Stress hormones are associated with the neuronal correlates of instructed fear conditioning

Biological Psychology

Volumn 92, Issue 1, 2013, Pages 82-89

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

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

Amygdala; Cortisol; FMRI; Oral contraceptives; Sex differences

Indexed keywords

HYDROCORTISONE; SEX HORMONE; STRESS HORMONE;

ADULT; AMYGDALOID NUCLEUS; ANTICIPATION; ARTICLE; BRAIN BLOOD FLOW; BRAIN FUNCTION; BRAIN REGION; CONDITIONED REFLEX; FEMALE; HUMAN; HUMAN EXPERIMENT; MALE; PRIORITY JOURNAL; SALIVA LEVEL; SEX DIFFERENCE; SEX HORMONE DETERMINATION;

ADULT; ANALYSIS OF VARIANCE; BRAIN; BRAIN MAPPING; CONDITIONING, CLASSICAL; CONDITIONING, OPERANT; ELECTRIC STIMULATION; FEAR; FEMALE; GALVANIC SKIN RESPONSE; GONADAL STEROID HORMONES; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; YOUNG ADULT;

EID: 84871721417     PISSN: 03010511     EISSN: 18736246     Source Type: Journal    
DOI: 10.1016/j.biopsycho.2012.02.017     Document Type: Article

References (81)

1. Aguilera G., Kiss A., Liu Y., Kamitakahara A. Negative regulation of corticotropin releasing factor expression and limitation of stress response. Stress - The International Journal on the Biology of Stress 2007, 10:153-161.
2. Ahs F., Furmark T., Michelgard A., Langstrom B., Appel L., Wolf O.T., Kirschbaum C., Fredrikson M. Hypothalamic blood flow correlates positively with stress-induced cortisol levels in subjects with social anxiety disorder. Psychosomatic Medicine 2006, 68:859-862.
3. Akirav I., Maroun M. The role of the medial prefrontal cortex-amygdala circuit in stress effects on the extinction of fear. Neural Plasticity 2007, 10.1155/2007/30873.
4. Amano T., Unal C.T., Paré D. Synaptic correlates of fear extinction in the amygdala. Nature Neuroscience 2010, 13:489-495.
5. Bangasser D.A., Shors T.J. Critical brain circuits at the intersection between stress and learning. Neuroscience and Biobehavioral Reviews 2010, 34:1223-1233.
6. Bentz D., Michael T., de Quervain D.J.-F., Wilhelm F.H. Enhancing exposure therapy for anxiety disorders with glucocorticoids: from basic mechanisms of emotional learning to clinical applications. Journal of Anxiety Disorders 2010, 24:223-230.
7. Biondi M., Picardi A. Psychological stress and neuroendocrine function in humans: the last two decades of research. Psychotherapy and Psychosomatics 1999, 68:114-150.
8. Buffet N.C., Djakoure C., Maitre S.C., Bouchard P. Regulation of the human menstrual cycle. Frontiers in Neuroendocrinology 1998, 19:151-186.
9. Cahill L.F. Why sex matters for neuroscience. Nature Reviews Neuroscience 2006, 7:477-484.
10. Cheng D.T., Knight D.C., Smith C.N., Helmstetter F.J. Human amygdala activity during the expression of fear responses. Behavioral Neuroscience 2006, 120:1187-1195.
11. Conrad C.D., LeDoux J.E., Magariños A.M., McEwen B.S. Repeated restraint stress facilitates fear conditioning independently of causing hippocampal CA3 dendritic atrophy. Behavioral Neuroscience 1999, 113:902-913.
12. Dalla C., Shors T.J. Sex differences in learning processes of classical and operant conditioning. Physiology & Behavior 2009, 97:229-238.
13. de Kloet E.R., Oitzl M.S., Joëls M. Stress and cognition: are corticosteroids good or bad guys?. Trends in Neurosciences 1999, 22:422-426.
14. de Quervain D.J.-F., Aerni A., Schelling G., Roozendaal B. Glucocorticoids and the regulation of memory in health and disease. Frontiers in Neuroendocrinology 2009, 30:358-370.
15. Dedovic K., Duchesne A., Andrews J., Engert V., Prüssner J.C. The brain and the stress axis: the neural correlates of cortisol regulation in response to stress. NeuroImage 2009, 47:864-871.
16. Delgado M.R., Olsson A., Phelps E.A. Extending animal models of fear conditioning to humans. Biological Psychology 2006, 73:39-48.
17. Diaz-Veliz G., Urresta F., Dussaubat N., Mora S. Effects of estradiol replacement in ovariectomized rats on conditioned avoidance responses and other behaviors. Physiology & Behavior 1991, 50:61-65.
18. Diorio D., Viau V., Meaney M.J. The role of the medial prefrontal cortex (cingulate gyrus) in the regulation of hypothalamic-pituitary-adrenal responses to stress. The Journal of Neuroscience 1993, 13:3839-3847.
19. Goosens K.A. Hippocampal regulation of aversive memories. Current Opinion in Neurobiology 2011, 21:1-7.
20. Henckens M.J.A.G., van Wingen G.A., Joëls M., Fernandez G. Time-dependent effects of corticosteroids on human amygdala processing. The Journal of Neuroscience 2010, 30:12725-12732.
21. Herman J.P., Figueiredo H., Mueller N.K., Ulrich-Lai Y., Ostrander M.M., Choi D.C., Cullinan W.E. Central mechanisms of stress integration: hierarchical circuitry controlling hypothalamo-pituitary-adrenocortical responsiveness. Frontiers in Neuroendocrinology 2003, 24:151-180.
22. Herman J.P., Ostrander M.M., Mueller N.K., Figueiredo H. Limbic system mechanisms of stress regulation: hypothalamo-pituitary-adrenocortical axis. Progress in Neuro-Psychopharmacology & Biological Psychiatry 2005, 29:1201-1213.
23. Hermann A., Schäfer A., Walter B., Stark R., Vaitl D., Schienle A. Emotion regulation in spider phobia: role of the medial prefrontal cortex. Social Cognitive and Affective Neuroscience 2009, 4:257-267.
24. Hofmann S.G. Cognitive processes during fear acquisition and extinction in animals and humans: implications for exposure therapy of anxiety disorders. Clinical Psychology Review 2008, 28:199-210.
25. Holsboer F., Ising M. Stress hormone regulation: biological role and translation into therapy. Annual Review of Psychology 2010, 61:81-109.
26. Hui G.K., Figueroa I.R., Poytress B.S., Roozendaal B., McGaugh J.L., Weinberger N.M. Memory enhancement of classical fear conditioning by post-training injections of corticosterone in rats. Neurobiology of Learning and Memory 2004, 81:67-74.
27. Izquierdo A., Wellman C.L., Holmes A. Brief uncontrollable stress causes dendritic retraction in infralimbic cortex and resistance to fear extinction in mice. The Journal of Neuroscience 2006, 26:5733-5738.
28. Jackson E.D., Payne J.D., Nadel L., Jacobs W.J. Stress differentially modulates fear conditioning in healthy men and women. Biological Psychiatry 2006, 59:516-522.
29. Kalisch R., Korenfeld E., Stephan K.E., Weiskopf N., Seymour B., Dolan R.J. Context-dependent human extinction memory is mediated by a ventromedial prefrontal and hippocampal network. The Journal of Neuroscience 2006, 26:9503-9511.
30. Kern S., Oakes T.R., Stone C.K., McAuliff E.M., Kirschbaum C., Davidson R.J. Glucose metabolic changes in the prefrontal cortex are associated with HPA axis response to a psychosocial stressor. Psychoneuroendocrinology 2008, 33:517-529.
31. 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. Archives of General Psychiatry 2005, 62:593-602.
32. Kirschbaum C., Kudielka B.M., Gaab J., Schommer N.C., Hellhammer D.H. Impact of gender, menstrual cycle phase, and oral contraceptives on the activity of the hypothalamus-pituitary-adrenal axis. Psychosomatic Medicine 1999, 61:154-162.
33. Knight D.C., Smith C.N., Stein E.A., Helmstetter F.J. Functional MRI of human Pavlovian fear conditioning: patterns of activation as a function of learning. Neuroreport 1999, 10:3665-3670.
34. Kuhlmann S., Wolf O.T. Cortisol and memory retrieval in women: influence of menstrual cycle and oral contraceptives. Psychopharmacology 2005, 183:65-71.
35. LeDoux J.E. Emotion circuits in the brain. Annual Review of Neuroscience 2000, 23:155-184.
36. Liberzon I., King A.P., Britton J.C., Phan K.L., Abelson J.L., Taylor S.F. Paralimbic and medial prefrontal cortical involvement in neuroendocrine responses to traumatic stimuli. The American Journal of Psychiatry 2007, 164:1250-1258.
37. Likhtik E., Pelletier J.G., Paz R., Paré D. Prefrontal control of the amygdala. The Journal of Neuroscience 2005, 25:7429-7437.
38. Lupien S.J., Maheu F.S., Tu M.T., Fiocco A., Schramek T.E. The effects of stress and stress hormones on human cognition: implications for the field of brain and cognition. Brain and Cognition 2007, 65:209-237.
39. Maren S. Building and burying fear memories in the brain. Neuroscientist 2005, 11:89-99.
40. McLean C.P., Asnaani A., Litz B.T., Hofmann S.G. Gender differences in anxiety disorders: prevalence, course of illness, comorbidity and burden of illness. Journal of Psychiatric Research 2011, 10.1016/j.jpsychires.2011.03.006.
41. 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.
42. 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.
43. 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. Social Cognitive and Affective Neuroscience, , in press. doi:10.1093/scan/NSR063.
44. Milad M.R., Wright C.I., Orr S.P., Pitman R.K., Quirk G.J., Rauch S.L. Recall of fear extinction in humans activates the ventromedial prefrontal cortex and hippocampus in concert. Biological Psychiatry 2007, 62:446-454.
45. Mineka S., Oehlberg K. The relevance of recent developments in classical conditioning to understanding the etiology and maintenance of anxiety disorders. Acta Psychologica 2008, 127:567-580.
46. Ochsner K.N., Gross J.J. The cognitive control of emotion. Trends in Cognitive Sciences 2005, 9:242-249.
47. 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 and Behavior 2007, 1:31-41.
48. Oldfield R.C. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 1971, 9:97-113.
49. Pape H.-C., Paré D. Plastic synaptic networks of the amygdala for the acquisition, expression, and extinction of conditioned fear. Physiological Reviews 2010, 90:419-463.
50. Paré D., Quirk G.J., LeDoux J.E. New vistas on amygdala networks in conditioned fear. Journal of Neurophysiology 2004, 92:1-9.
51. Phelps E.A., Delgado M.R., Nearing K.I., LeDoux J.E. Extinction learning in humans: role of the amygdala and vmPFC. Neuron 2004, 43:897-905.
52. Portella M.J., Harmer C.J., Flint J., Cowen P., Goodwin G.M. Enhanced early morning salivary cortisol in neuroticism. The American Journal of Psychiatry 2005, 162:807-809.
53. 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. Biological Psychiatry 2008, 63:234-240.
54. Quirk G.J., Likhtik E., Pelletier J.G., Paré D. Stimulation of medial prefrontal cortex decreases the responsiveness of central amygdala output neurons. The Journal of Neuroscience 2003, 23:8800-8807.
55. Rolls E.T. The Brain and Emotion 1999, Oxford University Press, New York.
56. Roozendaal B., Hui G.K., Hui I.R., Berlau D.J., McGaugh J.L., Weinberger N.M. Basolateral amygdala noradrenergic activity mediates corticosterone-induced enhancement of auditory fear conditioning. Neurobiology of Learning and Memory 2006, 86:249-255.
57. Rosenthal R. Parametric measures of effect size. The Handbook of Research Synthesis 1994, 231-244. Russell Sage Foundation, New York. H. Cooper, L.V. Hedges (Eds.).
58. Sandi C., Pinelo-Nava M.T. Stress and memory: behavioral effects and neurobiological mechanisms. Neural Plasticity 2007, 10.1155/2007/78970.
59. Schoofs D., Wolf O.T. Stress and memory retrieval in women: no strong impairing effect during the luteal phase. Behavioral Neuroscience 2009, 123:547-554.
60. Schulkin J., Gold P.W., McEwen B.S. Induction of corticotropin-releasing hormone gene expression by glucocorticoids: implication for understanding the states of fear and anxiety and allostatic load. Psychoneuroendocrinology 1998, 23:219-243.
61. Schwabe L., Joëls M., Roozendaal B., Wolf O.T., Oitzl M.S. Stress effects on memory: an update and integration. Neuroscience and Biobehavioral Reviews 2011, 10.1016/j.neubiorev.2011.07.002.
62. Sehlmeyer C., Schöning S., Zwitserlood P., Pfleiderer B., Kircher T., Arolt V., Konrad C. Human fear conditioning and extinction in neuroimaging: a systematic review. PLoS ONE 2009, 4:e5865.
63. Shors T.J. Learning during stressful times. Learning & Memory 2004, 11:137-144.
64. Shors T.J., Lewczyk C., Pacynski M., Mathew P.R., Pickett J. Stages of estrous mediate the stress-induced impairment of associative learning in the female rat. Neuroreport 1998, 9:419-423.
65. 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.
66. 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. Neurobiology of Learning and Memory 2010, 94:392-401.
67. 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. Social Cognitive and Affective Neuroscience 2011, 6:495-506.
68. Urry H.L., van Reekum C.M., Johnstone T., Kalin N.H., Thurow M.E., Schaefer H.S., Jackson C.A., Frye C.J., Greischar L.L., Alexander A.L., Davidson R.J. Amygdala and ventromedial prefrontal cortex are inversely coupled during regulation of negative affect and predict the diurnal pattern of cortisol secretion among older adults. The Journal of Neuroscience 2006, 26:4415-4425.
69. van Goozen S.H., Matthys W., Cohen-Kettenis P.T., Gispen-de Wied C., Wiegant V.M., van Engeland H. Salivary cortisol and cardiovascular activity during stress in oppositional-defiant disorder boys and normal controls. Biological Psychiatry 1998, 43:531-539.
70. van Stegeren A.H., Goekoop R., Everaerd W.T.A.M., Scheltens P., Barkhof F., Kuijer J.P.A., Rombouts S.A.R.B. Noradrenaline mediates amygdala activation in men and women during encoding of emotional material. NeuroImage 2005, 24:898-909.
71. 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. Neurobiology of Learning and Memory 2007, 87:57-66.
72. 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. Neurobiology of Learning and Memory 2010, 93:56-65.
73. van Strien N.M., Cappaert N.L.M., Witter M.P. The anatomy of memory: an interactive overview of the parahippocampal-hippocampal network. Nature Reviews Neuroscience 2009, 10:272-282.
74. Wager T.D., Phan K.L., Liberzon I., Taylor S.F. Valence, gender, and lateralization of functional brain anatomy in emotion: a meta-analysis of findings from neuroimaging. NeuroImage 2003, 19:513-531.
75. Wang J., Rao H.Y., Wetmore G.S., Furlan P.M., Korczykowski M., Dinges D.F., Detre J.A. Perfusion functional MRI reveals cerebral blood flow pattern under psychological stress. Proceedings of the National Academy of Sciences of the United States of America 2005, 102:17804-17809.
76. Wolf O.T. The influence of stress hormones on emotional memory: relevance for psychopathology. Acta Psychologica 2008, 513-531.
77. Wood G.E., Shors T.J. Stress facilitates classical conditioning in males, but impairs classical conditioning in females through activational effects of ovarian hormones. Proceedings of the National Academy of Sciences of the United States of America 1998, 95:4066-4071.
78. 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. Behavioral Neuroscience 2001, 115:175-187.
79. Zorawski M., Killcross S. Posttraining glucocorticoid receptor agonist enhances memory in appetitive and aversive Pavlovian discrete-cue conditioning paradigms. Neurobiology of Learning and Memory 2002, 78:458-464.
80. Zorawski M., Cook C.A., Kuhn C.M., LaBar K.S. Sex, stress, and fear: individual differences in conditioned learning. Cognitive Affective & Behavioral Neuroscience 2005, 5:191-201.
81. Zorawski M., Blanding N.Q., Kuhn C.M., LaBar K.S. Effects of stress and sex on acquisition and consolidation of human fear conditioning. Learning & Memory 2006, 13:441-450.