Psychoneuroendocrinology
Volume 32, Issue 7 , Pages 793-802 , August 2007

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

  • Peter Putman

      Affiliations

    • Department of Psychology, Experimental Psychology, Utrecht University, P.O. Box 80125, 3508 TC Utrecht, The Netherlands
    • Clinical-, Health- and Neuropsychology, Institute for Psychological Research, Leiden University, Wassenaarseweg 52, Postbus 9555, 2300 RB Leiden, The Netherlands
    • Corresponding Author InformationCorresponding author. Clinical-, Health-, and Neuropsychology, Institute for Psychological Research, Leiden University, Wassenaarseweg 52, Postbus 9555, 2300 RB Leiden, The Netherlands. Tel.: +31715274818; fax: +31715274678.
  • ,
  • Erno J. Hermans

      Affiliations

    • Department of Psychology, Experimental Psychology, Utrecht University, P.O. Box 80125, 3508 TC Utrecht, The Netherlands
    • FC Donders Center for Cognitive Neuroimaging, P.O. Box 9101, 6500 HB Nijmegen, The Netherlands
  • ,
  • Hans Koppeschaar

      Affiliations

    • Department of Endocrinology, University Medical Center Utrecht, Postbus 85500, 3508 GA Utrecht, The Netherlands
  • ,
  • Alexandra van Schijndel

      Affiliations

    • Department of Psychology, Experimental Psychology, Utrecht University, P.O. Box 80125, 3508 TC Utrecht, The Netherlands
  • ,
  • Jack van Honk

      Affiliations

    • Department of Psychology, Experimental Psychology, Utrecht University, P.O. Box 80125, 3508 TC Utrecht, The Netherlands

Received 20 September 2006 ,Revised 14 May 2007 ,Accepted 14 May 2007.

References 

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

PII: S0306-4530(07)00118-7

doi: 10.1016/j.psyneuen.2007.05.009

Psychoneuroendocrinology
Volume 32, Issue 7 , Pages 793-802 , August 2007