A quantitative and qualitative review of the effects of testosterone on the function and structure of the human social-emotional brain

Metabolic Brain Disease

Volumn 31, Issue 1, 2015, Pages 157-167

  Heany, Sarah J ^a   van Honk, Jack ^a,b,c   Stein, Dan J ^a   Brooks, Samantha J ^a,d  

^a UNIVERSITY OF CAPE TOWN   (South Africa)

^b UTRECHT UNIVERSITY   (Netherlands)

^c UNIVERSITY OF CAPE TOWN   (South Africa)

^d UPPSALA UNIVERSITY   (Sweden)

Author keywords

ALE; Amygdala; fMRI; Hippocampus; Testosterone; VBM

Indexed keywords

TESTOSTERONE;

AMYGDALA; ARTICLE; BRAIN FUNCTION; BRAIN REGION; BRAIN SIZE; BRAIN STEM; EMOTION; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GRAY MATTER; HUMAN; META ANALYSIS; NEUROANATOMY; NEUROIMAGING; PARAHIPPOCAMPAL GYRUS; QUALITATIVE ANALYSIS; QUANTITATIVE ANALYSIS; SEX DIFFERENCE; SOCIAL ASPECT; STRUCTURE ANALYSIS; SYLVIAN FISSURE; SYSTEMATIC REVIEW; TEMPORAL LOBE; VOXEL BASED MORPHOMETRY; ADULT; BRAIN; CHILD; DRUG EFFECTS; FEMALE; MALE; NUCLEAR MAGNETIC RESONANCE IMAGING; SOCIAL BEHAVIOR;

ADULT; BRAIN; CHILD; EMOTIONS; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; SOCIAL BEHAVIOR; TESTOSTERONE;

EID: 84930989089     PISSN: 08857490     EISSN: 15737365     Source Type: Journal    
DOI: 10.1007/s11011-015-9692-y     Document Type: Article

References (54)

1. Ackermann S, Spalek K, Rasch B, Gschwind L, Coynel D, Fastenrath M, Papassotiropoulos A, de Quervain DJ (2012) Testosterone levels in healthy men are related to amygdala reactivity and memory performance. Psychoneuroendocrinology 37:1417-1424
2. Batrinos ML (2012) The aging of the endocrine hypothalamus and its dependent endocrine glands. Horm (Athens) 11:241-253
3. Beyer F, Munte TF, Erdmann C, Kramer UM (2013). Emotional reactivity to threat modulates activity in mentalizing network during aggression. Soc Cogn Affect Neurosci 9:1552-1560
4. Bos PA, Hermans EJ, Montoya ER, Ramsey NF, van Honk J (2010) Testosterone administration modulates neural responses to crying infants in young females. Psychoneuroendocrinology 35:114-121
5. Bos PA, Hermans EJ, Ramsey NF, van Honk J (2012a) The neural mechanisms by which testosterone acts on interpersonal trust. NeuroImage 61:730-737
6. Bos PA, Panksepp J, Bluthe RM, van Honk J (2012b) Acute effects of steroid hormones and neuropeptides on human social-emotional behavior: a review of single administration studies. Front Neuroendocrinol 33:17-35
7. Bramen JE, Hranilovich JA, Dahl RE, Chen J, Rosso C, Forbes EE, Dinov ID, Worthman CM, Sowell ER (2012) Sex matters during adolescence: testosterone-related cortical thickness maturation differs between boys and girls. PLoS One 7:e33850
8. Bramen JE, Hranilovich JA, Dahl RE, Forbes EE, Chen J, Toga AW, Dinov ID, Worthman CM, Sowell ER (2011) Puberty influences medial temporal lobe and cortical gray matter maturation differently in boys than girls matched for sexual maturity. Cereb Cortex 21: 636-646
9. Brooks SJ, Cedernaes J, Sciöth HB (2013) Increased prefrontal and parahippocampal activation with reduced dorsolateral prefrontal and insular cortex activation to food images in obesity: a metaanalysis of fMRI studies. PLoS One 8:e60393
10. Brooks SJ, Savov V, Allzén E, Benedict C, Fredriksson R, Sciöth HB (2012) Exposure to subliminal arousing stimuli induces robust activation in the amygdala, hippocampus, anterior cingulate, insular cortex and primary visual cortex: a systematic meta-analysis of fMRI studies. NeuroImage 58:2962-2973
11. Choi JC, Yi DJ, Han BS, Lee PH, Kim JH, Kim BH (2011) Placebo effects on analgesia related to testosterone and premotor activation. Neuroreport 22:419-423
12. Chura LR, Lombardo MV, Ashwin E, Auyeung B, Chakrabarti B, Bullmore ET, Baron-Cohen S (2010) Organizational effects of fetal testosterone on human corpus callosum size and asymmetry. Psychoneuroendocrinology 35:122-132
13. Costafreda SG, Brammer MJ, David AS, Fu CH (2008) Predictors of amygdala activation during the processing of emotional stimuli: a meta-analysis of 385 PETand fMRI studies. Brain Res Rev 58:57-70
14. Dabbs JM Jr, Frady RL, Carr TS, Besch NF (1987) Saliva testosterone and criminal violence in young adult prison inmates. Psychosom Med 49, 174-182
15. Denson TF, Ronay R, von Hippel W, Schira MM (2013) Endogenous testosterone and cortisol modulate neural responses during induced anger control. Soc Neurosci 8:165-177
16. Eickhoff SB, Bzdok D, Laird AR, Kurth F, Fox PT (2012) Activation likelihood estimation meta-analysis revisited. NeuroImage 59: 2349-2361
17. Eickhoff SB, Stephan KE, Mohlberg H, Grefkes C, Fink GR, Amunts K, Zilles K (2005) A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. NeuroImage 25:1325-1335
18. Eisenegger C, Naef M, Snozzi R, Heinrichs M, Fehr E (2010) Prejudice and truth about the effect of testosterone on human bargaining behaviour. Nature 463:356-359
19. Hattingh CJ, Ipser J, Tromp SA, Syal S, Lochner C, Brooks SJ, Stein DJ (2013) Functional magnetic resonance imaging during emotion recognition in social anxiety disorder: an activation likelihood metaanalysis. Front Hum Neurosci 6:347
20. Hermans EJ, Bos PA, Ossewaarde L, Ramsey NF, Fernández G, van Honk J (2010) Effects of exogenous testosterone on the ventral striatal BOLD response during reward anticipation in healthy women. NeuroImage 52:277-283
21. 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 63:263-270
22. Herve PY, Leonard G, Perron M, Pike B, Pitiot A, Richer L, Veillette S, Pausova Z, Paus T (2009) Handedness, motor skills and maturation of the corticospinal tract in the adolescent brain. Hum Brain Mapp 30:3151-3162
23. Höfer P, Lanzenberger R, Kasper S (2013) Testosterone in the brain: neuroimaging findings and the potential role for neuropsychopharmacology. Eur Neuropsychopharmacol 23:79-88
24. Isidori AM, Giannetta E, Gianfrilli D, Greco EA, Bonifacio V, Aversa A, Isidori A, Fabbri A, Lenzi A (2005) Effects of testosterone on sexual function in men: results of a meta-analysis. Clin Endocrinol 63:381-394
25. Kallai J, Csatho A, Kover F, Makany T, Nemes J, Horvath K, Kovacs N, Manning JT, Nadel L, Nagy F (2005) MRI-assessed volume of left and right hippocampi in females correlates with the relative length of the second and fourth fingers (the 2D:4D ratio). Psychiatry Res 140: 199-210
26. Kuo PX, Carp J, Light KC, Grewen KM (2012) Neural responses to infants linked with behavioral interactions and testosterone in fathers. Biol Psychol 91:302-306
27. Lentini E, Kasahara M, Arver S, Savic I (2013) Sex differences in the human brain and the impact of sex chromosomes and sex hormones. Cereb Cortex 23:2322-2336
28. Lessov-Schlaggar CN, Reed T, Swan GE, Krasnow RE, DeCarli C, Marcus R, Holloway L, Wolf PA, Carmelli D (2005) Association of sex steroid hormones with brain morphology and cognition in healthy elderly men. Neurology 65:1591-1596
29. Lombardo MV, Ashwin E, Auyeung B, Chakrabarti B, Lai MC, Taylor K, Hackett G, Bullmore ET, Baron-Cohen S (2012) Fetal programming effects of testosterone on the reward systemand behavioral approach tendencies in humans. Biol Psychiatry 72:839-847
30. Manuck SB, Marsland AL, Flory JD, Gorka A, Ferrell RE, Hariri AR (2010) Salivary testosterone and a trinucleotide (CAG) length polymorphism in the androgen receptor gene predict amygdala reactivity in men. Psychoneuroendocrinology 35:94-104
31. Mehta PH, Beer J (2010) Neural mechanisms of the testosteroneaggression relation: the role of orbitofrontal cortex. J Cogn Neurosci 22:2357-2368
32. Moffat SD, Hampson E, Wickett JC, Vernon PA, Lee DH (1997) Testosterone is correlated with regional morphology of the human corpus callosum. Brain Res 767:297-304
33. Montoya ER, Terburg D, Bos PA, van Honk J (2012) Testosterone, cortisol, and serotonin as key regulators of social aggression: a review and theoretical perspective. Motiv Emot 36:65-73
34. Mueller SC, Merke DP, Leschek EW, Fromm S, Grillon C, Cornwell BR, VanRyzin C, Ernst M (2011a) Grey matter volume correlates with virtual water maze task performance in boys with androgen excess. Neuroscience 197:225-232
35. Mueller SC, Merke DP, Leschek EW, Fromm S, VanRyzin C, Ernst M (2011b) Increased medial temporal lobe and striatal grey-matter volume in a rare disorder of androgen excess: a voxel-based morphometry (VBM) study. Int J Neuropsychopharmacol 14:445-457
36. Neufang S, Specht K, Hausmann M, Gunturkun O, Herpertz-Dahlmann B, Fink GR, Konrad K (2009) Sex differences and the impact of steroid hormones on the developing human brain. Cereb Cortex 19: 464-473
37. Panksepp J, Biven L (2012) The archaeology of mind: neuroevolutionary origins of human emotions (Norton series on interpersonal neurobiology). WW Norton & Company
38. Patwardhan AJ, Eliez S, Bender B, Linden MG, Reiss AL (2000) Brain morphology in Klinefelter syndrome: extra X chromosome and testosterone supplementation. Neurology 54:2218-2223
39. Peper JS, Brouwer RM, Schnack HG, van Baal GC, van Leeuwen M, van den Berg SM, Delemarre-Van deWaal HA, Boomsma DI, Kahn RS, HulshoffPol HE (2009a) Sex steroids and brain structure in pubertal boys and girls. Psychoneuroendocrinology 34:332-342
40. Peper JS, Brouwer RM, van Baal GC, Schnack HG, van Leeuwen M, Boomsma DI, Kahn RS, HulshoffPol HE (2009b) Does having a twin brother make for a bigger brain? Eur J Endocrinol 160:739-746
41. Schulkin J, Gold PW, McEwen BS (1998) Induction of corticotropinreleasing hormone gene expression by glucocorticoids: implication for understanding the states of fear and anxiety and allostatic load. Psychoneuroendocrinology 23:219-243
42. Sergerie K, Chochol C, Armony JL (2008) The role of the amygdala in emotional processing: a quantitative meta-analysis of functional neuroimaging studies. Neurosci Biobehav Rev 32:811-830
43. Stanton SJ, Wirth MM, Waugh CE, Schultheiss OC (2009) Endogenous testosterone levels are associated with amygdala and ventromedial prefrontal cortex responses to anger faces in men but not women. Biol Psychol 81:118-122
44. Struber D, Luck M, Roth G (2008) Sex, aggression and impulse control: an integrative account. Neurocase 14:93-121
45. Swanson LW, Petrovich GD (1998) What is the amygdala? Trends Neurosci 21:323-331
46. Terburg D, van Honk J (2013) Approach-avoidance versus dominancesubmissiveness: a multi-level neural framework on how testosterone promotes social status. Emot Rev 5:296-302
47. Tuiten A, Van Honk J, Koppeschaar H, Bernaards C, Thijssen J, Verbaten R (2000) Time course of effects of testosterone administration on sexual arousal in women. Arch Gen Psychiatry 57:149-153 discussion 155-146
48. van der Westhuizen D, Solms M (2015) Social dominance and the affective neuroscience personality scales. Conscious Cogn 33:90-111
49. van Honk J, Montoya ER, Bos PA, van Vugt M, Terburg D (2012) New evidence on testosterone and cooperation. Nature 485:E4-E5 discussion E5-6
50. van Wingen G, Mattern C, Verkes RJ, Buitelaar J, Fernandez G (2008) Testosterone biases automatic memory processes in women towards potential mates. NeuroImage 43:114-120
51. van Wingen GA, Zylicz SA, Pieters S, Mattern C, Verkes RJ, Buitelaar JK, Fernandez G (2009) Testosterone increases amygdala reactivity in middle-aged women to a young adulthood level. Neuropsychopharmacology 34:539-547
52. Vincent K, Warnaby C, Stagg CJ, Moore J, Kennedy S, Tracey I (2013) Brain imaging reveals that engagement of descending inhibitory pain pathways in healthy women in a low endogenous estradiol state varies with testosterone. Pain 154:515-524
53. Volman I, Toni I, Verhagen L, Roelofs K (2011) Endogenous testosterone modulates prefrontal-amygdala connectivity during social emotional behavior. Cereb Cortex 21:2282-2290
54. Witte AV, Savli M, Holik A, Kasper S, Lanzenberger R (2010) Regional sex differences in grey matter volume are associated with sex hormones in the young adult human brain. NeuroImage 49:1205-1212