It feels real: physiological responses to a stressful virtual reality environment and its impact on working memory

Background: Virtual reality (VR) is increasingly used to study and treat psychiatric disorders. Its fidelity depends in part on the extent to which the VR environment provides a convincing simulation, for example whether a putatively stressful VR situation actually produces a stress response. Methods: We studied the stress response in 28 healthy men exposed either to a stressor VR elevator (which simulated travelling up the outside of a tall building and culminated in the participant being asked to step off the elevator platform), or to a control elevator. We measured psychological and physiological (salivary cortisol and alpha-amylase, blood pressure, pulse, skin conductance) stress indices. We also measured subsequent performance on the N-back task because acute stress has been reported to impact on working memory. Results: Compared to participants in the control elevator, those in the external elevator had increases in skin conductance, pulse and subjective stress and anxiety ratings, altered heart rate variability, and a delayed rise in cortisol. N-back performance was unaffected. Conclusions: A putatively stressful VR elevator produces a physiological as well as a psychological stress response, supporting its use in the investigation and treatment of stress-related disorders, and its potential value as an experimental laboratory stressor.

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

[2]  Beat Meier,et al.  Stress Effects on Working Memory, Explicit Memory, and Implicit Memory for Neutral and Emotional Stimuli in Healthy Men , 2008, Frontiers in behavioral neuroscience.

[3]  C. Kirschbaum,et al.  The 'Trier Social Stress Test'--a tool for investigating psychobiological stress responses in a laboratory setting. , 1993, Neuropsychobiology.

[4]  Lars Schwabe,et al.  Stress effects on memory: An update and integration , 2012, Neuroscience & Biobehavioral Reviews.

[5]  Helmut Hlavacs,et al.  Salivary cortisol and cardiovascular reactivity to a public speaking task in a virtual and real-life environment , 2016, Comput. Hum. Behav..

[6]  R. Stawski,et al.  Daily positive events and diurnal cortisol rhythms: Examination of between-person differences and within-person variation , 2017, Psychoneuroendocrinology.

[7]  J. Herman,et al.  Neural regulation of endocrine and autonomic stress responses , 2009, Nature Reviews Neuroscience.

[8]  S. Dickerson,et al.  Acute stressors and cortisol responses: a theoretical integration and synthesis of laboratory research. , 2004, Psychological bulletin.

[9]  U. Nater,et al.  Associations between salivary alpha-amylase and catecholamines – A multilevel modeling approach , 2014, Biological Psychology.

[10]  O. Wolf,et al.  Impaired Memory Retrieval after Psychosocial Stress in Healthy Young Men , 2005, The Journal of Neuroscience.

[11]  Hongwei Hsiao,et al.  Height Effects in Real and Virtual Environments , 2005, Hum. Factors.

[12]  Christian Grillon,et al.  Working memory performance after acute exposure to the cold pressor stress in healthy volunteers , 2009, Neurobiology of Learning and Memory.

[13]  J. Gross,et al.  Mechanisms of Virtual Reality Exposure Therapy: The Role of the Behavioral Activation and Behavioral Inhibition Systems , 2005, Applied psychophysiology and biofeedback.

[14]  Owen Kelly,et al.  Psychosocial Stress Evoked by a Virtual Audience: Relation to Neuroendocrine Activity , 2007, Cyberpsychology Behav. Soc. Netw..

[15]  H. Engler,et al.  Salivary alpha-amylase and noradrenaline responses to corticotropin-releasing hormone administration in humans , 2017, Biological Psychology.

[16]  Marian Joëls,et al.  Implications of psychosocial stress on memory formation in a typical male versus female student sample , 2011, Psychoneuroendocrinology.

[17]  A. Malliani,et al.  Heart rate variability. Standards of measurement, physiological interpretation, and clinical use , 1996 .

[18]  Matt G Kushner,et al.  Effect of quetiapine vs. placebo on response to two virtual public speaking exposures in individuals with social phobia. , 2009, Journal of anxiety disorders.

[19]  Ulrike Ehlert,et al.  Acute psychosocial stress: Does the emotional stress response correspond with physiological responses? , 2012, Psychoneuroendocrinology.

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

[21]  G. Johansson,et al.  Cardiovascular and cortisol reactivity and habituation to a virtual reality version of the Trier Social Stress Test: A pilot study , 2010, Psychoneuroendocrinology.

[22]  Riklef Weerda,et al.  Effects of acute psychosocial stress on working memory related brain activity in men , 2010, Human brain mapping.

[23]  Mel Slater,et al.  Automated psychological therapy using immersive virtual reality for treatment of fear of heights: a single-blind, parallel-group, randomised controlled trial , 2018, The lancet. Psychiatry.

[24]  F. Shaffer,et al.  An Overview of Heart Rate Variability Metrics and Norms , 2017, Front. Public Health.

[25]  G. Dunn,et al.  Virtual reality in the treatment of persecutory delusions: randomised controlled experimental study testing how to reduce delusional conviction , 2016, British Journal of Psychiatry.

[26]  Elizabeth M. Tunbridge,et al.  COMT Val158Met Genotype Determines the Direction of Cognitive Effects Produced by Catechol-O-Methyltransferase Inhibition , 2012, Biological Psychiatry.

[27]  Maria V. Sanchez-Vives,et al.  From presence to consciousness through virtual reality , 2005, Nature Reviews Neuroscience.

[28]  Stephan Hamann,et al.  The influence of perceived control and locus of control on the cortisol and subjective responses to stress , 2004, Biological Psychology.

[29]  P. Pauli,et al.  Virtual reality exposure in anxiety disorders: Impact on psychophysiological reactivity , 2014, The world journal of biological psychiatry : the official journal of the World Federation of Societies of Biological Psychiatry.

[30]  G. Billman The LF/HF ratio does not accurately measure cardiac sympatho-vagal balance , 2013, Front. Physio..

[31]  Willis J. Tompkins,et al.  A Real-Time QRS Detection Algorithm , 1985, IEEE Transactions on Biomedical Engineering.

[32]  Melissa R. Stauble,et al.  Increases in cortisol are positively associated with gains in encoding and maintenance working memory performance in young men , 2013, Stress.

[33]  J. Gross,et al.  The tie that binds? Coherence among emotion experience, behavior, and physiology. , 2005, Emotion.

[34]  G. Dunn,et al.  Automated psychological therapy using virtual reality (VR) for patients with persecutory delusions: study protocol for a single-blind parallel-group randomised controlled trial (THRIVE) , 2019, Trials.

[35]  Michael Meehan,et al.  Physiological measures of presence in stressful virtual environments , 2002, SIGGRAPH.

[36]  S. Grimm,et al.  Working memory-related frontal theta activity is decreased under acute stress , 2014, Psychoneuroendocrinology.

[37]  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.

[38]  V. Arolt,et al.  Acute anxiolytic effects of quetiapine during virtual reality exposure—A double-blind placebo-controlled trial in patients with specific phobia , 2013, European Neuropsychopharmacology.

[39]  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.

[40]  Daniel P Ferris,et al.  Effects of virtual reality high heights exposure during beam-walking on physiological stress and cognitive loading , 2018, PloS one.

[41]  M. Whitton,et al.  Review of Four Studies on the Use of Physiological Reaction as a Measure of Presence in StressfulVirtual Environments , 2005, Applied psychophysiology and biofeedback.

[42]  Mark G Carpenter,et al.  Influence of real and virtual heights on standing balance. , 2012, Gait & posture.

[43]  A. de Jongh,et al.  Efficacy of virtual reality exposure therapy for the treatment of dental phobia in adults: A randomized controlled trial. , 2019, Journal of anxiety disorders.

[44]  Maria V. Sanchez-Vives,et al.  Influence of Music on Anxiety Induced by Fear of Heights in Virtual Reality , 2016, Front. Psychol..

[45]  G. Billman Heart Rate Variability – A Historical Perspective , 2011, Front. Physio..

[46]  F. Holsboer,et al.  Stress and the brain: from adaptation to disease , 2005, Nature Reviews Neuroscience.

[47]  Guillén Fernández,et al.  Stressed Memories: How Acute Stress Affects Memory Formation in Humans , 2009, The Journal of Neuroscience.

[48]  M. Pulopulos,et al.  Acute stress and working memory: The role of sex and cognitive stress appraisal , 2016, Physiology & Behavior.

[49]  Andreas Mühlberger,et al.  Fear and physiological arousal during a virtual height challenge--effects in patients with acrophobia and healthy controls. , 2016, Journal of anxiety disorders.

[50]  Isabel L. Kampmann,et al.  Meta-analysis of technology-assisted interventions for social anxiety disorder. , 2016, Journal of anxiety disorders.

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

[52]  T. Dinan,et al.  Biological and psychological markers of stress in humans: Focus on the Trier Social Stress Test , 2014, Neuroscience & Biobehavioral Reviews.

[53]  Jens C. Pruessner,et al.  Low self-esteem, induced failure and the adrenocortical stress response , 1999 .