Stress-induced impairment in goal-directed instrumental behaviour is moderated by baseline working memory

Highlights112 healthy participants performed an instrumental learning task.Individual differences in baseline and stress‐induced working memory (WM) were assessed.Baseline WM capacity modulates effect of stress on instrumental behavior.Stress induces a shift to less goal‐directed behavior at low baseline WM. ABSTRACT Acute stress has been found to impair goal‐directed instrumental behaviour, a cognitively flexible behaviour that requires cognitive control. The current study aimed to investigate the role of individual differences in baseline and stress‐induced changes in working memory (WM) on the shift to less goal‐directed responding under stress. To this end, 112 healthy participants performed an instrumental learning task. In phase 1, participants learned instrumental actions that were associated with two different food rewards. In phase 2, one of these food rewards was devalued by eating until satiety. Before the extinction test in phase 3, participants were subjected to the Maastricht Acute Stress Test or a no‐stress control procedure. Results showed that the effect of stress on instrumental behaviour is modulated by baseline, but not stress‐induced changes in WM capacity. Specifically, only at low baseline WM capacity did stress induce a shift to less goal‐directed behaviour. These findings highlight that our cognitive resources are limited and for those who already have limited resources at baseline taking into account motivational value is impaired under stress.

[1]  A. Dickinson,et al.  The neuropsychological basis of addictive behaviour , 2001, Brain Research Reviews.

[2]  N. Makris,et al.  Sex Differences in Stress Response Circuitry Activation Dependent on Female Hormonal Cycle , 2010, The Journal of Neuroscience.

[3]  Oliver T Wolf,et al.  Cold pressor stress impairs performance on working memory tasks requiring executive functions in healthy young men. , 2009, Behavioral neuroscience.

[4]  F. Plessow,et al.  Classification Criteria for Distinguishing Cortisol Responders From Nonresponders to Psychosocial Stress: Evaluation of Salivary Cortisol Pulse Detection in Panel Designs , 2013, Psychosomatic medicine.

[5]  L. Schwabe,et al.  Stress Prompts Habit Behavior in Humans , 2009, The Journal of Neuroscience.

[6]  M J de Leon,et al.  Cortisol differentially affects memory in young and elderly men. , 2001, Behavioral neuroscience.

[7]  J. Morrison,et al.  The Brain on Stress: Vulnerability and Plasticity of the Prefrontal Cortex over the Life Course , 2013, Neuron.

[8]  James A. Waltz,et al.  Interactions Among Working Memory, Reinforcement Learning, and Effort in Value-Based Choice: A New Paradigm and Selective Deficits in Schizophrenia , 2017, Biological Psychiatry.

[9]  A. Arnsten.  Catecholamine modulation of prefrontal cortical cognitive function , 1998, Trends in Cognitive Sciences.

[10]  M. Fournier,et al.  Effects of psychosocial stress on the goal-directed and habit memory systems during learning and later execution , 2017, Psychoneuroendocrinology.

[11]  L. Schwabe,et al.  Glucocorticoids boost stimulus-response memory formation in humans , 2014, Psychoneuroendocrinology.

[12]  N. Weekes,et al.  Examination stress and components of working memory , 2008, Stress.

[13]  E. Montoya,et al.  How Oral Contraceptives Impact Social-Emotional Behavior and Brain Function , 2017, Trends in Cognitive Sciences.

[14]  S. Wit,et al.  Current limits of experimental research into habits and future directions , 2018, Current Opinion in Behavioral Sciences.

[15]  J. de Houwer,et al.  The Power of Goal-Directed Processes in the Causation of Emotional and Other Actions , 2017 .

[16]  Wolfgang M. Pauli,et al.  Learning, Reward, and Decision Making , 2017, Annual review of psychology.

[17]  D. Garner,et al.  The Eating Attitudes Test: psychometric features and clinical correlates , 1982, Psychological Medicine.

[18]  Lars Schwabe,et al.  Socially evaluated cold pressor stress after instrumental learning favors habits over goal-directed action , 2010, Psychoneuroendocrinology.

[19]  L. Schwabe,et al.  Memory dynamics under stress , 2018, Memory.

[20]  K. R. Ridderinkhof,et al.  Neurocognitive mechanisms of cognitive control: The role of prefrontal cortex in action selection, response inhibition, performance monitoring, and reward-based learning , 2004, Brain and Cognition.

[21]  Karin Roelofs,et al.  Cortisol-induced impairments of working memory require acute sympathetic activation. , 2005, Behavioral neuroscience.

[22]  S. Crewther,et al.  The Maastricht Acute Stress Test (MAST): Physiological and Subjective Responses in Anticipation, and Post-stress , 2017, Front. Psychol..

[23]  B. Bermond,et al.  Psychosocial stress impairs working memory at high loads: An association with cortisol levels and memory retrieval , 2006, Stress.

[24]  T. van Amelsvoort,et al.  Neuroendocrine stress responses predict catecholamine-dependent working memory-related dorsolateral prefrontal cortex activity , 2017, Social cognitive and affective neuroscience.

[25]  J. Horvitz,et al.  Dopaminergic Mechanisms in Actions and Habits , 2007, The Journal of Neuroscience.

[26]  Erno J. Hermans,et al.  Stress-induced reduction in reward-related prefrontal cortex function , 2011, NeuroImage.

[27]  L. Schwabe,et al.  Simultaneous Glucocorticoid and Noradrenergic Activity Disrupts the Neural Basis of Goal-Directed Action in the Human Brain , 2012, The Journal of Neuroscience.

[28]  A. Dickinson.  Actions and habits: the development of behavioural autonomy , 1985 .

[29]  Raymond J Dolan,et al.  Maintenance versus manipulation in verbal working memory revisited: an fMRI study , 2003, NeuroImage.

[30]  C. Quaedflieg,et al.  Stress-induced reliance on habitual behavior is moderated by cortisol reactivity , 2019, Brain and Cognition.

[31]  Alice Y. Chiang,et al.  Working-memory capacity protects model-based learning from stress , 2013, Proceedings of the National Academy of Sciences.

[32]  Kimberly M Albert,et al.  Estradiol levels modulate brain activity and negative responses to psychosocial stress across the menstrual cycle , 2015, Psychoneuroendocrinology.

[33]  C. Quaedflieg,et al.  Examining habituation and sensitization across repetitive laboratory stress inductions using the MAST , 2017, Psychoneuroendocrinology.

[34]  H. Merckelbach,et al.  The effect of acute stress on memory depends on word valence. , 2006, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[35]  L. Schwabe,et al.  Preventing the Stress-Induced Shift from Goal-Directed to Habit Action with a β-Adrenergic Antagonist , 2011, The Journal of Neuroscience.

[36]  G. Fernández,et al.  Acute Psychological Stress Reduces Working Memory-Related Activity in the Dorsolateral Prefrontal Cortex , 2009, Biological Psychiatry.

[37]  Marian Joëls,et al.  The neuro-symphony of stress , 2009, Nature Reviews Neuroscience.

[38]  K. Foerde.  What are habits and do they depend on the striatum? A view from the study of neuropsychological populations , 2018, Current Opinion in Behavioral Sciences.

[39]  G. Fernández,et al.  Dynamic adaptation of large-scale brain networks in response to acute stressors , 2014, Trends in Neurosciences.

[40]  L. Schwabe,et al.  Time dependent effects of stress prior to encoding on event-related potentials and 24h delayed retrieval , 2013, Psychoneuroendocrinology.

[41]  H. Merckelbach,et al.  The validity of individual frontal alpha asymmetry EEG neurofeedback. , 2016, Social cognitive and affective neuroscience.

[42]  M. al’Absi,et al.  The effect of acute stress on subsequent neuropsychological test performance (2003). , 2004, Archives of clinical neuropsychology : the official journal of the National Academy of Neuropsychologists.

[43]  F. Cantini,et al.  Classification Criteria , 2021, Large and Medium Size Vessel and Single Organ Vasculitis.

[44]  B. Balleine,et al.  Impairments in Goal-Directed Actions Predict Treatment Response to Cognitive-Behavioral Therapy in Social Anxiety Disorder , 2014, PloS one.

[45]  J. de Houwer,et al.  Kicking the Habit: Why Evidence for Habits in Humans Might Be Overestimated , 2017 .

[46]  R. Costa,et al.  Chronic Stress Causes Frontostriatal Reorganization and Affects Decision-Making , 2009, Science.

[47]  A. Moghimi,et al.  The Effect of Acute Stress on Formed Memory Recall after Prescription of Very Low to Regular Doses of Morphine in Rats , 2012 .

[48]  Oliver T. Wolf,et al.  Psychosocial stress induces working memory impairments in an n-back paradigm , 2008, Psychoneuroendocrinology.

[49]  B. McEwen,et al.  Cognitive Effects of Intravenous Hydrocortisone in Subjects with PTSD and Healthy Control Subjects , 2006, Annals of the New York Academy of Sciences.

[50]  R. Oostenveld,et al.  Stress-Related Noradrenergic Activity Prompts Large-Scale Neural Network Reconfiguration , 2011, Science.

[51]  L. Schwabe,et al.  Stress-induced modulation of instrumental behavior: From goal-directed to habitual control of action , 2011, Behavioural Brain Research.

[52]  B. Balleine,et al.  Human and Rodent Homologies in Action Control: Corticostriatal Determinants of Goal-Directed and Habitual Action , 2010, Neuropsychopharmacology.

[53]  L. Schwabe,et al.  Concurrent Glucocorticoid and Noradrenergic Activity Shifts Instrumental Behavior from Goal-Directed to Habitual Control , 2010, The Journal of Neuroscience.

[54]  Stefan Wüst,et al.  Why do we respond so differently? Reviewing determinants of human salivary cortisol responses to challenge , 2009, Psychoneuroendocrinology.

[55]  T. Robbins,et al.  Drug Addiction: Updating Actions to Habits to Compulsions Ten Years On. , 2016, Annual review of psychology.

[56]  L. Schwabe,et al.  Time dependent effects of stress prior to encoding on event-related potentials and 24 h delayed retrieval , 2013 .

[57]  O. Wolf,et al.  HPA axis and memory. , 2003, Best practice & research. Clinical endocrinology & metabolism.

[58]  D. Karus,et al.  Psychosocial , 1992 .

[59]  L. Schwabe,et al.  Habits under stress: mechanistic insights across different types of learning , 2018, Current Opinion in Behavioral Sciences.

[60]  H. Merckelbach,et al.  Introducing the Maastricht Acute Stress Test (MAST): A quick and non-invasive approach to elicit robust autonomic and glucocorticoid stress responses , 2012, Psychoneuroendocrinology.

[61]  P. Janak,et al.  Defining the place of habit in substance use disorders , 2017, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[62]  B. Balleine,et al.  A specific role for posterior dorsolateral striatum in human habit learning , 2009, The European journal of neuroscience.

[63]  Jennifer J. Richler,et al.  Effect size estimates: current use, calculations, and interpretation. , 2012, Journal of experimental psychology. General.

[64]  L. Schwabe,et al.  Stress, habits, and drug addiction: a psychoneuroendocrinological perspective. , 2011, Experimental and clinical psychopharmacology.