Working memory is differentially affected by stress in men and women

Behavioural Brain Research

Volumn 241, Issue 1, 2013, Pages 144-153

  Schoofs, Daniela ^a,b   Pabst, Stephan ^a   Brand, Matthias ^c,d   Wolf, Oliver T ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b AMEOS Clinic Hildesheim   (Germany)

^c UNIVERSITY OF DUISBURG ESSEN   (Germany)

^d ERWIN L HAHN INSTITUTE FOR MAGNETIC RESONANCE IMAGING   (Germany)

Author keywords

HPA; N back task; Sex differences; Trierer Social Stress Test (TSST); Working memory

Indexed keywords

AMYLASE; HYDROCORTISONE;

ADRENERGIC SYSTEM; ADULT; ARTICLE; CONTROLLED STUDY; ELECTROENCEPHALOGRAM; EMOTION; EMOTIONALITY; FEMALE; HUMAN; HUMAN EXPERIMENT; HYPOPHYSIS ADRENAL SYSTEM; MALE; NERVE STIMULATION; NEUROMODULATION; NORMAL HUMAN; PRIORITY JOURNAL; SALIVA LEVEL; SEX DIFFERENCE; SOCIAL STRESS; STRESS; TASK PERFORMANCE; WORKING MEMORY;

ADULT; FEMALE; HUMANS; HYDROCORTISONE; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; MALE; MEMORY, SHORT-TERM; NEUROPSYCHOLOGICAL TESTS; PITUITARY-ADRENAL SYSTEM; REACTION TIME; SALIVA; SALIVARY ALPHA-AMYLASES; SEX CHARACTERISTICS; STRESS, PSYCHOLOGICAL;

EID: 84871875020     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2012.12.004     Document Type: Article

References (94)

1. Fuster J.M. Executive frontal functions. Experimental Brain Research 2000, 133(1):66-70.
2. Arnsten A.F., Li B.M. Neurobiology of executive functions: catecholamine influences on prefrontal cortical functions. Biological Psychiatry 2005, 57(11):1377-1384.
3. D'Esposito M. From cognitive to neural models of working memory. Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences 2007, 362(1481):761-772.
4. Bechara A., Damasio H., Damasio A.R. Emotion, decision making and the orbitofrontal cortex. Cerebral Cortex 2000, 10(3):295-307.
5. Cardinal R.N., Parkinson J.A., Hall J., Everitt B.J. Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex. Neuroscience and Biobehavioral Reviews 2002, 26(3):321-352.
6. Herman J.P., Ostrander M.M., Mueller N.K., Figueiredo H. Limbic system mechanisms of stress regulation: hypothalamo-pituitary-adrenocortical axis. Progress in Neuro-Psychopharmacology and Biological Psychiatry 2005, 29(8):1201-1213.
7. Joels M., Karst H., DeRijk R., de Kloet E.R. The coming out of the brain mineralocorticoid receptor. Trends in Neurosciences 2008, 31(1):1-7.
8. Patel P.D., Katz M., Karssen A.M., Lyons D.M. Stress-induced changes in corticosteroid receptor expression in primate hippocampus and prefrontal cortex. Psychoneuroendocrinology 2008, 33(3):360-367.
9. Perlman W.R., Webster M.J., Herman M.M., Kleinman J.E., Weickert C.S. Age-related differences in glucocorticoid receptor mRNA levels in the human brain. Neurobiology of Aging 2007, 28(3):447-458.
10. Meaney M.J., Aitken D.H. [3H]Dexamethasone binding in rat frontal cortex. Brain Research 1985, 328(1):176-180.
11. Elling L., Steinberg C., Brockelmann A.K., Dobel C., Bolte J., Junghofer M. Acute stress alters auditory selective attention in humans independent of HPA: a study of evoked potentials. PLoS One 2011, 6(4):e18009.
12. Shackman A.J., Maxwell J.S., McMenamin B.W., Greischar L.L., Davidson R.J. Stress potentiates early and attenuates late stages of visual processing. Journal of Neuroscience 2011, 31(3):1156-1161.
13. Schwabe L., Wolf O.T. Emotional modulation of the attentional blink: is there an effect of stress?. Emotion 2010, 10(2):283-288.
14. Wolf O.T. Stress and memory in humans: twelve years of progress. Brain Research 2009, 1293:142-154.
15. Lupien S.J., McEwen B.S., Gunnar M.R., Heim C. Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nature Reviews Neuroscience 2009, 10(6):434-445.
16. Schoofs D., Wolf O.T., Smeets T. Cold pressor stress impairs performance on working memory tasks requiring executive functions in healthy young men. Behavioral Neuroscience 2009, 123(5):1066-1075.
17. Oei N.Y., Everaerd W.T., Elzinga B.M., van Well S., Bermond B. Psychosocial stress impairs working memory at high loads: an association with cortisol levels and memory retrieval. Stress 2006, 9(3):133-141.
18. Qin S., Hermans E.J., van Marle H.J., Luo J., Fernandez G. Acute psychological stress reduces working memory-related activity in the dorsolateral prefrontal cortex. Biological Psychiatry 2009, 66(1):25-32.
19. Smeets T., Jelicic M., Merckelbach H. The effect of acute stress on memory depends on word valence. International Journal of Psychophysiology 2006, 62(1):30-37.
20. Kuhlmann S., Piel M., Wolf O.T. Impaired memory retrieval after psychosocial stress in healthy young men. Journal of Neuroscience 2005, 25(11):2977-2982.
21. Hoffman R., Al'Absi M. The effect of acute stress on subsequent neuropsychological test performance. Archives of Clinical Neuropsychology 2004, 19(4):497-506.
22. Schoofs D., Preuss D., Wolf O.T. Psychosocial stress induces working memory impairments in an n-back paradigm. Psychoneuroendocrinology 2008, 33(5):643-653.
23. Lupien S.J., Gillin C.J., Hauger R.L. Working memory is more sensitive than declarative memory to the acute effects of corticosteroids: a dose-response study in humans. Behavioral Neuroscience 1999, 113(3):420-430.
24. Cornelisse S., van Stegeren A.H., Joels M. Implications of psychosocial stress on memory formation in a typical male versus female student sample. Psychoneuroendocrinology 2011, 36(4):569-578.
25. Duncko R., Johnson L., Merikangas K., Grillon C. Working memory performance after acute exposure to the cold pressor stress in healthy volunteers. Neurobiology of Learning and Memory 2009, 91(4):377-381.
26. Shansky R.M., Rubinow K., Brennan A., Arnsten A.F. The effects of sex and hormonal status on restraint-stress-induced working memory impairment. Behavioral and Brain Functions 2006, 7(2):8.
27. Oei N.Y., Tollenaar M.S., Spinhoven P., Elzinga B.M. Hydrocortisone reduces emotional distracter interference in working memory. Psychoneuroendocrinology 2009, 34(9):1284-1293.
28. 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 1993, 28(1-2):76-81.
29. Dickerson S.S., Kemeny M.E. Acute stressors and cortisol responses: a theoretical integration and synthesis of laboratory research. Psychological Bulletin 2004, 130(3):355-391.
30. 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 2009, 34:1075-1086.
31. Rohleder N., Nater U.M., Wolf J.M., Ehlert U., Kirschbaum C. Psychosocial stress-induced activation of salivary alpha-amylase: an indicator of sympathetic activity. Annals of the New York Academy of Sciences 2004, 1032:258-263.
32. Kudielka B.M., Schommer N.C., Hellhammer D.H., Kirschbaum C. Acute HPA axis responses, heart rate, and mood changes to psychosocial stress (TSST) in humans at different times of day. Psychoneuroendocrinology 2004, 29(8):983-992.
33. Nater U.M., Rohleder N. Salivary alpha-amylase as a non-invasive biomarker for the sympathetic nervous system: current state of research. Psychoneuroendocrinology 2009, 34(4):486-496.
34. Rohleder N., Nater U.M. Determinants of salivary alpha-amylase in humans and methodological considerations. Psychoneuroendocrinology 2009, 34(4):469-485.
35. van Stegeren A., Rohleder N., Everaerd W., Wolf O.T. Salivary alpha amylase as marker for adrenergic activity during stress: effect of betablockade. Psychoneuroendocrinology 2006, 31(1):137-141.
36. Watson D., Clark L.A., Tellegen A. Development and validation of brief measures of positive and negative affect: the PANAS scales. Journal of Personality and Social Psychology 1988, 54(6):1063-1070.
37. Erdfelder E., Faul F., Buchner A. GPower: a general power analysis program. Behavior Research Methods, Instruments, & Computers 1996, 28(1):1-11.
38. Dolcos F., Cabeza R. Event-related potentials of emotional memory: encoding pleasant, unpleasant, and neutral pictures. Cognitive, Affective, & Behavioral Neuroscience 2002, 2(3):252-263.
39. Cahill L., McGaugh J.L. Mechanisms of emotional arousal and lasting declarative memory. Trends in Neurosciences 1998, 21(7):294-299.
40. Roozendaal B. Stress and memory: opposing effects of glucocorticoids on memory consolidation and memory retrieval. Neurobiology of Learning and Memory 2002, 78(3):578-595.
41. Roozendaal B., Brunson K.L., Holloway B.L., McGaugh J.L., Baram T.Z. Involvement of stress-released corticotropin-releasing hormone in the basolateral amygdala in regulating memory consolidation. Proceedings of the National Academy of Sciences of the United States of America 2002, 99(21):13908-13913.
42. Dolcos F., McCarthy G. Brain systems mediating cognitive interference by emotional distraction. Journal of Neuroscience 2006, 26(7):2072-2079.
43. Kensinger E.A., Corkin S. Effect of negative emotional content on working memory and long-term memory. Emotion 2003, 3(4):378-393.
44. Oei N.Y., Veer I.M., Wolf O.T., Spinhoven P., Rombouts S.A., Elzinga B.M. Stress shifts brain activation towards ventral 'affective' areas during emotional distraction. Social Cognitive and Affective Neuroscience 2012, 7(4):403-412.
45. Putman P., Roelofs K. Effects of single cortisol administrations on human affect reviewed: coping with stress through adaptive regulation of automatic cognitive processing. Psychoneuroendocrinology 2011, 36(4):439-448.
46. Arnsten A.F. Stress signalling pathways that impair prefrontal cortex structure and function. Nature Reviews Neuroscience 2009, 10(6):410-422.
47. Oei N.Y., Tollenaar M.S., Elzinga B.M., Spinhoven P. Propranolol reduces emotional distraction in working memory: a partial mediating role of propranolol-induced cortisol increases?. Neurobiology of Learning and Memory 2010, 93(3):388-395.
48. Lang PJ, Bradley MM, Cuthbert BN. International Affective Picture System (IAPS): technical manual and affective ratings. Gainesville FL: Center for Research in Psychophysiology: University of Florida; 1997.
49. Cohen S., Kamarck T., Mermelstein R. A global measure of perceived stress. Journal of Health and Social Behavior 1983, 24(4):385-396.
50. Schoofs D., Wolf O.T. Are salivary gonadal steroid concentrations influenced by acute psychosocial stress? A study using the Trier Social Stress Test (TSST). International Journal of Psychophysiology 2011, 80(1):36-43.
51. Preuss D., Wolf O.T. Post-learning psychosocial stress enhances consolidation of neutral stimuli. Neurobiology of Learning and Memory 2009, 92:318-326.
52. Kudielka B.M., Hellhammer D.H., Wust S. Why do we respond so differently? Reviewing determinants of human salivary cortisol responses to challenge. Psychoneuroendocrinology 2009, 34(1):2-18.
53. Butts K.A., Weinberg J., Young A.H., Phillips A.G. Glucocorticoid receptors in the prefrontal cortex regulate stress-evoked dopamine efflux and aspects of executive function. Proceedings of the National Academy of Sciences of the United States of America 2011, 108(45):18459-18464.
54. Schoofs D., Hartmann R., Wolf O.T. Neuroendocrine stress responses to an oral academic examination: no strong influence of sex, repeated participation and personality traits. Stress 2008, 11(1):52-61.
55. Luethi M., Meier B., Sandi C. Stress effects on working memory, explicit memory, and implicit memory for neutral and emotional stimuli in healthy men. Frontiers in Behavioral Neuroscience 2009, 2:1-9.
56. Smeets T., Jelicic M., Merckelbach H. Stress-induced cortisol responses, sex differences, and false recollections in a DRM paradigm. Biological Psychology 2006, 72(2):164-172.
57. Porcelli A.J., Cruz D., Wenberg K., Patterson M.D., Biswal B.B., Rypma B. The effects of acute stress on human prefrontal working memory systems. Physiology and Behavior 2008, 95(3):282-289.
58. Weerda R., Muehlhan M., Wolf O.T., Thiel C.M. Effects of acute psychosocial stress on working memory related brain activity in men. Human Brain Mapping 2010, 31(9):1418-1429.
59. Cousijn H., Rijpkema M., Qin S., van Wingen G.A., Fernandez G. Phasic deactivation of the medial temporal lobe enables working memory processing under stress. Neuroimage 2012, 59(2):1161-1167.
60. Anticevic A., Repovs G., Shulman G.L., Barch D.M. When less is more: TPJ and default network deactivation during encoding predicts working memory performance. Neuroimage 2010, 49(3):2638-2648.
61. Pruessner J.C., Dedovic K., Khalili-Mahani N., Engert V., Pruessner M., Buss C., et al. Deactivation of the limbic system during acute psychosocial stress: evidence from positron emission tomography and functional magnetic resonance Imaging studies. Biological Psychiatry 2008, 63(2):234-240.
62. Buckert M., Kudielka B.M., Reuter M., Fiebach C.J. The COMT Val158Met polymorphism modulates working memory performance under acute stress. Psychoneuroendocrinology 2012, 37(11):1810-1821.
63. Klucken T., Brouwer A.M., Chatziastros A., Kagerer S., Netter P., Hennig J. The impact of coping style on gaze duration. PLoS One 2010, 5(11):e15395.
64. Zoccola P.M., Quas J.A., Yim I.S. Salivary cortisol responses to a psychosocial laboratory stressor and later verbal recall of the stressor: the role of trait and state rumination. Stress 2010, 13(5):435-443.
65. Schoofs D., Wolf O.T. Stress and memory retrieval in women: no strong impairing effect during the luteal phase. Behavioral Neuroscience 2009, 123(3):547-554.
66. Zorawski M., Blanding N.Q., Kuhn C.M., LaBar K.S. Effects of stress and sex on acquisition and consolidation of human fear conditioning. Learning and Memory 2006, 13(4):441-450.
67. Shansky R.M., Glavis-Bloom C., Lerman D., McRae P., Benson C., Miller K., et al. Estrogen mediates sex differences in stress-induced prefrontal cortex dysfunction. Molecular Psychiatry 2004, 9(5):531-538.
68. 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. Psychosomatic Medicine 1999, 61(2):154-162.
69. Merz C.J., Stark R., Vaitl D., Tabbert K., Wolf O.T. Stress hormones are associated with the neuronal correlates of instructed fear conditioning. Biol Psychol 2013, 92(1):82-89.
70. Jackson E.D., Payne J.D., Nadel L., Jacobs W.J. Stress differentially modulates fear conditioning in healthy men and women. Biological Psychiatry 2006, 59(6):516-522.
71. Andreano J.M., Cahill L. Glucocorticoid release and memory consolidation in men and women. Psychological Science 2006, 17(6):466-470.
72. Wolf O.T. Effects of stress on learning and memory: evidence for sex differences in humans. The handbook of stress: neuropsychological effects on the brain 2011, 545-559. Wiley-Blackwell, Chichester, West Sussex, United Kingdom. C.D. Conrad (Ed.).
73. Shors T.J. Learning during stressful times. Learning and Memory 2004, 11(2):137-144.
74. Beck K.D., Luine V.N. Evidence for sex-specific shifting of neural processes underlying learning and memory following stress. Physiology and Behavior 2010, 99(2):204-211.
75. Dalla C., Antoniou K., Kokras N., Drossopoulou G., Papathanasiou G., Bekris S., et al. Sex differences in the effects of two stress paradigms on dopaminergic neurotransmission. Physiology and Behavior 2008, 93(3):595-605.
76. McGaugh J.L., Cahill L., Roozendaal B. Involvement of the amygdala in memory storage: interaction with other brain systems. Proceedings of the National Academy of Sciences of the United States of America 1996, 93(24):13508-13514.
77. Cahill L. Sex- and hemisphere-related influences on the neurobiology of emotionally influenced memory. Progress in Neuro-Psychopharmacology and Biological Psychiatry 2003, 27(8):1235-1241.
78. Cahill L., Haier R.J., Fallon J., Alkire M.T., Tang C., Keator D., et al. Amygdala activity at encoding correlated with long-term, free recall of emotional information. Proceedings of the National Academy of Sciences of the United States of America 1996, 93(15):8016-8021.
79. LaBar K.S., Cabeza R. Cognitive neuroscience of emotional memory. Nature Reviews Neuroscience 2006, 7(1):54-64.
80. Buchanan T.W. Retrieval of emotional memories. Psychological Bulletin 2007, 133(5):761-779.
81. Dolcos F., Kragel P., Wang L., McCarthy G. Role of the inferior frontal cortex in coping with distracting emotions. Neuroreport 2006, 17(15):1591-1594.
82. Doehnel K., Sommer M., Ibach B., Rothmayr C., Meinhardt J., Hajak G. Neural correlates of emotional working memory in patients with mild cognitive impairment. Neuropsychologia 2008, 46(1):37-48.
83. King R., Schaefer A. The emotional startle effect is disrupted by a concurrent working memory task. Psychophysiology 2011.
84. Erthal F.S., de O.L., Mocaiber I., Pereira M.G., Hado-Pinheiro W., Volchan E., et al. Load-dependent modulation of affective picture processing. Cognitive, Affective, & Behavioral Neuroscience 2005, 5(4):388-395.
85. Vytal K., Cornwell B., Arkin N., Grillon C Describing the interplay between anxiety and cognition: From impaired performance under low cognitive load to reduced anxiety under high load. Psychophysiology 2012, 49(6):842-852.
86. Pessoa L. On the relationship between emotion and cognition. Nature Reviews Neuroscience 2008, 9(2):148-158.
87. Paivio A., Csapo K. Picture superiority in free recall: imagery or dual coding. Cognitive Psychology 1973, 5:176-206.
88. Curran T., Doyle J. Picture superiority double dissociates the ERP correlates of recollection and familiarity. Journal of Cognitive Neuroscience 2011, 23(5):1247-1262.
89. Andreano J.M., Arjomandi H., Cahill L. Menstrual cycle modulation of the relationship between cortisol and long-term memory. Psychoneuroendocrinology 2008, 33(6):874-882.
90. Smeets T., Otgaar H., Candel I., Wolf O.T. True or false? Memory is differentially affected by stress-induced cortisol elevations and sympathetic activity at consolidation and retrieval. Psychoneuroendocrinology 2008, 33(10):1378-1386.
91. Maheu F.S., Collicutt P., Kornik R., Moszkowski R., Lupien S.J. The perfect time to be stressed: a differential modulation of human memory by stress applied in the morning or in the afternoon. Progress in Neuro-Psychopharmacology and Biological Psychiatry 2005, 29(8):1281-1288.
92. Het S., Ramlow G., Wolf O.T. A meta-analytic review of the effects of acute cortisol administration on human memory. Psychoneuroendocrinology 2005, 30(8):771-784.
93. Roozendaal B., McReynolds J.R., McGaugh J.L. The basolateral amygdala interacts with the medial prefrontal cortex in regulating glucocorticoid effects on working memory impairment. Journal of Neuroscience 2004, 24(6):1385-1392.
94. Elzinga B.M., Roelofs K. Cortisol-induced impairments of working memory require acute sympathetic activation. Behavioral Neuroscience 2005, 119(1):98-103.