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Psychosocial stress induces working memory impairments in an n-back paradigm.
Abstract
In contrast to the substantial number of studies investigating the effects of stress on declarative memory, effects of stress on working memory have received less attention. We compared working memory (numerical n-back task with single digits) in 40 men exposed either to psychosocial stress (Trier Social Stress Test (TSST)) or a control condition. Task difficulty was varied using two conditions (2-back vs. 3-back). Salivary cortisol (as a marker of hypothalamus-pituitary-adrenal (HPA) activity) and salivary alpha-amylase (sAA as a marker of sympathetic nervous system (SNS) activity) were assessed immediately before and three times after the stress or control condition. As expected stress resulted in an increase in cortisol, sAA, and negative affect. Subjects exposed to stress showed significant working memory impairments in both workload conditions. The analysis of variance indicated a main effect of stress for reaction time as well as accuracy. In addition, for reaction time a stress-block interaction occurred. Follow up tests revealed that only during the first block at each level of difficulty performance was significantly impaired by stress. Thus, the effects of stress became smaller the longer the task was performed. Results provide further evidence for impaired working memory after acute stress and illustrate the time course of this phenomenon.
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“In humans experimental or pharmacological stress studies have reported inconsistent effects with impairments as well as enhancements being reported [42], [46], [47].”
From Dose-dependent effects of endotoxin on neurobehavioral functions in humans (2011) · cites this paper as [42]
In the citing paper
“Thus, in the current study we employed a computerized n-back paradigm (2-back version), a well-evaluated sensitive tool to analyze working memory functions [34], [41], [42].”
From Dose-dependent effects of endotoxin on neurobehavioral functions in humans (2011) · cites this paper as [42]
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“Since the physiological stress response seems to modulate prefrontal cortical functions (Fuchs et al., 2006; Diamond et al., 2007; McEwen, 2007) it might be possible that n-back performance is particularly impaired when the task processing strongly occupies the cognitive resources.”
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“For example a growing literature suggests that stress influences working memory, which relies on the prefrontal cortex (Lupien et al., 1999; Oei et al., 2006; Schoofs et al., 2008b ).”
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“…on hippocampus- and prefrontal cortex-dependent memory follow an inverted U-shaped function, with moderate stress levels facilitating, while high levels impairing, memory function (Cordero and Sandi, 1998; Del Arco et al., 2007; Sandi and Pinelo-Nava, 2007; Sandi et al., 1997; Selden et al., 1990).”
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“These findings together with other recent studies (Oei et al., 2006; Schoofs et al., 2008) indicate that stress impairs performance in demanding WM tasks requiring maintenance and executive processing of information.”
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“Importantly, stress and glucocorticoids are known to influence working memory especially under emotionally arousing test conditions, whereas the valence of the information acquired in working memory does not seem to be an important variable (36, 37).”
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“Thus, in the current study we employed a computerized n-back paradigm (2back version), a well-evaluated sensitive tool to analyze working memory functions [34,41,42].”
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“A second limitation is that sampling saliva in two-minute intervals somewhat changed the ‘‘normal’’ procedure of the TSST.”
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(2013) · Handbook of Clinical Neurology · doi:10.1016/b978-0-444-53491-0.00006-7 · Cited by 230
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“psychosocial stress [5], and pharmacological manipulations [6] create intra-individual variability in cognitive performance, such that an individual’s working memory capacity may vary at different times.”
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ResultSelf-citationPrefrontal cortex executive processes affected by stress in health and disease
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“Everaerd et al., 2006; Gärtner et al., 2014; Luethi et al., 2009; Schoofs et al., 2008), some find a beneficial effect (Cornelisse et al., 2011; Thompson and Morgan, 2013; Weerda et al., 2010) and others no differences ( al’Absi and Hoffman, 2004; Kuhlmann et al., 2005; Smeets et al., 2006).”
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“At present, the most reported concern is that acute stress can affect the learning and working memory ability of people and animals [3, 4].”
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“supra) while the no-stress control group completed a non-stressful control task of equal duration (i.e., delivering a speech and performing an undemanding counting task by themselves in an otherwise empty room; see Kuhlmann et al., 2005; Schoofs et al., 2008).”
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“Overall, these findings contrast with some (Elzinga and Roelofs, 2005; Oei et al., 2006; Luethi et al., 2008; Schoofs et al., 2008; Schoofs et al., 2009) but are in agreement with other studies on the effects of stress on working memory (Kuhlmann et al., 2005; Duncko et al., 2009; Oei et al., 2009;…”
InfluentialStress-Induced Cortisol Level Elevations Are Associated With Reduced Negative Affect After Stress
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“With regard to current affective state, the participants in the stress group reported more negative affect after the experimental manipulations, which is again in line with other studies (6,8,16,31).”
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“Stress is ubiquitous, and previous research suggests it can have both negative (Oei et al., 2006; Schoofs et al., 2008, 2009) and positive (Duncko et al., 2009; Weerda et al., 2010) effects on cognitive function.”
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“They then received instructions for the N-Back Task and completed practice trials.”
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“…of C a few human studies observed negative effects of high C-level or stress-treatment on working memory (Wolf et al., 2001; Elzinga and Roelofs, 2005; Oei et al., 2006; Schoofs et al., 2008), while mild stress is supposed to result in enhanced working memory performance (Schoofs et al., 2008).”
InfluentialEffects of Acute Laboratory Stress on Executive Functions
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“…demonstrated for a wide range of cognitive functions like working memory (Elzinga and Roelofs, 2005; Oei et al., 2006, 2009; Lupien et al., 2007; Schoofs et al., 2008; Weerda et al., 2010), declarative memory (de Quervain et al., 2000, 2003; Buchanan et al., 2006), emotional information…”
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“Recent studies also investigated other cognitive functions like working memory (e.g., Schoofs et al., 2008; see also Buckert et al., 2012) and executive functions (e.g., Scholz et al., 2009; Plessow et al., 2012) under acute stress.”
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“On the one hand, GCs released during (Elzinga and Roelofs, 2005) and after stress (Oei et al., 2006; Schoofs et al., 2008) have been related to reduced WM performance.”
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“Thus, some studies reported impairments in working memory after acute stress (Luethi et al., 2008; Schoofs et al. 2008, 2009) or after acute administration of corticosteroids (Lupien et al., 1999).”
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“Similar to previous studies [Porcelli et al., 2008; Qin et al., 2009; Schoofs et al., 2008], we found only a weak effect of stress on behavioral measures in the WM task.”
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“Others have found similar stress-related impairment to working memory tasks without reinforcement (e.g., Schoofs et al., 2008; Schoofs et al., 2009).”
HPA Axis Interactions with Behavioral Systems
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“…have shown that stress or pharmacological manipulations that increase glucocorticoids can impair spatial memory in rodents (32,135,136,422,450, 451,467,596) and humans (349,370,378,448,478,479,537, 590,591), while other studies have found that stress improves working memory performance (607,608).”
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Working memory-related frontal theta activity is decreased under acute stress
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“Consistent with this assumption it has been shown that impairing effects of stress on WM performance are especially strong in a time range in which both stress systems (SNS and HPA) are activated (Elzinga and Roelofs, 2005; Schoofs et al., 2008).”
BackgroundStress reduces use of negative feedback in a feedback-based learning task.
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Working memory and self-regulation
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Stress disrupts context-dependent memoryPreprint
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“…cortex, such as spatial or working memory, are often impaired when stress or cortisol was administered before learning (Lupien et al. 1999; Schwabe et al. 2007; Schoofs et al. 2008; but see also Nater et al. 2007 and Schwabe et al. 2008a for reports of enhanced memory following prelearning stress).”
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Hydrocortisone reduces emotional distracter interference in working memory
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“These results are inconsistent with several studies that found WM impairments after stress and GC administration (Lupien et al., 1999; Oei et al., 2006; Schoofs et al., 2008).”
InfluentialRoos, L. E., Knight, E. L., Beauchamp, K. G., Berkman, E. T., Faraday, K., Hyslop, K., & Fisher, P. A. (2017) · Biological Psychology · doi:10.1016/j.biopsycho.2017.03.004 · Cited by 97
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“In contrast to our hypothesis and to several (but not all) studies in adults (Elzinga and Roelofs, 2005; Oei et al., 2006; Luethi et al., 2008; Schoofs et al., 2008), no impairments were found on WM.”
MethodResultSelf-citationQin, S., Cousijn, H., Rijpkema, M., Luo, J., Franke, B., Hermans, E. J., & Fernández, G. (2012) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2012.00016 · Cited by 83
“, 2008, 2009), particularly when high levels of cortisol and noradrenergic activity occurred concurrently (Elzinga and Roelofs, 2005; Schoofs et al., 2008).”
BackgroundInfluentialOccupational stressors and job performance: An updated review and recommendations
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“The fMRI paradigm In the fMRI within-subject design, three different experimental tasks were used: an fMRI version of the original GDT (see description in Brand et al. 2005), the GDT plus a parallel 2-back task (c.f. Starcke et al. 2011), and a single 2-back task (c.f. Schoofs et al. 2008).”
BackgroundMethodSelf-citationDecomposing the n-back task: An individual differences study using the reference-back paradigm
Rac-Lubashevsky, R., & Kessler, Y. (2016) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2016.07.013 · Cited by 96
Angelidis, A., Solis, E. C., Lautenbach, F., van der Does, W. A. J., & Putman, P. (2019) · PLoS ONE · doi:10.1371/journal.pone.0210824 · Cited by 100
Impaired hippocampus-dependent and -independent learning in IL-6 deficient mice.
Baier, P. C., May, U., Scheller, J., Rose-John, S., & Schiffelholz, T. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.01.013 · Cited by 84
Shields, G. S., Moons, W. G., & Slavich, G. M. (2017) · Stress · doi:10.1080/10253890.2017.1286322 · Cited by 87
“Affective responses to the laboratory task Because stress is known to induce negative affect (e.g. Schoofs et al., 2008), we used a self-report questionnaire assessing negative affect as an additional manipulation check.”
Anticipatory stress interferes with utilitarian moral judgment
Starcke, K., Ludwig, A.-C., & Brand, M. (2012) · Judgment and Decision Making · doi:10.1017/s1930297500001832 · Cited by 81
TNF-α from hippocampal microglia induces working memory deficits by acute stress in mice
Ohgidani, M., Kato, T. A., Sagata, N., Hayakawa, K., Shimokawa, N., Sato‐Kasai, M., & Kanba, S. (2015) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2015.08.022 · Cited by 79
“Thus, the hippocampus is highly sensitive to stress 16 (Kim and Diamond, 2002; Roozendaal et al., 2009), and stress impairs working memory 17 (WM), which is a key hippocampal function in both rodents and humans (Conrad et al., 18 2004; Schoofs et al., 2008).”
Entringer, S., Buß, C., Kumsta, R., Hellhammer, D. H., Wadhwa, P. D., & Wüst, S. (2009) · Behavioral Neuroscience · doi:10.1037/a0016265 · Cited by 79
Schoofs, D., & Wolf, O. T. (2011) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2011.01.008 · Cited by 79
Self-citationParadoxical effects of stress and an executive task on decisions under risk.
Pabst, S., Schoofs, D., Pawlikowski, M., Brand, M., & Wolf, O. T. (2013) · Behavioral Neuroscience · doi:10.1037/a0032334 · Cited by 74
Self-citationHofmann, W., Finkel, E. J., & Fitzsimons, G. M. (2015) · Journal of Personality and Social Psychology · doi:10.1037/pspi0000020 · Cited by 85
“In line with earlier research from other domains (Kemps et al., 2008; Klein & Boals, 2001; Schmader & Johns, 2003; Schoofs et al., 2008), we suggest that negative, compared with positive, SRS creates relationship worries and distress that intrude into working memory, thus reducing people’s…”
ResultPornographic Picture Processing Interferes with Working Memory Performance
Laier, C., Schulte, F. P., & Brand, M. (2012) · The Journal of Sex Research · doi:10.1080/00224499.2012.716873 · Cited by 80
“Comparably to Schoofs, Preuss, and Wolf (2008), each image was shown for 500 milliseconds (ms), followed by an interstimulus interval of 2500 ms.”
MethodShields, G. S., Doty, D., Shields, R. H., Gower, G., Slavich, G. M., & Yonelinas, A. P. (2017) · Stress · doi:10.1080/10253890.2017.1380620 · Cited by 71
Acute psychosocial stress effects on memory performance: Relevance of age and sex
Hidalgo, V., Pulopulos, M. M., & Salvador, A. (2018) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2018.11.013 · Cited by 80
Berry, D. J. (2011) · Journal of Applied Developmental Psychology · doi:10.1016/j.appdev.2011.10.002 · Cited by 79
Stress and memory retrieval in women: No strong impairing effect during the luteal phase.
Schoofs, D., & Wolf, O. T. (2009) · Behavioral Neuroscience · doi:10.1037/a0015625 · Cited by 68
Self-citationCortisol modifies extinction learning of recently acquired fear in men
Merz, C. J., Hermann, A., Stark, R. M., & Wolf, O. T. (2013) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nst137 · Cited by 69
Self-citationRubin, L. H., Cook, J. Α., Weber, K. M., Cohen, M. H., Martin, E. M., Valcour, V., Milam, J. E., Anastos, K., Young, M., Alden, C. B., et al. (2015) · Journal of NeuroVirology · doi:10.1007/s13365-015-0331-5 · Cited by 66
“Although previous studies demonstrate that psychosocial stressors impair working memory (Olver et al. 2014; Schoofs et al. 2008), we did not find an association between stress and working memory in the present cohort.”
Ha, U., Lee, Y., Kim, H., Roh, T., Bae, J., Kim, C., & Yoo, H. (2016) · IEEE Transactions on Biomedical Circuits and Systems · doi:10.1109/tbcas.2015.2504959 · Cited by 65
“The result shows the increased accuracy for the tasks of the classification results in [20]–[22].”
MethodShields, G. S., Rivers, A. M., Ramey, M. M., Trainor, B. C., & Yonelinas, A. P. (2019) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2019.06.001 · Cited by 72
“We adopt such a definition because laboratory inductions of moderate stress produce a two- to threefold increase in cortisol (e.g., Oei et al., 2006; Preuß and Wolf, 2009; Schoofs et al., 2008; Shields et al., 2017b).”
MethodStress, Coping and Cognitive Deficits in Women After Surgery for Breast Cancer
Reid‐Arndt, S. A., & Cox, C. R. (2012) · Journal of Clinical Psychology in Medical Settings · doi:10.1007/s10880-011-9274-z · Cited by 69
Williams, T. B., Corbett, J., McMorris, T., Young, J. S., Dicks, M., Ando, S., Thelwell, R., Tipton, M., & Costello, J. T. (2019) · Experimental Physiology · doi:10.1113/ep087647 · Cited by 68
“The second, and slightly slower, response consists of activation of the HPA axis and leads to the release of glucocorticoids from the adrenal cortex (e.g. cortisol) (Schoofs et al., 2008).”
BackgroundAffective decision making under uncertainty during a plausible aviation task: An fMRI study
Causse, M., Péran, P., Dehais, F., Caravasso, C. F., Zeffiro, T. A., Sabatini, U., & Pastor, J. (2013) · NeuroImage · doi:10.1016/j.neuroimage.2012.12.060 · Cited by 63
Stenfors, C. U. D., Marklund, P., Magnusson Hanson, L. L., Theorell, T., & Nilsson, L.-G. (2013) · PLoS ONE · doi:10.1371/journal.pone.0083351 · Cited by 58
“Executive functions like WM and attentional shifting seem to be particularly vulnerable to detrimental effects from both acute [34-39] and chronic [40-44] stress exposures, which may be particularly relevant when considering SCC among individuals in the work force.”
BackgroundDerry, H. M., Reid, M. C., & Prigerson, H. G. (2019) · Cancer Medicine · doi:10.1002/cam4.2331 · Cited by 61
Stress, Sleep, and Performance on Standardized Tests: Understudied Pathways to the Achievement Gap
Heissel, J. A., Levy, D. J., & Adam, E. K. (2017) · AERA Open · doi:10.1177/2332858417713488 · Cited by 74
Control when it counts: Change in executive control under stress predicts depression symptoms.
Quinn, M. E., & Joormann, J. (2015) · Emotion · doi:10.1037/emo0000089 · Cited by 64
Self-regulation and its failure: The seven deadly threats to self-regulation.
Wagner, D. D., & Heatherton, T. F. (2014) · American Psychological Association eBooks · doi:10.1037/14341-026 · Cited by 66
Influence of acute stress on response inhibition in healthy men: An ERP study
Dierolf, A. M., Fechtner, J., Böhnke, R., Wolf, O. T., & Naumann, E. (2017) · Psychophysiology · doi:10.1111/psyp.12826 · Cited by 63
Self-citationEngert, V., Kok, B. E., Puhlmann, L. M. C., Stalder, T., Kirschbaum, C., Apostolakou, F., Papanastasopoulou, C., Papassotiriou, I., Pervanidou, P., Chrousos, G. P., et al. (2018) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2018.05.023 · Cited by 57
Stress & executive functioning: A review considering moderating factors
Plieger, T., & Reuter, M. (2020) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2020.107254 · Cited by 73
Metadata
- Authors
- Schoofs, D., Preuß, D., & Wolf, O. T.
- Affiliations
- Ruhr University Bochum (DE)
- Corresponding author
- Wolf, Oliver T.
- ORCID
- Wolf, Oliver T.
- Venue
- Psychoneuroendocrinology
- Publisher
- Elsevier BV
- Published
- 2008-06
- Volume
- 33
- Issue
- 5
- Pages
- 643-653
- ISSN
- 0306-4530 (ISSN-L)
- OpenAlex
- W2106673407
- Semantic Scholar
- 87cef5ba5bb29154704cb81de2376ff5360b6a6f
- Cited by
- 483
- References
- 93
- Citations by year
- 2026: 13 · 2025: 19 · 2024: 20 · 2023: 22 · 2022: 34 · 2021: 36 · 2020: 37 · 2019: 35 · 2018: 26 · 2017: 27 · 2016: 40 · 2015: 24 · 2014: 29 · 2013: 27 · 2012: 21
- FWCI
- 11.00
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Psychoneuroendocrinology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Deutsche Forschungsgemeinschaft
- Universität Bielefeld
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Cognitive Abilities and Testing
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Keywords
- psychosocial stress, working memory, n-back task, Trier Social Stress Test, salivary cortisol, salivary amylase, hypothalamic-pituitary-adrenal axis, sympathetic nervous system, negative affect, acute stress, task difficulty, reaction time, cognitive performance
- MeSH terms
- Adult, Affect, alpha-Amylases, Analysis of Variance, Humans, Hydrocortisone, Male, Memory, Memory Disorders, Reaction Time, Saliva, Stress, Psychological, Task Performance and Analysis, Time Factors
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