Basolateral amygdala noradrenergic activity mediates corticosterone-induced enhancement of auditory fear conditioning

Neurobiology of Learning and Memory

Volumn 86, Issue 3, 2006, Pages 249-255

  Roozendaal, Benno ^a   Hui, Gabriel K ^a   Hui, Isabel R ^a   Berlau, Daniel J ^a   McGaugh, James L ^a   Weinberger, Norman M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Emotion; Glucocorticoids; Memory consolidation; Norepinephrine; Rat

Indexed keywords

ATENOLOL; BETA 1 ADRENERGIC RECEPTOR; CORTICOSTERONE; GLUCOCORTICOID; SODIUM CHLORIDE;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASSOCIATION; AUDITORY STIMULATION; CONDITIONING; CONTROLLED STUDY; FEAR; LOCOMOTION; LONG TERM MEMORY; MALE; MEMORY CONSOLIDATION; NONHUMAN; NORADRENERGIC SYSTEM; RAT;

ACOUSTIC STIMULATION; ADRENERGIC BETA-1 RECEPTOR ANTAGONISTS; ADRENERGIC BETA-ANTAGONISTS; AMYGDALA; ANALYSIS OF VARIANCE; ANIMALS; ASSOCIATION LEARNING; ATENOLOL; CONDITIONING, CLASSICAL; CORTICOSTERONE; FEAR; INJECTIONS, SUBCUTANEOUS; MALE; MICROINJECTIONS; MOTOR ACTIVITY; NOREPINEPHRINE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, ADRENERGIC, BETA-1; RETENTION (PSYCHOLOGY); SIGNAL TRANSDUCTION;

EID: 33748948417     PISSN: 10747427     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nlm.2006.03.003     Document Type: Article

References (42)

1. Buchanan T.W., and Lovallo W.R. Enhanced memory for emotional material following stress-level cortisol treatment in humans. Psychoneuroendocrinology 26 3 (2001) 307-317
2. Conrad C.D., Lupien S.J., and 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
3. Cordero M.I., and Sandi C. A role for brain glucocorticoid receptors in contextual fear conditioning: dependence upon training intensity. Brain Research 786 1-2 (1998) 11-17
4. 2 adrenergic receptors suppresses fear conditioning: expression of c-Fos and phosphorylated CREB in mouse amygdala. Neuropsychopharmacology 29 2 (2004) 229-239
5. Davis M., Rainnie D., and Cassell M. Neurotransmission in the rat amygdala related to fear and anxiety. Trends in Neurosciences 17 5 (1994) 208-214
6. Debiec J., and LeDoux J.E. Disruption of reconsolidation but not consolidation of auditory fear conditioning by noradrenergic blockade in the amygdala. Neuroscience 129 2 (2004) 267-272
7. de Kloet E.R., Oitzl M.S., and Joëls M. Stress and cognition: are corticosteroids good or bad guys?. Trends in Neurosciences 22 10 (1999) 422-426
8. Flood J.F., Vidal D., Bennett E.L., Orme A.E., Vasquez S., and Jarvik M.E. Memory facilitating and anti-amnesic effects of corticosteroids. Pharmacology, Biochemistry and Behavior 8 1 (1978) 81-87
9. Galvez R., Mesches M.H., and McGaugh J.L. Norepinephrine release in the amygdala in response to footshock stimulation. Neurobiology of Learning and Memory 66 3 (1996) 253-257
10. Hendersen R.W. Fearful memories: the motivational significance of forgetting. In: Brush F.R., and Overmier J.B. (Eds). Affect, conditioning, and cognition: essays on the determinants of behavior (1985), Lawrence Erlbaum Associates, Hillsdale, NJ 43-53
11. Hennessy J.W., Smotherman W.P., and Levine S. Conditioned taste aversion and the pituitary-adrenal system. Behavioral Biology 16 4 (1976) 413-424
12. Heuer F., and Reisberg D. Vivid memories of emotional events: the accuracy of remembered minutiae. Memory and Cognition 18 5 (1990) 496-506
13. Hui G.K., Figueroa I.R., Poytress B.S., Roozendaal B., McGaugh J.L., and Weinberger N.M. Memory enhancement of classical fear conditioning by post-training injections of corticosterone in rats. Neurobiology of Learning and Memory 81 1 (2004) 67-74
14. Johnson L.R., Farb C., Morrison J.H., McEwen B.S., and LeDoux J.E. Localization of glucocorticoid receptors at postsynaptic membranes in the lateral amygdala. Neuroscience 136 1 (2005) 289-299
15. LeDoux J.E. Emotion circuits in the brain. Annual Review of Neuroscience 23 (2000) 155-184
16. Lee H.J., Berger S.Y., Stiedl O., Spiess J., and Kim J.J. Post-training injections of catecholaminergic drugs do not modulate fear conditioning in rats and mice. Neuroscience Letters 303 2 (2001) 123-126
17. McEwen B.S. Glucocorticoid-biogenic amine interactions in relation to mood and behavior. Biochemical Pharmacology 36 11 (1987)
18. McGaugh J.L. The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annual Review of Neuroscience 27 (2004) 1-28
19. McGaugh J.L., and Roozendaal B. Role of adrenal stress hormones in forming lasting memories in the brain. Current Opinion in Neurobiology 12 2 (2002) 205-210
20. McIntyre C.K., Hatfield T., and McGaugh J.L. Amygdala norepinephrine levels after training predict inhibitory avoidance retention performance in rats. European Journal of Neuroscience 16 7 (2002) 1223-1226
21. Micheau J., Destrade C., and 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 (1985) 39-46
22. Mormede P., and Dantzer R. Effects of dexamethasone on fear conditioning in pigs. Behavioral Biology 21 2 (1977) 225-235
23. Oitzl M.S., and de Kloet E.R. Selective corticosteroid antagonists modulate specific aspects of spatial orientation learning. Behavioral Neuroscience 106 1 (1992) 62-71
24. Okuda S., Roozendaal B., and McGaugh J.L. Glucocorticoid effects on object recognition memory require training-associated emotional arousal. Proceedings of the National Academy of Sciences of the United States of America 101 3 (2004) 853-858
25. Paxinos G., and Watson C. The rat brain in stereotaxic coordinates. third ed. (1997), Academic Press, San Diego
26. Pelletier J.G., Likhtik E., Filali M., and Paré D. Lasting increases in basolateral amygdala activity after emotional arousal: implications for facilitated consolidation of emotional memories. Learning and Memory 12 2 (2005) 96-102
27. Phillips R.G., and LeDoux J.E. Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behavioral Neuroscience 106 2 (1992) 274-285
28. Pugh C.R., Fleshner M., and 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
29. Pugh C.R., Tremblay D., Fleshner M., and Rudy J.W. A selective role for corticosterone in contextual-fear conditioning. Behavioral Neuroscience 111 3 (1997) 503-511
30. Quirarte G.L., Roozendaal B., and 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
31. Roozendaal B. Glucocorticoids and the regulation of memory consolidation. Psychoneuroendocrinology 25 3 (2000) 213-238
32. Roozendaal B., and 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
33. Roozendaal B., and 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
34. Roozendaal B., and 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
35. Roozendaal B., Nguyen B.T., Power A.E., and 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
36. Roozendaal B., Okuda S., de Quervain D.J.-F., and McGaugh J.L. Glucocorticoids interact with emotion-induced noradrenergic activation in influencing different memory functions. Neuroscience 138 3 (2006) 901-910
37. Roozendaal B., Quirarte G.L., and McGaugh J.L. Glucocorticoids interact with the basolateral amygdala β-adrenoceptor-cAMP/PKA system in influencing memory consolidation. European Journal of Neuroscience 15 5 (2002) 553-560
38. Roozendaal B., Williams C.L., and 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 4 (1999) 1317-1323
39. Stone E.A., McEwen B.S., Herrera A.S., and Carr K.D. Regulation of α and β components of noradrenergic cyclic cAMP response in cortical slices. European Journal of Pharmacology 141 3 (1987) 347-356
40. Wilensky A.E., Schafe G.E., and 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 1-5
41. Wilensky A.E., Schafe G.E., and 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
42. Zorawski M., and 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