Oral contraceptive usage alters the effects of cortisol on implicit fear learning

Hormones and Behavior

Volumn 62, Issue 4, 2012, Pages 531-538

  Merz, Christian Josef ^a   Tabbert, Katharina ^a   Schweckendiek, Jan ^a   Klucken, Tim ^a   Vaitl, Dieter ^a   Stark, Rudolf ^a   Wolf, Oliver Tobias ^b  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

^b RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

Amygdala; Estradiol; Fear conditioning; FMRI; Follicular phase; Hippocampus; Luteal phase; Progesterone; Stress hormone

Indexed keywords

ESTRADIOL; HYDROCORTISONE; ORAL CONTRACEPTIVE AGENT; PROGESTERONE; TESTOSTERONE;

ADULT; AMYGDALOID NUCLEUS; ARTICLE; BRAIN FUNCTION; ELECTROENCEPHALOGRAM; ELECTROSTIMULATION; EMOTION; FEAR; FEMALE; FOLLICULAR PHASE; HIPPOCAMPUS; HUMAN; HUMAN EXPERIMENT; LEARNING; LUTEAL PHASE; MALE; NORMAL HUMAN; PARAHIPPOCAMPAL GYRUS; PRIORITY JOURNAL; SENSORY STIMULATION;

ADOLESCENT; ADULT; CONDITIONING (PSYCHOLOGY); CONTRACEPTION BEHAVIOR; CONTRACEPTIVES, ORAL; DOUBLE-BLIND METHOD; ELECTRIC STIMULATION; FEAR; FEMALE; HUMANS; HYDROCORTISONE; LEARNING; MALE; PHOTIC STIMULATION; PLACEBOS; YOUNG ADULT;

EID: 84867661028     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2012.09.001     Document Type: Article

References (57)

1. Aerni A., Traber R., Hock C., Roozendaal B., Schelling G., Papassotiropoulos A., Nitsch R.M., Schnyder U., de Quervain D.J.-F. Low-dose cortisol for symptoms of posttraumatic stress disorder. Am. J. Psychiatry 2004, 161:1488-1490.
2. Andreano J.M., Cahill L. Menstrual cycle modulation of medial temporal activity evoked by negative emotion. Neuroimage 2010, 53:1286-1293.
3. Buffet N.C., Djakoure C., Maitre S.C., Bouchard P. Regulation of the human menstrual cycle. Front. Neuroendocrinol. 1998, 19:151-186.
4. Dalla C., Shors T.J. Sex differences in learning processes of classical and operant conditioning. Physiol. Behav. 2009, 97:229-238.
5. de Quervain D.J.-F., Henke K., Aerni A., Treyer V., McGaugh J.L., Berthold T., Nitsch R.M., Buck A., Roozendaal B., Hock C. Glucocorticoid-induced impairment of declarative memory retrieval is associated with reduced blood flow in the medial temporal lobe. Eur. J. Neurosci. 2003, 17:1296-1302.
6. de Quervain D.J.-F., Bentz D., Michael T., Bolt O.C., Wiederhold B.K., Margraf J., Wilhelm F.H. Glucocorticoids enhance extinction-based psychotherapy. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:6621-6625.
7. Duncko R., Cornwell B., Cui L., Merikangas K.R., Grillon C. Acute exposure to stress improves performance in trace eyeblink conditioning and spatial learning tasks in healthy men. Learn. Mem. 2007, 14:329-335.
8. Etkin A., Wager T.D. Functional neuroimaging of anxiety: a meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. Am. J. Psychiatry 2007, 164:1476-1488.
9. Gillies G.E., McArthur S. Estrogen actions in the brain and the basis for differential action in men and women: a case for sex-specific medicines. Pharmacol. Rev. 2010, 62:155-198.
10. Glover E.M., Jovanovic T., Mercer K.B., Kerley K., Bradley B., Ressler K.J., Norrholm S.D. Estrogen levels are associated with extinction deficits in women with posttraumatic stress disorder. Biol. Psychiatry 2012, 72:19-24.
11. Gupta R.R., Sen S., Diepenhorst L.L., Rudick C.N., Maren S. Estrogen modulates sexually dimorphic contextual fear conditioning and hippocampal long-term potentiation (LTP) in rats. Brain Res. 2001, 888:356-365.
12. Hamm A.O., Vaitl D. Affective learning: awareness and aversion. Psychophysiology 1996, 33:698-710.
13. Hamm A.O., Weike A.I. The neuropsychology of fear learning and fear regulation. Int. J. Psychophysiol. 2005, 57:5-14.
14. Henckens M.J.A.G., van Wingen G.A., Joëls M., Fernandez G. Time-dependent effects of corticosteroids on human amygdala processing. J. Neurosci. 2010, 30:12725-12732.
15. 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.
16. Kessler R.C., Berglund P., Demler O., Jin R., Merikangas K.R., Walters E.E. Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the national comorbidity survey replication. Arch. Gen. Psychiatry 2005, 62:593-602.
17. Klucken T., Tabbert K., Schweckendiek J., Merz C.J., Kagerer S., Vaitl D., Stark R. Contingency learning in human fear conditioning involves the ventral striatum. Hum. Brain Mapp. 2009, 30:3636-3644.
18. 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.
19. Knight D.C., Smith C.N., Cheng D.T., Stein E.A., Helmstetter F.J. Amygdala and hippocampal activity during acquisition and extinction of human fear conditioning. Cogn. Affect. Behav. Neurosci. 2004, 4:317-325.
20. Knight D.C., Waters N.S., Bandettini P.A. Neural substrates of explicit and implicit fear memory. Neuroimage 2009, 45:208-214.
21. Korte S.M. Corticosteroids in relation to fear, anxiety and psychopathology. Neurosci. Biobehav. Rev. 2001, 25:117-142.
22. Kukolja J., Schläpfer T.E., Keysers C., Klingmüller D., Maier W., Fink G.R., Hurlemann R. Modeling a negative response bias in the human amygdala by noradrenergic-glucocorticoid interactions. J. Neurosci. 2008, 28:12868-12876.
23. Lebron-Milad K., Graham B.M., Milad M.R. Low estradiol levels: a vulnerability factor for the development of posttraumatic stress disorder. Biol. Psychiatry 2012, 72:6-7.
24. LeDoux J.E. Emotion circuits in the brain. Annu. Rev. Neurosci. 2000, 23:155-184.
25. LeDoux J. The emotional brain, fear, and the amygdala. Cell. Mol. Neurobiol. 2003, 23:727-738.
26. Mechias M.-L., Etkin A., Kalisch R. A meta-analysis of instructed fear studies: implications for conscious appraisal of threat. Neuroimage 2010, 49:1760-1768.
27. 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.
28. Merz, C.J., Tabbert, K., Schweckendiek, J., Klucken, T., Vaitl, D., Stark, R., Wolf, O.T., in press. Neuronal correlates of extinction learning are modulated by sex hormones. Soc. Cogn. Affect. Neurosci., doi:10.1093/scan/NSR063.
29. Milad M.R., Goldstein J.M., Orr S.P., Wedig M.M., Klibanski A., Pitman R.K., Rauch S.L. Fear conditioning and extinction: influence of sex and menstrual cycle in healthy humans. Behav. Neurosci. 2006, 120:1196-1203.
30. 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.
31. Mitterling K.L., Spencer J.L., Dziedzic N., Shenoy S., McCarthy K., Waters E.M., McEwen B.S., Milner T.A. Cellular and subcellular localization of estrogen and progestin receptor immunoreactivities in the mouse hippocampus. J. Comp. Neurol. 2010, 518:2729-2743.
32. Morgan M.A., Pfaff D.W. Effects of estrogen on activity and fear-related behaviors in mice. Horm. Behav. 2001, 40:472-482.
33. Morgan M.A., Schulkin J., Pfaff D.W. Estrogens and non-reproductive behaviors related to activity and fear. Neurosci. Biobehav. Rev. 2004, 28:55-63.
34. Oei N.Y.L., Elzinga B.M., Wolf O.T., de Ruiter M.B., Damoiseaux J.S., Kuijer J.P.A., Veltman D.J., Scheltens P., Rombouts S.A.R.B. Glucocorticoids decrease hippocampal and prefrontal activation during declarative memory retrieval in young men. Brain Imaging Behav. 2007, 1:31-41.
35. Öhman A., Mineka S. Fears, phobias, and preparedness: toward an evolved module of fear and fear learning. Psychol. Rev. 2001, 108:483-522.
36. Oldfield R.C. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 1971, 9:97-113.
37. Prokasy W.F., Ebel H.C. Three components of the classically conditioned GSR in human subjects. J. Exp. Psychol. 1967, 73:247-256.
38. Prüssner J.C., Dedovic K., Khalili-Mahani N., Engert V., Prüssner M., Buss C., Renwick R., Dagher A., Meaney M.J., Lupien S.J. Deactivation of the limbic system during acute psychosocial stress: evidence from positron emission tomography and functional magnetic resonance imaging studies. Biol. Psychiatry 2008, 63:234-240.
39. Quirarte G.L., Roozendaal B., McGaugh J.L. Glucocorticoid enhancement of memory storage involves noradrenergic activation in the basolateral amygdala. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:14048-14053.
40. Rodrigues S.M., LeDoux J.E., Sapolsky R.M. The influence of stress hormones on fear circuitry. Annu. Rev. Neurosci. 2009, 32:289-313.
41. Rolls E.T. The Brain and Emotion 1999, Oxford University Press, New York.
42. 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. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:11642-11647.
43. Shin L.M., Liberzon I. The neurocircuitry of fear, stress, and anxiety disorders. Neuropsychopharmacology 2010, 35:169-191.
44. Shughrue P.J., Lane M.V., Merchenthaler I. Comparative distribution of estrogen receptor-alpha and -beta mRNA in the rat central nervous system. J. Comp. Neurol. 1997, 388:507-525.
45. Solomon M.B., Herman J.P. Sex differences in psychopathology: of gonads, adrenals and mental illness. Physiol. Behav. 2009, 97:250-258.
46. Soravia L.M., Heinrichs M., Aerni A., Maroni C., Schelling G., Ehlert U., Roozendaal B., de Quervain D.J.-F. Glucocorticoids reduce phobic fear in humans. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:5585-5590.
47. 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.
48. Tabbert K., Stark R., Kirsch P., Vaitl D. Dissociation of neural responses and skin conductance reactions during fear conditioning with and without awareness of stimulus contingencies. Neuroimage 2006, 32:761-770.
49. 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.
50. 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.
51. Toufexis D.J., Myers K.M., Davis M. The effect of gonadal hormones and gender on anxiety and emotional learning. Horm. Behav. 2006, 50:539-549.
52. van Stegeren A.H., Wolf O.T., Everaerd W.T.A.M., Scheltens P., Barkhof F., Rombouts S.A.R.B. Endogenous cortisol level interacts with noradrenergic activation in the human amygdala. Neurobiol. Learn. Mem. 2007, 87:57-66.
53. Wolf O.T. The influence of stress hormones on emotional memory: relevance for psychopathology. Acta Psychol. 2008, 127:513-531.
54. 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.
55. Wood G.E., Beylin A.V., Shors T.J. The contribution of adrenal and reproductive hormones to the opposing effects of stress on trace conditioning in males versus females. Behav. Neurosci. 2001, 115:175-187.
56. Zeidan M.A., Igoe S.A., Linnman C., Vitalo A., Levine J.B., Klibanski A., Goldstein J.M., Milad M.R. Estradiol modulates medial prefrontal cortex and amygdala activity during fear extinction in women and female rats. Biol. Psychiatry 2011, 70:920-927.
57. 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.