Elsevier

Biological Psychiatry

Volume 58, Issue 3, 1 August 2005, Pages 218-225
Biological Psychiatry

Original article
Testosterone Reduces Unconscious Fear but Not Consciously Experienced Anxiety: Implications for the Disorders of Fear and Anxiety

https://doi.org/10.1016/j.biopsych.2005.04.003Get rights and content

Background

The fear-reducing properties of testosterone have been firmly established in animals but not in humans. However, human data on the relation between testosterone, fear, and anxiety have predominantly involved questionnaires that index cortically executed conscious appraisal of anxious mood. Animal studies, on the other hand, indicate that the effects of testosterone on motivation and emotion are of subcortical origin and of unconscious nature. Presently, it was hypothesized that a single testosterone administration to humans would reduce unconscious fear but not consciously experienced anxiety.

Methods

In a placebo-controlled, double-blind crossover design, a single dose of testosterone (.5 mg) or placebo was administered to 16 healthy female volunteers. Afterward, a masked emotional Stroop task measured unconscious emotional responses to fearful faces, while multiple self-reports of mood indexed consciously experienced anxiety.

Results

As hypothesized, the habitual vigilant emotional response to the masked fearful face observed in the placebo condition was significantly reduced after testosterone was administered, while the self-reported measures of anxiety remained unaffected.

Conclusions

These data provide the first direct evidence for fear-reducing properties of testosterone in humans. Furthermore, by dissociating specific aspects of fear and anxiety in humans, this outcome highlights that testosterone’s effects on motivation and emotion concern the subcortical affective pathways of the brain.

Section snippets

Subjects

Participants were 16 right-handed, healthy young women, ranging in age from 19 to 26 years. Only women were recruited because the parameters (quantity and time course) for inducing effects in men after a single sublingual administration of testosterone are unknown (cf. Tuiten et al 2000). The testosterone-placebo testing days were run 2 days apart but both in the early follicular phase of the menstrual cycle when endogenous levels of hormones are low and most stable (Bjork et al 2001). The

Awareness Checks

There was no evidence of recognition of emotional valence during masked presentation by subjective check. For analyzing subjects’ performance on the objective check, we initially scrutinized possible effects of Order and Drug to see whether repeated measuring or testosterone had influenced perceptual thresholds in any way. There was no evidence for Order [Z(1,15) = −.22; ns] and Drug [Z(1,15) = −.13; ns] having the slightest effect on perceptual performance. This allowed us to collapse the

Discussion

The present study investigated the effects of testosterone on emotional responses to unconsciously processed fearful faces and consciously experienced states of anxiety. Concurring with fMRI and repetitive transcranial magnetic stimulation (rTMS) findings in healthy volunteers that involved emotional responses to unseen facial threat (Whalen et al 1998; van Honk et al 2002a), a vigilant emotional response to the masked fearful facial expression was observed after placebo administration (Figure 2

References (90)

  • M. Davis

    Are different parts of the extended amygdala involved in fear versus anxiety?

    Biol Psychiatry

    (1998)
  • E.O. Johnson et al.

    Mechanisms of stressA dynamic overview of hormonal and behavioral homeostasis

    Neurosci Biobehav Rev

    (1992)
  • P.J. Lang et al.

    Fear and anxietyAnimal models and human cognitive psychophysiology

    J Affect Disord

    (2000)
  • H. Norris

    The action of sedatives on brain stem oculomotor systems in man

    Neuropharmacology

    (1971)
  • A. Postma et al.

    Effects of testosterone administration on selective aspects of object-location memory in healthy young women

    Psychoneuroendocrinology

    (2000)
  • S.L. Rauch et al.

    Exaggerated amygdala response to masked facial stimuli in posttraumatic stress disorderA functional MRI study

    Biol Psychiatry

    (2000)
  • P. Renaud et al.

    The stress of Stroop performancePhysiological and emotional responses to color-word interference, task pacing, and pacing speed

    Int J Psychophysiol

    (1997)
  • J. Schulkin et al.

    Induction of corticotropin-releasing hormone gene expression by glucocorticoidsImplication for understanding the states of fear and anxiety and allostatic load

    Psychoneuroendocrinology

    (1998)
  • D.J.L.G. Schutter et al.

    Decoupling of midfrontal delta-beta oscillations after testosterone administration

    Int J Psychophysiol

    (2004)
  • D.J.L.G. Schutter et al.

    Salivary cortisol levels and the coupling of midfrontal delta-beta oscillations

    Int J Psychophysiol

    (2005)
  • Y.I. Sheline et al.

    Increased amygdala response to masked emotional faces in depressed subjects resolves with antidepressant treatmentAn fMRI study

    Biol Psychiatry

    (2001)
  • H. Soler et al.

    Biosocial aspects of domestic violence

    Psychoneuroendocrinology

    (2000)
  • B.L. Thompson et al.

    Corticosterone facilitates retention of contextually conditioned fear and increases CRH mRNA expression in the amygdala

    Behav Brain Res

    (2004)
  • J. van Honk et al.

    A left-prefrontal lateralized, sympathetic mechanism directs attention towards social threat in humansEvidence from repetitive transcranial magnetic stimulation

    Neurosci Lett

    (2002)
  • J. van Honk et al.

    Attentionally modulated effects of cortisol and mood on memory for emotional faces in healthy young males

    Psychoneuroendocrinology

    (2003)
  • J. van Honk et al.

    1Hz rTMS over the right prefrontal cortex reduces vigilant attention to unmasked but not to masked fearful faces

    Biol Psychiatry

    (2002)
  • J. van Honk et al.

    Testosterone shifts the balance between sensitivity for punishment and reward in healthy young women

    Psychoneuroendocrinology

    (2004)
  • J. van Honk et al.

    Baseline salivary cortisol levels and preconscious selective attention for threatA pilot study

    Psychoneuroendocrinology

    (1998)
  • J. van Honk et al.

    Conscious and preconscious selective attention to social threatDifferent neuroendocrine response patterns

    Psychoneuroendocrinology

    (2000)
  • J. van Honk et al.

    Correlations among salivary testosterone, mood, and selective attention to threat in humans

    Horm Behav

    (1999)
  • M. Van Selst et al.

    Perception below the objective threshold?

    Conscious Cogn

    (1993)
  • E.M. Wassermann et al.

    Therapeutic application of repetitive transcranial magnetic stimulationA review

    Clin Neurophysiol

    (2001)
  • R.I. Wood

    Functions of the steroid-responsive neural network in the control of male hamster sexual behavior

    Trends Endocrinol Metab

    (1996)
  • D.H. Barlow

    Anxiety and Its DisordersThe Nature and Treatment of Anxiety and Panic

    (1988)
  • G.G. Berntson et al.

    In the generation and regulation of affective experience

  • K.C. Berridge

    Comparing the emotional brains of humans and other animals

  • A. Bond et al.

    The use of analogue scales in rating subjective feelings

    Br J Med Psychol

    (1974)
  • A.S. Burris et al.

    A long-term, prospective study of the physiologic and behavioral effects of hormone replacement in untreated hypogonadal men

    J Androl

    (1992)
  • C.S. Carver et al.

    Behavioral inhibition, behavioral activation, and affective responses to impending reward and punishmentThe BIS/BAS scales

    J Pers Soc Psychol

    (1994)
  • D.S. Charney

    Psychobiological mechanisms of resilience and vulnerabilityImplications for successful adaptation to extreme stress

    Am J Psychiatry

    (2004)
  • J. Cohen

    Statistical Power Analysis for the Behavioral Sciences

    (1988)
  • K.P. Corodimas et al.

    Corticosterone potentiation of conditioned fear in rats

    Ann N Y Acad Sci

    (1994)
  • J.M. Dabbs

    Testosterone, smiling, and facial appearance

    J Nonverbal Behav

    (1997)
  • J.M. Dabbs et al.

    Age, testosterone, and behavior among female prison inmates

    Psychosom Med

    (1997)
  • J.M. Dabbs et al.

    Testosterone, social class, and antisocial behavior in a sample of 4,462 men

    Psychol Sci

    (1990)
  • Cited by (228)

    View all citing articles on Scopus
    View full text