Effects of Stress on Learning and Memory: Evidence for Sex Differences in Humans

The Handbook of Stress: Neuropsychological Effects on the Brain

Volumn , Issue , 2011, Pages 545-559

  Wolf, Oliver T ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

Effects of stress on episodic memory; Memory retrieval of learned information, impaired in stress; Sex differences influencing stress; Sex differences, stress affects on learning and memory; Stress and learning, classical conditioning paradigms; Stress on learning and memory and sex differences in humans; Stress on working memory; Stressors affecting learning and memory; Trier Social Stress Test (TSST); Women and men, and how they respond to stressors

Indexed keywords

EID: 84871869037     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9781118083222.ch27     Document Type: Chapter

References (73)

1. Andreano, J. M., & Cahill, L. (2006). Glucocorticoid release and memory consolidation in men and women. Psychological Science, 17, 466-470.
2. Andreano, J. M., & Cahill, L. (2009). Sex influences on the neurobiology of learning and memory. Learning & Memory, 16, 248-266.
3. Andreano, J. M., Arjomandi, H., & Cahill, L. (2008). Menstrual cycle modulation of the relationship between cortisol and long-term memory. Psychoneuroendocrinology, 33, 874-882.
4. Baran, S. E., Armstrong, C. E., Niren, D. C., Hanna, J. J., & Conrad, C. D. (2009). Chronic stress and sex differences on the recall of fear conditioning and extinction. Neurobiology of Learning and Memory, 91, 323-332.
5. Beck, K. D., & Luine, V. N. (2010). Evidence for sex-specific shifting of neural processes underlying learning and memory following stress. Physiology & Behavior, 99, 204-211.
6. Beckner, V. E., Tucker, D. M., Delville, Y., & Mohr, D. C. (2006). Stress facilitates consolidation of verbal memory for a film but does not affect retrieval. Behavioral Neuroscience, 120, 518-527.
7. Bowman, R. E., Zrull, M. C., & Luine, V. N. (2001). Chronic restraint stress enhances radial arm maze performance in female rats. Brain Research, 904, 279-289.
8. Cahill, L. (2006). Why sex matters for neuroscience. Nature Reviews Neuroscience, 7, 477-484.
9. Christian, K. M., & Thompson, R. F. (2003). Neural substrates of eyeblink conditioning: acquisition and retention. Learning & Memory, 10, 427-455.
10. Conrad, C. D. (2005). The relationship between acute glucocorticoid levels and hippocampal function depends upon task aversiveness and memory processing stage. Nonlinearity in Biology, Toxicology and Medicine, 3, 57-78.
11. Conrad, C. D., Jackson, J. L., Wieczorek, L., Baran, S. E., Harman, J. S., Wright, R. L., & Korol, D. L. (2004). Acute stress impairs spatial memory in male but not female rats: influence of estrous cycle. Pharmacology, Biochemistry, and Behavior, 78, 569-579.
12. Croiset, G., Nijsen, M. J., & Kamphuis, P. J. (2000). Role of corticotropin-releasing factor, vasopressin and the autonomic nervous system in learning and memory. European Journal of Pharmacology, 405, 225-234.
13. Dalla, C., & Shors, T. J. (2009). Sex differences in learning processes of classical and operant conditioning. Physiology & Behavior, 97, 229-238.
14. de Quervain, D. J., Aerni, A., Schelling, G., & Roozendaal, B. (2009). Glucocorticoids and the regulation of emotional memory in health and disease. Frontiers in Neuroendocrinology, 30, 358-370.
15. Diamond, D. M., Campbell, A. M., Park, C. R., Halonen, J., & Zoladz, P. R. (2007). The temporal dynamics model of emotional memory processing: a synthesis on the neurobiological basis of stress-induced amnesia, flashbulb and traumatic memories, and the Yerkes-Dodson law. Neural Plasticity, 60803.
16. Dias-Ferreira, E., Sousa, J. C., Melo, I., Morgado, P., Mesquita, A. R., Cerqueira, J. J., & Costa, R. M. (2009). Chronic stress causes frontostriatal reorganization and affects decision-making. Science, 325, 621-625.
17. Dickerson, S. S., & Kemeny, M. E. (2004). Acute stressors and cortisol responses: a theoretical integration and synthesis of laboratory research. Psychological Bulletin, 130, 355-391.
18. Duncko, R., Cornwell, B., Cui, L., Merikangas, K. R., & Grillon, C. (2007). Acute exposure to stress improves performance in trace eyeblink conditioning and spatial learning tasks in healthy men. Learning & Memory, 14, 329-335.
19. Grillon, C., Smith, K., Haynos, A., & Nieman, L. K. (2004). Deficits in hippocampus-mediated pavlovian conditioning in endogenous hypercortisolism. Biological Psychiatry, 56, 837-843.
20. Hamm, A. O., & Weike, A. I. (2005). The neuropsychology of fear learning and fear regulation. International Journal of Psychophysiology, 57, 5-14.
21. Jackson, E. D., Payne, J. D., Nadel, L., & Jacobs, W. J. (2006). Stress differentially modulates fear conditioning in healthy men and women. Biological Psychiatry, 59, 516-522.
22. Joels, M., & Baram, T. Z. (2009). The neuro-symphony of stress. Nature Reviews Neuroscience, 10, 459-466.
23. Joels, M., Pu, Z., Wiegert, O., Oitzl, M. S., & Krugers, H. J. (2006). Learning under stress: how does it work?. Trends in Cognitive Science, 10, 152-158.
24. Kajantie, E., & Phillips, D. I. (2006). The effects of sex and hormonal status on the physiological response to acute psychosocial stress. Psychoneuroendocrinology, 31, 151-178.
25. Kirschbaum, C., Pirke, K. M., & Hellhammer, D. H. (1993). The " Trier Social Stress Test "-a tool for investigating psychobiological stress responses in a laboratory setting. Neuropsychobiology, 28, 76-81.
26. Kirschbaum, C., Wolf, O. T., May, M., Wippich, W., & Hellhammer, D. H. (1996). Stress-and treatment-induced elevations of cortisol levels associated with impaired declarative memory in healthy adults. Life Sciences, 58, 1475-1483.
27. Kirschbaum, C., Kudielka, B. M., Gaab, J., Schommer, N. C., & Hellhammer, D. H. (1999). Impact of gender, menstrual cycle phase, and oral contraceptives on the activity of the hypothalamus-pituitary-adrenal axis. Psychosomatic Medicine, 61, 154-162.
28. Kudielka, B. M., & Kirschbaum, C. (2005). Sex differences in HPA axis responses to stress: a review. Biological Psychiatry, 69, 113-132.
29. Kuhlmann, S., & Wolf, O. T. (2005). Cortisol and memory retrieval in women: influence of menstrual cycle and oral contraceptives. Psychopharmacology, 183, 65-71.
30. Kuhlmann, S., Kirschbaum, C., & Wolf, O. T. (2005a). Effects of oral cortisol treatment in healthy young women on memory retrieval of negative and neutral words. Neurobiology of Learning and Memory, 83, 158-162.
31. Kuhlmann, S., Piel, M., & Wolf, O. T. (2005b). Impaired memory retrieval after psychosocial stress in healthy young men. Journal of Neuroscience, 25, 2977-2982.
32. LaBar, K. S., & Cabeza, R. (2006). Cognitive neuroscience of emotional memory. Nature Reviews Neuroscience, 7, 54-64.
33. Luethi, M., Meier, B., & Sandi, C. (2008). Stress effects on working memory, explicit memory, and implicit memory for neutral and emotional stimuli in healthy men. Frontiers in Behavioral Neuroscience, 2, 5.
34. Luine, V. (2002). Sex differences in chronic stress effects on memory in rats. Stress, 5, 205-216.
35. Lupien, S. J., Gillin, C. J., & Hauger, R. L. (1999). Working memory is more sensitive than declarative memory to the acute effects of corticosteroids: a dose-response study in humans. Behavioral Neuroscience, 113, 420-430.
36. Merz, C. J., Wolf, O. T., Tabbert, K., Schweckendiek, J., Klucken, T., Vaitl, D., & Stark, R. (2010). Investigating the impact of sex and cortisol on implicit fear conditioning with fMRI. Psychoneuroendocrinology, 35, 33-46.
37. Nadel, L., & Moscovitch, M. (1997). Memory consolidation, retrograde amnesia and the hippocampal complex. Current Opinions in Neurobiology, 7, 217-227.
38. Nemeroff, C. B., Bremner, J. D., Foa, E. B., Mayberg, H. S., North, C. S., & Stein, M. B. (2006). Posttraumatic stress disorder: a state-of-the-science review. Journal of Psychiatric Research, 40, 1-21.
39. Oei, N. Y., Everaerd, W. T., Elzinga, B. M., van Well, S., & Bermond, B. (2006). Psychosocial stress impairs working memory at high loads: An association with cortisol levels and memory retrieval. Stress, 9, 133-141.
40. Park, C. R., Zoladz, P. R., Conrad, C. D., Fleshner, M., & Diamond, D. M. (2008). Acute predator stress impairs the consolidation and retrieval of hippocampus-dependent memory in male and female rats. Learning & Memory, 15, 271-280.
41. Preuß, D., & Wolf, O. T. (2009). Post-learning psychosocial stress enhances consolidation of neutral stimuli. Neurobiology of Learning and Memory, 92, 318-326.
42. Roozendaal, B., Okuda, S., de Quervain, D. J., & McGaugh, J. L. (2006). Glucocorticoids interact with emotion-induced noradrenergic activation in influencing different memory functions. Neuroscience, 138, 901-910.
43. Roozendaal, B., McEwen, B. S., & Chattarji, S. (2009). Stress, memory and the amygdala. Nature Reviews Neuroscience, 10, 423-433.
44. Sandi, C., & Pinelo-Nava, M. T. (2007). Stress and memory: behavioral effects and neurobiological mechanisms. Neural Plasticity, 2007, 78970.
45. Schoofs, D., & Wolf, O. T. (2009). Stress and memory retrieval in women: No strong impairing effect during the luteal phase. Behavioral Neuroscience, 123, 547-554.
46. Schoofs, D., Hartmann, R., & Wolf, O. T. (2008a). Neuroendocrine stress responses to an oral academic examination: No strong influence of sex, repeated participation and personality traits. Stress, 11, 52-61.
47. Schoofs, D., Preuss, D., & Wolf, O. T. (2008b). Psychosocial stress induces working memory impairments in an n-back paradigm. Psychoneuroendocrinology, 33, 643-653.
48. Schoofs, D., Wolf, O. T., & Smeets, T. (2009). Cold pressor stress impairs performance on working memory tasks requiring executive functions in healthy young men. Behavioral Neuroscience, 123, 1066-1075.
49. Schwabe, L., & Wolf, O. T. (2009). Stress prompts habit behavior in humans. Journal of Neuroscience, 29, 7191-7198.
50. Schwabe, L., Oitzl, M. S., Philippsen, C., Richter, S., Bohringer, A., Wippich, W., & Oitzl, M. S. (2007). Stress modulates the use of spatial versus stimulus-response learning strategies in humans. Learning & Memory, 14, 109-116.
51. Schwabe, L., Wolf, O. T., & Oitzl, M. S. (2010). Memory formation under stress: quantity and quality. Neuroscience and Biobehavioral Reviews, 34, 584-591.
52. Shansky, R. M. (2009). Estrogen, stress and the brain: progress toward unraveling gender discrepancies in major depressive disorder. Expert Review of Neurotherapeutics, 9, 967-973.
53. Shansky, R. M., Glavis-Bloom, C., Lerman, D., McRae, P., Benson, C., Miller, K., Cosand, L., Horvath, T. L., & Arnsten, A. F. T. (2004). Estrogen mediates sex differences in stressinduced prefrontal cortex dysfunction. Molecular Psychiatry, 9, 531-538.
54. Shansky, R. M., Rubinow, K., Brennan, A., & Arnsten, A. F. (2006). The effects of sex and hormonal status on restraint-stress-induced working memory impairment. Behavioural Brain Function, 2, 8.
55. Shors, T. J. (2004). Learning during stressful times. Learning & Memory, 11, 137-144.
56. Smeets, T., Otgaar, H., Candel, I., & Wolf, O. T. (2008). True or false?. Memory is differentially affected by stress-induced cortisol elevations and sympathetic activity at consolidation and retrieval. Psychoneuroendocrinology, 33, 1378-1386.
57. Stark, R., Wolf, O. T., Tabbert, K., Kagerer, S., Zimmermann, M., Kirsch, P., Schienle, A., & Vaitl, D. (2006). Influence of the stress hormone cortisol on fear conditioning in humans: evidence for sex differences in the response of the prefrontal cortex. Neuroimage, 32, 1290-1298.
58. Stroud, L., Salovey, P., & Epel, E. (2002). Sex differences in stress responses: social rejection versus achievement stress. Biological Psychiatry, 52, 318-327.
59. Tabbert, K., Stark, R., Kirsch, P., & Vaitl, D. (2006). Dissociation of neural responses and skin conductance reactions during fear conditioning with and without awareness of stimulus contingencies. Neuroimage, 32, 761-770.
60. Takahashi, T., Ikeda, K., Ishikawa, M., Tsukasaki, T., Nakama, D., Tanida, S., & Kameda, T. (2004). Social stress-induced cortisol elevation acutely impairs social memory in humans. Neuroscience Letters, 363, 125-130.
61. Taylor, S. E., Klein, L. C., Lewis, B. P., Gruenewald, T. L., Gurung, R. A., & Updegraff, J. A. (2000). Biobehavioral responses to stress in females: tend-and-befriend, not fight-or-flight. Psychological Review, 107, 411-429.
62. Ulrich-Lai, Y. M., & Herman, J. P. (2009). Neural regulation of endocrine and autonomic stress responses. Nature Reviews Neuroscience, 10, 397-409.
63. Vythilingam, M., Lawley, M., Collin, C., Bonne, O., Agarwal, R., Hadd, K., Charney, D. S., & Grillon, C. (2006). Hydrocortisone impairs hippocampal-dependent trace eyeblink conditioning in post-traumatic stress disorder. Neuropsychopharmacology, 31, 182-188.
64. Wolf, O. T. (2008). The influence of stress hormones on emotional memory: Relevance for psychopathology. Acta Psychologica (Amsterdam), 127, 513-531.
65. Wolf, O. T. (2009). Stress and memory in humans: twelve years of progress?. Brain Research, 1293, 142-154.
66. Wolf, O. T., & Kudielka, B. M. (2008). Stress, health and ageing: a focus on postmenopausal women. Menopause International, 14, 129-133.
67. Wolf, O. T., Convit, A., McHugh, P. F., Kandil, E., Thorn, E. L., De Santi, S., McEwen, B. S., & de Leon, M. J. (2001a). Cortisol differentially affects memory in young and elderly men. Behavioral Neuroscience, 105, 1002-1011.
68. Wolf, O. T., Schommer, N. C., Hellhammer, D. H., McEwen, B. S., & Kirschbaum, C. (2001b). The relationship between stress induced cortisol levels and memory differs between men and women. Psychoneuroendocrinology, 26, 711-720.
69. Wolf, O. T., Minnebusch, D., & Daum, I. (2009). Stress impairs acquisition of delay eyeblink conditioning in men and women. Neurobiology of Learning and Memory, 91, 431-436.
70. Yehuda, R. (2002). Post-traumatic stress disorder. New England Journal of Medicine, 346, 108-114.
71. Zahn-Waxler, C., Shirtcliff, E. A., & Marceau, K. (2008). Disorders of childhood and adolescence: gender and psychopathology. Annual Review of Clinical Psychology, 4, 275-303.
72. Zorawski, M., Cook, C. A., Kuhn, C. M., & LaBar, K. S. (2005). Sex, stress, and fear: individual differences in conditioned learning. Cognitive, Affective, & Behavioral Neuroscience, 5, 191-201.
73. Zorawski, M., Blanding, N. Q., Kuhn, C. M., & LaBar, K. S. (2006). Effects of stress and sex on acquisition and consolidation of human fear conditioning. Learning & Memory, 13, 441-450.