Acute stress improves the effectivity of cognitive emotion regulation in men.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
14 07 2020
14 07 2020
Historique:
received:
15
11
2019
accepted:
17
06
2020
entrez:
16
7
2020
pubmed:
16
7
2020
medline:
15
12
2020
Statut:
epublish
Résumé
Emotion regulation is crucial for coping with stressors but in turn can also be influenced by stress. Initial studies provided mixed evidence showing either beneficial or impairing stress effects on cognitive emotion regulation depending on stress timing, sex or the regulatory strategy. Here, we investigated the impact of acute stress on different emotion regulation strategies in men and women. N = 118 healthy participants were subjected to the Trier Social Stress Test or a control condition after which they completed an emotion regulation paradigm, requiring them to regulate their emotions in response to negative pictures using reappraisal or distraction. Cortisol levels were repeatedly measured to quantify changes in HPA axis activity. Affective ratings and pupil dilation served to measure emotion regulation success and the cognitive effort to regulate emotions. Stress reduced arousal and increased valence and success ratings for reappraisal in men, whereas no significant stress effects were found in women. Moreover, stressed men displayed a significant expansion of pupil diameter during reappraisal suggesting enhanced cognitive regulatory engagement, which ultimately may have led to better emotion regulation outcomes. Cortisol secretion positively correlated with subjective reappraisal success in men, suggesting a glucocorticoid-driven mechanism that may promote emotion regulatory performance in the aftermath of stress.
Identifiants
pubmed: 32665617
doi: 10.1038/s41598-020-68137-5
pii: 10.1038/s41598-020-68137-5
pmc: PMC7360604
doi:
Substances chimiques
Hydrocortisone
WI4X0X7BPJ
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
11571Références
Berking, M. & Wupperman, P. Emotion regulation and mental health: Recent findings, current challenges, and future directions. Curr. Opin. Psychiatry 25, 128–134 (2012).
pubmed: 22262030
Sheppes, G., Suri, G. & Gross, J. J. Emotion regulation and psychopathology. Annu. Rev. Clin. Psychol. 11, 379–405 (2015).
pubmed: 25581242
Zilverstand, A., Parvaz, M. A. & Goldstein, R. Z. Neuroimaging cognitive reappraisal in clinical populations to define neural targets for enhancing emotion regulation. A systematic review. Neuroimage 151, 105–116 (2017).
pubmed: 27288319
Picó-Pérez, M., Radua, J., Steward, T., Menchón, J. M. & Soriano-Mas, C. Emotion regulation in mood and anxiety disorders: A meta-analysis of fMRI cognitive reappraisal studies. Prog. Neuro-Psychopharmacol. Biol. Psychiatry 79, 96–104 (2017).
Eftekhari, A., Zoellner, L. A. & Vigil, S. A. Patterns of emotion regulation and psychopathology. Anxiety Stress Coping 22, 571–586 (2009).
pubmed: 19381989
pmcid: 3234115
Aldao, A., Sheppes, G. & Gross, J. J. Emotion regulation flexibility. Cogn. Ther. Res. 39, 263–278 (2015).
Webb, T. L., Miles, E. & Sheeran, P. Dealing with feeling: A meta-analysis of the effectiveness of strategies derived from the process model of emotion regulation. Psychol. Bull. 138, 775–808 (2012).
pubmed: 22582737
Etkin, A., Büchel, C. & Gross, J. J. The neural bases of emotion regulation. Nat. Rev. Neurosci. 16, 693–700 (2015).
pubmed: 26481098
Kanske, P., Heissler, J., Schönfelder, S., Bongers, A. & Wessa, M. How to regulate emotion? Neural networks for reappraisal and distraction. Cereb. Cortex 21, 1379–1388 (2011).
pubmed: 21041200
Ochsner, K. N., Silvers, J. A. & Buhle, J. T. Functional imaging studies of emotion regulation: A synthetic review and evolving model of the cognitive control of emotion. Ann. N. Y. Acad. Sci. 1251, E1–E24 (2012).
pubmed: 23025352
pmcid: 4133790
Kalisch, R. The functional neuroanatomy of reappraisal: Time matters. Neurosci. Biobehav. Rev. 33, 1215–1226 (2009).
pubmed: 19539645
Wang, M. & Saudino, K. J. Emotion regulation and stress. J. Adult Dev. 18, 95–103 (2011).
Joëls, M. & Baram, T. Z. The neuro-symphony of stress. Nat. Rev. Neurosci. 10, 459–466 (2009).
pubmed: 19339973
pmcid: 2844123
Dedovic, K., Duchesne, A., Andrews, J., Engert, V. & Pruessner, J. C. The brain and the stress axis: The neural correlates of cortisol regulation in response to stress. Neuroimage 47, 864–871 (2009).
pubmed: 19500680
De Kloet, E. R. Hormones and the stressed brain. Ann. N. Y. Acad. Sci. 1018, 1–15 (2004).
pubmed: 15240347
Ochsner, K. N. & Gross, J. J. The cognitive control of emotion. Trends Cogn. Sci. 9, 242–249 (2005).
pubmed: 15866151
Raio, C. M., Orederu, T. A., Palazzolo, L., Shurick, A. A. & Phelps, E. A. Cognitive emotion regulation fails the stress test. Proc. Natl. Acad. Sci. 110, 15139–15144 (2013).
pubmed: 23980142
Arnsten, A. F. T. Stress signalling pathways that impair prefrontal cortex structure and function. Nat. Rev. Neurosci. 10, 410–422 (2009).
pubmed: 19455173
pmcid: 19455173
Nater, U. M. & Rohleder, N. Salivary alpha-amylase as a non-invasive biomarker for the sympathetic nervous system: Current state of research. Psychoneuroendocrinology 34, 486–496 (2009).
pubmed: 19249160
Hermans, E. J., Henckens, M. J. A. G., Joëls, M. & Fernández, G. Dynamic adaptation of large-scale brain networks in response to acute stressors. Trends Neurosci. 37, 304–314 (2014).
pubmed: 24766931
Schwabe, L. & Wolf, O. T. Stress and multiple memory systems: From ‘thinking’ to ‘doing’. Trends Cogn. Sci. 17, 68 (2013).
Fournier, M., d’Arripe-Longueville, F. & Radel, R. Effects of psychosocial stress on the goal-directed and habit memory systems during learning and later execution. Psychoneuroendocrinology 77, 275–283 (2017).
pubmed: 28131067
Wirz, L., Bogdanov, M. & Schwabe, L. Habits under stress: Mechanistic insights across different types of learning. Curr. Opin. Behav. Sci. 20, 9–16 (2018).
Kinner, V. L., Het, S. & Wolf, O. T. Emotion regulation: Exploring the impact of stress and sex. Front. Behav. Neurosci. 8, 1–8 (2014).
Jentsch, V. L., Merz, C. J. & Wolf, O. T. Restoring emotional stability: Cortisol effects on the neural network of cognitive emotion regulation. Behav. Brain Res. 374, 111880 (2019).
pubmed: 30946860
Het, S., Schoofs, D., Rohleder, N. & Wolf, O. T. Stress-induced cortisol level elevations are associated with reduced negative affect after stress: Indications for a mood-buffering cortisol effect. Psychosom. Med. 74, 23–32 (2012).
pubmed: 22155939
Reuter, M. Impact of cortisol on emotions under stress and nonstress conditions: A pharmacopsychological approach. Neuropsychobiology 46, 41–48 (2002).
pubmed: 12207146
Soravia, L. M. et al. Glucocorticoids reduce phobic fear in humans. Proc. Natl. Acad. Sci. 103, 5585–5590 (2006).
pubmed: 16567641
Denson, T. F., Creswell, J. D., Terides, M. D. & Blundell, K. Cognitive reappraisal increases neuroendocrine reactivity to acute social stress and physical pain. Psychoneuroendocrinology 49, 69–78 (2014).
pubmed: 25063879
Lam, S., Dickerson, S. S., Zoccola, P. M. & Zaldivar, F. Emotion regulation and cortisol reactivity to a social-evaluative speech task. Psychoneuroendocrinology 34, 1355–1362 (2009).
pubmed: 19464808
Roos, L. G., Levens, S. M. & Bennett, J. M. Stressful life events, relationship stressors, and cortisol reactivity: The moderating role of suppression. Psychoneuroendocrinology 89, 69–77 (2018).
pubmed: 29331801
pmcid: 5878721
Het, S. & Wolf, O. T. Mood changes in response to psychosocial stress in healthy young women: Effects of pretreatment with cortisol. Behav. Neurosci. 121, 11–20 (2007).
pubmed: 17324047
McRae, K., Ochsner, K. N., Mauss, I. B., Gabrieli, J. J. D. & Gross, J. J. Gender differences in emotion regulation: An fMRI study of cognitive reappraisal. Gr. Process. Intergr. Relat. 11, 143–162 (2008).
Bradley, M. M., Codispoti, M., Sabatinelli, D. & Lang, P. J. Emotion and motivation II: Sex differences in picture processing. Emotion 1, 300–319 (2001).
pubmed: 12934688
Goubet, K. E. & Chrysikou, E. G. Emotion regulation flexibility: Gender differences in context sensitivity and repertoire. Front. Psychol. 10 (2019).
Kinner, V. L. et al. What our eyes tell us about feelings: Tracking pupillary responses during emotion regulation processes. Psychophysiology 54, 508–518 (2017).
pubmed: 28072452
Urry, H. L. Amygdala and ventromedial prefrontal cortex are inversely coupled during regulation of negative affect and predict the diurnal pattern of cortisol secretion among older adults. J. Neurosci. 26, 4415–4425 (2006).
pubmed: 16624961
pmcid: 6673990
van Reekum, C. M. et al. Gaze fixations predict brain activation during the voluntary regulation of picture-induced negative affect. Neuroimage 36, 1041–1055 (2007).
pubmed: 17493834
Kirschbaum, C., Kudielka, B. M., Gaab, J., Schommer, N. C. & Hellhammer, D. H. Impact of gender, menstrual cycle phase, and oral contraceptives on the activity of the hypothalamus–pituitary–adrenal axis. Psychosom. Med. 61, 154–162 (1999).
pubmed: 10204967
Pagliaccio, D. et al. Amygdala functional connectivity, HPA axis genetic variation, and life stress in children and relations to anxiety and emotion regulation. J. Abnorm. Psychol. 124, 817–833 (2015).
pubmed: 26595470
pmcid: 4662045
Henckens, M. J. A. G., Van Wingen, G. A., Joëls, M. & Fernández, G. Time-dependent effects of corticosteroids on human amygdala processing. J. Neurosci. 30, 12725–12732 (2010).
pubmed: 20861377
pmcid: 6633587
Putman, P., Hermans, E. J., Koppeschaar, H., van Schijndel, A. & van Honk, J. A single administration of cortisol acutely reduces preconscious attention for fear in anxious young men. Psychoneuroendocrinology 32, 793–802 (2007).
pubmed: 17604912
Allaert, J., Sanchez-Lopez, A., De Raedt, R., Baeken, C. & Vanderhasselt, M. A. Inverse effects of tDCS over the left versus right DLPC on emotional processing: A pupillometry study. PLoS ONE 14, 1–16 (2019).
Peña-Gómez, C., Vidal-Piñeiro, D., Clemente, I. C., Pascual-Leone, Á. & Bartrés-Faz, D. Down-regulation of negative emotional processing by transcranial direct current stimulation: Effects of personality characteristics. PLoS One 6 (2011).
Otto, A. R., Raio, C. M., Chiang, A., Phelps, E. A. & Daw, N. D. Working-memory capacity protects model-based learning from stress. Proc. Natl. Acad. Sci. 110, 20941–20946 (2013).
pubmed: 24324166
Hermans, E. J. et al. Stress-related noradrenergic activity prompts large-scale neural network reconfiguration. Science (80-). 334, 1151–1153 (2011).
Oei, N. Y. L. et al. Stress shifts brain activation towards ventral ‘affective’ areas during emotional distraction. Soc. Cogn. Affect. Neurosci. 7, 403–412 (2012).
pubmed: 21498384
Luethi, M., Meier, B. & Sandi, C. Stress effects on working memory, explicit memory, and implicit memory for neutral and emotional stimuli in healthy men. Front. Behav. Neurosci. 3, 1–9 (2009).
Liu, J. J. W. et al. Sex differences in salivary cortisol reactivity to the Trier Social Stress Test (TSST): A meta-analysis. Psychoneuroendocrinology 82, 26–37 (2017).
pubmed: 28486178
De Kloet, E. R., Oitzl, M. S. & Joëls, M. Stress and cognition: Are corticosteroids good or bad guys?. Trends Neurosci. 22, 422–426 (1999).
pubmed: 10481183
Joëls, M. Corticosteroid effects in the brain: U-shape it. Trends Pharmacol. Sci. 27, 244–250 (2006).
pubmed: 16584791
Merz, C. J. & Wolf, O. T. Sex differences in stress effects on emotional learning. J. Neurosci. Res. 95, 93–105 (2017).
pubmed: 27870431
Andreano, J. M. & Cahill, L. Glucocorticoid release and memory consolidation in men and women. Psychol. Sci. 17, 466–470 (2006).
pubmed: 16771794
Cornelisse, S., van Stegeren, A. H. & Joëls, M. Implications of psychosocial stress on memory formation in a typical male versus female student sample. Psychoneuroendocrinology 36, 569–578 (2011).
pubmed: 20933337
Merz, C. J. Contribution of stress and sex hormones to memory encoding. Psychoneuroendocrinology 82, 51–58 (2017).
pubmed: 28501551
ter Horst, J. P., de Kloet, E. R., Schächinger, H. & Oitzl, M. S. Relevance of stress and female sex hormones for emotion and cognition. Cell. Mol. Neurobiol. 32, 725–735 (2012).
pubmed: 22113371
Lennartsson, A. K., Kushnir, M. M., Bergquist, J. & Jonsdottir, I. H. DHEA and DHEA-S response to acute psychosocial stress in healthy men and women. Biol. Psychol. 90, 143–149 (2012).
pubmed: 22445967
Shields, G. S., Sazma, M. A. & Yonelinas, A. P. The effects of acute stress on core executive functions: A meta-analysis and comparison with cortisol. Neurosci. Biobehav. Rev. 68, 651–668 (2016).
pubmed: 27371161
pmcid: 5003767
McEwen, B. S., Nasca, C. & Gray, J. D. Stress effects on neuronal structure: Hippocampus, amygdala, and prefrontal cortex. Neuropsychopharmacology 41, 3–23 (2016).
pubmed: 26076834
Schoofs, D. & Wolf, O. T. Stress and memory retrieval in women: No strong impairing effect during the luteal phase. Behav. Neurosci. 123, 547–554 (2009).
pubmed: 19485561
Krishnan, A. V., Swami, S. & Feldman, D. Estradiol inhibits glucocorticoid receptor expression and induces glucocorticoid resistance in MCF-7 human breast cancer cells. J. Steroid Biochem. Mol. Biol. 77, 29–37 (2001).
pubmed: 11358672
Zaehringer, J., Jennen-Steinmetz, C., Schmahl, C., Ende, G. & Paret, C. Psychophysiological effects of downregulating negative emotions: Insights from a meta-analysis of healthy adults. Front. Psychol. 11 (2020).
Zaehringer, J., Falquez, R., Schubert, A. L., Nees, F. & Barnow, S. Neural correlates of reappraisal considering working memory capacity and cognitive flexibility. Brain Imaging Behav. 0, 1–15 (2018).
Matejka, M. et al. Talking about emotion: Prosody and skin conductance indicate emotion regulation. Front. Psychol. 4, 1–11 (2013).
Appelhans, B. M. & Luecken, L. J. Heart rate variability as an index of regulated emotional responding. Rev. Gen. Psychol. 10, 229–240 (2006).
Guilliams, T. G. & Edwards, L. E. Chronic stress and the HPA Axis: Clinical assessment and therapeutic considerations. Stand. 9 (2010).
Dickerson, S. S. & Kemeny, M. E. Acute stressors and cortisol responses: A theoretical integration and synthesis of laboratory research. Psychol. Bull. 130, 355–391 (2004).
pubmed: 15122924
Kirschbaum, C., Pirke, K. M. & Hellhammer, D. H. The ‘Trier social stress test’—A tool for investigating psychobiological stress responses in a laboratory setting. Neuropsychobiology 28, 76–81 (1993).
pubmed: 8255414
pmcid: 8255414
Het, S., Rohleder, N., Schoofs, D., Kirschbaum, C. & Wolf, O. T. Neuroendocrine and psychometric evaluation of a placebo version of the ‘Trier Social Stress Test’. Psychoneuroendocrinology 34, 1075–1086 (2009).
pubmed: 19307062
Lorentz, K., Gütschow, B. & Renner, F. Evaluation of a direct α-amylase assay using 2-chloro-4-nitrophenyl-α-D-maltotrioside. Clin. Chem. Lab. Med. 37, 1053–1062 (1999).
pubmed: 10726812
Grillon, C., Quispe-Escudero, D., Mathur, A. & Ernst, M. Mental fatigue impairs emotion regulation. Emotion 15, 383–389 (2015).
pubmed: 25706833
pmcid: 4437828
Strauss, G. P., Ossenfort, K. L. & Whearty, K. M. Reappraisal and distraction emotion regulation strategies are associated with distinct patterns of visual attention and differing levels of cognitive demand. PLoS ONE 11, 1–18 (2016).
Feeser, M., Prehn, K., Kazzer, P., Mungee, A. & Bajbouj, M. Transcranial direct current stimulation enhances cognitive control during emotion regulation. Brain Stimul. 7, 105–112 (2014).
pubmed: 24095257
Marchewka, A., Zurawski, Ł, Jednoróg, K. & Grabowska, A. The Nencki Affective Picture System (NAPS): Introduction to a novel, standardized, wide-range, high-quality, realistic picture database. Behav. Res. Methods 46, 596–610 (2014).
pubmed: 23996831
Bardeen, J. R. & Daniel, T. A. An eye-tracking examination of emotion regulation, attentional bias, and pupillary response to threat stimuli. Cogn. Ther. Res. 41, 853–866 (2017).
Kret, M. E., Tomonaga, M. & Matsuzawa, T. Chimpanzees and humans mimic pupil-size of conspecifics. PLoS One 9 (2014).
Kret, M. E. & Sjak-Shie, E. E. Preprocessing pupil size data: Guidelines and code. Behav. Res. Methods https://doi.org/10.3758/s13428-018-1075-y (2018).
doi: 10.3758/s13428-018-1075-y
pmcid: 6538573