Stress and memory: Opposing effects of glucocorticoids on memory consolidation and memory retrieval

Neurobiology of Learning and Memory

Volumn 78, Issue 3, 2002, Pages 578-595

  Roozendaal, Benno ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Amygdala; Corticosterone; Dexamethasone; Emotional arousal; Hippocampus; Memory storage; Norepinephrine

Indexed keywords

11BETA,17BETA DIHYDROXY 6 METHYL 17ALPHA (1 PROPYNYL)ANDROSTA 1,4,6 TRIEN 3 ONE; CATECHOLAMINE; CENTRAL STIMULANT AGENT; GLUCOCORTICOID; GLUCOCORTICOID RECEPTOR AGONIST; UNCLASSIFIED DRUG;

ADRENAL CORTEX; AMYGDALOID NUCLEUS; BRAIN REGION; COGNITION; HORMONE RELEASE; HUMAN; HYPOTHESIS; MEMORY; MEMORY CONSOLIDATION; NONHUMAN; NORADRENERGIC SYSTEM; REVIEW; STRESS; TRAINING;

EID: 0036880914     PISSN: 10747427     EISSN: None     Source Type: Journal    
DOI: 10.1006/nlme.2002.4080     Document Type: Review

References (93)

1. Arbel I., Kadar T., Silbermann M., Levy A. The effects of long-term corticosterone administration on hippocampal morphology and cognitive performance of middle-aged rats. Brain Research. 657:1994;227-235.
2. Arnsten A. F. Stress impairs prefrontal cortical function in rats and monkeys: Role of dopamine D1 and norepinephrine alpha-1 receptor mechanisms. Progress in Brain Research. 126:2000;183-192.
3. Barbazanges A., Vincenzo P., Le Moal M., Maccari S. Maternal glucocorticoid secretion mediates long-term effects of prenatal stress. Journal of Neuroscience. 16:1996;3943-3949.
4. Belanoff J. K., Gross K., Yager A., Schatzberg A. F. Corticosteroids and cognition. Journal of Psychiatric Research. 35:2001;127-145.
5. Bodnoff S. R., Humphreyz A. G., Lehman J. C., Diamond D. M., Rose G. M., Meaney M. J. Enduring effects of chronic corticosterone treatment on spatial learning, synaptic plasticity, and hippocampal neuropathology in young and mid-aged rats. Journal of Neuroscience. 15:1995;61-69.
6. Bohus B. Humoral modulation of learning and memory processes: Physiological significance of brain and peripheral mechanisms. Delacour J. The memory system of the brain. 1994;337-364 World Scientific.
7. Borrell J., de Kloet E. R., Versteeg D. H. G., Bohus B. Inhibitory avoidance deficit following short-term adrenalectomy in the rat: The role of adrenal catecholamines. Behavioral and Neural Biology. 39:1983;241-258.
8. Buchanan T. W., Lovallo W. R. Enhanced memory for emotional material following stress-level cortisol treatment in humans. Psychoneuroendocrinology. 26:2001;307-317.
9. Cahill L., McGaugh J. L. NMDA-induced lesions of the amygdaloid complex block the retention enhancing effect of posttraining epinephrine. Psychobiology. 19:1991;206-210.
10. Conrad C. D., Galea L. A. M., Kuroda Y., McEwen B. S. Chronic stress impairs rat spatial memory on the Y-maze, and this effect is blocked by tianeptine pretreatment. Behavioral Neuroscience. 110:1996;1321-1334.
11. Conrad, C. D., Lupien, S. J., & McEwen, B. S. (1999). Support for a bimodal role for Type II adrenal steroid receptors in spatial memory. Neurobiology of Learning and Memory, 72, 39-46,
12. Cordero M. I., Sandi C. A role for brain glucocorticoid receptors in contextual fear conditioning: Dependence upon training intensity. Brain Research. 786:1998;11-17.
13. Cottrell G. A., Nakajima S. Effects of corticosteroids in the hippocampus on passive avoidance behavior in the rat. Pharmacology, Biochemistry & Behavior. 7:1977;277-280.
14. Dachir S., Kadar T., Robinzon B., Levy A. Cognitive deficits induced in young rats by long-term corticosterone administration. Behavioral and Neural Biology. 60:1993;103-109.
15. Daly J. W., Padgett Y., Creveling D., Cantacuzene D., Kirk K. L. Cyclic AMP-generating systems: Regional differences in activation by adrenergic receptors in rat brain. Journal of Neuroscience. 1:1981;49-59.
16. Davis H. P., Squire L. R. Protein synthesis and memory: A review. Psychological Bulletin. 96:1984;518-559.
17. de Kloet E. R. Brain corticosteroid receptor balance and homeostatic control. Frontiers in Neuroendocrinology. 12:1991;95-164.
18. de Kloet E. R., de Kock S., Schild V., Veldhuis H. D. Antiglucocorticoid RU 38486 attenuates retention of a behavior and disinhibits the hypothalamic-pituitary-adrenal axis at different sites. Neuroendocrinology. 47:1988;109-115.
19. de Kloet E. R., Oitzl M. S., Joëls M. Stress and cognition: Are corticosteroids good or bad guys? Trends in Neuroscience. 22:1999;422-426.
20. de Quervain D. J.-F., Roozendaal B., McGaugh J. L. Stress and glucocorticoids impair retrieval of long-term spatial memory. Nature. 394:1998;787-790.
21. de Quervain D. J.-F., Roozendaal B., Nitsch R. M., McGaugh J. L., Hock C. Acute cortisone administration impairs retrieval of long-term declarative memory in humans. Nature Neuroscience. 3:2000;313-314.
22. Diamond D. M., Park C. R., Heman K. L., Rose G. M. Exposing rats to a predator impairs spatial working memory in the radial arm water maze. Hippocampus. 9:1999;542-552.
23. Duncan C. P. The retroactive effect of electroshock on learning. Journal of Comparative and Physiological Psychology. 42:1949;32-44.
24. Fallon J. H., Ciofi P. Distribution of monoamines within the amygdala. Aggleton J. The amygdala: Neurobiological aspects of emotion, memory, and mental dysfunction. 1992;94-114 Wiley-Liss, New York.
25. 1-adrenoceptors. Journal of Neuroscience. 19:1999;5119-5123.
26. Flood J. F., Bennett E. L., Orme A. E., Rosenzweig M. R. Relation of memory formation to controlled amounts of brain protein synthesis. Physiology and Behavior. 15:1975;97-102.
27. Flood J. F., Vidal D., Bennett E. L., Orme A. E., Vasquez S., Jarvik M. E. Memory facilitating and anti-amnestic effects of corticosteroids. Pharmacology, Biochemistry & Behavior. 8:1978;81-87.
28. Floresco S. B., Blaha C. D., Yang C. R., Phillips A. G. Modulation of hippocampal and amygdalar-evoked activity of nucleus accumbens neurons by dopamine: Cellular mechanisms of input selection. Journal of Neuroscience. 21:2001;2851-2860.
29. Gold P. E., van Buskirk R. B. Facilitation of time-dependent memory processes with posttrial epinephrine injections. Behavioral Biology. 13:1975;145-153.
30. Härfstrand A., Fuxe K., Cintra A., Agnati L. F., Zini I., Wikström A. C., Okret S., Yu Z. Y., Goldstein M., Steinbusch H., Verhofstad A., Gustafsson J. Å. Glucocorticoid receptor immunoreactivity in monoaminergic neurons of rat brain. Proceedings of the National Academy of Sciences of the United States of America. 83:1987;9779-9783.
31. Honkaniemi J., Pelto-Huikko M., Rechardt L., Isola J., Lammi A., Fuxe K., Gustafsson J. Å., Wikström A. C., Hökfelt T. Colocalization of peptide and glucocorticoid receptor immunoreactivities in the rat central amygdaloid nucleus. Neuroendocrinology. 55:1992;451-459.
32. Ikegaya Y., Saito H., Abe K. Requirement of basolateral amygdala neuron activity for the induction of long-term potentiation in the dentate gyrus in vivo. Brain Research. 671:1995;351-354.
33. Ikegaya Y., Nakanishi K., Saito H., Abe K. Amygdala β-noradrenergic influence on hippocampal long-term potentiation in vivo. NeuroReport. 8:1997;3143-3146.
34. Introini-Collison I. B., Miyazaki B., McGaugh J. L. Involvement of the amygdala in the memory-enhancing effects of clenbuterol. Psychopharmacology. 104:1991;541-544.
35. Izquierdo L. A., Barros D. M., Ardenghi P. G., Pereira P., Rodrigues C., Choi H., Medina J. H., Izquierdo I. Different hippocampal molecular requirements for short- and long-term retrieval of one-trial avoidance learning. Behavioural Brain Research. 111:2000;93-98.
36. Izquierdo I., Diaz R. D. Influences on memory of posttraining or pre-test injections of ACTH, vasopressin, epinephrine, or β-endorphin and their interaction with naloxone. Psychoneuroendocrinology. 10:1985;165-172.
37. Jackson M. E., Moghaddam B. Amygdala regulation of nucleus accumbens dopamine output is governed by the prefrontal cortex. Journal of Neuroscience. 21:2001;676-681.
38. Joëls M. Corticosteroid actions in the hippocampus. Journal of Neuroendocrinology. 13:2001;657-669.
39. Karten Y. J. G., Slagter E., Joëls M. Effects of long-term elevated corticosteroid levels on synaptically evoked population spikes in the rat CA1 hippocampal area. Neuroscience Letters. 265:1999;41-44.
40. 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. 21:2001;5222-5228.
41. 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. 58:1996;1475-1483.
42. Korte S. M., de Kloet E. R., Buwalda B., Bouman S. D., Bohus B. Antisense to the glucocorticoid receptor in hippocampal dentate gyrus reduces immobility in forced swim test. European Journal of Pharmacology. 301:1996;19-25.
43. Kovacs G. L., Telegdy G., Lissak K. Dose-dependent action of corticosteroids on brain serotonin content and passive avoidance behavior. Hormones & Behavior. 8:1977;155-165.
44. γ-immunoreactivity. Hippocampus. 7:1997;427-436.
45. Liang K. C. Epinephrine modulation of memory: Amygdala activation and regulation of long-term memory storage. Gold P. E., Greenough W. T. Memory consolidation: Essays in honor of James L. McGaugh. 2001;165-183 Am. Psychol. Assoc. Washington.
46. Liang K. C., Chen L. L., Huang T. E. The role of amygdala norepinephrine in memory formation: Involvement of memory enhancing effect of peripheral epinephrine. Chinese Journal of Physiology. 38:1995;81-91.
47. Liang K. C., Juler R., McGaugh J. L. Modulating effects of posttraining epinephrine on memory: Involvement of the amygdala noradrenergic system. Brain Research. 368:1986;125-133.
48. Luine V. N., Spencer R. L., McEwen B. S. Effects of chronic corticosterone ingestion on spatial memory performance and hippocampal serotonergic function. Brain Research. 616:1993;65-70.
49. Luine V., Villegas M., Martinez C., McEwen B. S. Repeated stress causes reversible impairments of spatial memory performance. Brain Research. 639:1994;167-170.
50. Lupien S. J., Gaudreau S., Tchiteya B. M., Maheu F., Sharma S., Nair N. P. V., Hauger R. L., McEwen B. S., Meaney M. J. Stress-induced declarative memory impairment in healthy elderly subjects: Relationship to cortisol reactivity. Journal of Clinical Endocrinology and Metabolism. 82:1997;2070-2075.
51. Lupien S. J., Gillin C. J., Hauger R. L. Working memory is more sensitive than declarative memory to the acute effects of corticosteroids: A dose-response study in humans. Behavioral Neuroscience. 113:1999;420-430.
52. Lupien S. J., McEwen B. S. The acute effects of corticosteroids on cognition: Integration of animal and human model studies. Brain Research Reviews. 24:1997;1-27.
53. Mao Z. M., Arnsten A. F., Li B. M. Local infusion of an alpha-1 adrenergic agonist into the prefrontal cortex impairs spatial working memory performance in monkeys. Biological Psychiatry. 46:1999;1259-1265.
54. Markey K. A., Towle A. C., Sze P. Y. Glucocorticoid influence on tyrosine hydroxylase in mouse locus coeruleus during postnatal development. Endocrinology. 111:1982;1519-1523.
55. McEwen B. S. Glucocorticoid-biogenic amine interaction in relation to mood and behavior. Biochemical Pharmacology. 36:1987;1755-1763.
56. McGaugh J. L. Time-dependent processes in memory storage. Science. 153:1966;1351-1358.
57. McGaugh J. L. Memory - A century of consolidation. Science. 287:2000;248-251.
58. McGaugh J. L., Cahill L., Roozendaal B. Involvement of the amygdala in memory storage: Interaction with other brain systems. Proceedings of the National Academy of Sciences of the United States of America. 93:1996;13508-13514.
59. McGaugh J. L., Ferry B., Vazdarjanova A., Roozendaal B. Amygdala: Role in modulation of memory storage. Aggleton J. P. The amygdala: A functional analysis. 2000;391-423 Oxford Univ. Press, Oxford.
60. McGaugh J. L., Roozendaal B. Role of adrenal stress hormones in forming lasting memories in the brain. Current Opinion in Neurobiology. 12:2002;205-210.
61. Micheau J., Destrade C., Soumireu-Mourat B. Time-dependent effects of posttraining intrahippocampal injections of corticosterone on retention of appetitive learning tasks in mice. European Journal of Pharmacology. 106:1985;39-46.
62. Newcomer J. W., Craft S., Hershey T., Askins K., Bardgett M. E. Glucocorticoid-induced impairment in declarative memory performance in adult humans. Journal of Neuroscience. 14:1994;2047-2053.
63. Oitzl M. S., de Kloet E. R. Selective corticosteroid antagonists modulate specific aspects of spatial orientation learning. Behavioral Neuroscience. 106:1992;62-71.
64. Pfaff D. W., Silva M. T. A., Weiss J. M. Telemetred recording of hormone effects on hippocampal neurons. Science. 171:1971;394-395.
65. Pikkarainen M., Rönkkö S., Savander V., Insausti R., Pitkänen A. Projections from the lateral, basal, and accessory basal nuclei of the amygdala to the hippocampal formation in rat. Journal of Comparative Neurology. 403:1999;229-260.
66. Pugh C. R., Tremblay D., Fleshner M., Rudy J. W. A selective role for corticosterone in contextual-fear conditioning. Behavioral Neuroscience. 111:1997;503-511.
67. Quirarte G. L., Roozendaal B., McGaugh J. L. Glucocorticoid enhancement of memory storage involves noradrenergic activation in the basolateral amygdala. Proceedings of the National Academy of Sciences of the United States of America. 94:1997;14048-14053.
68. Reul J. M. H. M., de Kloet E. R. Two receptor systems for corticosterone in the rat brain: Microdistribution and differential occupation. Endocrinology. 117:1985;2505-2512.
69. Reus Y. Hormonal mediation of the memory disorder in depression. Drug Level Research. 4:1984;489-500.
70. Roozendaal B. Glucocorticoids and the regulation of memory consolidation. Psychoneuroendocrinology. 25:2000;213-238.
71. Roozendaal B., Carmi O., McGaugh J. L. Adrenocortical suppression blocks the memory-enhancing effects of amphetamine and epinephrine. Proceedings of the National Academy of Sciences of the United States of America. 93:1996a;1429-1433.
72. Roozendaal B., de Quervain D. J.-F., Ferry B., Setlow B., McGaugh J. L. Basolateral amygdala-nucleus accumbens interactions in mediating glucocorticoid enhancement of memory consolidation. Journal of Neuroscience. 21:2001a;2518-2525.
73. Roozendaal, B., & McGaugh, J. L. (1996). Amygdala nuclei lesions differentially affect glucocorticoid-induced memory enhancement in an inhibitory avoidance task. Neurobiology of Learning and Memory, 65, 1-8,
74. Roozendaal, B., & McGaugh, J. L. (1997a). Glucocorticoid receptor agonist and antagonist administration into the basolateral but not central amygdala modulates memory storage. Neurobiology of Learning and Memory, 67, 176-179,
75. Roozendaal B., McGaugh J. L. Basolateral amygdala lesions block the memory-enhancing effect of glucocorticoid administration in the dorsal hippocampus of rats. European Journal of Neuroscience. 9:1997b;76-83.
76. 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. Proceedings of the National Academy of Sciences of the United States of America. 96:1999a;11642-11647.
77. Roozendaal B., Phillips R. G., Power A. E., Brooke S. M., Sapolsky R. M., McGaugh J. L. Memory retrieval impairment induced by hippocampal CA3 lesions is blocked by adrenocortical suppression. Nature Neuroscience. 4:2001b;1169-1171.
78. Roozendaal B., Portillo-Marquez G., McGaugh J. L. Basolateral amygdala lesions block glucocorticoid-induced modulation of memory for spatial learning. Behavioral Neuroscience. 110:1996b;1074-1083.
79. Roozendaal B., Quirarte G. L., McGaugh J. L. Glucocorticoids interact with the basolateral amygdala β-adrenoceptor-cAMP/PKA system in influencing memory consolidation. European Journal of Neuroscience. 15:2002;553-560.
80. Roozendaal B., Sapolsky R. M., McGaugh J. L. Basolateral amygdala lesions block the disruptive effects of long-term adrenalectomy on spatial memory. Neuroscience. 84:1998;453-465.
81. Roozendaal B., Williams C. L., McGaugh J. L. Glucocorticoid receptor activation in the rat nucleus of the solitary tract facilitates memory consolidation: Involvement of the basolateral amygdala. European Journal of Neuroscience. 11:1999b;1317-1323.
82. Rosenkranz J. A., Grace A. A. Dopamine attenuates prefrontal cortical suppression of sensory inputs to the basolateral amygdala of rats. Journal of Neuroscience. 21:2001;4090-4103.
83. Sandi C., Loscertales M., Guanza C. Experience-dependent facilitating effect of corticosterone on spatial memory formation in the water maze. European Journal of Neuroscience. 9:1997;637-642.
84. Sandi C., Rose S. P. R. Corticosterone enhances long-term memory in one day-old chicks trained in a weak passive avoidance learning paradigm. Brain Research. 647:1994a;106-112.
85. Sandi C., Rose S. P. R. Corticosteroid receptor antagonists are amnestic for passive avoidance learning in day-old chicks. European Journal of Neuroscience. 6:1994b;1292-1297.
86. Sandi C., Rose S. P. R. Training-dependent biphasic effects of corticosterone in memory formation for a passive avoidance task in chicks. Psychopharmacology. 133:1997;152-160.
87. Sapolsky R., Krey L., McEwen B. S. Prolonged glucocorticoid exposure reduces hippocampal neuron number: Implications for aging. Journal of Neuroscience. 5:1985;1222-1227.
88. Setlow B., Roozendaal B., McGaugh J. L. Involvement of a basolateral amygdala complex-nucleus accumbens pathway in glucocorticoid-induced modulation of memory consolidation. European Journal of Neuroscience. 12:2000;367-375.
89. Sternberg D. B., Isaacs K. R., Gold P. E., McGaugh J. L. Epinephrine facilitation of appetitive learning: Attenuation with adrenergic receptor antagonists. Behavioral and Neural Biology. 44:1985;447-453.
90. Szapiro G., Izquierdo L. A., Alonso M., Barros D., Paratcha G., Ardenghi P., Pereira P., Medina J. H., Izquierdo I. Participation of hippocampal metabotropic glutamate receptors, protein kinase A and mitogen-activated protein kinases in memory retrieval. Neuroscience. 99:2000;1-5.
91. Whelan T. B., Schteingart D. E., Starkman M. N., Smith A. Neuropsychological deficits in Cushing's syndrome. Journal of Nervous and Mental Disease. 168:1980;753-757.
92. Williams C. L., Men D., Clayton E. C., Gold P. E. Norepinephrine release in the amygdala following systemic injection of epinephrine or escapable footshock: Contribution of the nucleus of the solitary tract. Behavioral Neuroscience. 112:1998;1414-1422.
93. Wolkowitz O. M., Weingartner H. Defining cognitive changes in depression and anxiety: A psychobiological analysis. Psychiatrical Psychobiology. 3:1988;1315-1385.