Memory enhancement of classical fear conditioning by post-training injections of corticosterone in rats

Neurobiology of Learning and Memory

Volumn 81, Issue 1, 2004, Pages 67-74

  Hui, Gabriel K ^a   Figueroa, Isabel R ^a   Poytress, Bonnie S ^a   Roozendaal, Benno ^a   McGaugh, James L ^a   Weinberger, Norman M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Auditory fear conditioning; Emotion; Glucocorticoids; Learning; Memory consolidation; Stress hormone

Indexed keywords

CORTICOSTERONE;

ANIMAL EXPERIMENT; ARTICLE; ASSOCIATION; AUDITORY STIMULATION; CONDITIONING; CONTROLLED STUDY; DOSE RESPONSE; FEAR; INJECTION; LOCOMOTION; LONG TERM MEMORY; MALE; MEMORY; MEMORY CONSOLIDATION; MOUSE; NONHUMAN; RAT; SHOCK; SOUND; SPATIAL MEMORY; STATE DEPENDENT LEARNING; STIMULUS RESPONSE; TIME; TRAINING;

EID: 0345549650     PISSN: 10747427     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nlm.2003.09.002     Document Type: Article

References (56)

1. Abercrombie H.C., Kalin N.H., Thurow M.E., Rosenkranz M.A., Davidson R.J. Cortisol variation in humans affects memory for emotionally laden and neutral information. Behavioral Neuroscience. 117(3):2003;505-516.
2. Akirav I., Richter-Levin G. Biphasic modulation of hippocampal plasticity by behavioral stress and basolateral amygdala stimulation in the rat. Journal of Neuroscience. 19(23):1999;10530-10535.
3. Buchanan T.W., Lovallo W.R. Enhanced memory for emotional material following stress-level cortisol treatment in humans. Psychoneuroendocrinology. 26(3):2001;307-317.
4. Cahill L., Alkire M.T. Epinephrine enhancement of human memory consolidation: Interaction with arousal at encoding. Neurobiology of Learning and Memory. 79(2):2003;194-198.
5. Cahill L., van Stegeren A. Sex-related impairment of memory for emotional events with beta-adrenergic blockade. Neurobiology of Learning and Memory. 79(1):2003;81-88.
6. Conrad C.D., LeDoux J.E., Magariños A.M., McEwen B.S. Repeated restraint stress facilitates fear conditioning independently of causing hippocampal CA3 dendritic atrophy. Behavioral Neuroscience. 113(5):1999;902-913.
7. Conrad C.D., Lupien S.J., McEwen B.S. Support for a bimodal role for type II adrenal steroid receptors in spatial memory. Neurobiology of Learning and Memory. 72(1):1999;39-46.
8. Conrad C.D., Mauldin M.L., Hobbs R.J. Metyrapone reveals that previous chronic stress differentially impairs hippocampal-dependent memory. Stress. 4:2001;305-318.
9. Cordero M.I., Sandi C. A role for brain glucocorticoid receptors in contextual fear conditioning: Dependence upon training intensity. Brain Research. 786(1-2):1998;11-17.
10. Corodimas K.P., LeDoux J.E., Gold P.W., Schulkin J. Corticosterone potentiation of conditioned fear in rats. Annals of the New York Academy of Sciences. 746:1994;392-393.
11. Cottrell G.A., Nakajima S. Effect of corticosteroids in the hippocampus on passive avoidance behavior in the rat. Pharmacology, Biochemistry and Behavior. 7(3):1977;277-280.
12. Davis M., Rainnie D., Cassell M. Neurotransmission in the rat amygdala related to fear and anxiety. Trends in Neurosciences. 17(5):1994;208-214.
13. de Kloet E.R., Oitzl M.S., Joëls M. Stress and cognition: Are corticosteroids good or bad guys? Trends in Neuroscience. 22(10):1999;422-426.
14. de Quervain D.J., Roozendaal B., McGaugh J.L. Stress and glucocorticoids impair retrieval of long-term spatial memory. Nature. 394(6695):1998;787-790.
15. Diamond D.M., Bennett M.C., Fleshner M., Rose G.M. Inverted-U relationship between the level of peripheral corticosterone and the magnitude of hippocampal primed burst potentiation. Hippocampus. 2(4):1992;421-430.
16. 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 and Behavior. 8(1):1978;81-87.
17. Gold P.E., Van Buskirk R.B. Facilitation of time-dependent memory processes with posttrial epinephrine injections. Behavioral Biology. 13(2):1975;145-153.
18. Hendersen R.W. Fearful memories: The motivational significance of forgetting. Brush F.R., Overmier J.B. Affect, conditioning, and cognition: Essays on the determinants of behavior. 1985;43-53 Lawrence Erlbaum Associates, Hillsdale, NJ.
19. Heuer F., Reisberg D. Vivid memories of emotional events: The accuracy of remembered minutiae. Memory and Cognition. 18(5):1990;496-506.
20. Ikegaya Y., Saito H., Abe K. High-frequency stimulation of the basolateral amygdala facilitates the induction of long-term potentiation in the dentate gyrus in vivo. Neuroscience Research. 22(2):1995;203-207.
21. 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(14):2001;5222-5228.
22. Kim J.J., Rison R.A., Fanselow M.S. Effects of amygdala, hippocampus, and periaqueductal gray lesions on short- and long-term contextual fear. Behavioral Neuroscience. 107(6):1993;1093-1098.
23. Liang K.C., Chen L.L., Huang T.E. The role of amygdala norepinephrine in memory formation: Involvement in the memory enhancing effect of peripheral epinephrine. Chinese Journal of Physiology. 38(2):1995;81-91.
24. Liang K.C., Juler R.G., McGaugh J.L. Modulating effects of posttraining epinephrine on memory: Involvement of the amygdala noradrenergic system. Brain Research. 368(1):1986;125-133.
25. Liu L., Tsuji M., Takeda H., Takada K., Matsumiya T. Adrenocortical suppression blocks the enhancement of memory storage produced by exposure to psychological stress in rats. Brain Research. 821(1):1999;134-140.
26. Maren S., Aharonov G., Fanselow M.S. Neurotoxic lesions of the dorsal hippocampus and Pavlovian fear conditioning in rats. Behavioural Brain Research. 88(2):1997;261-274.
27. McEwen B.S., Weiss J.M., Schwartz L.S. Uptake of corticosterone by rat brain and its concentration by certain limbic structures. Brain Research. 16(1):1969;227-241.
28. McGaugh J.L., Roozendaal B. Role of adrenal stress hormones in forming lasting memories in the brain. Current Opinion in Neurobiology. 12(2):2002;205-210.
29. 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(1):1984;39-46.
30. Mormede P., Dantzer R. Effects of dexamethasone on fear conditioning in pigs. Behavioral Biology. 21(2):1977;225-235.
31. Oitzl M.S., de Kloet E.R. Selective corticosteroid antagonists modulate specific aspects of spatial orientation learning. Behavioral Neuroscience. 106(1):1992;62-71.
32. 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. Proceedings of the National Academy of Sciences of the United States of America. 98(22):2001;12790-12795.
33. Pavlides C., Watanabe Y., McEwen B.S. Effects of glucocorticoids on hippocampal long-term potentiation. Hippocampus. 3(2):1993;183-192.
34. Phillips R.G., LeDoux J.E. Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behavioral Neuroscience. 106(2):1992;274-285.
35. Phillips R.G., LeDoux J.E. Lesions of the dorsal hippocampal formation interfere with background but not foreground contextual fear conditioning. Learning and Memory. 1(1):1994;34-44.
36. Pugh C.R., Fleshner M., Rudy J.W. Type II glucocorticoid receptor antagonists impair contextual but not auditory-cue fear conditioning in juvenile rats. Neurobiology of Learning and Memory. 67(1):1997;75-79.
37. Pugh C.R., Tremblay D., Fleshner M., Rudy J.W. A selective role for corticosterone in contextual-fear conditioning. Behavioral Neuroscience. 111(3):1997;503-511.
38. 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(25):1997;14048-14053.
39. Reul J.M., de Kloet E.R. Two receptor systems for corticosterone in rat brain: Microdistribution and differential occupation. Endocrinology. 117(6):1985;2505-2511.
40. Roozendaal B. Glucocorticoids and the regulation of memory consolidation. Psychoneuroendocrinology. 25(3):2000;213-238.
41. Roozendaal B. Stress and memory: Opposing effects of glucocorticoids on memory consolidation and memory retrieval. Neurobiology of Learning and Memory. 78(3):2002;578-595.
42. 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(4):1996;1429-1433.
43. 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(7):2001;2518-2525.
44. Roozendaal B., McGaugh J.L. Amygdaloid nuclei lesions differentially affect glucocorticoid-induced memory enhancement in an inhibitory avoidance task. Neurobiology of Learning and Memory. 65(1):1996;1-8.
45. 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(1):1997;76-83.
46. Roozendaal B., McGaugh J.L. Glucocorticoid receptor agonist and antagonist administration into the basolateral but not central amygdala modulates memory storage. Neurobiology of Learning and Memory. 67(2):1997;176-179.
47. 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(20):1999;11642-11647.
48. Roozendaal B., Portillo-Marquez G., McGaugh J.L. Basolateral amygdala lesions block glucocorticoid-induced modulation of memory for spatial learning. Behavioral Neuroscience. 110(5):1996;1074-1083.
49. 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(3):2002;553-560.
50. Sakurai Y. Coding of auditory temporal and pitch information by hippocampal individual cells and cell assemblies in the rat. Neuroscience. 115(4):2002;1153-1163.
51. Sandi C., Rose S.P.R. Corticosterone enhances long-term retention in one-day-old chicks trained in a weak passive avoidance learning paradigm. Brain Research. 647(1):1994;106-112.
52. Sandi C., Rose S.P.R. Training-dependent biphasic effects of corticosterone in memory formation for a passive avoidance task in chicks. Psychopharmacology. 133(2):1997;152-160.
53. Wilensky A.E., Schafe G.E., LeDoux J.E. Functional inactivation of the amygdala before but not after auditory fear conditioning prevents memory formation. Journal of Neuroscience. 19(24):1999;RC48.
54. Wilensky A.E., Schafe G.E., LeDoux J.E. The amygdala modulates memory consolidation of fear-motivated inhibitory avoidance learning but not classical fear conditioning. Journal of Neuroscience. 20(18):2000;7059-7066.
55. Xu L., Anwyl R., Rowan M.J. Behavioural stress facilitates the induction of long-term depression in the hippocampus. Nature. 387(6632):1997;497-500.
56. Zorawski M., Killcross S. Posttraining glucocorticoid receptor agonist enhances memory in appetitive and aversive Pavlovian discrete-cue conditioning paradigms. Neurobiology of Learning and Memory. 78(2):2002;458-464.