmetric learning could be explained by changes in the learning rates of reward value and action cost [condition-by-learning rate (αR, αE) interaction: F(1,78)= 6.42, p = 0.01, n2G= 0.03; αE> αR in control condition: t(39) = -4.75, p < 0.001]. This process was associated with distinct alterations in pupil size fluctuations. Data and scripts are available (https://osf.io/ydv2q/).CONCLUSIONS: Here we demonstrate that acute stress is associated with asymmetric learning about reward value versus action cost, thereby providing new insights into learning strategies under acute stress, which, depending on the context, may be maladaptive or beneficial. Our pupillometry and physiological results tentatively link asymmetric cost and benefit learning to stress-related changes in catecholamine activity.

AB - BACKGROUND: Humans are continuously exposed to stressful challenges in everyday life. Such stressful events trigger a complex physiological reaction - the fight-or-flight response - that can hamper flexible decision-making and learning. Inspired by key neural and peripheral characteristics of the fight-or-flight response, here, we ask whether acute stress changes how humans learn about costs and benefits.METHODS: Healthy adults were randomly exposed to an acute stress (age mean=23.48, 21/40 female) or no-stress control (age mean=23.80, 22/40 female) condition, after which they completed a reinforcement learning task in which they minimize cost (physical effort) and maximize benefits (monetary rewards). During the task pupillometry data were collected. A computational model of cost-benefit reinforcement learning was employed to investigate the effect of acute stress on cost and benefit learning and decision-making.RESULTS: Acute stress improved learning to maximize rewards relative to minimizing physical effort (Condition-by-Trial Type interaction: F(1,78)= 6.53, p = 0.01, n2G= 0.04; reward > effort in stress condition: t(39) = 5.40, p < 0.01). Computational modelling revealed that asymmetric learning could be explained by changes in the learning rates of reward value and action cost [condition-by-learning rate (αR, αE) interaction: F(1,78)= 6.42, p = 0.01, n2G= 0.03; αE> αR in control condition: t(39) = -4.75, p < 0.001]. This process was associated with distinct alterations in pupil size fluctuations. Data and scripts are available (https://osf.io/ydv2q/).CONCLUSIONS: Here we demonstrate that acute stress is associated with asymmetric learning about reward value versus action cost, thereby providing new insights into learning strategies under acute stress, which, depending on the context, may be maladaptive or beneficial. Our pupillometry and physiological results tentatively link asymmetric cost and benefit learning to stress-related changes in catecholamine activity.

KW - Acute stress

KW - Reinforcement learning

KW - Computational modelling

KW - Costs and benefits

KW - Reward

KW - Effort

KW - DOPAMINE NEURONS

KW - REWARD

KW - ADAPTATION

KW - PREDICTION

KW - NETWORKS

KW - DYNAMICS

KW - CORTISOL

KW - BRAIN

U2 - 10.1016/j.psyneuen.2021.105646

DO - 10.1016/j.psyneuen.2021.105646

M3 - Article

C2 - 35065334

SN - 0306-4530

VL - 138

JO - Psychoneuroendocrinology

JF - Psychoneuroendocrinology

M1 - 105646

ER -