Sex differences in stress effects on response and spatial memory formation

Neurobiology of Learning and Memory

Volumn 109, Issue , 2014, Pages 46-55

  Guenzel, Friederike M ^a   Wolf, Oliver T ^a   Schwabe, Lars ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

Glucocorticoids; Hippocampus; Response learning; Spatial learning; Stress; Striatum

Indexed keywords

ACUTE STRESS; ADULT; ARTICLE; COLD PRESSOR TEST; CONTROLLED STUDY; FEMALE; HIPPOCAMPUS; HORMONE RESPONSE; HUMAN; LEARNING DISORDER; MALE; MEMORY DISORDER; MENTAL DEVELOPMENT; MENTAL PERFORMANCE; MENTAL STRESS; MENTAL TASK; MENTAL TEST; SEX DIFFERENCE; SOCIAL STRESS; SPATIAL LEARNING; SPATIAL MEMORY; YOUNG ADULT;

GLUCOCORTICOIDS; HIPPOCAMPUS; RESPONSE LEARNING; SPATIAL LEARNING; STRESS; STRIATUM;

ADULT; FEMALE; HUMANS; HYDROCORTISONE; MALE; MAZE LEARNING; MEMORY; SEX FACTORS; SPACE PERCEPTION; STRESS, PSYCHOLOGICAL; YOUNG ADULT;

EID: 84891118299     PISSN: 10747427     EISSN: 10959564     Source Type: Journal    
DOI: 10.1016/j.nlm.2013.11.020     Document Type: Article

References (58)

1. Andreano J.M., Arjomandi H., Cahill L. Menstrual cycle modulation of the relationship between cortisol and long-term memory. Psychoneuroendocrinology 2008, 33:874-882.
2. Andreano J.M., Cahill L. Glucocorticoid release and memory consolidation in men and women. Psychological Science 2006, 17:466-470.
3. Andreano J.M., Cahill L. Sex influences on the neurobiology of learning and memory. Learning & Memory 2009, 16:248-266.
4. Bohbot V.D., Lerch J., Thorndycraft B., Iaria G., Zijdenbos A.P. Gray matter differences correlate with spontaneous strategies in a human virtual navigation task. The Journal of Neuroscience 2007, 27(38):10078-10083.
5. Bowman R.E., Ferguson D., Luine V.N. Effects of chronic restraint stress and estradiol on open field activity, spatial memory, and monoaminergic neurotransmitters in ovariectomized rats. Neuroscience 2002, 113(2):401-410.
6. Burgess N., Maguire E.A., O'Keefe J. The human hippocampus and spatial and episodic memory. Neuron 2002, 35(4):625-641.
7. Cahill L. His brain, her brain. Scientific American 2005, 40-47.
8. Cahill L. Why sex matters for neuroscience. Nature Reviews Neuroscience 2006, 1-7.
9. Cahill L., Gorski L., Le K. Enhanced human memory consolidation with post-learning stress: Interaction with the degree of arousal at encoding. Learning & Memory 2003, 10(4):270-274.
10. 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, 78:569-579.
11. De Kloet E.R., Joëls M., Holsboer F. Stress and the brain: From adaptation to disease. Nature Reviews Neuroscience 2005, 6:463-475.
12. De Quervain D.J.-F., Roozendaal B., McGaugh J.L. Stress and glucocorticoids impair retrieval of long-term spatial memory. Nature 1998, 394:787-790.
13. 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, 16:571-576.
14. Eldridge L.L., Knowlton B.J., Furmanski C.S., Bookheimer S.Y., Engel S.A. Remembering episodes: A selective role for the hippocampus during retrieval. Nature Neuroscience 2000, 3(11):1149-1152.
15. Elzinga B.M., Bakker A., Bremner J.D. Stress-induced cortisol elevations are associated with impaired delayed, but not immediate recall. Psychiatry Research 2005, 134:211-223.
16. Foy M.R., Baudry M., Thompson R. Estrogen and hippocampal synaptic plasticity. Neuron Glia Biology 2004, 1:327-338.
17. Ghaem O., Mellet E., Crivello F., Tzourio N., Mazoyer B., Berthoz A., et al. Mental navigation along memorized routes activates the hippocampus, precuneus, and insula. NeuroReport 1997, 8:739-744.
18. Goodman J., Leong K.-C., Packard M.G. Emotional modulation of multiple memory systems: Implications for the neurobiology of post-traumatic stress disorder. Reviews in the Neurosciences 2012, 23(5-6):627-643.
19. Guenzel F.M., Wolf O.T., Schwabe L. Stress disrupts response memory retrieval. Psychoneuroendocrinology 2013, 38:1460-1465.
20. Iaria G., Petrides M., Dagher A., Pike B., Bohbot V.D. Cognitive strategies dependent on the hippocampus and caudate nucleus in human navigation: Variability and change with practice. The Journal of Neuroscience 2003, 23(13):5945-5952.
21. Jahn K., Deutschländer A., Stephan T., Strupp M., Wiesmann M., Brandt T. Brain activation patterns during imagined stance and locomotion in functional magnetic resonance imaging. NeuroImage 2004, 22:1722-1731.
22. Joëls 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.
23. Kajantie E., Phillips D.I. The effects of sex and hormonal status on the physiological response to acute psychosocial stress. Psychoneuroendocrinology 2006, 31:151-178.
24. 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. The Journal of Neuroscience 2001, 21(14):5222-5228.
25. 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.
26. Kirschbaum C., Wolf O.T., May M., Wippich W., Hellhammer D.H. Stress- and treatment-induced elevations of cortisol levels associated with impaired declarative memory in healthy adults. Life Sciences 1996, 58(17):1475-1483.
27. Kudielka B.M., Kirschbaum C. Sex differences in HPA axis responses to stress: A review. Biological Psychology 2005, 69:113-132.
28. Kuhlmann S., Piel M., Wolf O.T. Impaired memory retrieval after psychosocial stress in healthy young men. The Journal of Neuroscience 2005, 25(11):2977-2982.
29. Luine V. Sex differences in chronic stress effects on memory in rats. Stress 2002, 5(3):205-216.
30. Lupien S.J., Lepage M. Stress, memory and the hippocampus: Can't live with it, can't live without it. Behavioural Brain Research 2001, 127:137-158.
31. Maguire E.A., Burgess N., Donnett J.G., Frackowiak R.S.J., Frith C.D., O'Keefe J. Knowing where and getting there: A human navigation network. Science 1998, 280:921-924.
32. Maguire E.A., Gadian D.G., Johnsrude I.S., Good C.D., Ashburner J., Frackowiak R.S.J., et al. Navigation-related structural change in the hippocampi of taxi drivers. Proceedings of the National Academy of Sciences 2000, 97(8):4398-4403.
33. Maguire E.A., Woollett K., Spiers H.J. London taxi drivers and bus drivers: A structural MRI and neuropsychological analysis. Hippocampus 2006, 16:1091-1101.
34. Maren S., De Oca B., Fanselow M.S. Sex differences in hippocampal long-term potentiation (LTP) and pavlovian fear conditioning in rats: Positive correlation between LTP and contextual learning. Brain Research 1994, 661(1-2):25-34.
35. McEwen B.S. The neurobiology of stress: From serendipity to clinical relevance. Brain Research 2000, 886:172-189.
36. Medina A.C., Charles J.R., Espinoza-González V., Sánchez-Resendis O., Prado-Alcalá R.A., Roozendaal B., et al. Glucocorticoid administration into the dorsal striatum facilitates memory consolidation of inhibitory avoidance training but not of the context or footshock components. Learning & Memory 2007, 14:673-677.
37. Morris R.G.M., Garrud P., Rawlins J.N.P., O'Keefe J. Place navigation impaired in rats with hippocampal lesions. Nature 1982, 297:681-683.
38. Nyberg L., McIntosh A.R., Houle S., Nilsson L.-G., Tulving E. Activation of medial temporal structures during episodic memory retrieval. Nature 1996, 380:715-717.
39. Packard M.G., Goodman J. Emotional arousal and multiple memory systems in the mammalian brain. Frontiers in Behavioral Neuroscience 2012, 6(14).
40. 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 & Memory 2007, 14:861-868.
41. Quirarte G.L., Ledesma de la Teja I.S., Casillas M., Serafín N., Prado-Alcalá R.A., Roozendaal B. Corticosterone infused into the dorsal striatum selectively enhances memory consolidation of cued water-maze training. Learning & Memory 2009, 16:586-589.
42. Roof R.L., Havens M.D. Testosterone improves maze performance and induces development of a male hippocampus in females. Brain Research 1992, 572:310-313.
43. Roozendaal B., McEwen B.S., Chattarji S. Stress, memory and the amygdala. Nature Reviews Neuroscience 2009, 10:423-433.
44. Ryan L., Nadel L., Keil K., Putnam K., Schnyer D., Trouard T., et al. Hippocampal complex and retrieval of recent and very remote autobiographical memories: Evidende from functional magnetic resonance imaging in neurologically intact people. Hippocampus 2001, 11:707-714.
45. Schwabe L. Stress and the engagement of multiple memory systems: Integration of animal and human studies. Hippocampus 2013, 23:1035-1043.
46. 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(44-53).
47. Schwabe L., Haddad L., Schachinger H. HPA axis activation by a socially evaluated cold-pressor test. Psychoneuroendocrinology 2008, 33:890-895.
48. Schwabe L., Joëls M., Roozendaal B., Wolf O.T., Oitzl M.S. Stress effects on memory: An update and integration. Neuroscience & Biobehavioral Reviews 2012, 36:1740-1749.
49. Schwabe L., Oitzl M.S., Philippsen C., Richter S., Bohringer A., Wippich W., et al. Stress modulates the use of spatial versus stimulus-response learning strategies in humans. Learning & Memory 2007, 14:109-116.
50. Schwabe L., Schächinger H., de Kloet E.R., Oitzl M.S. Corticosteroids operate as a switch between memory systems. Journal of Cognitive Neuroscience 2010, 22(7):1362-1372.
51. Schwabe L., Wolf O.T. Stress prompts habit behavior in humans. The Journal of Neuroscience 2009, 29(22):7191-7198.
52. Schwabe L., Wolf O.T. Stress and multiple memory systems: From 'thinking' to 'doing'. Trends in Cognitive Sciences 2013, 17(2):60-68.
53. Schwabe L., Wolf O.T., Oitzl M.S. Memory formation under stress: Quantity and quality. Neuroscience & Biobehavioural Reviews 2010, 34:584-591.
54. Smeets T., Giesbrecht T., Jelicic M., Merckelbach H. Context-dependent enhancement of declarative memory performance following acute psychosocial stress. Biological Psychology 2007, 76:116-123.
55. 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, 33:1378-1386.
56. Warren S.G., Humphreys A.G., Juraska J.M., Greenough W.T. LTP varies across the estrous cycle: Enhanced synaptic plasticity in proestrus rats. Brain Research 1995, 703:26-30.
57. Wingard J.C., Packard M.G. The amygdala and emotional modulation of competition between cognitive and habit memory. Behavioural Brain Research 2008, 193(1):126-131.
58. 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.