Testosterone reduces unconscious fear but not consciously experienced anxiety: Implications for the disorders of fear and anxiety

Biological Psychiatry

Volumn 58, Issue 3, 2005, Pages 218-225

  Van Honk, Jack ^a   Peper, Jiska S ^b   Schutter, Dennis J L G ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

Anxiety; Conscious and unconscious processing; Emotional facial expressions; Fear; Motivated attention; Testosterone

Indexed keywords

PLACEBO; TESTOSTERONE;

ADULT; AFFECT; ANXIETY; ANXIETY DISORDER; ARTICLE; CLINICAL TRIAL; CONSCIOUSNESS; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; CROSSOVER PROCEDURE; DOUBLE BLIND PROCEDURE; DRUG EFFECT; EMOTION; FACIAL EXPRESSION; FEAR; FEMALE; HORMONE ACTION; HUMAN; MOTIVATION; NEUROPSYCHOLOGICAL TEST; NORMAL HUMAN; PHOBIA; PRIORITY JOURNAL; SELF REPORT; SINGLE DRUG DOSE; TASK PERFORMANCE;

ADULT; ANXIETY; ATTENTION; CONSCIOUSNESS; CROSS-OVER STUDIES; DOUBLE-BLIND METHOD; FACIAL EXPRESSION; FEAR; FEMALE; HUMANS; PHOTIC STIMULATION; PSYCHIATRIC STATUS RATING SCALES; QUESTIONNAIRES; REACTION TIME; TASK PERFORMANCE AND ANALYSIS; TESTOSTERONE; TIME FACTORS; UNCONSCIOUS (PSYCHOLOGY);

EID: 23444432727     PISSN: 00063223     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biopsych.2005.04.003     Document Type: Article

References (90)

1. J.L. Aikey, J.G. Nyby, D.M. Anmuth, P.J. James Testosterone rapidly reduces anxiety in male house mice (Mus musculus) Horm Behav 42 2002 448 460
2. A. Aleman, E. Bronk, R.P.C. Kessels, H.P.F. Koppeschaar, J. van Honk A single administration of testosterone improves visuospatial ability in young women Psychoneuroendocrinology 290 2004 612 617
3. P.A. Arnett Autonomic responsivity in psychopaths A critical review and theoretical proposal Clin Psychol Rev 17 1997 903 936
4. D.H. Barlow Anxiety and Its Disorders The Nature and Treatment of Anxiety and Panic 1988 Guilford Press New York
5. A. Bechara, A.R. Damasio, H. Damasio, S.W. Anderson Insensitivity to future consequences following damage to the human prefrontal cortex Cognition 50 1994 7 15
6. G.G. Berntson, J.T. Cacioppo, M. Sarter In the generation and regulation of affective experience R.J. Davidson K.R. Scherer H.H. Goldsmith Handbook of Affective Sciences 2003 Oxford University Press New York 1105 1116
7. K.C. Berridge Comparing the emotional brains of humans and other animals R.J. Davidson K.R. Scherer H.H. Goldsmith Handbook of Affective Sciences 2003 Oxford University Press New York 25 51
8. J.M. Bjork, F.G. Moeller, D.M. Dougherty, A.C. Swann Endogenous plasma testosterone levels and commission errors in women A preliminary report Physiol Behav 73 2001 217 221
9. A. Boissy, M.F. Bouissou Effects of androgen treatment on behavioral and physiological responses of heifers to fear-eliciting situations Horm Behav 28 1994 66 83
10. A. Bond, M. Lader The use of analogue scales in rating subjective feelings Br J Med Psychol 80 1974 1 46
11. M.F. Bouissou, M. Vandenheede Long-term effects of androgen treatment on fear reactions in ewes Horm Behav 30 1996 93 99
12. A.S. Burris, S.M. Banks, C.S. Carter, J.M. Davidson, R.J. Sherins A long-term, prospective study of the physiologic and behavioral effects of hormone replacement in untreated hypogonadal men J Androl 13 1992 297 304
13. C.S. Carver, T.L. White Behavioral inhibition, behavioral activation, and affective responses to impending reward and punishment The BIS/BAS scales J Pers Soc Psychol 67 1994 319 333
14. E. Cashdan Hormones, sex, and status in women Horm Behav 29 1995 354 366
15. D.S. Charney Psychobiological mechanisms of resilience and vulnerability Implications for successful adaptation to extreme stress Am J Psychiatry 161 2004 195 216
16. J. Cohen Statistical Power Analysis for the Behavioral Sciences 1988 Lawrence Erlbaum Hillsdale, NJ
17. J.D. Coplan, R.B. Lydiard Brain circuits in panic disorder Biol Psychiatry 44 1998 1264 1276
18. K.P. Corodimas, J.E. LeDoux, P.W. Gold, J. Schulkin Corticosterone potentiation of conditioned fear in rats Ann N Y Acad Sci 746 1994 392 393
19. J.M. Dabbs Testosterone, smiling, and facial appearance J Nonverbal Behav 21 1997 45 55
20. J.M. Dabbs, M.F. Hargrove Age, testosterone, and behavior among female prison inmates Psychosom Med 59 1997 477 480
21. J.M. Dabbs, R. Morris Testosterone, social class, and antisocial behavior in a sample of 4,462 men Psychol Sci 1 1990 209 211
22. J.M. Dabbs Jr, R.L. Frady, T.S. Carr, N.F. Besch Saliva testosterone and criminal violence in young adult prison inmates Psychosom Med 49 1987 174 182
23. A. D′Alfonso, J. van Honk, E.J. Hermans, A. Postma, E. De Haan Laterality effects in selective attention to threat after repetitive transcranial magnetic stimulation at the prefrontal cortex in female subjects Neurosci Lett 280 2000 195 198
24. M. Davis Are different parts of the extended amygdala involved in fear versus anxiety? Biol Psychiatry 44 1998 1239 1247
25. P. Ekman, W. Friesen Pictures of Facial Effect 1976 Consulting Psychologist Press Palo Alto, CA
26. F. Esteves, A. Öhman Masking the face Recognition of emotional facial expressions as a function of the parameters of backward masking Scand J Psychol 34 1993 1 18
27. C.A. Frye, A.M. Seliga Testosterone increases analgesia, anxiolysis, and cognitive performance of male rats Cogn Affect Behav Neurosci 1 2001 371 381
28. M. Gallagher, P.C. Holland The amygdala complex Multiple roles in associative learning and attention Proc Natl Acad Sci U S A 91 1994 11771 11776
29. K. Goldapple, Z. Segal, C. Garson, M. Lau, P. Bieling, S. Kennedy Modulation of cortical-limbic pathways in major depression Treatment-specific effects of cognitive behavior therapy Arch Gen Psychiatry 61 2004 34 41
30. J.A. Gray The Psychology of Fear and Stress 1987 Cambridge University Press New York
31. C. Grillion, J. Baas A review of the modulation of the startle reflex by affective states and its application in psychiatry Clin Neurophysiol 114 2004 1557 1579
32. C. Gross, R. Hen The developmental origins of anxiety Nat Rev Neurosci 5 2004 545 552
33. E.J. Hermans, N. Ramsey, A. Tuiten, J. van Honk The amygdala and anger Responses to angry facial expressions after administration of a single dose of testosterone Hum Brain Mapp 23 2004 S188
34. E.O. Johnson, T.C. Kamilaris, G.P. Chrousos, P.W. Gold Mechanisms of stress A dynamic overview of hormonal and behavioral homeostasis Neurosci Biobehav Rev 16 1992 115 130
35. S.M. Kemp-Wheeler, A.B. Hill Semantic priming without awareness Some methodological considerations Q J Exp Psychol A 40 1988 671 692
36. T.A. Ketter, P.W. Wang, A. Lembke, N. Sachs Physiological and pharmacological induction of affect R.J. Davidson K.R. Scherer H.H. Goldsmith Handbook of Affective Sciences 2003 Oxford University Press New York 930 962
37. A.S. Kling, L.A. Brothers The amygdala and social behavior J.P. Aggleton The Amygdala 1992 Wiley Liss NewYork 353 377
38. P.J. Lang, M. Davis, A. Öhman Fear and anxiety Animal models and human cognitive psychophysiology J Affect Disord 61 2000 137 159
39. J.E. LeDoux The Emotional Brain 1996 Simon & Schuster New York
40. A. Mathews, B.A. Mackintosh Cognitive model of selective processing in anxiety Cognit Ther Res 22 1999 539 560
41. H.S. Mayberg, M. Liotti, S.K. Brannan, S. McGinnis, R.K. Mahurin, P.A. Jerabek Reciprocal limbic-cortical function and negative mood Converging PET findings in depression and normal sadness Am J Psychiatry 156 1999 675 682
42. A. Mazur, A. Booth Testosterone and dominance in men Behav Brain Sci 21 1998 353 363
43. D.C. McClelland, R. Koestner, J. Weinberger How do self-attributed and implicit motives differ? Psychol Rev 96 1989 690 702
44. J.S. Morris, A. Öhman, R.J. Dolan A subcortical pathway to the right amygdala mediating "unseen" fear Proc Natl Acad Sci U S A 96 1999 1680 1685
45. H. Norris The action of sedatives on brain stem oculomotor systems in man Neuropharmacology 10 1971 181 191
46. H.G. Pope Jr, G.H. Cohane, G. Kanayama, A.J. Siegel, J.I. Hudson Testosterone gel supplementation for men with refractory depression A randomized, placebo-controlled trial Am J Psychiatry 160 2003 105 111
47. A. Postma, G. Meyer, A. Tuiten, J. van Honk, R.P. Kessels, J. Thijsen Effects of testosterone administration on selective aspects of object-location memory in healthy young women Psychoneuroendocrinology 25 2000 563 575
48. P. Putman, E. Hermans, J. van Honk Emotional Stroop performance for masked angry faces It's BAS, not BIS Emotion 4 2004 305 311
49. S.L. Rauch, P.J. Whalen, L.M. Shin, S.C. McInerney, M.L. Macklin, N.B. Lasko Exaggerated amygdala response to masked facial stimuli in posttraumatic stress disorder A functional MRI study Biol Psychiatry 47 2000 769 776
50. P. Renaud, J.P. Blondin The stress of Stroop performance Physiological and emotional responses to color-word interference, task pacing, and pacing speed Int J Psychophysiol 27 1997 87 97
51. J.B. Rosen, J. Schulkin From normal fear to pathological anxiety Psychol Rev 105 1998 325 350
52. J. Schulkin Rethinking Homeostasis Allostatic Regulation in Physiology and Pathophysiology 2003 MIT Press Cambridge, MA
53. J. Schulkin, P.W. Gold, B.S. McEwen Induction of corticotropin-releasing hormone gene expression by glucocorticoids Implication for understanding the states of fear and anxiety and allostatic load Psychoneuroendocrinology 23 1998 219 243
54. Schutter DJLG, Peper JS, Koppeschaar RPF, Kahn RS, van Honk J (in press): Administration of testosterone increases functional connectivity in a cortico-cortical depression circuit. J Neuropsychiatry Clin Neurosci.
55. D.J.L.G. Schutter, J. van Honk Decoupling of midfrontal delta-beta oscillations after testosterone administration Int J Psychophysiol 51 2004 71 73
56. D.J.L.G. Schutter, J. van Honk Salivary cortisol levels and the coupling of midfrontal delta-beta oscillations Int J Psychophysiol 55 2005 127 129
57. D.J.L.G. Schutter, J. van Honk, A.A.L. D'Alfonso, A. Postma, E.H.F. De Haan Effects of slow rTMS at the right dorsolateral prefrontal cortex on EEG asymmetry and mood Neuroreport 12 2001 445 447
58. S. Shacham A shortened version of the Profile of Mood States J Pers Assess 47 1983 305 306
59. Y.I. Sheline, D.M. Barch, J.M. Donnelly, J.M. Ollinger, A.Z. Snyder, M.A. Mintun Increased amygdala response to masked emotional faces in depressed subjects resolves with antidepressant treatment An fMRI study Biol Psychiatry 50 2001 651 658
60. H. Soler, P. Vinayak, D. Quadagno Biosocial aspects of domestic violence Psychoneuroendocrinology 25 2000 721 739
61. C.D. Spielberger Manual of the State-Trait Anxiety Inventory (STAXI) 1988 Psychological Assessment Resources Odessa, FL
62. K.M. Thomas, W.C. Drevets, R.E. Dahl, N.D. Ryan, B. Birmaher, C.H. Eccard Amygdala response to fearful faces in anxious and depressed children Arch Gen Psychiatry 58 2001 1057 1063
63. B.L. Thompson, K. Erickson, J. Schulkin, J.B. Rosen Corticosterone facilitates retention of contextually conditioned fear and increases CRH mRNA expression in the amygdala Behav Brain Res 149 2004 209 215
64. A.J. Tilbrook, A.I. Turner, I.J. Clarke Effects of stress on reproduction in non-rodent mammals The role of glucocorticoids and sex differences Rev Reprod 5 2000 105 113
65. M. Tillfors, T. Furmark, I. Marteinsdottir, H. Fischer, A. Pissiota, B. Langstrom Cerebral blood flow in subjects with social phobia during stressful speaking tasks A PET study Am J Psychiatry 158 2001 1220 1226
66. A. Tuiten, J. van Honk, H. Koppeschaar, C. Bernaards, J. Thijssen, R. Verbaten Time course of effects of testosterone administration on sexual arousal in women Arch Gen Psychiatry 57 2000 149 153
67. A. Tuiten, J. van Honk, R. Verbaten, E. Laan, W. Everaerd, H. Stam Can sublingual testosterone increase subjective and physiological measures of laboratory-induced sexual arousal? Arch Gen Psychiatry 59 2002 465 466
68. J. van Honk, E. De Haan Cortical and subcortical routes for conscious and unconscious processing of emotional faces B. De Gelder C.A. Heywood E. De Haan Varieties of Unconscious Processing 2001 Oxford University Press Oxford, England 222 237
69. J. van Honk, E.J. Hermans, A.A.L. D'Alfonso, D.J.L.G. Schutter, L. Van Doornen, E. De Haan A left-prefrontal lateralized, sympathetic mechanism directs attention towards social threat in humans Evidence from repetitive transcranial magnetic stimulation Neurosci Lett 319 2002 99 102
70. J. van Honk, R.P.C. Kessels, P. Putman, G. Jager, H. Koppeschaar, A. Postma Attentionally modulated effects of cortisol and mood on memory for emotional faces in healthy young males Psychoneuroendocrinology 28 2003 941 948
71. van Honk J, Schutter DJLG (in press-a): Unmasking feigned sanity: A neurobiological model of emotion processing in primary psychopathy. Cogn Neuropsychiatry.
72. van Honk J, Schutter DJLG (in press-b): Dynamic brain systems in quest for emotional homeostasis. Behav Brain Sci.
73. J. van Honk, D.J.L.G. Schutter, A.A.L. D'Alfonso, R.P.C. Kessels, E.H.F. De Haan 1Hz rTMS over the right prefrontal cortex reduces vigilant attention to unmasked but not to masked fearful faces Biol Psychiatry 52 2002 312 317
74. J. van Honk, D.J.L.G. Schutter, E.J. Hermans, P. Putman Low cortisol levels and the balance between punishment sensitivity and reward dependency Neuroreport 14 2003 1993 1996
75. J. van Honk, D.J.L.G. Schutter, E.J. Hermans, P. Putman, A. Tuiten, H. Koppeschaar Testosterone shifts the balance between sensitivity for punishment and reward in healthy young women Psychoneuroendocrinology 29 2004 937 943
76. J. van Honk, A. Tuiten, E.J. Hermans, P. Putman, H. Koppeschaar, J. Thijssen A single administration of testosterone elevates cardiac defence reflexes to angry faces in healthy young women Behav Neurosci 115 2001 238 242
77. J. van Honk, A. Tuiten, M. Van den Hout, H. Koppeschaar, J. Thijssen, E. De Haan Baseline salivary cortisol levels and preconscious selective attention for threat A pilot study Psychoneuroendocrinology 23 1998 741 747
78. J. van Honk, A. Tuiten, M. Van den Hout, H. Koppeschaar, J. Thijssen, E. De Haan Conscious and preconscious selective attention to social threat Different neuroendocrine response patterns Psychoneuroendocrinology 25 2000 577 591
79. J. van Honk, A. Tuiten, R. Verbaten, M. Van den Hout, H. Koppeschaar, J. Thijssen Correlations among salivary testosterone, mood, and selective attention to threat in humans Horm Behav 36 1999 17 24
80. M. Van Selst, P. Merikle Perception below the objective threshold? Conscious Cogn 2 1993 194 203
81. V. Viau Functional cross-talk between the hypothalamic-pituitary-gonadal and adrenal axes J Neuroendocrinol 14 2002 506 513
82. V. Viau, M.J. Meaney The inhibitory effect of testosterone on hypothalamic-pituitary-adrenal responses to stress is mediated by the medial preoptic area J Neurosci 16 1996 1866 1876
83. C. Wang, D.R. Eyre, R. Clark, D. Kleinberg, C. Newman, A. Iranmanesh Sublingual testosterone replacement improves muscle mass and strength, decreases bone resorption, and increases bone formation markers in hypogonadal men J Clin Endocrinol Metab 81 1996 3654 3662
84. E.M. Wassermann, S.H. Lisanby Therapeutic application of repetitive transcranial magnetic stimulation A review Clin Neurophysiol 112 2001 1367 1377
85. A. Wells, G. Matthews Attention and Emotion A Clinical Perspective 1994 Lawrence Erlbaum Associates, Inc Hillsdale, NJ
86. P.J. Whalen Fear, vigilance, and ambiguity Initial neuroimaging studies of the human amygdala Curr Dir Psychol Sci 7 1998 177 188
87. P.J. Whalen, S.L. Rauch, N.L. Etcoff, S.C. McInerney, M.B. Lee, M.A. Jenike Masked presentations of emotional facial expressions modulate amygdala activity without explicit knowledge J Neurosci 18 1998 411 418
88. J.M. Williams, A. Mathews, C. MacLeod The emotional Stroop task and psychopathology Psychol Bull 120 1996 3 24
89. R.I. Wood Functions of the steroid-responsive neural network in the control of male hamster sexual behavior Trends Endocrinol Metab 7 1996 338 344
90. M. Zuckerman Psychobiology of Personality 1991 Cambridge University Press Cambridge, UK