Interacting noradrenergic and corticosteroid systems shift human brain activation patterns during encoding

Neurobiology of Learning and Memory

Volumn 93, Issue 1, 2010, Pages 56-65

  van Stegeren, Anda H ^a   Roozendaal, Benno ^b   Kindt, Merel ^a   Wolf, Oliver T ^c   Joëls, Marian ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

^c RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

Adrenaline; Amygdala; Corticosteroid; Cortisol; Encoding; fMRI; Hippocampus; Memory; Noradrenaline; Prefrontal cortex; Stress

Indexed keywords

AMYLASE; CORTICOSTEROID; CORTICOSTERONE; HYDROCORTISONE; NORADRENALIN; STRESS HORMONE; YOHIMBINE;

ADULT; AMYGDALOID NUCLEUS; ARTICLE; BRAIN FUNCTION; CONTROLLED STUDY; DRUG EFFECT; EPISODIC MEMORY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HIPPOCAMPUS; HUMAN; HUMAN EXPERIMENT; INFORMATION PROCESSING; MALE; MEMORY CONSOLIDATION; MENTAL PERFORMANCE; NORADRENERGIC SYSTEM; NORMAL HUMAN; PATTERN RECOGNITION; PERCEPTIVE DISCRIMINATION; PHARMACOLOGICAL STIMULATION; PREFRONTAL CORTEX; VISUAL STIMULATION;

ADOLESCENT; ADRENAL CORTEX HORMONES; ADRENERGIC ALPHA-ANTAGONISTS; ADULT; AMYGDALA; BRAIN; CENTRAL NERVOUS SYSTEM AGENTS; HIPPOCAMPUS; HUMANS; HYDROCORTISONE; MAGNETIC RESONANCE IMAGING; MALE; NEURAL PATHWAYS; NOREPINEPHRINE; PREFRONTAL CORTEX; RECOGNITION (PSYCHOLOGY); YOHIMBINE; YOUNG ADULT;

EID: 74649086301     PISSN: 10747427     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nlm.2009.08.004     Document Type: Article

References (78)

1. Abercrombie H.C., Kalin N.H., Thurow M.E., Rosenkranz M.A., and Davidson R.J. Cortisol variation in humans affects memory for emotionally laden and neutral information. Behavioral Neuroscience 117 (2003) 505-516
2. Bernabeu R., Bevilaqua L., Ardenghi P., Bromberg E., Schmitz P., Bianchin M., et al. Involvement of hippocampal cAMP/cAMP-dependent protein kinase signaling pathways in a late memory consolidation phase of aversively motivated learning in rats. Proceedings of the National Academy of Sciences of the United States of America 94 (1997) 7041-7046
3. Bremner J.D. The relationship between cognitive and brain changes in posttraumatic stress disorder. Annals of the New York Academy of Sciences 1071 (2006) 80-86
4. Buchanan T.W., and Lovallo W.R. Enhanced memory for emotional material following stress-level cortisol treatment in humans. Psychoneuroendocrinology 26 (2001) 307-317
5. Cahill L., and Alkire M.T. Epinephrine enhancement of human memory consolidation: Interaction with arousal at encoding. Neurobiology of Learning and Memory 79 (2003) 194-198
6. Cahill L., Gorski L., and Le K. Enhanced human memory consolidation with post-learning stress: Interaction with the degree of arousal at encoding. Learning and Memory 10 (2003) 270-274
7. Cahill L., Haier R.J., Fallon J., Alkire M.T., Tang C., Keator D., et al. Amygdala activity at encoding correlated with long-term, free recall of emotional information. Proceedings of the National Academy of Sciences of the United States of America 93 (1996) 8016-8021
8. Cahill L., Prins B., Weber M., and McGaugh J.L. Beta-adrenergic activation and memory for emotional events. Nature 371 (1994) 702-704
9. Cahill L., and van Stegeren A. Sex-related impairment of memory for emotional events with beta-adrenergic blockade. Neurobiology of Learning and Memory 79 (2003) 81-88
10. Cerqueira J.J., Mailliet F., Almeida O.F., Jay T.M., and Sousa N. The prefrontal cortex as a key target of the maladaptive response to stress. Journal of Neuroscience 27 (2007) 2781-2787
11. Christianson S.A., and Loftus E. Memory for traumatic events. Applied Cognitive Psychology 1 (1987) 225-239
12. Christianson S.-A., and Loftus E.F. Remembering emotional events: The fate of detailed information. Cognition and Emotion 5 (1991) 81-108
13. Daselaar S.M., Prince S.E., and Cabeza R. When less means more: Deactivations during encoding that predict subsequent memory. Neuroimage 23 (2004) 921-927
14. Davidson R.J., Fox A., and Kalin N.H. Neural bases of emotion regulation in nonhuman primates and humans. In: Gross J.J. (Ed). Handbook of emotion regulation (2007), Guilford Press, New York 47-68
15. de Kloet E.R., Oitzl M.S., and Joëls M. Stress and cognition: Are corticosteroids good or bad guys?. Trends in Neurosciences 22 (1999) 422-426
16. Diamond D.M., Campbell A.M., Park C.R., Halonen J., and 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 Plasticity 2007 (2007) 60803
17. Dolcos F., LaBar K.S., and Cabeza R. Dissociable effects of arousal and valence on prefrontal activity indexing emotional evaluation and subsequent memory: An event-related fMRI study. Neuroimage 23 (2004) 64-74
18. Dolcos F., LaBar K.S., and Cabeza R. Interaction between the amygdala and the medial temporal lobe memory system predicts better memory for emotional events. Neuron 42 (2004) 855-863
19. Dolcos F., Miller B., Kragel P., Jha A., and McCarthy G. Regional brain differences in the effect of distraction during the delay interval of a working memory task. Brain Research 1152 (2007) 171-181
20. Easterbrook J.A. The effect of emotion on cue utilization and the organization of behavior. Psychological Review 66 (1959) 183-201
21. Goldin P.R., McRae K., Ramel W., and Gross J.J. The neural bases of emotion regulation: Reappraisal and suppression of negative emotion. Biological Psychiatry 63 (2008) 577-586
22. Gomez R.L., Bootzin R.R., and Nadel L. Naps promote abstraction in language-learning infants. Psychological Science 17 (2006) 670-674
23. Grimm S., Schmidt C.F., Bermpohl F., Heinzel A., Dahlem Y., Wyss M., et al. Segregated neural representation of distinct emotion dimensions in the prefrontal cortex-an fMRI study. Neuroimage 30 (2006) 325-340
24. Gusnard D.A., Akbudak E., Shulman G.L., and Raichle M.E. Medial prefrontal cortex and self-referential mental activity: Relation to a default mode of brain function. Proceedings of the National Academy of Sciences of the United States of America 98 (2001) 4259-4264
25. Heuer F., and Reisberg D. Vivid memories of emotional events: The accuracy of remembered minutiae. Memory and Cognition 18 (1990) 496-506
26. Hurlemann R., Hawellek B., Matusch A., Kolsch H., Wollersen H., Madea B., et al. Noradrenergic modulation of emotion-induced forgetting and remembering. Journal of Neuroscience 25 (2005) 6343-6349
27. Hurlemann R., Matusch A., Hawellek B., Klingmuller D., Kolsch H., Maier W., et al. Emotion-induced retrograde amnesia varies as a function of noradrenergic-glucocorticoid activity. Psychopharmacology (Berlin) 194 (2007) 261-269
28. Kellendonk C., Gass P., Kretz O., Schutz G., and Tronche F. Corticosteroid receptors in the brain: Gene targeting studies. Brain Research Bulletin 57 (2002) 73-83
29. Kensinger E.A., Krendl A.C., and Corkin S. Memories of an emotional and a nonemotional event: Effects of aging and delay interval. Experimental Aging Research 32 (2006) 23-45
30. Kensinger E.A., and Schacter D.L. Processing emotional pictures and words: Effects of valence and arousal. Cognitive, Affective, and Behavioral Neuroscience 6 (2006) 110-126
31. Kern S., Oakes T.R., Stone C.K., McAuliff E.M., Kirschbaum C., and Davidson R.J. Glucose metabolic changes in the prefrontal cortex are associated with HPA axis response to a psychosocial stressor. Psychoneuroendocrinology (2008)
32. Kilpatrick L., and Cahill L. Amygdala modulation of parahippocampal and frontal regions during emotionally influenced memory storage. Neuroimage 20 (2003) 2091-2099
33. Kirschbaum C., and Hellhammer D.H. Salivary cortisol in psychoneuroendocrine research: Recent developments and applications. Psychoneuroendocrinology 19 (1994) 313-333
34. Kuhlmann S., and Wolf O.T. Arousal and cortisol interact in modulating memory consolidation in healthy young men. Behavioral Neuroscience 120 (2006) 217-223
35. Labar K.S., and Cabeza R. Cognitive neuroscience of emotional memory. Nature Reviews Neuroscience 7 (2006) 54-64
36. Lang, P. J., Bradley, M. M., & Cuthbert, B. N. (1997). International affective picture system (IAPS) technical manual and affective ratings: NIMH center for the study of emotion and attention, University of Florida, Gainesville, FL.
37. Liang K.C., Juler R.G., and McGaugh J.L. Modulating effects of posttraining epinephrine on memory: Involvement of the amygdala noradrenergic system. Brain Research 368 (1986) 125-133
38. Liberzon I., and Sripada C.S. The functional neuroanatomy of PTSD: A critical review. Progress in Brain Research 167 (2008) 151-169
39. Lupien S.J., Wilkinson C.W., Briere S., Menard C., Ng Ying Kin N.M., and Nair N.P. The modulatory effects of corticosteroids on cognition: Studies in young human populations. Psychoneuroendocrinology 27 (2002) 401-416
40. Maheu F.S., Joober R., Beaulieu S., and Lupien S.J. Differential effects of adrenergic and corticosteroid hormonal systems on human short- and long-term declarative memory for emotionally arousing material. Behavioral Neuroscience 118 (2004) 420-428
41. Maheu F.S., Joober R., and Lupien S.J. Declarative memory after stress in humans: Differential involvement of the beta-adrenergic and corticosteroid systems. Journal of Clinical Endocrinology and Metabolism 90 (2005) 1697-1704
42. McGaugh J.L. Memory - a century of consolidation. Science 287 (2000) 248-251
43. McGaugh J.L. The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annual Review of Neuroscience 27 (2004) 1-28
44. McGaugh J.L., and Roozendaal B. Role of adrenal stress hormones in forming lasting memories in the brain. Current Opinion in Neurobiology 12 (2002) 205-210
45. Nater U.M., Rohleder N., Schlotz W., Ehlert U., and Kirschbaum C. Determinants of the diurnal course of salivary alpha-amylase. Psychoneuroendocrinology 32 (2007) 392-401
46. Nomura M., Ohira H., Haneda K., Iidaka T., Sadato N., Okada T., et al. Functional association of the amygdala and ventral prefrontal cortex during cognitive evaluation of facial expressions primed by masked angry faces: An event-related fMRI study. Neuroimage 21 (2004) 352-363
47. O'Carroll R.E., Drysdale E., Cahill L., Shajahan P., and Ebmeier K.P. Stimulation of the noradrenergic system enhances and blockade reduces memory for emotional material in man. Psychological Medicine 29 (1999) 1083-1088
48. Ochsner K.N., and Gross J.J. The neural architecture of emotion regulation. In: Gross J.J. (Ed). Handbook of emotion regulation (2007), Guilford Press, New York 87-109
49. Oitzl M.S., Reichardt H.M., Joëls M., and 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 (2001) 12790-12795
50. Payne J.D., Jackson E.D., Hoscheidt S., Ryan L., Jacobs W.J., and Nadel L. Stress administered prior to encoding impairs neutral but enhances emotional long-term episodic memories. Learning and Memory 14 (2007) 861-868
51. Phan K.L., Taylor S.F., Welsh R.C., Decker L.R., Noll D.C., Nichols T.E., et al. Activation of the medial prefrontal cortex and extended amygdala by individual ratings of emotional arousal: A fMRI study. Biological Psychiatry 53 (2003) 211-215
52. Phan K.L., Wager T., Taylor S.F., and Liberzon I. Functional neuroanatomy of emotion: A meta-analysis of emotion activation studies in PET and fMRI. Neuroimage 16 (2002) 331-348
53. Pruessner J.C., Dedovic K., Khalili-Mahani N., Engert V., Pruessner M., Buss C., et al. Deactivation of the limbic system during acute psychosocial stress: Evidence from positron emission tomography and functional magnetic resonance imaging studies. Biological Psychiatry 63 (2008) 234-240
54. Pu Z., Krugers H.J., and Joëls M. Corticosterone time-dependently modulates beta-adrenergic effects on long-term potentiation in the hippocampal dentate gyrus. Learning and Memory 14 (2007) 359-367
55. 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 (1997) 14048-14053
56. Raichle M.E., MacLeod A.M., Snyder A.Z., Powers W.J., Gusnard D.A., and Shulman G.L. A default mode of brain function. Proceedings of the National Academy of Sciences of the United States of America 98 (2001) 676-682
57. Raichle M.E., and Snyder A.Z. A default mode of brain function: A brief history of an evolving idea. Neuroimage 37 (2007) 1083-1090 discussion 1097-1089
58. Roozendaal B. 1999 Curt P. Richter award. Glucocorticoids and the regulation of memory consolidation. Psychoneuroendocrinology 25 (2000) 213-238
59. Roozendaal B., Barsegyan A., and Lee S. Adrenal stress hormones, amygdala activation, and memory for emotionally arousing experiences. Progress in Brain Research 167 (2008) 79-97
60. Roozendaal B., Carmi O., and 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 (1996) 1429-1433
61. 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 (1997) 76-83
62. 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 (1999) 11642-11647
63. Roozendaal B., Okuda S., Van der Zee E.A., and McGaugh J.L. Glucocorticoid enhancement of memory requires arousal-induced noradrenergic activation in the basolateral amygdala. Proceedings of the National Academy of Sciences of the United States of America 103 (2006) 6741-6746
64. Roozendaal B., Quirarte G.L., and McGaugh J.L. Glucocorticoids interact with the basolateral amygdala beta-adrenoceptor - cAMP/PKA system in influencing memory consolidation. European Journal of Neuroscience 15 (2002) 553-560
65. Shin L.M., Rauch S.L., and Pitman R.K. Amygdala, medial prefrontal cortex, and hippocampal function in PTSD. Annals of the New York Academy of Sciences 1071 (2006) 67-79
66. Southwick S.M., Davis M., Horner B., Cahill L., Morgan III C.A., Gold P.E., et al. Relationship of enhanced norepinephrine activity during memory consolidation to enhanced long-term memory in humans. American Journal of Psychiatry 159 (2002) 1420-1422
67. Staresina B.P., and Davachi L. Differential encoding mechanisms for subsequent associative recognition and free recall. Journal of Neuroscience 26 (2006) 9162-9172
68. Stark R., Wolf O.T., Tabbert K., Kagerer S., Zimmermann M., Kirsch P., et al. Influence of the stress hormone cortisol on fear conditioning in humans: Evidence for sex differences in the response of the prefrontal cortex. Neuroimage 32 (2006) 1290-1298
69. Strange B.A., and Dolan R.J. Beta-adrenergic modulation of emotional memory-evoked human amygdala and hippocampal responses. Proceedings of the National Academy of Sciences of the United States of America 101 (2004) 11454-11458
70. Urry H.L., van Reekum C.M., Johnstone T., Kalin N.H., Thurow M.E., Schaefer H.S., et al. Amygdala and ventromedial prefrontal cortex are inversely coupled during regulation of negative affect and predict the diurnal pattern of cortisol secretion among older adults. Journal of Neuroscience 26 (2006) 4415-4425
71. van Stegeren A.H. The role of the noradrenergic system in emotional memory. Acta Psychologica (Amsterdam) 127 (2008) 532-541
72. van Stegeren A.H. Imaging stress effects on memory: A review of neuroimaging studies. Canadian Journal of Psychiatry. Revue Canadienne de Psychiatrie 54 (2009) 16-27
73. van Stegeren A.H., Everaerd W., Cahill L., McGaugh J.L., and Gooren L.J. Memory for emotional events: Differential effects of centrally versus peripherally acting beta-blocking agents. Psychopharmacology (Berlin) 138 (1998) 305-310
74. van Stegeren A.H., Goekoop R., Everaerd W., Scheltens P., Barkhof F., Kuijer J.P., et al. Noradrenaline mediates amygdala activation in men and women during encoding of emotional material. Neuroimage 24 (2005) 898-909
75. van Stegeren A., Rohleder N., Everaerd W., and Wolf O.T. Salivary alpha amylase as marker for adrenergic activity during stress: Effect of betablockade. Psychoneuroendocrinology 31 (2006) 137-141
76. van Stegeren A.H., Wolf O.T., Everaerd W., Scheltens P., Barkhof F., and Rombouts S.A. Endogenous cortisol level interacts with noradrenergic activation in the human amygdala. Neurobiology of Learning and Memory 87 (2007) 57-66
77. Wang J., Korczykowski M., Rao H., Fan Y., Pluta J., Gur R.C., et al. Gender difference in neural response to psychological stress. Social Cognitive Affective Neuroscience 2 (2007) 227-239
78. Wolf O.T. The influence of stress hormones on emotional memory: Relevance for psychopathology. Acta Psychologica (Amsterdam) 127 (2008) 513-531