Stress and emotional memory: A matter of timing

Trends in Cognitive Sciences

Volumn 15, Issue 6, 2011, Pages 280-288

  Joëls, Marian ^a   Fernandez, Guillen ^b   Roozendaal, Benno ^c  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b RADBOUD UNIVERSITY   (Netherlands)

^c UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN REGIONS; DYNAMIC INTERACTION; PROTECTIVE CAPACITY;

BRAIN; MAMMALS;

DRUG PRODUCTS;

CHLORPHENIRAMINE MALEATE PLUS PHENYLEPHRINE; CORTICOSTEROID; CORTICOSTEROID RECEPTOR; CORTICOTROPIN; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; DNA; HYDROCORTISONE; ISOPRENALINE; MINERALOCORTICOID RECEPTOR; NORADRENALIN; PROPRANOLOL; PROTEIN KINASE C; STEROID HORMONE; YOHIMBINE;

AMYGDALOID NUCLEUS; BRAIN REGION; CELL FUNCTION; EMOTION; HORMONE BINDING; HUMAN; MEMORY; NERVE CELL; NEUROTRANSMISSION; NONHUMAN; NORADRENALIN RELEASE; NORADRENERGIC SYSTEM; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION; STRESS; TRAINING; TRANSCRIPTION REGULATION;

ADRENAL CORTEX HORMONES; ANIMALS; BRAIN; EMOTIONS; HUMANS; MEMORY; NOREPINEPHRINE; RECEPTORS, AMPA; SIGNAL TRANSDUCTION; STRESS, PSYCHOLOGICAL;

EID: 79957853186     PISSN: 13646613     EISSN: 1879307X     Source Type: Journal    
DOI: 10.1016/j.tics.2011.04.004     Document Type: Review

References (70)

1. McEwen B.S., Gianaros P.J. Stress- and allostasis-induced brain plasticity. Annu. Rev. Med. 2010, 62:431-445.
2. De Kloet E.R., et al. Stress and the brain: from adaptation to disease. Nat. Rev. Neurosci. 2005, 6:463-475.
3. Sara S.J. The locus coerlueus and noradrenergic modulation of cognition. Nat. Rev. Neurosci. 2009, 10:211-223.
4. McIntyre C.K., et al. Amygdala norepinephrine levels after training predict inhibitory avoidance retention performance in rats. Eur. J. Neurosci. 2002, 16:1223-1226.
5. Droste S.K., et al. Corticosterone levels in the brain show a distinct ultradian rhythm but a delayed response to forced swim stress. Endocrinology 2008, 149:3244-3253.
6. Joëls M., Baram T.Z. The neuro-symphony of stress. Nat. Rev. Neurosci. 2009, 10:459-466.
7. Tasker J., et al. Minireview: rapid glucocorticoid signaling via membrane-associated receptors. Endocrinology 2006, 147:5549-5556.
8. LeDoux J.E. Emotion circuits in the brain. Annu. Rev. Neurosci. 2000, 23:155-184.
9. Rodrigues S.M., et al. The influence of stress hormones on fear circuitry. Annu. Rev. Neurosci. 2009, 32:289-313.
10. Roozendaal B., et al. Stress, memory and the amygdala. Nat. Rev. Neurosci. 2009, 10:423-433.
11. Likhtik E., et al. Prefrontal control of the amygdala. J. Neurosci. 2005, 25:7429-7437.
12. Power J.M., et al. Location and function of the slow afterhyperpolarization channels in the basolateral amygdala. J. Neurosci. 2011, 31:526-537.
13. John S., et al. Chromatin accessibility pre-determines glucocorticoid receptor binding patterns. Nat. Genet. 2011, 43:264-268.
14. Rumpel S., et al. Postsynaptic receptor trafficking underlying a form of associative learning. Science 2005, 308:83-88.
15. Isaac J.T., et al. The role of the GluR2 subunit in AMPA receptor function and synaptic plasticity. Neuron 2007, 54:859-871.
16. Hu H., et al. Emotion enhances learning via norepinephrine regulation of AMPA-receptor trafficking. Cell 2007, 131:160-173.
17. Joiner M.L., et al. Assembly of a beta2-adrenergic receptor--GluR1 signalling complex for localized cAMP signalling. EMBO J. 2010, 29:482-495.
18. Groc L., et al. The stress hormone corticosterone conditions AMPAR surface trafficking and synaptic potentiation. Nat. Neurosci. 2008, 11:868-870.
19. Martin S., et al. Corticosterone alters AMPAR mobility and facilitates bidirectional synaptic plasticity. PLoS ONE 2009, 4:e4714.
20. Karst H., Joëls M. Corticosterone slowly enhances miniature excitatory postsynaptic current amplitude in mice CA1 hippocampal cells. J. Neurophysiol. 2005, 94:3479-3486.
21. Yuen E.Y., et al. Acute stress enhances glutamatergic transmission in prefrontal cortex and facilitates working memory. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:14075-14079.
22. Karst H., et al. Mineralocorticoid receptors are indispensable for nongenomic modulation of hippocampal glutamate transmission by corticosterone. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:19204-19207.
23. Karst H., et al. Metaplasticity of amygdalar responses to the stress hormone corticosterone. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:14449-14454.
24. Pu Z., et al. Corticosterone time-dependently modulates beta-adrenergic effects on long-term potentiation in the hippocampal dentate gyrus. Learn Mem. 2007, 14:359-367.
25. Pu Z., et al. Beta-adrenergic facilitation of synaptic plasticity in the rat basolateral amygdala in vitro is gradually reversed by corticosterone. Learn Mem. 2009, 16:155-160.
26. Liebmann L., et al. Effects of corticosterone and the beta-agonist isoproterenol on glutamate receptor-mediated synaptic currents in the rat basolateral amygdala. Eur. J. Neurosci. 2009, 30:800-807.
27. Ferry B., et al. Basolateral amygdala noradrenergic influences on memory storage are mediated by an interaction between β- and α1-adrenoceptors. J. Neurosci. 1999, 19:5119-5123.
28. Borrell J., et al. Corticosterone decreases the efficacy of adrenaline to affect passive avoidance retention of adrenalectomized rats. Life Sci. 1984, 34:99-104.
29. Roozendaal B., et al. Glucocorticoids interact with the basolateral amygdala β-adrenoceptor-cAMP/PKA system in influencing memory consolidation. Eur. J. Neurosci. 2002, 15:553-560.
30. Quirarte G.L., et al. Glucocorticoid enhancement of memory storage involves noradrenergic activation in the basolateral amygdala. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:14048-14053.
31. Roozendaal B., et al. 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.
32. Roozendaal B., et al. Glucocorticoid enhancement of memory requires arousal-induced noradrenergic activation in the basolateral amygdala. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:6741-6746.
33. Okuda S., et al. Glucocorticoid effects on object recognition memory require training-associated emotional arousal. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:853-858.
34. McGaugh J.L., Roozendaal B. Role of adrenal stress hormones in forming lasting memories in the brain. Curr. Opin. Neurobiol. 2002, 12:205-210.
35. McReynolds J.R., et al. Memory-enhancing corticosterone treatment increases amygdala norepinephrine and Arc protein expression in hippocampal synaptic fractions. Neurobiol. Learn. Mem. 2010, 93:312-321.
36. Roozendaal B., et al. Glucocorticoid receptor activation in the rat nucleus of the solitary tract facilitates memory consolidation: involvement of the basolateral amygdala. Eur. J. Neurosci. 1999, 11:1317-1323.
37. Campolongo P., et al. Endocannabinoids in the rat basolateral amygdala enhance memory consolidation and enable glucocorticoid modulation of memory. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:4888-4893.
38. Hill M.N., et al. Rapid induction of limbic endocannabinoid signaling by glucocorticoid hormones in vivo. Psychoneuroendocrinol 2010, 35:1333-1338.
39. Hill M.N., McEwen B.S. Endocannabinoids: the silent partner of glucocorticoids in the synapse. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:4579-4580.
40. Perez-Jaranay J.M., Vives F. Electrophysiological study of the response of medial prefrontal cortex neurons to stimulation of the basolateral nucleus of the amygdala in the rat. Brain Res. 1991, 564:97-101.
41. Akirav I., Richter-Levin G. Biphasic modulation of hippocampal plasticity by behavioral stress and basolateral amygdala stimulation in the rat. J. Neurosci. 1999, 19:10530-10535.
42. Miranda M.I., et al. Glucocorticoids enhance taste aversion memory via actions in the insular cortex and basolateral amygdala. Learn. Mem. 2008, 15:468-476.
43. Roozendaal B., et al. Glucocorticoid effects on memory consolidation depend on functional interactions between the medial prefrontal cortex and basolateral amygdala. J. Neurosci. 2009, 29:14299-14308.
44. Barsegyan A., et al. 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.
45. Roozendaal B., et al. Membrane-associated glucocorticoid activity is necessary for modulation of long-term memory via chromatin modification. J. Neurosci. 2010, 30:5037-5046.
46. Cahill L., et al. Amygdala activity at encoding correlated with long-term, free recall of emotional information. Proc. Natl. Acad. Sci. U.S.A. 1996, 93:8016-8021.
47. Canli T., et al. Event-related activation in the human amygdala associates with later memory for individual emotional experience. J. Neurosci. 2000, 20:RC99.
48. Richardson M.P., et al. Encoding of emotional memories depends on amygdala and hippocampus and their interactions. Nat. Neurosci. 2004, 7:278-285.
49. Strange B.A., Dolan R.J. Beta-adrenergic modulation of emotional memory-evoked human amygdala and hippocampal responses. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:11454-11458.
50. Onur O.A., et al. Noradrenergic enhancement of amygdala responses to fear. Soc. Cogn. Affect. Neurosci. 2009, 4:119-126.
51. Rasch B., et al. A genetic variation of the noradrenergic system is related to differential amygdala activation during encoding of emotional memories. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:19191-19196.
52. Urner, M. et al. Genetic variation of the α2b-adrenoceptor affects neural correlates of successful emotional memory formation. Hum. Brain. Mapp. doi:10.1002/hbm.21171.
53. Cahill L., et al. Beta-adrenergic activation and memory for emotional events. Nature 1994, 371:702-704.
54. de Quervain D.J., et al. A deletion variant of the alpha2b-adrenoceptor is related to emotional memory in Europeans and Africans. Nat. Neurosci. 2007, 10:1137-1139.
55. van Marle H.J., et al. From specificity to sensitivity: how acute stress affects amygdala processing of biologically salient stimuli. Biol. Psychiatry 2009, 66:649-655.
56. Mobbs D., et al. Neural activity associated with monitoring the oscillating threat value of a tarantula. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:20582-20586.
57. Cousijn H., et al. Acute stress modulates genotype effects on amygdala processing in humans. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:9867-9872.
58. Klumpers F., et al. Prefrontal mechanisms of fear reduction after threat offset. Biol. Psychiatry 2010, 68:1031-1038.
59. van Marle H.J., et al. Enhanced resting-state connectivity of amygdala in the immediate aftermath of acute psychological stress. Neuroimage 2010, 53:348-354.
60. van Stegeren A.H., et al. Endogenous cortisol level interacts with noradrenergic activation in the human amygdala. Neurobiol. Learn. Mem. 2007, 87:57-66.
61. Cunningham-Bussel A.C., et al. Diurnal cortisol amplitude and fronto-limbic activity in response to stressful stimuli. Psychoneuroendocrinology 2009, 34:694-704.
62. Henckens M.J., et al. Time-dependent effects of corticosteroids on human amygdala processing. J. Neurosci. 2010, 30:12725-12732.
63. Lovallo W.R., et al. Acute effects of hydrocortisone on the human brain: an fMRI study. Psychoneuroendocrinology 2010, 35:15-20.
64. Tessner K.D., et al. Cortisol responses of healthy volunteers undergoing magnetic resonance imaging. Hum. Brain Mapp. 2006, 27:889-895.
65. Kukolja J., et al. Modeling a negative response bias in the human amygdala by noradrenergic-glucocorticoid interactions. J. Neurosci. 2008, 28:12868-12876.
66. van Stegeren A.H., et al. Interacting noradrenergic and corticosteroid systems shift human brain activation patterns during encoding. Neurobiol. Learn. Mem. 2010, 93:56-65.
67. Yehuda R. Status of glucocorticoid alterations in post-traumatic stress disorder. Ann. N.Y. Acad. Sci. 2009, 1179:56-69.
68. Moriceau S., et al. Early-life stress disrupts attachment learning: the role of amygdala corticosterone, locus ceruleus corticotropin releasing hormone, and olfactory bulb norepinephrine. J. Neurosci. 2009, 29:15745-15755.
69. Valentino R.J., Van Bockstaele Convergent regulation of locus coeruleus activity as an adaptive response to stress. Eur. J. Pharmacol. 2008, 583:194-203.
70. Lightman S.L., Conway-Campbell B.L. The crucial role of pulsatile activity of the HPA axis for continuous dynamic equilibration. Nat. Rev. Neurosci. 2010, 11:710-718.