Pre-learning stress that is temporally removed from acquisition exerts sex-specific effects on long-term memory

Neurobiology of Learning and Memory

Volumn 100, Issue , 2013, Pages 77-87

  Zoladz, Phillip R ^a   Warnecke, Ashlee J ^a   Woelke, Sarah A ^a   Burke, Hanna M ^a   Frigo, Rachael M ^a   Pisansky, Julia M ^a   Lyle, Sarah M ^a   Talbot, Jeffery N ^a  

^a OHIO NORTHERN UNIVERSITY   (United States)

Author keywords

Amygdala; Cortisol; Hippocampus; Learning; Memory; Stress

Indexed keywords

HYDROCORTISONE;

ADULT; AROUSAL; ARTICLE; CONTROLLED STUDY; DIASTOLIC BLOOD PRESSURE; EMOTIONALITY; FEMALE; HEART RATE; HORMONE RESPONSE; HUMAN; HUMAN EXPERIMENT; LONG TERM MEMORY; MALE; MENTAL STRESS; NORMAL HUMAN; PAIN; PHYSIOLOGICAL STRESS; PRELEARNING STRESS; RECALL; SALIVA LEVEL; SEX DIFFERENCE; SYSTOLIC BLOOD PRESSURE; WORD RECOGNITION;

ADOLESCENT; AROUSAL; FEMALE; HUMANS; HYDROCORTISONE; LEARNING; MALE; MEMORY, LONG-TERM; MENTAL RECALL; SALIVA; SEX FACTORS; STRESS, PHYSIOLOGICAL; STRESS, PSYCHOLOGICAL; YOUNG ADULT;

EID: 84872367341     PISSN: 10747427     EISSN: 10959564     Source Type: Journal    
DOI: 10.1016/j.nlm.2012.12.012     Document Type: Article

References (75)

1. Adolphs R., Cahill L., Schul R., Babinsky R. Impaired declarative memory for emotional material following bilateral amygdala damage in humans. Learning and Memory 1997, 4(3):291-300.
2. Akirav I., Richter-Levin G. Biphasic modulation of hippocampal plasticity by behavioral stress and basolateral amygdala stimulation in the rat. Journal of Neuroscience 1999, 19(23):10530-10535.
3. Akirav I., Richter-Levin G. Mechanisms of amygdala modulation of hippocampal plasticity. Journal of Neuroscience 2002, 22(22):9912-9921.
4. 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.
5. Andreano J.M., Cahill L. Glucocorticoid release and memory consolidation in men and women. Psychological Science 2006, 17(6):466-470.
6. Andreano J.M., Cahill L. Sex influences on the neurobiology of learning and memory. Learning and Memory 2009, 16(4):248-266.
7. Andreano J.M., Cahill L. Menstrual cycle modulation of medial temporal activity evoked by negative emotion. Neuroimage 2010, 53(4):1286-1293.
8. 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.
9. Beckner V.E., Tucker D.M., Delville Y., Mohr D.C. Stress facilitates consolidation of verbal memory for a film but does not affect retrieval. Behavioral Neuroscience 2006, 120(3):518-527.
10. Bradley, M. M., & Lang, P. J. (1999). Affective norms for English words (ANEW): instruction manual and affective ratings. Technical report C-1. The Center for Research in Psychophysiology, University of Florida.
11. Buchanan T.W., Tranel D. Stress and emotional memory retrieval: Effects of sex and cortisol response. Neurobiology of Learning and Memory 2008, 89(2):134-141.
12. Buchanan T.W., Tranel D., Adolphs R. Impaired memory retrieval correlates with individual differences in cortisol response but not autonomic response. Learning and Memory 2006, 13(3):382-387.
13. Cahill L., Gorski L., Le K. Enhanced human memory consolidation with post-learning stress: Interaction with the degree of arousal at encoding. Learning and Memory 2003, 10(4):270-274.
14. 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 Academic Science USA 1996, 93(15):8016-8021.
15. Cahill L., Haier R.J., White N.S., Fallon J., Kilpatrick L., Lawrence C., et al. Sex-related difference in amygdala activity during emotionally influenced memory storage. Neurobiology of Learning and Memory 2001, 75(1):1-9.
16. Cahill L., Uncapher M., Kilpatrick L., Alkire M.T., Turner J. Sex-related hemispheric lateralization of amygdala function in emotionally influenced memory: An FMRI investigation. Learning and Memory 2004, 11(3):261-266.
17. Cahill L., van Stegeren A. Sex-related impairment of memory for emotional events with beta-adrenergic blockade. Neurobiology of Learning and Memory 2003, 79(1):81-88.
18. Canli T., Desmond J.E., Zhao Z., Gabrieli J.D. Sex differences in the neural basis of emotional memories. Proceedings of the National Academic Science USA 2002, 99(16):10789-10794.
19. Canli T., Zhao Z., Brewer J., Gabrieli J.D., Cahill L. Event-related activation in the human amygdala associates with later memory for individual emotional experience. Journal of Neuroscience 2000, 20(19):RC99.
20. Conrad C.D., Jackson J.L., Wieczorek L., Baran S.E., Harman J.S., Wright R.L., et al. Acute stress impairs spatial memory in male but not female rats: Influence of estrous cycle. Pharmacology, Biochemistry and Behavior 2004, 78(3):569-579.
21. 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.
22. de Quervain D.J., Roozendaal B., McGaugh J.L. Stress and glucocorticoids impair retrieval of long-term spatial memory. Nature 1998, 394(6695):787-790.
23. Diamond D.M., Campbell A.M., Park C.R., Halonen J., Zoladz P.R. 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 2007, 2007:60803.
24. Diamond D.M., Campbell A.M., Park C.R., Woodson J.C., Conrad C.D., Bachstetter A.D., et al. Influence of predator stress on the consolidation versus retrieval of long-term spatial memory and hippocampal spinogenesis. Hippocampus 2006, 16(7):571-576.
25. Dolcos F., LaBar K.S., Cabeza R. Interaction between the amygdala and the medial temporal lobe memory system predicts better memory for emotional events. Neuron 2004, 42(5):855-863.
26. 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.
27. Elzinga B.M., Bakker A., Bremner J.D. Stress-induced cortisol elevations are associated with impaired delayed, but not immediate recall. Psychiatry Research 2005, 134(3):211-223.
28. Ertman N., Andreano J.M., Cahill L. Progesterone at encoding predicts subsequent emotional memory. Learning and Memory 2011, 18(12):759-763.
29. Felmingham K.L., Fong W.C., Bryant R.A. The impact of progesterone on memory consolidation of threatening images in women. Psychoneuroendocrinology 2012, 37(11):1896-1900.
30. Fink G.R., Halligan P.W., Marshall J.C., Frith C.D., Frackowiak R.S., Dolan R.J. Where in the brain does visual attention select the forest and the trees?. Nature 1996, 382(6592):626-628.
31. Fink G.R., Marshall J.C., Halligan P.W., Dolan R.J. Hemispheric asymmetries in global/local processing are modulated by perceptual salience. Neuropsychologia 1999, 37(1):31-40.
32. Frey S., Bergado-Rosado J., Seidenbecher T., Pape H.C., Frey J.U. Reinforcement of early long-term potentiation (early-LTP) in dentate gyrus by stimulation of the basolateral amygdala: Heterosynaptic induction mechanisms of late-LTP. Journal of Neuroscience 2001, 21(10):3697-3703.
33. Halonen, J. D., Zoladz, P. R., Park, C. R., & Diamond, D. M. (2007). Propranolol blocks the stress-induced enhancement, but not impairment, of long-term spatial memory in adult rats. Paper presented at the thirty-seventh annual meeting of the society for neuroscience, San Diego, CA.
34. Hui I.R., Hui G.K., Roozendaal B., McGaugh J.L., Weinberger N.M. Posttraining handling facilitates memory for auditory-cue fear conditioning in rats. Neurobiology of Learning and Memory 2006, 86(2):160-163.
35. 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.
36. Jelicic M., Geraerts E., Merckelbach H., Guerrieri R. Acute stress enhances memory for emotional words, but impairs memory for neutral words. International Journal of Neuroscience 2004, 114(10):1343-1351.
37. Joels M., Fernandez G., Roozendaal B. Stress and emotional memory: A matter of timing. Trends in Cognitive Sciences 2011, 15(6):280-288.
38. Joels M., Pu Z., Wiegert O., Oitzl M.S., Krugers H.J. Learning under stress: How does it work?. Trends in Cognitive Sciences 2006, 10(4):152-158.
39. Joels M., Velzing E., Nair S., Verkuyl J.M., Karst H. Acute stress increases calcium current amplitude in rat hippocampus: Temporal changes in physiology and gene expression. European Journal of Neuroscience 2003, 18(5):1315-1324.
40. Karst H., Berger S., Turiault M., Tronche F., Schutz G., Joels M. Mineralocorticoid receptors are indispensable for nongenomic modulation of hippocampal glutamate transmission by corticosterone. Proceedings of the National Academic Science USA 2005, 102(52):19204-19207.
41. Kim J.J., Koo J.W., Lee H.J., Han J.S. Amygdalar inactivation blocks stress-induced impairments in hippocampal long-term potentiation and spatial memory. Journal of Neuroscience 2005, 25(6):1532-1539.
42. Kim J.J., Lee H.J., Han J.S., Packard M.G. Amygdala is critical for stress-induced modulation of hippocampal long-term potentiation and learning. Journal of Neuroscience 2001, 21(14):5222-5228.
43. 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.
44. Mackiewicz K.L., Sarinopoulos I., Cleven K.L., Nitschke J.B. The effect of anticipation and the specificity of sex differences for amygdala and hippocampus function in emotional memory. Proceedings of the National Academic Science USA 2006, 103(38):14200-14205.
45. McGaugh J.L. The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annual Review of Neuroscience 2004, 27:1-28.
46. Minson C.T., Halliwill J.R., Young T.M., Joyner M.J. Influence of the menstrual cycle on sympathetic activity, baroreflex sensitivity, and vascular transduction in young women. Circulation 2000, 101(8):862-868.
47. Nater U.M., Moor C., Okere U., Stallkamp R., Martin M., Ehlert U., et al. Performance on a declarative memory task is better in high than low cortisol responders to psychosocial stress. Psychoneuroendocrinology 2007, 32(6):758-763.
48. Park C.R., Zoladz P.R., Conrad C.D., Fleshner M., Diamond D.M. Acute predator stress impairs the consolidation and retrieval of hippocampus-dependent memory in male and female rats. Learning and Memory 2008, 15(4):271-280.
49. Payne J.D., Jackson E.D., Hoscheidt S., Ryan L., Jacobs W.J., Nadel L. Stress administered prior to encoding impairs neutral but enhances emotional long-term episodic memories. Learning and Memory 2007, 14(12):861-868.
50. Payne J.D., Jackson E.D., Ryan L., Hoscheidt S., Jacobs J.W., Nadel L. The impact of stress on neutral and emotional aspects of episodic memory. Memory 2006, 14(1):1-16.
51. Payne J.D., Nadel L., Allen J.J., Thomas K.G., Jacobs W.J. The effects of experimentally induced stress on false recognition. Memory 2002, 10(1):1-6.
52. Preuss D., Wolf O.T. Post-learning psychosocial stress enhances consolidation of neutral stimuli. Neurobiology of Learning and Memory 2009, 92(3):318-326.
53. Richter-Levin G., Akirav I. Emotional tagging of memory formation-in the search for neural mechanisms. Brain Research. Brain Research Reviews 2003, 43(3):247-256.
54. Rohleder N., Schommer N.C., Hellhammer D.H., Engel R., Kirschbaum C. Sex differences in glucocorticoid sensitivity of proinflammatory cytokine production after psychosocial stress. Psychosomatic Medicine 2001, 63(6):966-972.
55. Rohleder N., Wolf J.M., Kirschbaum C., Wolf O.T. Effects of cortisol on emotional but not on neutral memory are correlated with peripheral glucocorticoid sensitivity of inflammatory cytokine production. International Journal of Psychophysiology 2009, 72(1):74-80.
56. Sandi C. Glucocorticoids act on glutamatergic pathways to affect memory processes. Trends in Neurosciences 2011, 34(4):165-176.
57. Schwabe L., Bohringer A., Chatterjee M., Schachinger H. Effects of pre-learning stress on memory for neutral, positive and negative words: Different roles of cortisol and autonomic arousal. Neurobiology of Learning and Memory 2008, 90(1):44-53.
58. Schwabe L., Haddad L., Schachinger H. HPA axis activation by a socially evaluated cold-pressor test. Psychoneuroendocrinology 2008, 33(6):890-895.
59. Schwabe L., Joels M., Roozendaal B., Wolf O.T., Oitzl M.S. Stress effects on memory: An update and integration. Neuroscience and Biobehavioral Reviews 2012, 36(7):1740-1749.
60. Schwabe L., Romer S., Richter S., Dockendorf S., Bilak B., Schachinger H. Stress effects on declarative memory retrieval are blocked by a beta-adrenoceptor antagonist in humans. Psychoneuroendocrinology 2009, 34(3):446-454.
61. Schwabe L., Wolf O.T., Oitzl M.S. Memory formation under stress: Quantity and quality. Neuroscience and Biobehavioral Reviews 2010, 34(4):584-591.
62. 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.
63. Smeets T., Wolf O.T., Giesbrecht T., Sijstermans K., Telgen S., Joels M. Stress selectively and lastingly promotes learning of context-related high arousing information. Psychoneuroendocrinology 2009, 34(8):1152-1161.
64. Strange B.A., Dolan R.J. Beta-adrenergic modulation of emotional memory-evoked human amygdala and hippocampal responses. Proceedings of the National Academic Science USA 2004, 101(31):11454-11458.
65. Tollenaar M.S., Elzinga B.M., Spinhoven P., Everaerd W. Long-term outcomes of memory retrieval under stress. Behavioral Neuroscience 2008, 122(3):697-703.
66. Vouimba R.M., Yaniv D., Richter-Levin G. Glucocorticoid receptors and beta-adrenoceptors in basolateral amygdala modulate synaptic plasticity in hippocampal dentate gyrus, but not in area CA1. Neuropharmacology 2007, 52(1):244-252.
67. Wickens T.D. Elementary signal detection theory 2002, University Press, Oxford.
68. Wiegert O., Joels M., Krugers H. Timing is essential for rapid effects of corticosterone on synaptic potentiation in the mouse hippocampus. Learning and Memory 2006, 13(2):110-113.
69. Wolf O.T. Stress and memory in humans: Twelve years of progress?. Brain Research 2009, 1293:142-154.
70. Wolf O.T., Schommer N.C., Hellhammer D.H., McEwen B.S., Kirschbaum C. The relationship between stress induced cortisol levels and memory differs between men and women. Psychoneuroendocrinology 2001, 26(7):711-720.
71. Wood G.E., Beylin A.V., Shors T.J. The contribution of adrenal and reproductive hormones to the opposing effects of stress on trace conditioning in males versus females. Behavioral Neuroscience 2001, 115(1):175-187.
72. Yang Y., Cao J., Xiong W., Zhang J., Zhou Q., Wei H., et al. Both stress experience and age determine the impairment or enhancement effect of stress on spatial memory retrieval. Journal of Endocrinology 2003, 178(1):45-54.
73. Zoladz P.R., Clark B., Warnecke A., Smith L., Tabar J., Talbot J.N. Pre-learning stress differentially affects long-term memory for emotional words, depending on temporal proximity to the learning experience. Physiology & Behavior 2011, 103(5):467-476.
74. Zoladz, P. R., Park, C. R., & Diamond, D. M. (2011b). Neurobiological basis of the complex effects of stress on memory and synaptic plasticity. In C. D. Conrad (Ed.), The handbook of stress: Neuropsychological effects on the brain (pp. 157-178). Oxford, UK: Wiley-Blackwell.
75. 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.