Stress effects on memory: An update and integration

Neuroscience and Biobehavioral Reviews

Volumn 36, Issue 7, 2012, Pages 1740-1749

  Schwabe, Lars ^a   Joëls, Marian ^b   Roozendaal, Benno ^c   Wolf, Oliver T ^a   Oitzl, Melly S ^d  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^c UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^d LEIDEN UNIVERSITY   (Netherlands)

Author keywords

Consolidation; Encoding; Glucocorticoids; Memory; Multiple memory systems; Noradrenaline; Retrieval; Stress

Indexed keywords

CATECHOLAMINE; GLUCOCORTICOID;

ACUTE STRESS; ADRENERGIC TRANSMISSION; AMYGDALOID NUCLEUS; BEHAVIOR CHANGE; BRAIN REGION; CORPUS STRIATUM; DISEASE ASSOCIATION; EARLY LIFE STRESS; ELECTROENCEPHALOGRAM; HIPPOCAMPUS; HUMAN; INFORMATION RETRIEVAL; LONG TERM MEMORY; MEMORY; MEMORY CONSOLIDATION; MENTAL TASK; MOLECULAR DYNAMICS; MOLECULAR MODEL; NONHUMAN; PRENATAL STRESS; PRIORITY JOURNAL; REVIEW; STIMULUS RESPONSE; TASK PERFORMANCE; TREND STUDY;

AMYGDALA; ANIMALS; GLUCOCORTICOIDS; HIPPOCAMPUS; HUMANS; MEMORY, LONG-TERM; NEURONAL PLASTICITY; STRESS, PSYCHOLOGICAL;

EID: 84857774507     PISSN: 01497634     EISSN: 18737528     Source Type: Journal    
DOI: 10.1016/j.neubiorev.2011.07.002     Document Type: Review

References (132)

1. Abercrombie H.C., Speck N.S., Monticelli R.M. Endogenous cortisol elevations are related to memory facilitation only in individuals who are emotionally aroused. Psychoneuroendocrinology 2006, 31:187-196.
2. Akirav I., Richter-Levin G. Mechanisms of amygdala modulation of hippocampal plasticity. J. Neurosci. 2002, 22:9912-9921.
3. Andreano J.M., Cahill L. Glucocorticoid release and memory consolidation in men and women. Psychol. Sci. 2006, 17:466-470.
4. Balleine B.W., Dickinson A. Goal-directed instrumental action: contingency and incentive learning and their cortical substrates. Neuropharmacology 1998, 37:407-419.
5. Barsegyan A., Mackenzie S.M., Kurose B.D., McGaugh J.L., Roozendaal B. Glucocorticoids in the prefrontal cortex enhance memory consolidation and impair working memory by a common neural mechanism. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:16655-16660.
6. Beckner V.E., Tiucker D.M., Delville Y., Mohr D.C. Stress facilitates consolidation of verbal memory for a film but does not affect memory retrieval. Behav. Neurosci. 2006, 120:518-527.
7. Borrell J., De Kloet E.R., Bohus B. Corticosterone decreases the efficacy of adrenaline to affect passive avoidance retention of adrenalectomized rats. Life Sci. 1984, 34:99-104.
8. Bredy T.W., Zhang T.Y., Grant R.J., Diorio J., Meaney M.J. Peripubertal environmental enrichment reverses the effects of maternal care on hippocampal development and glutamate receptor subunit expression. Eur. J. Neurosci. 2004, 20:1355-1362.
9. Brunson K.L., Kramar E., Lin B., Chen Y., Colgin L.L., Yanagihara T.K., Lynch G., Baram T.Z. Mechanisms of late-onset cognitive decline after early-life stress. J. Neurosci. 2005, 25:9328-9338.
10. Buchanan T.W., Lovallo W.R. Enhanced memory for emotional material following stress-level cortisol treatment in humans. Psychoneuroendocrinology 2001, 26:307-317.
11. Buchanan T.W., Tranel D. Stress and emotional memory retrieval: effects of sex and cortisol response. Neurobiol. Learn. Mem. 2008, 89:134-141.
12. Buchanan T.W., Tranel D., Adolphs R. Impaired memory retrieval correlates with individual differences in cortisol response but not autonomic response. Learn. Mem. 2006, 13:382-387.
13. Cahill L., Gorski L., Le K. Enhanced human memory consolidation with post-learning stress: interaction with the degree of arousal at encoding. Learn. Mem. 2003, 10:270-274.
14. Cai W.H., Blundell J., Han J., Greene R.W., Powell C.M. Postreactivation glucocorticoids impair recall of established fear memory. J. Neurosci. 2006, 26:9560-9566.
15. Champagne D.L., Bagot R.C., van Hasselt F., Ramakers G., Meaney M.J., de Kloet E.R., Joëls M., Krugers H. Maternal care and hippocampal plasticity: evidence for experience-dependent structural plasticity, altered synaptic functioning, and differential responsiveness to glucocorticoids and stress. J. Neurosci. 2008, 28:6037-6045.
16. Cottrell E.C., Seckl J.R. Prenatal stress, glucocorticoids and the programming of adult disease. Front. Behav. Neurosci. 2009, 3:1-9.
17. de Kloet E.R., Oitzl M.S., Joëls M. Stress and cognition: are corticosteroids good or bad guys?. Trends Neurosci. 1999, 22:422-426.
18. de Kloet E.R., Joëls M., Holsboer F. Stress and the brain: from adaptation to disease. Nat. Rev. Neurosci. 2005, 6:463-475.
19. De Quervain D.J., Aerni A., Roozendaal B. Preventive effect of β-adrenoceptor blockade on glucocorticoid-induced memory retrieval deficits. Am. J. Psychiatry 2007, 164:967-969.
20. De Quervain D.J., Roozendaal B., McGaugh J.L. Stress and glucocorticoids impair retrieval of long-term spatial memory. Nature 1998, 394:787-790.
21. De Quervain D.J., Roozendaal B., Nitsch R.M., McGaugh J.L., Hock C. Acute cortisone administration impairs retrieval of long-term declarative memory in humans. Nat. Neurosci. 2000, 3:313-314.
22. 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 Plast. 2007, 2007:60803.
23. Diamond D.M., Campbell A.M., Park C.R., Woodson J.C., Conrad C.D., Bachstetter A.D., Mervis R.F. Influence of predator stress on the consolidation versus retrieval of the long-term spatial memory and hippocampal spinogenesis. Hippocampus 2006, 16:571-576.
24. Diamond D.M., Park C.R., Woodson J.C. Stress generates emotional memories and retrograde amnesia by inducing an endogenous form of hippocampal LTP. Hippocampus 2004, 14:281-291.
25. Dias-Ferreira E., Sousa J.C., Melo I., Morgado P., Mesquita A.R., Cerqueira J.J., Costa R.M., Sousa N. Chronic stress causes frontostriatal reorganization and affects decision-making. Science 2009, 325:621-625.
26. Dickinson A. Actions and habits: the development of behavioral autonomy. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 1985, 308:67-78.
27. Domes G., Heinrichs M., Reichwald U., Hautzinger M. Hypothalamic-pituitary-adrenal axis reactivity to psychological stress and memory in middle-aged women: high responders exhibit enhanced declarative memory performance. Psychoneuroendocrinology 2002, 27:843-853.
28. Dudai Y. Reconsolidation: the advantage of being refocused. Curr. Opin. Neurobiol. 2006, 16:174-178.
29. Elzinga B.M., Bakker A., Bremner J.D. Stress-induced cortisol elevations are associated with impaired delayed, but not immediate recall. Psychiatry Res. 2005, 134:211-223.
30. Gelinas J.N., Nguyen P.V. Beta-adrenergic receptor activation facilitates induction of a protein synthesis-dependent late phase of long-term potentiation. J. Neurosci. 2005, 25:3294-3303.
31. Graybiel A.M. Habits, rituals, and the evaluative brain. Ann. Rev. Neurosci. 2008, 31:359-387.
32. Groeneweg F.L., Karst H., de Kloet E.R., Joëls M. Rapid non-genomic effects of corticosteroids and their role in the central stress response. J. Endocrinol. 2011, 209(2):153-167.
33. Gunnar M., Quevedo K. The neurobiology of stress and development. Annu. Rev. Psychol. 2007, 58:145-173.
34. Gutteling B.M., de Weerth C., Zandbelt N., Mulder E.J., Visser G.H., Buitelaar J.K. Does maternal prenatal stress adversely affect the child's learning and memory at age six?. J. Abnorm. Child Psychol. 2006, 34:789-798.
35. Henckens M.J.A.G., Hermans E.J., Pu Z., Joels M., Fernandez G. Stressed memories: how acute stress affects memory formation in humans. J. Neurosci. 2009, 29:10111-10119.
36. Henckens M.J.A.G., van Wingen G.A., Joëls M., Fernandez G. Time-dependent effects of corticosteroids on human amygdala processing. J. Neurosci. 2010, 30:12725-12732.
37. Hopkins W.F., Johnston D. Frequency-dependent noradrenergic modulation of long-term potentiation in the hippocampus. Science 1984, 226:350-352.
38. Huang Y.Y., Kandel E.R. Modulation of both the early and the late phase of mossy fiber LTP by the activation of beta-adrenergic receptors. Neuron 1996, 16:611-617.
39. Joëls M. Corticosteroid effects in the brain: U-shape it. Trends Pharmacol. Sci. 2006, 27:244-250.
40. Joëls M., Baram T.Z. The neuro-symphony of stress. Nat. Rev. Neurosci. 2009, 10:459-466.
41. Joëls M., Fernandez G., Roozendaal B. Stress and emotional memory: a matter of timing. Trends Cogn. Sci. 2011, 15:280-288.
42. Joëls M., Pu Z., Wiegert O., Oitzl M.S., Krugers H.J. Learning under stress: how does it work?. Trends Cogn. Sci. 2006, 10:152-158.
43. Karst H., Berger S., Erdmann G., Schütz G., Joëls M. Metaplasticity of amygdalar responses to the stress hormone corticosterone. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:14449-14454.
44. Karst H., Berger S., Turiault M., Tronche F., Schutz G., Joëls M. Mineralocorticoid receptors are indispensable for nongenomic modulation of hippocampal glutamate transmission by corticosterone. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:19204-19207.
45. Katsuki H., Izumi Y., Zorumski C.F. Noradrenergic regulation of synaptic plasticity in the hippocampal CA1 region. J. Neurophysiol. 1997, 77:3013-3020.
46. Kavushansky A., Richter-Levin G. Effects of stress and corticosterone on activity and plasticity in the amygdala. J. Neurosci. Res. 2006, 84:1580-1587.
47. Kim J., Lee H., Han J., Packard M. Amygdala is critical for stress-induced modulation of hippocampal long-term potentiation and learning. J. Neurosci. 2001, 21:5222-5228.
48. Kim J.J., Baxter M.G. Multiple brain-memory systems: the whole does not equal the sum of its parts. Trends Neurosci. 2001, 24:324-330.
49. Kim J.J., Diamond D.M. The stressed hippocampus, synaptic plasticity and lost memories. Nat. Rev. Neurosci. 2002, 3:453-462.
50. 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. J. Neurosci. 2005, 25:1532-1539.
51. 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 Sci. 1996, 58:1475-1483.
52. Kuhlmann S., Piel M., Wolf O.T. Impaired memory retrieval after psychosocial stress in healthy young men. J. Neurosci. 2005, 25:2977-2982.
53. Kuhlmann S., Wolf O.T. A non-arousing test situation abolishes the impairing effects of cortisol on delayed memory retrieval in healthy women. Neurosci. Lett. 2006, 399:268-272.
54. Laplante D.P., Brunet A., Schmitz N., Ciampi A., King S. Project ice storm: prenatal maternal stress affects cognitive and linguistic functioning in 5 1/2-year-old children. J. Am. Acad. Child Adolesc. Psychiatry 2008, 47:1063-1072.
55. LeDoux J.E. The Emotional Brain 1996, Simon and Schuster, New York.
56. Lemaire V., Lamarque S., LeMoal M., Piazza P.V., Abrous D.N. Postnatal stimulation of the pups counteracts prenatal stress-induced deficits in hippocampal neurogenesis. Biol. Psychiatry 2006, 59:786-792.
57. Loman M.M., Gunnar M.R. Early experience and the development of stress reactivity and regulation in children. Neurosci. Biobehav. Rev. 2010, 34(6):867-876.
58. Lovallo W.R., Robinson J.L., Glahn D.C., Fox P.T. Acute effects of hydrocortisone on the human brain: an fMRI study. Psychoneuroendocrinology 2010, 35:15-20.
59. Lupien S., Lepage M. Stress, memory, and the hippocampus: can't live with it, can't live without it. Behav. Brain Res. 2001, 127:137-158.
60. Lupien S.J., McEwen B.S., Gunnar M.R., Heim C. Effects of stress throughout the lifespan on the brain, behavior and cognition. Nat. Rev. Neurosci. 2009, 10(6):434-445.
61. Lupien S.J., Wilkinson C.W., Briere S., Menard C., Ng Ying Kin N.M., Nair N.P. The modulatory effects of corticosteroids on cognition: studies in young human populations. Psychoneuroendocrinology 2002, 27:401-416.
62. Maroun M., Akirav I. Arousal and stress effects on consolidation and reconsolidation of recognition memory. Neuropsychopharmacology 2008, 33:394-405.
63. McGaugh J. Memory-a century of consolidation. Science 2000, 287:248-251.
64. Medina A.C., Charles J.R., Espinoza-Gonzalez V., Sanchez-Resendis O., Prado-Alcala R.A., Roozendaal B., Quirarte G.L. Glucocorticoid administration into the dorsal striatum facilitates memory consolidation of inhibitory avoidance training but not of the context or food shock components. Learn. Mem. 2007, 14:673-677.
65. Miranda M.I., Quirarte G.L., Rodriguez-Garcia G., McGaugh J.L., Roozendaal B. Glucocorticoids enhance taste aversion memory via actions in the insular cortex and basolateral amygdala. Learn. Mem. 2008, 15:468-476.
66. Morimoto M., Morita N., Ozawa H., Yokoyama K., Kawata M. Distribution of glucocorticoid receptor immunoreactivity and mRNA in the rat brain: an immunohistochemical and in situ hybridization study. Neurosci. Res. 1996, 26:235-269.
67. Morris R.G., Anderson E., Lynch G.S., Baudry M. Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5. Nature 1986, 319:774-776.
68. Oitzl M.S., de Kloet E.R. Selective corticosteroid antagonists modulate specific aspects of spatial orientation learning. Behav. Neurosci. 1992, 106:62-71.
69. Oitzl M.S., Fluttert M., de Kloet E.R. Acute blockade of hippocampal glucocorticoid receptors facilitate spatial learning in rats. Brain Res. 1998, 797:159-162.
70. Oitzl M.S., Fluttert M., Sutanto W., de Kloet E.R. Continuous blockade of brain glucocorticoid receptors facilitates spatial learning and memory in rats. Eur. J. Neurosci. 1998, 10:3759-3766.
71. Oitzl M.S., Workel J.O., Fluttert M., Frosch F., de Kloet E.R. Maternal deprivation affects behaviour from youth to senescence: amplification of individual differences in spatial learning and memory in senescent Brown Norway rats. Eur. J. Neurosci. 2000, 12:3771-3780.
72. Oitzl M.S., Reichardt H.M., Joëls M., de Kloet E.R. Point mutation in the mouse glucocorticoid receptor preventing DNA binding impairs spatial memory. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:12790-12795.
73. Oitzl M.S., Champagne D.L., van der Veen R., de Kloet E.R. Brain development under stress: hypotheses of glucocorticoid actions revisited. Neurosci. Biobehav. Rev. 2010, 34:853-866.
74. Okuda S., Roozendaal B., McGaugh J.L. Glucocorticoid effects on object recognition memory require training-associated emotional arousal. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:853-858.
75. Oomen C.A., Soeters H., Audureau N., Vermunt L., van Hasselt F., Manders E.M., Joëls M., Lucassen P.J., Krugers H. Severe early life stress hampers spatial learning and neurogenesis, but improves hippocampal synaptic plasticity and emotional learning under high-stress conditions in adulthood. J. Neurosci. 2010, 30:6635-6645.
76. Packard M., Wingard J.C. Amygdala and " emotional" modulation of the relative use of multiple memory systems. Neurobiol. Learn. Mem. 2004, 82:243-252.
77. Packard M.G., Knowlton B.J. Learning and memory functions of the basal ganglia. Ann. Rev. Neurosci. 2002, 25:563-593.
78. Packard M.G., Teather L.A. Amygdala modulation of multiple memory systems: hippocampus and caudate-putamen. Neurobiol. Learn. Mem. 1998, 69:163-203.
79. 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. Learn. Mem. 2007, 14:861-868.
80. Poldrack R.A., Packard M. Competition among multiple memory systems: converging evidence from animal and human brain studies. Neuropsychologia 2003, 41:245-251.
81. Quirarte G.L., Ledesma de la Teja I.S., Casillas M., Serafin N., Prado-Alcala R.A., Roozendaal B. Corticosterone infused into the dorsal striatum selectively enhances memory consolidation of cued water-maze training. Learn. Mem. 2009, 16:586-589.
82. Quirarte G.L., Roozendaal B., McGaugh J.L. Glucocorticoid enhancement of memory storage involves noradrenergic activation in the basolateral amygdala. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:14048-14053.
83. Reul J.M., de Kloet E.R. Two receptor systems for corticosterone in rat brain: microdistribution and differential occupation. Endocrinology 1985, 117:2505-2511.
84. Roozendaal B. Stress and memory: opposing effects of glucocorticoids on memory consolidation and memory retrieval. Neurobiol. Learn. Mem. 2002, 78:578-595.
85. Roozendaal B., Barsegyan A., Lee S. Adrenal stress hormones, amygdala activation, and memory for emotionally arousing experiences. Progress in Brain Research 2008, 167:79-97. Elsevier.
86. Roozendaal B., Bohus B., McGaugh J.L. Dose-dependent suppression of adrenocortical activity with metyrapone: effects on emotion and memory. Psychoneuroendocrinolgy 1996, 21:681-693.
87. Roozendaal B., Griffith Q.K., Buranday J., De Quervain D.J., McGaugh J.L. The hippocampus mediates glucocorticoid-induced impairment of spatial memory retrieval: dependence on the basolateral amygdala. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:1328-1333.
88. Roozendaal B., Hernandez A., Cabrera S.M., Hagewood R., Malvaez M., Stefanko D.P., Haettig J., Wood M.A. Membrane-associated glucocorticoid activity is necessary for modulation of long-term memory via chromatin modification. J. Neurosci. 2010, 30:5037-5046.
89. Roozendaal B., McEwen B.S., Chattarji S. Stress, memory and the amygdala. Nat. Rev. Neurosci. 2009, 10:423-433.
90. Roozendaal B., McGaugh J.L. Amygdaloid nuclei lesions differentially affect glucocorticoid-induced memory enhancement in an inhibitory avoidance task. Neurobiol. Learn. Mem. 1996, 65:1-8.
91. Roozendaal B., McGaugh J.L. Basolateral amygdala lesions block the memory-enhancing effect of glucocorticoid administration in the dorsal hippocampus of rats. Eur. J. Neurosci. 1997, 9:76-83.
92. Roozendaal B., McGaugh J.L. Glucocorticoid receptor agonist and antagonist administration into the basolateral but not central amygdala modulates memory storage. Neurobiol. Learn. Mem. 1997, 67:176-179.
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. J. Neurosci. 2004, 24:1385-1392.
94. Roozendaal B., McReynolds J.R., van der Zee E.A., Lee S., McGaugh J.L., McIntyre C.K. Glucocorticoid effects on memory consolidation depend on functional interactions between the medial prefrontal cortex and basolateral amygdala. J. Neurosci. 2009, 29:14299-14308.
95. Roozendaal B., Nguyen B.T., Power A.E., McGaugh J.L. Basolateral amygdala noradrenergic influence enables enhancement of memory consolidation induced by hippocampal glucocorticoid receptor activation. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:11642-11647.
96. Roozendaal B., Okuda S., De Quervain D.J., McGaugh J.L. Glucocorticoids interact with emotion-induced noradrenergic activation in influencing different memory functions. Neuroscience 2006, 138:901-910.
97. Roozendaal B., Okuda S., Van der Zee E.A., McGaugh J.L. Glucocorticoid enhancement of memory requires arousal-induced noradrenergic activation in the basolateral amygdala. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:6741-6746.
98. Roozendaal B., Quirarte G.L., McGaugh J.L. Glucocorticoids interact with the basolateral amygdala beta-adrenoceptor - cAMP/PKA system in influencing memory consolidation. Eur. J. Neurosci. 2002, 15:553-560.
99. Salehi B., Cordero M.I., Sandi C. Learning under stress: the inverted-u-shape function revisited. Learn. Mem. 2010, 17:522-530.
100. Sandi C., Loscertales M., Guaza C. Experience-dependent facilitating effect of corticosterone on spatial memory formation in the water maze. Eur. J. Neurosci. 1997, 9:637-642.
101. 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. Neurobiol. Learn. Mem. 2008, 90:44-53.
102. Schwabe L., Dalm S., Schachinger H., Oitzl M.S. Chronic stress modulates the use of spatial and stimulus-response learning strategies in mice and man. Neurobiol. Learn. Mem. 2008, 90:495-503.
103. Schwabe L., Oitzl M.S., Philippsen C., Böhringer A., Richter S., Wippich W., Schächinger H. Stress modulates the use of spatial and stimulus-response learning strategies in humans. Learn. Mem. 2007, 14:109-116.
104. Schwabe L., Oitzl M.S., Richter S., Schächinger H. Modulation of spatial and stimulus-response learning strategies by exogenous cortisol in healthy young women. Psychoneuroendocrinology 2009, 34:358-366.
105. Schwabe L., Römer S., Richter S., Dockendorf S., Bilak B., Schachinger H. Stress effects on declarative memory retrieval are blocked by a β-adrenoceptor antagonist in humans. Psychoneuroendocrinology 2009, 34:446-454.
106. Schwabe L., Schächinger H., de Kloet E.R., Oitzl M.S. Corticosteroids operate as switch between memory systems. J. Cogn. Neurosci. 2010, 22:1362-1372.
107. Schwabe L., Tegenthoff M., Höffken O., Wolf O.T. Concurrent glucocorticoid and noradrenergic activity shifts instrumental behavior from goal-directed to habitual control. J. Neurosci. 2010, 30:8190-8196.
108. Schwabe L., Wolf O.T. The context counts: congruent learning and testing environments prevent memory retrieval impairment following stress. Cogn. Affect. Behav. Neurosci. 2009, 9:229-236.
109. Schwabe L., Wolf O.T. Stress prompts habit behavior in humans. J. Neurosci. 2009, 29:7191-7198.
110. Schwabe L., Wolf O.T. Learning under stress impairs memory formation. Neurobiol. Learn. Mem. 2010, 93:183-188.
111. Schwabe L., Wolf O.T. Stress impairs the reconsolidation of autobiographical memories. Neurobiol. Learn. Mem. 2010, 94:153-157.
112. Schwabe L., Wolf O.T., Oitzl M.S. Memory formation under stress: quantity and quality. Neurosci. Biobehav. Rev. 2010, 34:584-591.
113. Smeets T., Giesbrecht T., Jelicic M., Merckelbach H. Context-dependent enhancement of declarative memory performance following acute psychosocial stress. Biol. Psychol. 2007, 76:116-123.
114. 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. Psychoneuroendocrinolgy 2008, 33:1378-1386.
115. Smeets T., Wolf O.T., Giesbrecht T., Sijstermans K., Telgen S., Joëls M. Stress selectively and lastingly promotes learning of context-related high arousing information. Psychoneuroendocrinolgy 2009, 34:1152-1161.
116. Squire L.R. Memory systems of the brain: a brief history and current perspective. Neurobiol. Learn. Mem. 2004, 82:171-177.
117. Sutherland R.J., McDonald R.J., Savage D.D. Prenatal exposure to moderate levels of ethanol can have long-lasting effects on learning and memory in adult offspring. Psychobiology 2000, 28:532-539.
118. Toki S., Morinobu S., Imanaka A., Yamamoto S., Yamawaki S., Honma K. Importance of early lighting conditions in maternal care by dam as well as anxiety and memory later in life of offspring. Eur. J. Neurosci. 2007, 25:815-829.
119. Tollenaar M.S., Elzinga B.M., Spinhoven P., Everaerd W. Immediate and prolonged effects of cortisol, but not propranolol, on memory retrieval in healthy young men. Neurobiol. Learn. Mem. 2009, 91:23-31.
120. Van Stegeren A.H., Roozendaal B., Kindt M., Wolf O.T., Joels M. Interacting noradrenergic and corticosteroid systems shift human brain activation patterns during encoding. Neurobiol. Learn. Mem. 2010, 93:56-65.
121. Van Stegeren A.H., Wolf O.T., Everaerd W., Scheltens P., Barkhof F., Rombouts S.A.R.B. Endogenous cortisol level interacts with noradrenergic activation in the human amygdala. Neurobiol. Learn. Mem. 2007, 87:57-66.
122. Voermans N.C., Petersson K.M., Daudey L., Weber B., van Spaendonck K.P., Kremer H.P.H., Fernandez G. Interaction between the human hippocampus and the caudate nucleus during route recognition. Neuron 2004, 43:427-435.
123. Wang X.Y., Zhao M., Ghitza U.E., Li Y.Q., Lu L. Stress impairs reconsolidation of drug memory via glucocorticoid receptors in the basolateral amygdala. J. Neurosci. 2008, 28:5602-5610.
124. Weinstock M. The long-term behavioural consequences of prenatal stress. Neurosci. Biobehav. Rev. 2008, 32:1073-1086.
125. Weymar, M., Schwabe, L., Löw, A., Hamm, A.O., (under review). Stress sensitizes the brain: Increased processing of unpleasant pictures after exposure to acute stress.
126. White N.M. Mnemonic functions of the basal ganglia. Curr. Opin. Neurobiol. 1997, 7:164-169.
127. Wiegert O., Joëls M., Krugers H.J. Timing is essential for rapid effects of corticosterone on synaptic potentiation in the mouse hippocampus. Learn. Mem. 2006, 13:110-113.
128. Williams C.L., Clayton E.C. Contribution of brainstem structures in modulating memory storage processes. Memory Consolidation: Essays in Honor of James L. McGaugh 2001, 141-163. American Psychological Association, Washington D.C. P.E. Gold, W.T. Greenough (Eds.).
129. Yaka R., Salomon S., Matzner H., Weinstock M. Effect of varied gestational stress on acquisition of spatial memory, hippocampal LTP and synaptic proteins in juvenile male rats. Behav. Brain Res. 2007, 179:126-132.
130. Yang J., Han H., Cao J., Li L., Xu L. Prenatal stress modifies hippocampal synaptic plasticity and spatial learning in young rat offspring. Hippocampus 2006, 16:431-436.
131. Zhao L.Y., Zhang X.L., Shi J., Epstein D.H., Lu L. Psychosocial stress after reactivation of drug-related memory impairs later recall in abstinent heroin addicts. Psychopharmacology 2009, 203:599-608.
132. 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. Physiol. Behav. 2011, 103:467-476.