A single administration of cortisol acutely reduces preconscious attention for fear in anxious young men

Psychoneuroendocrinology

Volumn 32, Issue 7, 2007, Pages 793-802

  Putman, Peter ^a,b   Hermans, Erno J ^a,c   Koppeschaar, Hans ^d   van Schijndel, Alexandra ^a   van Honk, Jack ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

^b LEIDEN UNIVERSITY   (Netherlands)

^c RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^d UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

Anxiety; Anxiety disorders; Cortisol; Emotional Stroop; Fear; Fearful; Glucocorticoid; Selective attention

Indexed keywords

HYDROCORTISONE; PLACEBO;

ADULT; ANXIETY; ARTICLE; ATTENTION; AWARENESS; CLINICAL TRIAL; COLOR DISCRIMINATION; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; CROSSOVER PROCEDURE; DOUBLE BLIND PROCEDURE; DRUG MECHANISM; DRUG SALIVA LEVEL; FEAR; HUMAN; HUMAN EXPERIMENT; LATENT PERIOD; MALE; NORMAL HUMAN; PRIORITY JOURNAL; RESPONSE TIME; SELECTIVE ATTENTION; SELF REPORT; SINGLE DRUG DOSE; STATE TRAIT ANXIETY INVENTORY;

ADULT; ANXIETY; AROUSAL; ATTENTION; AWARENESS; CROSS-OVER STUDIES; DATA INTERPRETATION, STATISTICAL; DOUBLE-BLIND METHOD; EXPRESSED EMOTION; FACIAL EXPRESSION; FEAR; HUMANS; HYDROCORTISONE; MALE; PHOTIC STIMULATION; SALIVA;

EID: 34547560531     PISSN: 03064530     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2007.05.009     Document Type: Article

References (85)

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. Behav. Neurosci. 117 (2003) 505-516
2. Abercrombie H.C., Speck N.S., and Monticelli R.M. Endogenous cortisol elevations are related to memory facilitation only in individuals who are emotionally aroused. Psychoneuroendocrinology 31 (2006) 187-196
3. Adolphs R. Cognitive neuroscience of human social behaviour. Nat. Rev. Neurosci. 4 (2003) 165-178
4. Aerni A., Traber R., Hock C., Roozendaal B., Schelling G., Papassotiropoulos A., Nitsch R.M., Schnyder U., and de Quervain D.J. Low-dose cortisol for symptoms of posttraumatic stress disorder. Am. J. Psychiatry 161 (2004) 1488-1490
5. Arborelius L., Owens M.J., Plotsky P.M., and Nemeroff C.B. The role of corticotropin-releasing factor in depression and anxiety disorders. J. Endocrinol. 160 (1999) 1-12
6. Bakshi V.P., and Kalin N.H. Corticotropin-releasing hormone and animal models of anxiety: gene-environment interactions. Biol. Psychiatry 48 (2000) 1175-1198
7. Beck A.T., and Emery G. Anxiety Disorders and Phobias: A Cognitive Perspective (1985), Basic Books, New York
8. Bhagwagar Z., Cowen P.J., Goodwin G.M., and Harmer C.J. Normalization of enhanced fear recognition by acute SSRI treatment in subjects with a previous history of depression. Am. J. Psychiatry 161 (2004) 166-168
9. Booij L., Van der Does A.J., Haffmans P.M., Riedel W.J., Fekkes D., and Blom M.J. The effects of high-dose and low-dose tryptophan depletion on mood and cognitive functions of remitted depressed patients. J. Psychopharmacol. 19 (2005) 267-275
10. Brown L.L., Tomarken A.J., Orth D.N., Loosen P.T., Kalin N.H., and Davidson R.J. Individual differences in repressive-defensiveness predict basal salivary cortisol levels. J. Pers. Soc. Psychol. 70 (1996) 362-371
11. Buchanan T.W., and Lovallo W.R. Enhanced memory for emotional material following stress-level cortisol treatment in humans. Psychoneuroendocrinology 26 (2001) 307-317
12. Buchanan T.W., Brechtel A., Sollers J.J., and Lovallo W.R. Exogenous cortisol exerts effects on the startle reflex independent of emotional modulation. Pharmacol. Biochem. Behav. 68 (2001) 203-210
13. Cahill L., Haier R.J., Fallon J., Alkire M.T., Tang C., Keator D., Wu J., and McGaugh J.L. Amygdala activity at encoding correlated with long-term, free recall of emotional information. Proc. Nat. Acad. Sci. USA 93 (1996) 8016-8021
14. de Kloet C.S., Vermetten E., Geuze E., Kavelaars A., Heijnen C.J., and Westenberg H.G. Assessment of HPA-axis function in posttraumatic stress disorder: pharmacological and non-pharmacological challenge tests, a review. J. Psychiatr. Res. (2005)
15. Delahanty D.L., Raimonde A.J., and Spoonster E. Initial posttraumatic urinary cortisol levels predict subsequent PTSD symptoms in motor vehicle accident victims. Biol. Psychiatry 48 (2000) 940-947
16. Delahanty D.L., Raimonde A.J., Spoonster E., and Cullado M. Injury severity, prior trauma history, urinary cortisol levels, and acute PTSD in motor vehicle accident victims. J. Anxiety Disord. 17 (2003) 149-164
17. Ekman P., and Friesen W.V. Pictures of Facial Affect (1976), Consulting Psychologists Press, Palo Alto
18. Ellenbogen M.A., Schwartzman A.E., Stewart J., and Walker C.D. Automatic and effortful emotional information processing regulates different aspects of the stress response. Psychoneuroendocrinology 31 (2006) 373-387
19. Fox E., Russo R., and Georgiou G.A. Anxiety modulates the degree of attentive resources required to process emotional faces. Cogn. Affect. Behav. Neurosci. 5 (2005) 396-404
20. Galard R., Catalan R., Castellanos J.M., and Gallart J.M. Plasma corticotropin-releasing factor in depressed patients before and after the dexamethasone suppression test. Biol. Psychiatry 51 (2002) 463-468
21. Harmer C.J., Hill S.A., Taylor M.J., Cowen P.J., and Goodwin G.M. Toward a neuropsychological theory of antidepressant drug action: increase in positive emotional bias after potentiation of norepinephrine activity. Am. J. Psychiatry 160 (2003) 990-992
22. Harmer C.J., Shelley N.C., Cowen P.J., and Goodwin G.M. Increased positive versus negative affective perception and memory in healthy volunteers following selective serotonin and norepinephrine reuptake inhibition. Am. J. Psychiatry 161 (2004) 1256-1263
23. Harvey A., Watkins E., Mansell W., and Shafran R. Cognitive Behavioural Processes Across Psychological Disorders: A Transdiagnostic Approach to Research and Treatment (2004), Oxford University Press, Oxford
24. Kagan J., Reznick J.S., and Snidman N. The physiology and psychology of behavioral inhibition in children. Child Dev. 58 (1987) 1459-1473
25. Kalin N.H. Nonhuman primate studies of fear, anxiety, and temperament and the role of benzodiazepine receptors and GABA systems. J. Clin. Psychiatry 64 Suppl 3 (2003) 41-44
26. Kalin N.H., Larson C., Shelton S.E., and Davidson R.J. Asymmetric frontal brain activity, cortisol, and behavior associated with fearful temperament in rhesus monkeys. Behav. Neurosci. 112 (1998) 286-292
27. Korte S.M., de Boer S.F., de Kloet E.R., and Bohus B. Anxiolytic-like effects of selective mineralocorticoid and glucocorticoid antagonists on fear-enhanced behavior in the elevated plus-maze. Psychoneuroendocrinology 20 (1995) 385-394
28. Kuhlmann S., Kirschbaum C., and Wolf O.T. Effects of oral cortisol treatment in healthy young women on memory retrieval of negative and neutral words. Neurobiol. Learn. Mem. 83 (2005) 158-162
29. LeDoux J.E. The Emotional Brain: The Mysterious Underpinnings of Emotional Life (1996), Simon and Schuster, New York
30. Lundqvist D., Flykt A., and Öhman A. The Karolinska Directed Emotional Faces (1998), Karolinska Institutet, Stockholm
31. Lupien S.J., and McEwen B.S. The acute effects of corticosteroids on cognition: integration of animal and human model studies. Brain Res. Brain Res. Rev. 24 (1997) 1-27
32. MacLeod C., and Hagan R. Individual differences in the selective processing of threatening information, and emotional responses to a stressful life event. Behav. Res. Ther. 33 (1995) 451-454
33. Majewska M.D., Bisserbe J.C., and Eskay R.L. Glucocorticoids are modulators of GABAA receptors in brain. Brain Res. 339 (1985) 178-182
34. Majewska M.D., Harrison N.L., Schwartz R.D., Barker J.L., and Paul S.M. Steroid hormone metabolites are barbiturate-like modulators of the GABA receptor. Science 232 (1986) 1004-1007
35. Makara G.B., and Haller J. Non-genomic effects of glucocorticoids in the neural system. Evidence, mechanisms and implications. Prog. Neurobiol. 65 (2001) 367-390
36. McEwen B.S. Mood disorders and allostatic load. Biol. Psychiatry 54 (2003) 200-207
37. McNally R.J. Information-processing abnormalities in anxiety disorders: implications for cognitive neuroscience. Cogn. Emotion 12 (1998) 479-495
38. McNally R.J., Kaspi S.P., Riemann B.C., and Zeitlin S.B. Selective processing of threat cues in posttraumatic stress disorder. J. Abnorm. Psychol. 99 (1990) 398-402
39. Mogg K., and Bradley B.P. A cognitive-motivational analysis of anxiety. Behav. Res. Ther. 36 (1998) 809-848
40. Morris J.S., Öhman A., and Dolan R.J. A subcortical pathway to the right amygdala mediating "unseen" fear. Proc. Nat. Acad. Sci. USA 96 (1999) 1680-1685
41. Naveh-Benjamin M., Craik F.I., Guez J., and Dori H. Effects of divided attention on encoding and retrieval processes in human memory: further support for an asymmetry. J. Exp. Psychol. Learn. Mem. Cogn. 24 (1998) 1091-1104
42. Öhman A. A fast blink of the eye: evolutionary preparedness for preattentive processing of threat. In: Lang P.J., Simons R.F., and Balaban M.T. (Eds). Attention and Orienting: Sensory and Motivational Processing (1997), Erlbaum, New Jersey 165-184
43. Parker K.J., Schatzberg A.F., and Lyons D.M. Neuroendocrine aspects of hypercortisolism in major depression. Horm. Behav. 43 (2003) 60-66
44. Putman P., Hermans E., and van Honk J. Emotional stroop performance for masked angry faces: it's BAS, not BIS. Emotion 4 (2004) 305-311
45. Putman P., Van Honk J., Kessels R.P., Mulder M., and Koppeschaar H.P. Salivary cortisol and short and long-term memory for emotional faces in healthy young women. Psychoneuroendocrinology 29 (2004) 953-960
46. Putman P., Hermans E., and van Honk J. Anxiety meets fear in perception of dynamic expressive gaze. Emotion 6 (2006) 94-102
47. Rauch S.L., Whalen P.J., Shin L.M., McInerney S.C., Macklin M.L., Lasko N.B., Orr S.P., and Pitman R.K. Exaggerated amygdala response to masked facial stimuli in posttraumatic stress disorder: a functional MRI study. Biol. Psychiatry 47 (2000) 769-776
48. Rauch S.L., Whalen P.J., Shin L.M., McInerney S.C., Macklin M.L., Lasko N.B., Orr S.P., and Pitman R.K. Exaggerated amygdala response to masked facial stimuli in posttraumatic stress disorder: a functional MRI study. Biol. Psychiatry 47 (2000) 769-776
49. Reddy D.S., and Rogawski M.A. Stress-induced deoxycorticosterone-derived neurosteroids modulate GABA(A) receptor function and seizure susceptibility. J. Neurosci. 22 (2002) 3795-3805
50. Reuter M. Impact of cortisol on emotions under stress and nonstress conditions: a pharmacopsychological approach. Neuropsychobiology 46 (2002) 41-48
51. Rimmele U., Domes G., Mathiak K., and Hautzinger M. Cortisol has different effects on human memory for emotional and neutral stimuli. Neuroreport 14 (2003) 2485-2488
52. Roozendaal B. Glucocorticoids and the regulation of memory consolidation. Psychoneuroendocrinology 25 (2000) 213-238 (1999 Curt P. Richter award)
53. 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. Proc. Nat. Acad. Sci. USA 103 (2006) 6741-6746
54. Rosen J.B., and Schulkin J. From normal fear to pathological anxiety. Psychol. Rev. 105 (1998) 325-350
55. Sandi C., Venero C., and Guaza C. Nitric oxide synthesis inhibitors prevent rapid behavioral effects of corticosterone in rats. Neuroendocrinology 63 (1996) 446-453
56. Schelling G., Briegel J., Roozendaal B., Stoll C., Rothenhausler H.B., and Kapfhammer H.P. The effect of stress doses of hydrocortisone during septic shock on posttraumatic stress disorder in survivors. Biol. Psychiatry 50 (2001) 978-985
57. Schelling G., Kilger E., Roozendaal B., de Quervain D.J., Briegel J., Dagge A., Rothenhausler H.B., Krauseneck T., Nollert G., and Kapfhammer H.P. Stress doses of hydrocortisone, traumatic memories, and symptoms of posttraumatic stress disorder in patients after cardiac surgery: a randomized study. Biol. Psychiatry 55 (2004) 627-633
58. Schelling G., Roozendaal B., and De Quervain D.J. Can posttraumatic stress disorder be prevented with glucocorticoids?. Ann. NY Acad. Sci. 1032 (2004) 158-166
59. Schulkin J., Morgan M.A., and Rosen J.B. A neuroendocrine mechanism for sustaining fear. Trends Neurosci. 28 (2005) 629-635
60. Smider N.A., Essex M.J., Kalin N.H., Buss K.A., Klein M.H., Davidson R.J., and Goldsmith H.H. Salivary cortisol as a predictor of socioemotional adjustment during kindergarten: a prospective study. Child Dev. 73 (2002) 75-92
61. Smythe J.W., Murphy D., Timothy C., and Costall B. Hippocampal mineralocorticoid, but not glucocorticoid, receptors modulate anxiety-like behavior in rats. Pharmacol. Biochem. Behav. 56 (1997) 507-513
62. Soravia L.M., Heinrichs M., Aerni A., Maroni C., Schelling G., Ehlert U., Roozendaal B., and de Quervain D.J. Glucocorticoids reduce phobic fear in humans. Proc. Nat. Acad. Sci. USA 103 (2006) 5585-5590
63. Spielberger C.D., Gorusch R.L., and Lushene R.E. State-Trait Anxiety Inventory (1970), Consulting Psychologists Press, Palo Alto
64. Strömberg J., Bäckström T., and Lundgren P. Rapid non-genomic effect of glucocorticoid metabolites and neurosteroids on the gamma-aminobutyric acid-A receptor. Eur. J. Neurosci. 21 (2005) 2083-2088
65. Strome E.M., Wheler G.H., Higley J.D., Loriaux D.L., Suomi S.J., and Doudet D.J. Intracerebroventricular corticotropin-releasing factor increases limbic glucose metabolism and has social context-dependent behavioral effects in nonhuman primates. Proc. Nat. Acad. Sci. USA 99 (2002) 15749-15754
66. Takahashi T., Ikeda K., Ishikawa M., Kitamura N., Tsukasaki T., Nakama D., and Kameda T. Anxiety, reactivity, and social stress-induced cortisol elevation in humans. Neuroendocrinol. Lett. 26 (2005) 351-354
67. Thomas K.M., Drevets W.C., Dahl R.E., Ryan N.D., Birmaher B., Eccard C.H., Axelson D., Whalen P.J., and Casey B.J. Amygdala response to fearful faces in anxious and depressed children. Arch. Gen. Psychiatry 58 (2001) 1057-1063
68. Thomas K.M., Drevets W.C., Whalen P.J., Eccard C.H., Dahl R.E., Ryan N.D., and Casey B.J. Amygdala response to facial expressions in children and adults. Biol. Psychiatry 49 (2001) 309-316
69. Tops M., van der Pompe G., Baas D., Mulder L.J., Den Boer J.A., Meijman T.F., and Korf J. Acute cortisol effects on immediate free recall and recognition of nouns depend on stimulus valence. Psychophysiology 40 (2003) 167-173
70. Tops M., Wijers A.A., Koch T., and Korf J. Modulation of rotational behavior in healthy volunteers by cortisol administration. Biol. Psychol. 71 (2006) 240-243
71. Tops M., Wijers A.A., van Staveren A.S., Bruin K.J., Den Boer J.A., Meijman T.F., and Korf J. Acute cortisol administration modulates EEG alpha asymmetry in volunteers: relevance to depression. Biol. Psychol. 69 (2005) 181-193
72. Van Den Hout M., Tenney N., Huygens K., Merckelbach H., and Kindt M. Responding to subliminal threat cues is related to trait anxiety and emotional vulnerability: a successful replication of Macleod and Hagan (1992). Behav. Res. Ther. 33 (1995) 451-454
73. Van Honk J., Kessels R.P., Putman P., Jager G., Koppeschaar H.P., and Postma A. Attentionally modulated effects of cortisol and mood on memory for emotional faces in healthy young males. Psychoneuroendocrinology 28 (2003) 941-948
74. van Honk J., Tuiten A., van den Hout M., Koppeschaar H., Thijssen J., de Haan E., and Verbaten R. Baseline salivary cortisol levels and preconscious selective attention for threat. A pilot study. Psychoneuroendocrinology 23 (1998) 741-747
75. van Honk J., Tuiten A., van den Hout M., Koppeschaar H., Thijssen J., de Haan E., and Verbaten R. Conscious and preconscious selective attention to social threat: different neuroendocrine response patterns. Psychoneuroendocrinology 25 (2000) 577-591
76. van Honk J., Tuiten A., de Haan E., van den Hout M., and Stam H. Attentional biases for angry faces: relationships to trait anger and anxiety. Cogn. Emotion 15 (2001) 279-297
77. van Honk J., Schutter D.J., d'Alfonso A.A., Kessels R.P., and de Haan E.H. 1 Hz rTMS over the right prefrontal cortex reduces vigilant attention to unmasked but not to masked fearful faces. Biol. Psychiatry 52 (2002) 312-317
78. van Honk J., Peper J.S., and Schutter D.J. Testosterone reduces unconscious fear but not consciously experienced anxiety: implications for the disorders of fear and anxiety. Biol. Psychiatry 58 (2005) 218-225
79. Wedekind D., Bandelow B., Broocks A., Hajak G., and Ruther E. Salivary, total plasma and plasma free cortisol in panic disorder. J. Neural Transm. 107 (2000) 831-837
80. Whalen P.J., Rauch S.L., Etcoff N.L., McInerney S.C., Lee M.B., and Jenike M.A. Masked presentations of emotional facial expressions modulate amygdala activity without explicit knowledge. J. Neurosci. 18 (1998) 411-418
81. Williams J.M., Mathews A., and MacLeod C. The emotional Stroop task and psychopathology. Psychol. Bull. 120 (1996) 3-24
82. Williams J.M.G., Mathews A., and MacLeod C. Cognitive Psychology and Emotional Disorders (1996), Chisester, Wiley
83. Yehuda R. Sensitization of the hypothalamic-pituitary-adrenal axis in posttraumatic stress disorder. Ann. NY Acad. Sci. 821 (1997) 57-75
84. Yehuda R., McFarlane A.C., and Shalev A.Y. Predicting the development of posttraumatic stress disorder from the acute response to a traumatic event. Biol. Psychiatry 44 (1998) 1305-1313
85. Young E.A., and Breslau N. Cortisol and catecholamines in posttraumatic stress disorder: an epidemiologic community study. Arch. Gen. Psychiatry 61 (2004) 394-401