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Neural and Behavioral Measures of Stress-induced Impairment in Error Awareness and Post-error Adjustment

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Abstract

Exposure to stress negatively affects error processing, but the impact of stress on error awareness remains to be determined. In the present study, we examined the temporal dynamics of error awareness and post-error adjustment following acute stress. Forty-nine healthy men were randomly assigned to the control (n = 26) or stress group (n = 23). After stress induction, participants completed the error awareness task, and their brain activity was assessed by electroencephalography. Compared to the control group, the stress group demonstrated lower error awareness accuracy and smaller Pe (error positivity) and ΔPe amplitudes following aware error responses, which indicated impairment of error awareness following stress. Furthermore, the stress group had lower accuracy in post-aware error responses than in post-unaware error responses and the control group, which indicated poor post-error adjustment following stress. Our results showed a stress effect on sequential stages of error processing. Stress induces impaired error identification, which further generates maladaptive post-error performance.

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Data Availability

Data supporting the findings of this study are available from the corresponding author upon reasonable request.

References

  1. Munck A, Guyre PM, Holbrook NJ. Physiological functions of glucocorticoids in stress and their relation to pharmacological actions. Endocr Rev 1984, 5: 25–44.

    Article  CAS  PubMed  Google Scholar 

  2. Sousa N, Cerqueira JJ, Almeida OF. Corticosteroid receptors and neuroplasticity. Brain Res Rev 2008, 57: 561–570.

    Article  CAS  PubMed  Google Scholar 

  3. Ulrich-Lai YM, Herman JP. Neural regulation of endocrine and autonomic stress responses. Nat Rev Neurosci 2009, 10: 397–409.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. de Kloet ER, Joëls M, Holsboer F. Stress and the brain: From adaptation to disease. Nat Rev Neurosci 2005, 6: 463–475.

    Article  PubMed  Google Scholar 

  5. Roozendaal B, Okuda S, van der Zee EA, McGaugh JL. Glucocorticoid enhancement of memory requires arousal-induced noradrenergic activation in the basolateral amygdala. Proc Natl Acad Sci U S A 2006, 103: 6741–6746.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Arnsten AF. Stress signalling pathways that impair prefrontal cortex structure and function. Nat Rev Neurosci 2009, 10: 410–422.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Plessow F, Fischer R, Kirschbaum C, Goschke T. Inflexibly focused under stress: Acute psychosocial stress increases shielding of action goals at the expense of reduced cognitive flexibility with increasing time lag to the stressor. J Cogn Neurosci 2011, 23: 3218–3227.

    Article  PubMed  Google Scholar 

  8. Sänger J, Bechtold L, Schoofs D, Blaszkewicz M, Wascher E. The influence of acute stress on attention mechanisms and its electrophysiological correlates. Front Behav Neurosci 2014, 8: 353.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Gehring WJ, Goss B, Coles MGH, Meyer DE, Donchin E. The error-related negativity. Perspect Psychol Sci 2018, 13: 200–204.

    Article  PubMed  Google Scholar 

  10. Laming D. Choice reaction performance following an error. Acta Psychol 1979, 43: 199–224.

    Article  Google Scholar 

  11. Li Q, Hu N, Li Y, Long Q, Gu Y, Tang Y. Error-induced adaptability: Behavioral and neural dynamics of response-stimulus interval modulations on posterror slowing. J Exp Psychol Gen 2021, 150: 851–863.

    Article  PubMed  Google Scholar 

  12. Botvinick MM, Braver TS, Barch DM, Carter CS, Cohen JD. Conflict monitoring and cognitive control. Psychol Rev 2001, 108: 624–652.

    Article  CAS  PubMed  Google Scholar 

  13. van Veen V, Krug MK, Carter CS. The neural and computational basis of controlled speed-accuracy tradeoff during task performance. J Cogn Neurosci 2008, 20: 1952–1965.

    Article  PubMed  Google Scholar 

  14. Clemans ZA, El-Baz AS, Hollifield M, Sokhadze EM. Single trial time-frequency domain analysis of error processing in post-traumatic stress disorder. Neurosci Lett 2012, 525: 105–110.

    Article  CAS  PubMed  Google Scholar 

  15. Cavanagh JF, Allen JJ. Multiple aspects of the stress response under social evaluative threat: An electrophysiological investigation. Psychoneuroendocrinology 2008, 33: 41–53.

    Article  PubMed  Google Scholar 

  16. Hu N, Hu X, Xu Z, Li Q, Long Q, Gu Y, et al. Temporal dynamic modulation of acute stress on error processing in healthy males. Psychophysiology 2019, 56: e13398.

    Article  PubMed  Google Scholar 

  17. Whitton AE, Van’t Veer A, Kakani P, Dillon DG, Ironside ML, Haile A, et al. Acute stress impairs frontocingulate activation during error monitoring in remitted depression. Psychoneuroendocrinology 2017, 75: 164–172.

    Article  PubMed  Google Scholar 

  18. Themanson JR, Ball AB, Khatcherian SM, Rosen PJ. The effects of social exclusion on the ERN and the cognitive control of action monitoring. Psychophysiology 2014, 51: 215–225.

    Article  PubMed  Google Scholar 

  19. di Gregorio F, Steinhauser M, Maier ME. Error-related brain activity and error awareness in an error classification paradigm. Neuroimage 2016, 139: 202–210.

    Article  PubMed  Google Scholar 

  20. Endrass T, Reuter B, Kathmann N. ERP correlates of conscious error recognition: Aware and unaware errors in an antisaccade task. Eur J Neurosci 2007, 26: 1714–1720.

    Article  PubMed  Google Scholar 

  21. Wang L, Gu Y, Zhao G, Chen A. Error-related negativity and error awareness in a Go/No-go task. Sci Rep 2020, 10: 4026.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Ullsperger M, Harsay HA, Wessel JR, Ridderinkhof KR. Conscious perception of errors and its relation to the anterior insula. Brain Struct Funct 2010, 214: 629–643.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Harty S, Robertson IH, Miniussi C, Sheehy OC, Devine CA, McCreery S, et al. Transcranial direct current stimulation over right dorsolateral prefrontal cortex enhances error awareness in older age. J Neurosci 2014, 34: 3646–3652.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Orr C, Hester R. Error-related anterior cingulate cortex activity and the prediction of conscious error awareness. Front Hum Neurosci 2012, 6: 177.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Dali G, Brosnan M, Tiego J, Johnson BP, Fornito A, Bellgrove MA, et al. Examining the neural correlates of error awareness in a large fMRI study. Cereb Cortex 2022, 33: 458–468.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Hermans EJ, Henckens MJ, Joëls M, Fernández G. Dynamic adaptation of large-scale brain networks in response to acute stressors. Trends Neurosci 2014, 37: 304–314.

    Article  CAS  PubMed  Google Scholar 

  27. Arnsten AF. Stress weakens prefrontal networks: Molecular insults to higher cognition. Nat Neurosci 2015, 18: 1376–1385.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Falconer E, Bryant R, Felmingham KL, Kemp AH, Gordon E, Peduto A, et al. The neural networks of inhibitory control in posttraumatic stress disorder. J Psychiatry Neurosci 2008, 33: 413–422.

    PubMed  PubMed Central  Google Scholar 

  29. Mora F, Segovia G, Del Arco A, de Blas M, Garrido P. Stress, neurotransmitters, corticosterone and body-brain integration. Brain Res 2012, 1476: 71–85.

    Article  CAS  PubMed  Google Scholar 

  30. Hester R, Foxe JJ, Molholm S, Shpaner M, Garavan H. Neural mechanisms involved in error processing: A comparison of errors made with and without awareness. Neuroimage 2005, 27: 602–608.

    Article  PubMed  Google Scholar 

  31. Hester R, Nandam LS, O’Connell RG, Wagner J, Strudwick M, Nathan PJ, et al. Neurochemical enhancement of conscious error awareness. J Neurosci 2012, 32: 2619–2627.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. O’Connell RG, Bellgrove MA, Dockree PM, Lau A, Hester R, Garavan H, et al. The neural correlates of deficient error awareness in attention-deficit hyperactivity disorder (ADHD). Neuropsychologia 2009, 47: 1149–1159.

    Article  PubMed  Google Scholar 

  33. Gehring WJ, Liu Y, Orr JM, Carp J. The error-related negativity (ERN/Ne). In: Oxford Handbook of Event-related Potential Components. OUP publishing, 2012: 231–291.

  34. Yeung N, Botvinick MM, Cohen JD. The neural basis of error detection: Conflict monitoring and the error-related negativity. Psychol Rev 2004, 111: 931–959.

    Article  PubMed  Google Scholar 

  35. Shalgi S, Barkan I, Deouell LY. On the positive side of error processing: Error-awareness positivity revisited. Eur J Neurosci 2009, 29: 1522–1532.

    Article  PubMed  Google Scholar 

  36. Falkenstein M, Hoormann J, Christ S, Hohnsbein J. ERP components on reaction errors and their functional significance: A tutorial. Biol Psychol 2000, 51: 87–107.

    Article  CAS  PubMed  Google Scholar 

  37. Navarro-Cebrian A, Knight RT, Kayser AS. Frontal monitoring and parietal evidence: Mechanisms of error correction. J Cogn Neurosci 2016, 28: 1166–1177.

    Article  PubMed  Google Scholar 

  38. Scheffers MK, Coles MGH. Performance monitoring in a confusing world: Error-related brain activity, judgments of response accuracy, and types of errors. J Exp Psychol Hum Percept Perform 2000, 26: 141–151.

    Article  PubMed  Google Scholar 

  39. Murphy PR, Robertson IH, Allen D, Hester R, O’Connell RG. An electrophysiological signal that precisely tracks the emergence of error awareness. Front Hum Neurosci 2012, 6: 65.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Steinhauser M, Yeung N. Decision processes in human performance monitoring. J Neurosci 2010, 30: 15643–15653.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Herrmann MJ, Römmler J, Ehlis AC, Heidrich A, Fallgatter AJ. Source localization (LORETA) of the error-related-negativity (ERN/Ne) and positivity (pe). Brain Res Cogn Brain Res 2004, 20: 294–299.

    Article  PubMed  Google Scholar 

  42. Masina F, Tarantino V, Vallesi A, Mapelli D. Repetitive TMS over the left dorsolateral prefrontal cortex modulates the error positivity: An ERP study. Neuropsychologia 2019, 133: 107153.

    Article  PubMed  Google Scholar 

  43. van Veen V, Carter CS. Error detection, correction, and prevention in the brain: A brief review of data and theories. Clin EEG Neurosci 2006, 37: 330–335.

    Article  PubMed  Google Scholar 

  44. Buchanan TW, Bagley SL, Stansfield RB, Preston SD. The empathic, physiological resonance of stress. Soc Neurosci 2012, 7: 191–201.

    Article  PubMed  Google Scholar 

  45. Kirschbaum C, Kudielka BM, Gaab J, Schommer NC, Hellhammer DH. Impact of gender, menstrual cycle phase, and oral contraceptives on the activity of the hypothalamus-pituitary-adrenal axis. Psychosom Med 1999, 61: 154–162.

    Article  CAS  PubMed  Google Scholar 

  46. Laredo SA, Steinman MQ, Robles CF, Ferrer E, Ragen BJ, Trainor BC. Effects of defeat stress on behavioral flexibility in males and females: Modulation by the mu-opioid receptor. Eur J Neurosci 2015, 41: 434–441.

    Article  PubMed  PubMed Central  Google Scholar 

  47. Beck AT, Ward CH, Mendelson M, Mock J, Erbaugh J. An inventory for measuring depression. Arch Gen Psychiat 1961, 4: 561–571.

    Article  CAS  PubMed  Google Scholar 

  48. Zheng Y, Yang D. Stressful life events (SLE) investigated among 4050 Chinese normal subjects aged 16 years and over. (1) The SLE characteristics by occupation. Chinese Mental Health Journal 1990, 4: 262–267.

    Google Scholar 

  49. Spielberger CD. State-trait anxiety inventory for adults (STAI-AD). APA PsycTests 1983, https://doi.org/10.1037/t06496-000.

    Article  Google Scholar 

  50. Watson D, Clark LA, Tellegen A. Development and validation of brief measures of positive and negative affect: The PANAS scales. J Pers Soc Psychol 1988, 54: 1063–1070.

    Article  CAS  PubMed  Google Scholar 

  51. Engvall E, Perlmann P. Enzyme-linked immunosorbent assay (ELISA) quantitative assay of immunoglobulin G. Immunochemistry 1971, 8: 871–874.

    Article  CAS  PubMed  Google Scholar 

  52. McMahon CM, Henderson HA. Error-monitoring in response to social stimuli in individuals with higher-functioning Autism Spectrum Disorder. Dev Sci 2015, 18: 389–403.

    Article  PubMed  Google Scholar 

  53. Dutilh G, Vandekerckhove J, Forstmann BU, Keuleers E, Brysbaert M, Wagenmakers EJ. Testing theories of post-error slowing. Atten Percept Psychophys 2012, 74: 454–465.

    Article  PubMed  Google Scholar 

  54. Hu N, Chen A, Wang Y, Li Q, Xu Z, Long Q. Acute stress impairs error monitoring and post-error adjustment. Acta Psychol Sinica 2020, 52: 162–172.

    Article  Google Scholar 

  55. Luu P, Collins P, Tucker DM. Mood, personality, and self-monitoring: Negative affect and emotionality in relation to frontal lobe mechanisms of error monitoring. J Exp Psychol Gen 2000, 129: 43–60.

    Article  PubMed  Google Scholar 

  56. Riesel A, Weinberg A, Endrass T, Kathmann N, Hajcak G. Punishment has a lasting impact on error-related brain activity. Psychophysiology 2012, 49: 239–247.

    Article  PubMed  Google Scholar 

  57. McAvinue L, O’Keeffe F, McMackin D, Robertson IH. Impaired sustained attention and error awareness in traumatic brain injury: Implications for insight. Neuropsychol Rehabil 2005, 15: 569–587.

    Article  PubMed  Google Scholar 

  58. Wessel JR, Klein TA, Ott DV, Ullsperger M. Lesions to the prefrontal performance-monitoring network disrupt neural processing and adaptive behaviors after both errors and novelty. Cortex 2014, 50: 45–54.

    Article  PubMed  Google Scholar 

  59. Wu J, Ge Y, Shi Z, Duan X, Wang L, Sun X, et al. Response inhibition in adolescent earthquake survivors with and without posttraumatic stress disorder: A combined behavioral and ERP study. Neurosci Lett 2010, 486: 117–121.

    Article  CAS  PubMed  Google Scholar 

  60. Wessel JR, Danielmeier C, Ullsperger M. Error awareness revisited: Accumulation of multimodal evidence from central and autonomic nervous systems. J Cogn Neurosci 2011, 23: 3021–3036.

    Article  PubMed  Google Scholar 

  61. Dehaene S, Charles L, King JR, Marti S. Toward a computational theory of conscious processing. Curr Opin Neurobiol 2014, 25: 76–84.

    Article  CAS  PubMed  Google Scholar 

  62. Boldt A, Yeung N. Shared neural markers of decision confidence and error detection. J Neurosci 2015, 35: 3478–3484.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Hester R, Simões-Franklin C, Garavan H. Post-error behavior in active cocaine users: Poor awareness of errors in the presence of intact performance adjustments. Neuropsychopharmacology 2007, 32: 1974–1984.

    Article  CAS  PubMed  Google Scholar 

  64. Jentzsch I, Dudschig C. Why do we slow down after an error? Mechanisms underlying the effects of posterror slowing. Q J Exp Psychol (Hove) 2009, 62: 209–218.

    Article  PubMed  Google Scholar 

  65. Ullsperger M, Danielmeier C. Reducing speed and sight: How adaptive is post-error slowing? Neuron 2016, 89: 430–432.

    Article  CAS  PubMed  Google Scholar 

  66. Danielmeier C, Ullsperger M. Post-error adjustments. Front. Psychology 2011, 2: 233.

    Google Scholar 

  67. Steinhauser M, Ernst B, Ibald KW. Isolating component processes of posterror slowing with the psychological refractory period paradigm. J Exp Psychol Learn Mem Cogn 2017, 43: 653–659.

    Article  PubMed  Google Scholar 

  68. Qin S, Cousijn H, Rijpkema M, Luo J, Franke B, Hermans EJ, et al. The effect of moderate acute psychological stress on working memory-related neural activity is modulated by a genetic variation in catecholaminergic function in humans. Front Integr Neurosci 2012, 6: 16.

    Article  PubMed  PubMed Central  Google Scholar 

  69. Olver JS, Pinney M, Maruff P, Norman TR. Impairments of spatial working memory and attention following acute psychosocial stress. Stress Health 2015, 31: 115–123.

    Article  PubMed  Google Scholar 

  70. Pessoa L. How do emotion and motivation direct executive control? Trends Cogn Sci 2009, 13: 160–166.

    Article  PubMed  PubMed Central  Google Scholar 

  71. Inzlicht M, Bartholow BD, Hirsh JB. Emotional foundations of cognitive control. Trends Cogn Sci 2015, 19: 126–132.

    Article  PubMed  PubMed Central  Google Scholar 

  72. Shields GS, Trainor BC, Lam JC, Yonelinas AP. Acute stress impairs cognitive flexibility in men, not women. Stress 2016, 19: 542–546.

    Article  PubMed  PubMed Central  Google Scholar 

  73. Wessel JR. Error awareness and the error-related negativity: Evaluating the first decade of evidence. Front Hum Neurosci 2012, 6: 88.

    Article  PubMed  PubMed Central  Google Scholar 

  74. Tops M, Boksem MA. Cortisol involvement in mechanisms of behavioral inhibition. Psychophysiology 2011, 48: 723–732.

    Article  PubMed  Google Scholar 

  75. Zhang L, Duan H, Qin S, Yuan Y, Buchanan TW, Zhang K, et al. High cortisol awakening response is associated with impaired error monitoring and decreased post-error adjustment. Stress 2015, 18: 561–568.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by grants from the National Natural Science Foundation of China (32200878 and 32260206), the Annual 2022 Joint Project of Basic Research in Local Universities (part) in Yunnan province (202101BA070001-156), the Annual 2021 Educational Science Planning Project of Yunnan Province (BFSJY006), and the Kunming University Talent Introduction Research Project (YJW2213).

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Authors and Affiliations

  1. School of Preschool and Special Education, Kunming University, Kunming, 650214, China

    Na Hu & Xiaoxi Wang

  2. Faculty of Education, Yunnan Normal University, Kunming, 650214, China

    Quanshan Long

  3. College of Teacher Education, Qujing Normal University, Qujing, 655099, China

    Quan Li

  4. Key Laboratory of Cognition and Personality of Ministry of Education, Faculty of Psychology, Southwest University, Chongqing, 400715, China

    Qing Li

  5. School of Psychology, Shanghai University of Sport, Shanghai, 200438, China

    Antao Chen

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  1. Na Hu
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Hu, N., Long, Q., Wang, X. et al. Neural and Behavioral Measures of Stress-induced Impairment in Error Awareness and Post-error Adjustment. Neurosci. Bull. (2023). https://doi.org/10.1007/s12264-023-01154-2

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