Delayed effects of cortisol enhance fear memory of trace conditioning

Psychoneuroendocrinology

Volumn 40, Issue 1, 2014, Pages 257-268

  Cornelisse, Sandra ^a,b   van Ast, Vanessa A ^b,c   Joëls, Marian ^a,b   Kindt, Merel ^b  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c RADBOUD UNIVERSITY   (Netherlands)

Author keywords

Cortisol; Fear conditioning; Fear potentiated startle; Memory; PTSD; Trace and delay

Indexed keywords

CORTICOSTEROID; HYDROCORTISONE;

ADULT; ARTICLE; CONDITIONING; CONTROLLED STUDY; FEAR; HIPPOCAMPUS; HORMONE RESPONSE; HUMAN; HUMAN EXPERIMENT; MALE; MEMORY; NORMAL HUMAN; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; SKIN CONDUCTANCE; STARTLE REFLEX; STIMULUS RESPONSE;

CORTISOL; FEAR CONDITIONING; FEAR POTENTIATED STARTLE; MEMORY; PTSD; TRACE AND DELAY;

ADULT; CONDITIONING (PSYCHOLOGY); CUES; DOUBLE-BLIND METHOD; FEAR; HABITUATION, PSYCHOPHYSIOLOGIC; HUMANS; HYDROCORTISONE; LEARNING; MALE; MEMORY; STARTLE REACTION; TIME FACTORS; YOUNG ADULT;

EID: 84893351507     PISSN: 03064530     EISSN: 18733360     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2013.11.013     Document Type: Article

References (69)

1. Van Ast V.A., Vervliet B., Kindt M. Contextual control over expression of fear is affected by cortisol. Front. Behav. Neurosci. 2012, 11:6-67.
2. Van Ast V.A., Cornelisse S., Meeter M., Joëls M., Kindt M. Time-dependent effects of cortisol on the contextualization of emotional memories. Biol. Psychiatry 2013, 74:809-816.
3. Barsegyan A., Mackenzie S.M., Kurose B.D., McGaugh J.L., Roozendaal B. 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.
4. Berns G.S., Laibson D., Loewenstein G. Intertemporal choice - toward an integrative framework. Trends Cogn. Sci. 2007, 11:482-488.
5. Buchanan T.W., Brechtel A., Sollers J.J., Lovallo W.R. Exogenous cortisol exerts effects on the startle reflex independent of emotional modulation. Pharmacol. Biochem. Behav. 2001, 68:203-210.
6. Burman M.A., Starr M.J., Gewirtz J.C. Dissociable effects of hippocampus lesions on expression of fear and trace fear conditioning memories in rats. Hippocampus 2006, 16:103-113.
7. Cahill L. Why sex matters for neuroscience. Nat. Rev. Neurosci. 2006, 7:477-484.
8. Carter R.M., Hofstotter C., Tsuchiya N., Koch C. Working memory and fear conditioning. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:1399-1404.
9. Cheng D.T., Disterhoft J.F., Power J.M., Ellis D.A., Desmond J.E. Neural substrates underlying human delay and trace eyeblink conditioning. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:8108-8113.
10. Diamond D.M., Campbell A.M., Park C.R., Halonen J., 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 Plast. 2007, 2007:60803.
11. Dirikx T., Vansteenwegen D., Eelen P., Hermans D. Non-differential return of fear in humans after a reinstatement procedure. Acta Psychol. (Amst.) 2009, 130:175-182.
12. Elzinga B.M., Roelofs K. Cortisol-induced impairments of working memory require acute sympathetic activation. Behav. Neurosci. 2005, 119:98-103.
13. Fridlund A.J., Cacioppo J.T. Guidelines for human electromyographic research. Psychophysiology 1986, 23:567-589.
14. Hamm A.O., Weike A.I. The neuropsychology of fear learning and fear regulation. Int. J. Psychophysiol. 2005, 57:5-14.
15. Han C.J., O'Tuathaigh C.M., van Trigt L., Quinn J.J., Fanselow M.S., Mongeau R., Koch C., Anderson D.J. Trace but not delay fear conditioning requires attention and the anterior cingulate cortex. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:13087-13092.
16. Henckens M.J.A.G., van Wingen G.A., Joëls M., Fernández G. Time-dependent effects of corticosteroids on human amygdala processing. J. Neurosci. 2010, 30:12725-12732.
17. Henckens M.J.A.G., van Wingen G.A., Joëls M., Fernández G. Time-dependent corticosteroid modulation of prefrontal working memory processing. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:5801-5806.
18. Henckens M.J.A.G., van Wingen G.A., Joëls M., Fernández G. Time-dependent effects of cortisol on selective attention and emotional interference: a functional MRI study. Front. Integr. Neurosci. 2012, 6:66.
19. Hermans E.J., van Marle H.J.F., Ossewaarde L., Henckens M.J.A.G., Qin S., van Kesteren M.T.R., Schoots V.C., Cousijn H., Rijpkema M., Oostenveld R., et al. Stress-related noradrenergic activity prompts large-scale neural network reconfiguration. Science 2011, 334:1151-1153.
20. Jackson E.D., Payne J.D., Nadel L., Jacobs W.J. Stress differentially modulates fear conditioning in healthy men and women. Biol. Psychiatry 2006, 59:516-522.
21. Joëls M., Pu Z., Wiegert O., Oitzl M.S., Krugers H.J. Learning under stress: how does it work?. Trends Cogn. Sci. (Regul. Ed.) 2006, 10:152-158.
22. Joëls M., Fernandez G., Roozendaal B. Stress and emotional memory: a matter of timing. Trends Cogn. Sci. (Regul. Ed.) 2011, 15:280-288.
23. Joëls M., Sarabdjitsingh R.A., Karst H. Unraveling the time domains of corticosteroid hormone influences on brain activity: rapid, slow, and chronic modes. Pharmacol. Rev. 2012, 64:901-938.
24. Karst H., Berger S., Turiault M., Tronche F., Schütz G., Joëls M. Mineralocorticoid receptors are indispensable for nongenomic modulation of hippocampal glutamate transmission by corticosterone. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:19204-19207.
25. Karst H., Berger S., Erdmann G., Schütz G., Joëls M. Metaplasticity of amygdalar responses to the stress hormone corticosterone. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:14449-14454.
26. Kessler R.C., Sonnega A., Bromet E., Hughes M., Nelson C.B. Posttraumatic stress disorder in the National Comorbidity Survey. Arch. Gen. Psychiatry 1995, 52:1048-1060.
27. Kindt M., Soeter M., Vervliet B. Beyond extinction: erasing human fear responses and preventing the return of fear. Nat. Neurosci. 2009, 12:256-258.
28. De Kloet E.R., Joëls M., Holsboer F. Stress and the brain: from adaptation to disease. Nat. Rev. Neurosci. 2005, 6:463-475.
29. Kajantie E., Philips D.I.W. The effects of sex and hormonal status on the physiological response to acute social stress. Psychoneuroendocrinology 2006, 31:151-178.
30. Knight D.C., Cheng D.T., Smith C.N., Stein E.A., Helmstetter F.J. Neural substrates mediating human delay and trace fear conditioning. J. Neurosci. 2004, 24:218-228.
31. Korte S.M. Corticosteroids in relation to fear, anxiety and psychopathology. Neurosci. Biobehav. Rev. 2001, 25:117-142.
32. Kuehl L.K., Lass-Hennemann J., Richter S., Blumenthal T.D., Oitzl M., Schachinger H. Accelerated trace eyeblink conditioning after cortisol IV-infusion. Neurobiol. Learn. Mem. 2010, 94:547-553.
33. Langner O., Dotsch R., Bijlstra G., Wigboldus D.H.J., Hawk S.T., van Knippenberg A. Presentation and validation of the Radboud Faces Database. Cogn. Emot. 2010, 24:1377-1388.
34. Van Marle H.J.F., Hermans E.J., Qin S., Fernández G. Enhanced resting-state connectivity of amygdala in the immediate aftermath of acute psychological stress. Neuroimage 2010, 53:348-354.
35. McGaugh J.L. Time-dependent processes in memory storage. Science 1966, 153:1351-1358.
36. Merz C.J., Tabbert K., Schweckendiek J., Klucken T., Vaitl D., Stark R., Wolf O.T. Investigating the impact of sex and cortisol on implicit fear conditioning with fMRI. Psychoneuroendocrinology 2010, 35:33-46.
37. Merz C.J., Tabbert K., Schweckendiek J., Klucken T., Vaitl D., Stark R., Wolf O.T. Neuronal correlates of extinction learning are modulated by sex hormones. Soc. Cogn. Affect. Neurosci. 2012, 7:819-830.
38. Merz C.J., Tabbert K., Schweckendiek J., Klucken T., Vaitl D., Stark R., Wolf O.T. Oral contraceptive usage alters the effects of cortisol on implicit fear learning. Horm. Behav. 2012, 62:531-538.
39. Merz C.J., Stark R., Vaitl D., Tabbert K., Wolf O.T. Stress hormones are associated with the neuronal correlates of instructed fear conditioning. Biol. Psychol. 2013, 92:82-89.
40. Merz C.J., Wolf O.T., Schweckendiek J., Klucken T., Vaitl D., Stark R. Stress differentially affects fear conditioning in men and women. Psychoneuroendocrinology 2013.
41. Milad M.R., Zeidan M.A., Contero A., Pitman R.K., Klibanski A., Rauch S.L., Goldstein J.M. The influence of gonadal hormones on conditioned fear extinction in healthy humans. Neuroscience 2010, 168:652-658.
42. Mineka S., Oehlberg K. The relevance of recent developments in classical conditioning to understanding the etiology and maintenance of anxiety disorders. Acta Psychol. (Amst.) 2008, 127:567-580.
43. Morsink M.C., Steenbergen P.J., Vos J.B., Karst H., Joëls M., De Kloet E.R., Datson N.A. Acute activation of hippocampal glucocorticoid receptors results in different waves of gene expression throughout time. J. Neuroendocrinol. 2006, 18:239-252.
44. Nees F., Richter S., Lass-Hennemann J., Blumenthal T.D., Schächinger H. Inhibition of cortisol production by metyrapone enhances trace, but not delay, eyeblink conditioning. Psychopharmacology (Berl.) 2008, 199:183-190.
45. 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. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:12790-12795.
46. Pruessner J.C., Wolf O.T., Hellhammer D.H., Buske-Kirschbaum A., von Auer K., Jobst S., Kaspers F., Kirschbaum C. Free cortisol levels after awakening: a reliable biological marker for the assessment of adrenocortical activity. Life Sci. 1997, 61:2539-2549.
47. Qin S., Hermans E.J., van Marle H.J.F., Luo J., Fernández G. Acute psychological stress reduces working memory-related activity in the dorsolateral prefrontal cortex. Biol. Psychiatry 2009, 66:25-32.
48. De Quervain D.J.-F., Margraf J. Glucocorticoids for the treatment of post-traumatic stress disorder and phobias: a novel therapeutic approach. Eur. J. Pharmacol. 2008, 583:365-371.
49. De Quervain D.J.-F., Aerni A., Schelling G., Roozendaal B. Glucocorticoids and the regulation of memory in health and disease. Front. Neuroendocrinol. 2009, 30:358-370.
50. Reul J.M., de Kloet E.R. Two receptor systems for corticosterone in rat brain: microdistribution and differential occupation. Endocrinology 1985, 117:2505-2511.
51. Richter-Levin G., Akirav I. Emotional tagging of memory formation - in the search for neural mechanisms. Brain Res. Brain Res. Rev. 2003, 43:247-256.
52. Rodrigues S.M., LeDoux J.E., Sapolsky R.M. The influence of stress hormones on fear circuitry. Annu. Rev. Neurosci. 2009, 32:289-313.
53. Roozendaal B., Okuda S., de Quervain D.J.-F., McGaugh J.L. Glucocorticoids interact with emotion-induced noradrenergic activation in influencing different memory functions. Neuroscience 2006, 138:901-910.
54. Schwabe L., Schächinger H., de Kloet E.R., Oitzl M.S. Corticosteroids operate as a switch between memory systems. J. Cogn. Neurosci. 2010, 22:1362-1372.
55. Soeter M., Kindt M. Noradrenergic enhancement of associative fear memory in humans. Neurobiol. Learn. Mem. 2011, 96:263-271.
56. Soeter M., Kindt M. Stimulation of the noradrenergic system during memory formation impairs extinction learning but not the disruption of reconsolidation. Neuropsychopharmacology 2012, 37:1204-1215.
57. Spielberger C., Gorsuch R., Lusthene R. Manual for the State-Trait Anxiety Inventory 1970, Psychologist Press, Palo Alto, CA.
58. Stark R., Wolf O.T., Tabbert K., Kagerer S., Zimmermann M., Kirsch P., Schienle A., Vaitl D. Influence of the stress hormone cortisol on fear conditioning in humans: evidence for sex differences in the response of the prefrontal cortex. Neuroimage 2006, 32:1290-1298.
59. Van Stegeren A.H., Roozendaal B., Kindt M., Wolf O.T., Joëls M. Interacting noradrenergic and corticosteroid systems shift human brain activation patterns during encoding. Neurobiol. Learn. Mem. 2010, 93:56-65.
60. Tabbert K., Merz C.J., Klucken T., Schweckendiek J., Vaitl D., Wolf O.T., Stark R. Cortisol enhances neural differentiation during fear acquisition and extinction in contingency aware young women. Neurobiol. Learn. Mem. 2010, 94:392-401.
61. Tabbert K., Merz C.J., Klucken T., Schweckendiek J., Vaitl D., Wolf O.T., Stark R. Influence of contingency awareness on neural, electrodermal and evaluative responses during fear conditioning. Soc. Cogn. Affect. Neurosci. 2011, 6:495-506.
62. Vedhara K., Hyde J., Gilchrist I.D., Tytherleigh M., Plummer S. Acute stress, memory, attention and cortisol. Psychoneuroendocrinology 2000, 25:535-549.
63. Watson D., Clark L.A., Tellegen A. Development and validation of brief measures of positive and negative affect: the PANAS scales. J. Pers. Soc. Psychol. 1988, 54:1063-1070.
64. Weike A.I., Schupp H.T., Hamm A.O. Fear acquisition requires awareness in trace but not delay conditioning. Psychophysiology 2007, 44:170-180.
65. Wiegert O., Pu Z., Shor S., Joëls M., Krugers H. Glucocorticoid receptor activation selectively hampers N-methyl-d-aspartate receptor dependent hippocampal synaptic plasticity in vitro. Neuroscience 2005, 135:403-411.
66. Wolf O.T., Minnebusch D., Daum I. Stress impairs acquisition of delay eyeblink conditioning in men and women. Neurobiol. Learn. Mem. 2009, 91:431-436.
67. Wolf O.T., Bauser D.S., Daum I. Eyeblink conditional discrimination learning in healthy young men is impaired after stress exposure. Psychophysiology 2012, 49:164-171.
68. Zorawski M., Cook C.A., Kuhn C.M., LaBar K.S. Sex, stress, and fear: individual differences in conditioned learning. Cogn. Affect. Behav. Neurosci. 2005, 5:191-201.
69. Zorawski M., Blanding N.Q., Kuhn C.M., LaBar K.S. Effects of stress and sex on acquisition and consolidation of human fear conditioning. Learn. Mem. 2006, 13:441-450.