Eyeblink conditional discrimination learning in healthy young men is impaired after stress exposure

Psychophysiology

Volumn 49, Issue 2, 2012, Pages 164-171

  Wolf, Oliver T ^a   Bauser, Denise Soria ^a   Daum, Irene ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

Conditional discrimination learning; Cortisol; Hippocampus; Humans; Stress

Indexed keywords

EID: 84856100329     PISSN: 00485772     EISSN: 14698986     Source Type: Journal    
DOI: 10.1111/j.1469-8986.2011.01294.x     Document Type: Article

References (63)

1. Andreano, J. M., Arjomandi, H., & Cahill, L. (2008). Menstrual cycle modulation of the relationship between cortisol and long-term memory. Psychoneuroendocrinology, 33, 874-882. doi: 10.1016/j.psyneuen.2008.03.009
2. Bangasser, D. A., & Shors, T. J. (2007). The hippocampus is necessary for enhancements and impairments of learning following stress. Nature Neuroscience, 10, 1401-1403. doi: 10.1038/nn1973
3. Bellebaum, C., & Daum, I. (2004). Effects of age and awareness on eyeblink conditional discrimination learning. Behavioral Neuroscience, 118, 1157-1165. doi: 10.1037/0735-7044.118.6.1157
4. Chang, C. H., & Maren, S. (2009). Early extinction after fear conditioning yields a context-independent and short-term suppression of conditional freezing in rats. Learning & Memory, 16, 62-68. doi: 10.1101/lm.1085009
5. Christian, K. M., & Thompson, R. F. (2003). Neural substrates of eyeblink conditioning: Acquisition and retention. Learning & Memory, 10, 427-455. doi: 10.1101/lm.59603
6. Cornelisse, S., van Stegeren, A. H., & Joels, M. (2011). Implications of psychosocial stress on memory formation in a typical male versus female student sample. Psychoneuroendocrinology, 36, 569-578. doi: 10.1016/j.psyneuen.2010.09.002
7. Dalla, C., & Shors, T. J. (2009). Sex differences in learning processes of classical and operant conditioning. Physiology & Behavior, 97, 229-238. doi: 10.1016/j.physbeh.2009.02.035
8. Daum, I., Channon, S., Polkey, C. E., & Gray, J. A. (1991). Classical conditioning after temporal lobe lesions in man: Impairment in conditional discrimination. Behavioral Neuroscience, 105, 396-408. doi: 10.1037/0735-7044.105.3.396
9. Daum, I., Schugens, M. M., Ackermann, H., Lutzenberger, W., Dichgans, J., & Birbaumer, N. (1993). Classical conditioning after cerebellar lesions in humans. Behavioral Neuroscience, 107, 748-756. doi: 10.1037/0735-7044.107.5.748
10. de Quervain, D. J., Henke, K., Aerni, A., Treyer, V., McGaugh, J. L., Berthold, T., ... Honk, C. (2003). Glucocorticoid-induced impairment of declarative memory retrieval is associated with reduced blood flow in the medial temporal lobe. European Journal of Neuroscience, 17, 1296-1302. doi: 10.1046/j.1460-9568.2003.02542.x
11. 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. Retrieved from
12. 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. doi: 10.1101/lm.483807
13. Fester, C. S., & Skinner, B. F. (1957). Schedules of reinforcement. New York, NY: Appleton-Century-Crofts. doi: 10.1037/10627-000
14. Fortier, C. B., Disterhoft, J. F., Capozzi, S., Kilduff, P., Cronin-Golomb, A., & McGlinchey, R. E. (2003). Conditional discrimination learning in patients with bilateral medial temporal lobe amnesia. Behavioral Neuroscience, 117, 1181-1195. doi: 10.1037/0735-7044.117.6.1181
15. Green, J. T., & Woodruff-Pak, D. S. (2000). Eyeblink classical conditioning: Hippocampal formation is for neutral stimulus associations as cerebellum is for association-response. Psychological Bulletin, 126, 138-158. doi: 10.1037/0033-2909.126.1.138
16. Grillon, C., Smith, K., Haynos, A., & Nieman, L. K. (2004). Deficits in hippocampus-mediated Pavlovian conditioning in endogenous hypercortisolism. Biological Psychiatry, 56, 837-843. doi: 10.1016/j.biopsych.2004.09.003
17. Henckens, M. J., Hermans, E. J., Pu, Z., Joels, M., & Fernandez, G. (2009). Stressed memories: How acute stress affects memory formation in humans. Journal of Neuroscience, 29, 10111-10119. doi: 10.1523/JNEUROSCI.1184-09.2009
18. Het, S., Rohleder, N., Schoofs, D., Kirschbaum, C., & Wolf, O. T. (2009). Neuroendocrine and psychometric evaluation of a placebo version of the "Trier Social Stress Test." Psychoneuroendocrinology, 34, 1075-1086. doi: 10.1016/j.psyneuen.2009.02.008
19. 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. doi: 10.1016/j.biopsych.2005.08.002
20. Joels, M., & Baram, T. Z. (2009). The neuro-symphony of stress. Nature Reviews Neuroscience, 10, 459-466.
21. Joels, M., Karst, H., DeRijk, R., & De Kloet, E. R. (2008). The coming out of the brain mineralocorticoid receptor. Trends in Neurosciences, 31, 1-7. doi: 10.1016/j.tins.2007.10.005
22. 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. doi: 10.1016/j.tics.2006.02.002
23. 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.
24. 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. doi: 10.1159/000119004
25. Kirschbaum, C., Pirke, K. M., & Hellhammer, D. H. (1995). Preliminary evidence for reduced cortisol responsivity to psychological stress in women using oral contraceptive medication. Psychoneuroendocrinology, 20, 509-514. doi: 10.1016/0306-4530(94)00078-O
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. doi: 10.1016/0024-3205(96)00118-X
27. Konkel, A., & Cohen, N. J. (2009). Relational memory and the hippocampus: Representations and methods. Frontiers in Neuroscience, 3, 166-174. doi: 10.3389/neuro.01.023.2009
28. Kuhlmann, S., Piel, M., & Wolf, O. T. (2005). Impaired memory retrieval after psychosocial stress in healthy young men. Journal of Neuroscience, 25, 2977-2982. doi: 10.1523/JNEUROSCI.5139-04.2005
29. Kuhlmann, S., & Wolf, O. T. (2005). Cortisol and memory retrieval in women: Influence of menstrual cycle and oral contraceptives. Psychopharmacology, 183, 65-71. doi: 10.1007/s00213-005-0143-z
30. Lupien, S. J., Maheu, F., Tu, M., Fiocco, A., & Schramek, T. E. (2007). The effects of stress and stress hormones on human cognition: Implications for the field of brain and cognition. Brain Cognition, 65, 209-237. doi: 10.1016/j.bandc.2007.02.007
31. Maren, S., & Chang, C. H. (2006). Recent fear is resistant to extinction. Proceedings of the National Academy of Sciences U.S.A, 103, 18020-18025. doi: 10.1073/pnas.0608398103
32. Merz, C. J., Tabbert, K., Schweckendiek, J., Klucken, T., Vaitl, D., Stark, R., ... Wolf, O.T. (2010). Investigating the impact of sex and cortisol on implicit fear conditioning with fMRI. Psychoneuroendocrinology, 35, 33-46. doi: 10.1016/j.psyneuen.2009.07.009
33. Nees, F., Richter, S., Lass-Hennemann, J., Blumenthal, T. D., & Schachinger, H. (2008). Inhibition of cortisol production by metyrapone enhances trace, but not delay, eyeblink conditioning. Psychopharmacology (Berl), 199, 183-190. doi: 10.1007/s00213-008-1155-2
34. Oei, N. Y., Elzinga, B. M., Wolf, O. T., de Ruiter, M. B., Damoiseaux, J. S., Kuijer, J. P., ... Rombouts, S. A. (2007). Glucocorticoids decrease hippocampal and prefrontal activation during declarative memory retrieval in young men. Brain Imaging and Behavior, 1, 31-41. doi: 10.1007/s11682-007-9003-2
35. Preuß, D., & Wolf, O. T. (2009). Post-learning psychosocial stress enhances consolidation of neutral stimuli. Neurobiology of Learning & Memory, 92, 318-326. doi: 10.1016/j.nlm.2009.03.009
36. Pruessner, J. C., Dedovic, K., Khalili-Mahani, N., Engert, V., Pruessner, M., Buss, C., ... Lupien, S. (2008). Deactivation of the limbic system during acute psychosocial stress: Evidence from positron emission tomography and functional magnetic resonance imaging studies. Biological Psychiatry, 63, 234-240. doi: 10.1016/j.biopsych.2007.04.041
37. Pruessner, J. C., Kirschbaum, C., Meinlschmid, G., & Hellhammer, D. H. (2003). Two formulas for computation of the area under the curve represent measures of total hormone concentration versus time-dependent change. Psychoneuroendocrinology, 28, 916-931. doi: 10.1016/S0306-4530(02)00108-7
38. Quirk, G. J., & Mueller, D. (2008). Neural mechanisms of extinction learning and retrieval. Neuropsychopharmacology, 33, 56-72. doi: 10.1038/sj.npp.1301555
39. Rodrigues, S. M., LeDoux, J. E., & Sapolsky, R. M. (2009). The influence of stress hormones on fear circuitry. Annual Review of Neuroscience, 32, 289-313. doi: 10.1146/annurev.neuro.051508.135620
40. Ross, R. T., Orr, W. B., Holland, P. C., & Berger, T. W. (1984). Hippocampectomy disrupts acquisition and retention of learned conditional responding. Behavioral Neuroscience, 98, 211-225. doi: 10.1037/0735-7044.98.2.211
41. Sandi, C., & Pinelo-Nava, M. T. (2007). Stress and memory: Behavioral effects and neurobiological mechanisms. Neural Plasticity, 78970. doi: 10.1155/2007/78970 Retrieved from
42. Schlosser, N., Wolf, O. T., & Wingenfeld, K. (2011). Cognitive correlates of hypothalamic-pituitary-adrenal axis in major depressive disorder. Expert Review of Endocrinology & Metabolism, 6, 109-126. doi: 10.1586/eem.10.79
43. Schoofs, D., Preuss, D., & Wolf, O. T. (2008). Psychosocial stress induces working memory impairments in an n-back paradigm. Psychoneuroendocrinology, 33, 643-653. doi: 10.1016/j.psyneuen.2008.02.004
44. 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. doi: 10.1037/a0015625
45. Schwabe, L., Tegenthoff, M., Hoffken, O., & Wolf, O. T. (2010). Concurrent glucocorticoid and noradrenergic activity shifts instrumental behavior from goal-directed to habitual control. Journal of Neuroscience, 30, 8190-8196. doi: 10.1523/JNEUROSCI.0734-10.2010
46. Schwabe, L., & Wolf, O. T. (2009). Stress prompts habit behavior in humans. Journal of Neuroscience, 29, 7191-7198. doi: 10.1523/JNEUROSCI.0979-09.2009
47. Schwabe, L., & Wolf, O. T. (in press). Socially evaluated cold pressor stress after instrumental learning favors habits over goal-directed action. Psychoneuroendocrinology .
48. Schwabe, L., Wolf, O. T., & Oitzl, M. S. (2010). Memory formation under stress: Quantity and quality. Neuroscience & Biobehavioral Reviews, 34, 584-591. doi: 10.1016/j.neubiorev.2009.11.015
49. Shors, T. J. (2004). Learning during stressful times. Learning & Memory, 11, 137-144. doi: 10.1101/lm.66604
50. Stark, R., Wolf, O. T., Tabbert, K., Kagerer, S., Zimmermann, M., Kirsch, P., & 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. doi: 10.1016/j.neuroimage.2006.05.046
51. Stawski, R. S., Sliwinski, M. J., & Smyth, J. M. (2006). Stress-related cognitive interference predicts cognitive function in old age. Psychological Aging, 21, 535-544. doi: 10.1037/0882-7974.21.3.535
52. Stawski, R. S., Sliwinski, M. J., & Smyth, J. M. (2009). The effects of an acute psychosocial stressor on episodic memory. European Journal of Cognitive Psychology, 21, 897-918. doi: 10.1080/09541440802333042
53. Vythilingam, M., Lawley, M., Collin, C., Bonne, O., Agarwal, R., Hadd, K., ... Grillon, C. (2006). Hydrocortisone impairs hippocampal-dependent trace eyeblink conditioning in post-traumatic stress disorder. Neuropsychopharmacology, 31, 182-188.
54. Waddell, J., Bangasser, D. A., & Shors, T. J. (2008). The basolateral nucleus of the amygdala is necessary to induce the opposing effects of stressful experience on learning in males and females. Journal of Neuroscience, 28, 5290-5294. doi: 10.1523/JNEUROSCI.1129-08.2008
55. Wallenstein, G. V., Eichenbaum, H., & Hasselmo, M. E. (1998). The hippocampus as an associator of discontiguous events. Trends in Neuroscience, 21, 317-323. doi: 10.1016/S0166-2236(97)01220-4
56. Watson, D., Clark, L. A., & Tellegen, A. (1988). Development and validation of brief measures of positive and negative affect: The PANAS scales. Journal of Personality & Social Psychology, 54, 1063-1070. doi: 10.1037/0022-3514.54.6.1063
57. Weerda, R., Muehlhan, M., Wolf, O. T., & Thiel, C. M. (2010). Effects of acute psychosocial stress on working memory related brain activity in men. Human Brain Mapping, 31, 1418-1431. doi: 10.1002/hbm.20945
58. Wingenfeld, K., & Wolf, O. T. (in press). HPA axis alterations in mental disorders: Impact on memory and its relevance for therapeutic interventions. CNS Neuroscience & Therapeutics doi: 10.1111/j.1755-5949.2010.00207.x
59. Wolf, O. T. (2008). The influence of stress hormones on emotional memory: Relevance for psychopathology. Acta Psychologica (Amst), 127, 513-531. doi: 10.1016/j.actpsy.2007.08.002
60. Wolf, O. T. (2009). Stress and memory in humans: Twelve years of progress? Brain Research, 1293, 142-154. doi: 10.1016/j.brainres.2009.04.013
61. Wolf, O. T., Minnebusch, D., & Daum, I. (2009). Stress impairs acquisition of delay eyeblink conditioning in men and women. Neurobiology of Learning & Memory, 91, 431-436. doi: 10.1016/j.nlm.2008.11.002
62. Wolf, O. T., Schommer, N. C., Hellhammer, D. H., McEwen, B. S., & Kirschbaum, C. (2001). The relationship between stress induced cortisol levels and memory differs between men and women. Psychoneuroendocrinology, 26, 711-720. doi: 10.1016/S0306-4530(01)00025-7
63. 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. doi: 10.1101/lm.189106