Anabolic androgenic steroid dependence is associated with impaired emotion recognition

  • Lisa E. HaugerEmail author
  • Dominic Sagoe
  • Anja Vaskinn
  • Espen A. Arnevik
  • Siri Leknes
  • Marie L. Jørstad
  • Astrid Bjørnebekk
Original Investigation



Illicit use of anabolic androgenic steroids (AAS) has grown into a serious public health concern throughout the Western World. AAS use is associated with adverse medical, psychological, and social consequences. Around 30% of AAS users develop a dependence syndrome with sustained use despite adverse side effects. AAS dependence is associated with a high frequency of intra- and interpersonal problems, and it is central to identify factors related to the development and maintenance of dependence.


The present study investigated the ability to recognize emotion from biological motion. The emotional biological motion task was administered to male AAS dependent users (AAS dependents; n = 45), AAS non-dependent users (AAS non-dependents; n = 38) and a comparison-group of non-using weightlifters (non-users; n = 69).


Multivariate analysis of variance showed a general impairment in emotion recognition in AAS dependents, compared to the non-using weightlifters, whereas no significant impairment was observed in AAS non-dependents. Furthermore, AAS dependents showed impaired recognition of fearful stimuli compared to both AAS non-dependents and non-using weightlifters. The between-group effect remained significant after controlling for Intelligence Quotient (IQ), past 6 months of non-AAS drug use, antisocial personality problems, anxiety, and depression.


AAS dependents show impaired emotion recognition from body movement, fear in particular, which could potentially contribute to higher frequency of interpersonal problems and antisocial behaviors in this population.


Anabolic androgenic steroids Testosterone Dependence Social cognition Body language Emotion processing Emotion recognition 



This research was funded by grants 2013087 and 2016049 (Dr Bjørnebekk) from the South-Eastern Norway Regional Health Authority, and internal research grants from the Division on Mental Health and Addiction (Dr Bjørnebekk).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


The founding organizations had no role in the design or conduct of the study; in the collection, analysis, or interpretation of data; or in the preparation, review, or approval of the manuscript.


  1. Achenbach TM, Rescorla LA (2003) Manual for the ASEBA Adult forms and profiles. University of Vermont, Research Center for Children, Youth & Families, BurlingtonGoogle Scholar
  2. Adolphs R (2002) Neural systems for recognizing emotion. Curr Opin Neurobiol 12:169–177CrossRefGoogle Scholar
  3. Aikey JL, Nyby JG, Anmuth DM, James PJ (2002) Testosterone rapidly reduces anxiety in male house mice (Mus musculus). Horm Behav 42:448–460CrossRefGoogle Scholar
  4. Baron-Cohen S, Richler J, Bisarya D, Gurunathan N, Wheelwright S (2003) The systemizing quotient: an investigation of adults with Asperger syndrome or high–functioning autism, and normal sex differences. Philos Trans R Soc Lond B Biol Sci 358:361–374CrossRefGoogle Scholar
  5. Baron-Cohen S, Knickmeyer RC, Belmonte MK (2005) Sex differences in the brain: implications for explaining autism. Science 310:819–823CrossRefGoogle Scholar
  6. Bertozzi G et al (2017) The role of anabolic androgenic steroids in disruption of the physiological function in discrete areas of the central nervous system. Mol Neurobiol:1–9Google Scholar
  7. Birbaumer N, Veit R, Lotze M, Erb M, Hermann C, Grodd W, Flor H (2005) Deficient fear conditioning in psychopathy: a functional magnetic resonance imaging study. Arch Gen Psychiatry 62:799–805CrossRefGoogle Scholar
  8. Bjørnebekk A, Walhovd KB, Jørstad ML, Due-Tønnessen P, Hullstein IR, Fjell AM (2017) Structural brain imaging of long-term anabolic-androgenic steroid users and nonusing weightlifters. Biol Psychiatry 82:294–302CrossRefGoogle Scholar
  9. Blair R (2006) The emergence of psychopathy: implications for the neuropsychological approach to developmental disorders. Cognition 101:414–442CrossRefGoogle Scholar
  10. Booth A, Johnson DR, Granger DA (1999) Testosterone and men’s depression: the role of social behavior. J Health Soc Behav:130–140Google Scholar
  11. Bos PA, Terburg D, Van Honk J (2010) Testosterone decreases trust in socially naive humans. Proc Natl Acad Sci 107:9991–9995CrossRefGoogle Scholar
  12. Bos PA, Panksepp J, Bluthé R-M, van Honk J (2012) Acute effects of steroid hormones and neuropeptides on human social–emotional behavior: a review of single administration studies. Front Neuroendocrinol 33:17–35CrossRefGoogle Scholar
  13. Bos PA, van Honk J, Ramsey NF, Stein DJ, Hermans EJ (2013) Testosterone administration in women increases amygdala responses to fearful and happy faces. Psychoneuroendocrinology 38:808–817CrossRefGoogle Scholar
  14. Brothers L (1990) The neural basis of primate social communication. Motiv Emot 14:81–91CrossRefGoogle Scholar
  15. Brower KJ (2002) Anabolic steroid abuse and dependence. Curr Psychiatry Rep 4:377–387CrossRefGoogle Scholar
  16. Copeland J, Peters R, Dillon P (1998) A study of 100 anabolic-androgenic steroid users. Med J Aust 168:311–312CrossRefGoogle Scholar
  17. Copeland J, Peters R, Dillon P (2000) Anabolic-androgenic steroid use disorders among a sample of Australian competitive and recreational users. Drug Alcohol Depend 60:91–96CrossRefGoogle Scholar
  18. Couture S, Penn D, Losh M, Adolphs R, Hurley R, Piven J (2010) Comparison of social cognitive functioning in schizophrenia and high functioning autism: more convergence than divergence. Psychol Med 40:569–579CrossRefGoogle Scholar
  19. de Souza GL, Hallak J (2011) Anabolic steroids and male infertility: a comprehensive review. BJU Int 108:1860–1865CrossRefGoogle Scholar
  20. Engelstad KN, Sundet KS, Andreassen OA, Vaskinn A (2017) Body language reading of emotion in schizophrenia: associations with symptoms and functional outcome. Scand J Psychol 58:359–366CrossRefGoogle Scholar
  21. First MB, Gibbon M, Spitzer RL, Benjamin LS (1997) User’s guide for the structured clinical interview for DSM-IV axis II personality disorders: SCID-II. American Psychiatric Pub, Washington, DCGoogle Scholar
  22. Goldstein RZ, Volkow ND (2002) Drug addiction and its underlying neurobiological basis: neuroimaging evidence for the involvement of the frontal cortex. Am J Psychiatry 159:1642–1652CrossRefGoogle Scholar
  23. Hall RC, Hall RC, Chapman MJ (2005) Psychiatric complications of anabolic steroid abuse. Psychosomatics 46:285–290CrossRefGoogle Scholar
  24. Heberlein AS, Adolphs R, Tranel D, Damasio H (2004) Cortical regions for judgments of emotions and personality traits from point-light walkers. J Cogn Neurosci 16:1143–1158CrossRefGoogle Scholar
  25. Heffernan T, Battersby L, Bishop P, O’Neill T (2015) Everyday memory deficits associated with anabolic-androgenic steroid use in regular gymnasium users. The Open Psychiatry Journal 9:1–6Google Scholar
  26. Hermans EJ, Putman P, Baas JM, Koppeschaar HP, van Honk J (2006a) A single administration of testosterone reduces fear-potentiated startle in humans. Biol Psychiatry 59:872–874CrossRefGoogle Scholar
  27. Hermans EJ, Putman P, Van Honk J (2006b) Testosterone administration reduces empathetic behavior: a facial mimicry study. Psychoneuroendocrinology 31:859–866CrossRefGoogle Scholar
  28. Hermans EJ, Ramsey NF, van Honk J (2008) Exogenous testosterone enhances responsiveness to social threat in the neural circuitry of social aggression in humans. Biol Psychiatry 63:263–270CrossRefGoogle Scholar
  29. Hubert B, Wicker B, Moore DG, Monfardini E, Duverger H, Da Fonseca D, Deruelle C (2007) Brief report: recognition of emotional and non-emotional biological motion in individuals with autistic spectrum disorders. J Autism Dev Disord 37:1386–1392CrossRefGoogle Scholar
  30. Johansson G (1973) Visual perception of biological motion and a model for its analysis. Percept Psychophys 14:201–211CrossRefGoogle Scholar
  31. Kanayama G, Hudson JI, Pope HG (2008) Long-term psychiatric and medical consequences of anabolic–androgenic steroid abuse: a looming public health concern? Drug Alcohol Depend 98:1–12CrossRefGoogle Scholar
  32. Kanayama G, Brower KJ, Wood RI, Hudson JI, Pope HG Jr (2009a) Anabolic–androgenic steroid dependence: an emerging disorder. Addiction 104:1966–1978CrossRefGoogle Scholar
  33. Kanayama G, Brower KJ, Wood RI, Hudson JI, Pope M Jr, Harrison G (2009b) Issues for DSM-V: clarifying the diagnostic criteria for anabolic-androgenic steroid dependence. Am Psychiatric Assoc, PhiladelphiaGoogle Scholar
  34. Kanayama G, Hudson JI, Pope HG (2009c) Features of men with anabolic-androgenic steroid dependence: A comparison with nondependent AAS users and with AAS nonusers. Drug Alcohol Depend 102:130–137CrossRefGoogle Scholar
  35. Kanayama G, Hudson JI, Pope HG Jr (2010) Illicit anabolic–androgenic steroid use. Horm Behav 58:111–121CrossRefGoogle Scholar
  36. Kanayama G, Kean J, Hudson JI, Pope HG (2013) Cognitive deficits in long-term anabolic-androgenic steroid users. Drug Alcohol Depend 130:208–214CrossRefGoogle Scholar
  37. Kanayama G, Pope HG, Hudson JI (2018) Associations of anabolic-androgenic steroid use with other behavioral disorders: an analysis using directed acyclic graphs Psychol Med 48(15):2601–2608Google Scholar
  38. Keverne EB, Martel FL, Nevison CM (1996) Primate brain evolution: genetic and functional considerations, Proc. R. Soc. Lond. B, vol 1371. The Royal Society, London, pp 689–696Google Scholar
  39. King JA, De Oliveira WL, Patel N (2005) Deficits in testosterone facilitate enhanced fear response. Psychoneuroendocrinology 30:333–340CrossRefGoogle Scholar
  40. Leppänen JM (2006) Emotional information processing in mood disorders: a review of behavioral and neuroimaging findings. Curr Opin Psychiatry 19:34–39CrossRefGoogle Scholar
  41. Loi F, Vaidya JG, Paradiso S (2013) Recognition of emotion from body language among patients with unipolar depression. Psychiatry Res 209:40–49CrossRefGoogle Scholar
  42. López R, Poy R, Patrick CJ, Moltó J (2013) Deficient fear conditioning and self-reported psychopathy: the role of fearless dominance. Psychophysiology 50:210–218CrossRefGoogle Scholar
  43. Mareck U et al (2010) Reporting and managing elevated testosterone/epitestosterone ratios—novel aspects after five years’ experience. Drug Test Anal 2:637–642CrossRefGoogle Scholar
  44. Menard CS, Harlan RE (1993) Up-regulation of androgen receptor immunoreactivity in the rat brain by androgenic-anabolic steroids. Brain Res 622:226–236CrossRefGoogle Scholar
  45. Michael RP, Clancy AN, Zumpe D (1995) Distribution of androgen receptor-like immunoreactivity in the brains of cynomolgus monkeys. J Neuroendocrinol 7:713–719CrossRefGoogle Scholar
  46. Miller KE, Hoffman JH, Barnes GM, Sabo D, Melnick MJ, Farrell MP (2005) Adolescent anabolic steroid use, gender, physical activity, and other problem behaviors. Subst Use Misuse 40:1637–1657CrossRefGoogle Scholar
  47. Oberlander JG, Henderson LP (2012) The Sturm und Drang of anabolic steroid use: angst, anxiety, and aggression. Trends Neurosci 35:382–392CrossRefGoogle Scholar
  48. Ochsner KN, Gross JJ (2008) Cognitive emotion regulation: insights from social cognitive and affective neuroscience. Curr Dir Psychol Sci 17:153–158CrossRefGoogle Scholar
  49. Okruszek Ł (2018) It is not just in faces! Processing of Emotion and Intention from Biological Motion in Psychiatric Disorders. Front Hum Neurosci 12:48CrossRefGoogle Scholar
  50. Olbert CM, Penn DL, Kern RS, Lee J, Horan WP, Reise SP, Ochsner KN, Marder SR, Green MF (2013) Adapting social neuroscience measures for schizophrenia clinical trials, part 3: fathoming external validity. Schizophr Bull 39:1211–1218CrossRefGoogle Scholar
  51. Oskui PM, French WJ, Herring MJ, Mayeda GS, Burstein S, Kloner RA (2013) Testosterone and the cardiovascular system: a comprehensive review of the clinical literature. J Am Heart Assoc 2:e000272CrossRefGoogle Scholar
  52. Osório FL, de Paula Cassis JM, Machado de Sousa JP, Poli-Neto O, Martín-Santos R (2018) Sex Hormones and Processing of Facial Expressions of Emotion: A Systematic Literature Review. Front Psychol 9:529CrossRefGoogle Scholar
  53. Pavlova MA (2011) Biological motion processing as a hallmark of social cognition. Cereb Cortex 22:981–995CrossRefGoogle Scholar
  54. Pechtel P, Pizzagalli DA (2011) Effects of early life stress on cognitive and affective function: an integrated review of human literature. Psychopharmacology 214:55–70CrossRefGoogle Scholar
  55. Piacentino D, Kotzalidis GD, del Casale A, Rosaria Aromatario M, Pomara C, Girardi P, Sani G (2015) Anabolic-androgenic steroid use and psychopathology in athletes. A systematic review. Curr Neuropharmacol 13:101–121CrossRefGoogle Scholar
  56. Pope HG Jr (1994) Psychiatric and medical effects of anabolic-androgenic steroid use. Arch Gen Psychiatry 51:375–382CrossRefGoogle Scholar
  57. Pope HG Jr, Kean J, Nash A, Kanayama G, Samuel DB, Bickel WK, Hudson JI (2010) A diagnostic interview module for anabolic-androgenic steroid dependence: preliminary evidence of reliability and validity. Exp Clin Psychopharmacol 18:203CrossRefGoogle Scholar
  58. Pope HG Jr, Wood RI, Rogol A, Nyberg F, Bowers L, Bhasin S (2013) Adverse health consequences of performance-enhancing drugs: an Endocrine Society scientific statement. Endocr Rev 35:341–375CrossRefGoogle Scholar
  59. Pope HG, Katz DL (1994) Psychiatric and medical effects of anabolic-androgenic steroid use: a controlled study of 160 athletes. Arch Gen Psychiatry 51:375–382CrossRefGoogle Scholar
  60. Pope H, Katz D (2003) Psychiatric effects of exogenous anabolic-androgenic steroids. In: Psychoneuroendocrinology: the scientific basis of clinical practice. American Psychiatric Press, Washington, DC, pp 331–358Google Scholar
  61. Puce A, Perrett D (2003) Electrophysiology and brain imaging of biological motion. Philos Trans R Soc B Biol Sci 358:435–445CrossRefGoogle Scholar
  62. Rockhold R (1993) Cardiovascular toxicity of anabolic steroids. Annu Rev Pharmacol Toxicol 33:497–520CrossRefGoogle Scholar
  63. Sagoe D, Pallesen S (2018) Androgen abuse epidemiology current opinion in endocrinology. Diabetes and Obesity 25:185–194Google Scholar
  64. Sagoe D, Molde H, Andreassen CS, Torsheim T, Pallesen S (2014) The global epidemiology of anabolic-androgenic steroid use: a meta-analysis and meta-regression analysis. Ann Epidemiol 24:383–398CrossRefGoogle Scholar
  65. Simerly R, Swanson L, Chang C, Muramatsu M (1990) Distribution of androgen and estrogen receptor mRNA-containing cells in the rat brain: an in situ hybridization study. J Comp Neurol 294:76–95CrossRefGoogle Scholar
  66. Su T-P, Pagliaro M, Schmidt PJ, Pickar D, Wolkowitz O, Rubinow DR (1993) Neuropsychiatric effects of anabolic steroids in male normal volunteers. J Am Med Assoc 269:2760–2760CrossRefGoogle Scholar
  67. Townshend JM, Duka T (2003) Mixed emotions: alcoholics’ impairments in the recognition of specific emotional facial expressions. Neuropsychologia 41:773–782CrossRefGoogle Scholar
  68. Van Honk J, Schutter DJ (2007) Testosterone reduces conscious detection of signals serving social correction: implications for antisocial behavior. Psychol Sci 18:663–667CrossRefGoogle Scholar
  69. Van Honk J, Tuiten A, Verbaten R, van den Hout M, Koppeschaar H, Thijssen J, de Haan E (1999) Correlations among salivary testosterone, mood, and selective attention to threat in humans. Horm Behav 36:17–24CrossRefGoogle Scholar
  70. van Honk J, Peper JS, Schutter DJ (2005) Testosterone reduces unconscious fear but not consciously experienced anxiety: implications for the disorders of fear and anxiety. Biol Psychiatry 58:218–225CrossRefGoogle Scholar
  71. Van Honk J, Schutter DJ, Bos PA, Kruijt A-W, Lentjes EG, Baron-Cohen S (2011) Testosterone administration impairs cognitive empathy in women depending on second-to-fourth digit ratio. Proc Natl Acad Sci 108:3448–3452CrossRefGoogle Scholar
  72. van Honk J, Bos PA, Terburg D, Heany S, Stein DJ (2015) Neuroendocrine models of social anxiety disorder. Dialogues Clin Neurosci 17:287Google Scholar
  73. Van Overwalle F (2009) Social cognition and the brain: a meta-analysis. Hum Brain Mapp 30:829–858CrossRefGoogle Scholar
  74. Vaskinn A, Sundet K, Østefjells T, Nymo K, Melle I, Ueland T (2016) Reading emotions from body movement: a generalized impairment in schizophrenia. Front Psychol 6:2058CrossRefGoogle Scholar
  75. Vaskinn A, Lagerberg TV, Bjella TD, Simonsen C, Andreassen OA, Ueland T, Sundet K (2017) Impairment in emotion perception from body movements in individuals with bipolar I and bipolar II disorder is associated with functional capacity. Int J Bipolar Disord 5:13CrossRefGoogle Scholar
  76. Veenema AH (2009) Early life stress, the development of aggression and neuroendocrine and neurobiological correlates: what can we learn from animal models? Front Neuroendocrinol 30:497–518CrossRefGoogle Scholar
  77. Verdejo-García A, Bechara A, Recknor EC, Perez-Garcia M (2006) Executive dysfunction in substance dependent individuals during drug use and abstinence: an examination of the behavioral, cognitive and emotional correlates of addiction. J Int Neuropsychol Soc 12:405–415Google Scholar
  78. WADA (2016) WADA Technical Document - TD2016EAAS. (W.1.E.). Accessed 08.12 2018
  79. Wechsler D (1999) Manual for the Wechsler abbreviated intelligence scale (WASI). The Psychological Corporation, San AntonioGoogle Scholar
  80. Welker KM, Gruber J, Mehta PH (2015) A positive affective neuroendocrinology approach to reward and behavioral dysregulation. Front Psychiatry 6:93CrossRefGoogle Scholar
  81. Westlye LT, Kaufmann T, Alnæs D, Hullstein IR, Bjørnebekk A (2017) Brain connectivity aberrations in anabolic-androgenic steroid users. Neuroimage Clin 13:62–69CrossRefGoogle Scholar
  82. Wood RI (2008) Anabolic–androgenic steroid dependence? Insights from animals and humans. Front Neuroendocrinol 29:490–506CrossRefGoogle Scholar
  83. Yildirim BO, Derksen JJ (2012) A review on the relationship between testosterone and life-course persistent antisocial behavior. Psychiatry Res 200:984–1010CrossRefGoogle Scholar
  84. Yovel G, O’Toole AJ (2016) Recognizing people in motion. Trends Cogn Sci 20:383–395CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.The Anabolic Androgenic Steroid Research Group, National Advisory Unit on Substance Use Disorder Treatment, the Division of Mental Health and AddictionOslo University HospitalOsloNorway
  2. 2.Department of Psychosocial ScienceUniversity of BergenBergenNorway
  3. 3.Norwegian Centre for Mental Disorders Research, KG Jebsen Centre for Psychosis Research, Division of Mental Health and AddictionOslo University HospitalOsloNorway
  4. 4.Department of PsychologyUniversity of OsloOsloNorway

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