Fetal testosterone influences sexually dimorphic gray matter in the human brain

Journal of Neuroscience

Volumn 32, Issue 2, 2012, Pages 674-680

  Lombardo, Michael V ^a   Ashwin, Emma ^a,b   Auyeung, Bonnie ^a   Chakrabarti, Bhismadev ^a,c   Taylor, Kevin ^d   Hackett, Gerald ^e   Bullmore, Edward T ^f   Baron Cohen, Simon ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b University of Bath   (United Kingdom)

^c UNIVERSITY OF READING   (United Kingdom)

^d ADDENBROOKE S HOSPITAL   (United Kingdom)

^e Rosie Maternity Hospital   (United Kingdom)

^f UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FETAL TESTOSTERONE; TESTOSTERONE; UNCLASSIFIED DRUG;

AMNION FLUID; AMYGDALOID NUCLEUS; ARTICLE; BRAIN REGION; CHILD; FEMALE; GRAY MATTER; HORMONE ACTION; HUMAN; HUMAN EXPERIMENT; HYPOTHALAMUS; MALE; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; ORBITAL CORTEX; PARIETAL OPERCULUM; PLANUM TEMPORALE; PRIORITY JOURNAL; RADIOIMMUNOASSAY; SCHOOL CHILD; SEX DIFFERENCE; SUPERIOR TEMPORAL SULCUS; TEMPOROPARIETAL JUNCTION; VOXEL BASED MORPHOMETRY;

BODY PATTERNING; BRAIN; CHILD; COHORT STUDIES; FEMALE; FETUS; FUNCTIONAL LATERALITY; HUMANS; MALE; SEX CHARACTERISTICS; SEX DIFFERENTIATION; TESTOSTERONE; TIME;

EID: 84855669393     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4389-11.2012     Document Type: Article

References (58)

1. Amunts K, Kedo O, Kindler M, Pieperhoff P, Mohlberg H, Shah NJ, Habel U, Schneider F, Zilles K (2005) Cytoarchitectonic mapping of the human amygdala, hippocampal region and entorhinal cortex: intersubject variability and probability maps. Anat Embryol (Berl) 210:343-352
2. Arnold AP (2009) The organizational-activational hypothesis as the foundation for a unified theory of sexual differentiation of all mammalian tissues. Horm Behav 55:570-578
3. Arnold AP, Breedlove SM (1985) Organizational and activational effects of sex steroids on brain and behavior: a reanalysis. Horm Behav 19:469-498
4. Ashburner J (2007) A fast diffeomorphic image registration algorithm. Neuroimage 38:95-113
5. Auyeung B, Baron-Cohen S, Ashwin E, Knickmeyer R, Taylor K, Hackett G (2009) Fetal testosterone and autistic traits. Br J Psychol 100:1-22
6. Auyeung B, Taylor K, Hackett G, Baron-Cohen S (2010) Foetal testosterone and autistic traits in 18 to 24-month-old children. Mol Autism 1:11.
7. Baron-Cohen S (2002) The extreme male brain theory of autism. Trends Cogn Sci 6:248-254
8. Baron-Cohen S, Lutchmaya S, Knickmeyer R (2004) Prenatal testosterone in mind. Cambridge: MIT.
9. Baron-Cohen S, Lombardo MV, Auyeung B, Ashwin E, Chakrabarti B, Knickmeyer R (2011) Why are autism spectrum conditions more prevalent in males? PLoS Biol 9:e1001081.
10. Bergman K, Glover V, Sarkar P, Abbott DH, O'Connor TG (2010) In utero cortisol and testosterone exposure and fear reactivity in infancy. Horm Behav 57:306-312
11. Brain Development Cooperative Group, Evans AC (2006) The NIH MRI study of normal brain development. Neuroimage 30:184-202
12. Catani M, Jones DK, ffytche DH (2005) Perisylvian language networks of the human brain. Ann Neurol 57:8-16
13. Chapman E, Baron-Cohen S, Auyeung B, Knickmeyer R, Taylor K, Hackett G (2006) Fetal testosterone and empathy: evidence from the empathy quotient (EQ) and the "reading the mind in the eyes" test. Soc Neurosci 1:135-148
14. Cooke BM, Tabibnia G, Breedlove SM (1999) A brain sexual dimorphism controlled by adult circulating androgens. Proc Natl Acad Sci U S A 96:7538-7540
15. Decety J, Lamm C (2007) The role of the right temporoparietal junction in social interaction: how low-level computational processes contribute to meta-cognition. Neuroscientist 13:580-593
16. De Vries GJ, Rissman EF, Simerly RB, Yang LY, Scordalakes EM, Auger CJ, Swain A, Lovell-Badge R, Burgoyne PS, Arnold AP (2002) A model system for study of sex chromosome effects on sexually dimorphic neural and behavioral traits. J Neurosci 22:9005-9014
17. Escobar JC, Carr BR (2011) The protein kinase a pathway regulates CYP17 expression and androgen production in the human placenta. J Clin Endocrinol Metab 96:2869-2873
18. Escobar JC, Patel SS, Beshay VE, Suzuki T, Carr BR (2011) The human placenta expresses CYP17 and generates androgens de novo. J Clin Endocrinol Metab 96:1385-1392
19. Forman SD, Cohen JD, Fitzgerald M, Eddy WF, Mintun MA, NollDC (1995) Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-size threshold. Magn Reson Med 33:636-647
20. Friston KJ (1997) Testing for anatomically specified regional effects. Hum Brain Mapp 5:133-136
21. Gervais H, Belin P, Boddaert N, Leboyer M, Coez A, Sfaello I, Barthe ́le ́my C, Brunelle F, Samson Y, Zilbovicius M (2004) Abnormal cortical voice processing in autism. Nat Neurosci 7:801-802
22. Geschwind N, Galaburda AM (1985) Cerebral lateralization: biological mechanisms, associations, and pathology. I. A hypothesis and a program for research. Arch Neurol 42:428-459
23. Good CD, Johnsrude I, Ashburner J, Henson RN, Friston KJ, Frackowiak RS (2001) Cerebral asymmetry and the effects of sex and handedness on brain structure: a voxel-based morphometric analysis of 465 normal adult human brains. Neuroimage 14:685-700
24. Good CD, Lawrence K, Thomas NS, Price CJ, Ashburner J, Friston KJ, Frackowiak RS, Oreland L, Skuse DH (2003) Dosage-sensitive X-linked locus influences the development of amygdala and orbitofrontal cortex, and fear recognition in humans. Brain 126:2431-2446
25. Grimshaw GM, Sitarenios G, Finegan JA (1995) Mental rotation at 7 years: relations with prenatal testosterone levels and spatial play experiences. Brain Cogn 29:85-100
26. Hines M (2004) Brain gender. New York: Oxford UP.
27. Jacobson CD, Csernus VJ, Shryne JE, Gorski RA (1981) The influence of gonadectomy, androgen exposure, or a gonadal graft in the neonatal rat on the volume of the sexually dimorphic nucleus of the preoptic area. J Neurosci 1:1142-1147
28. Klein A, Andersson J, Ardekani BA, Ashburner J, Avants B, Chiang MC, Christensen GE, Collins DL, Gee J, Hellier P, Song JH, Jenkinson M, Lepage C, Rueckert D, Thompson P, Vercauteren T, Woods RP, Mann JJ, Parsey RV (2009) Evaluation of 14 nonlinear deformation algorithms applied to human brain MRI registration. Neuroimage 46:786-802
29. Knickmeyer R, Baron-Cohen S, Raggatt P, Taylor K, Hackett G (2006) Fetal testosterone and empathy. Horm Behav 49:282-292
30. Lombardo MV, Chakrabarti B, Bullmore ET, Baron-Cohen S (2011) Specialization of right temporo-parietal junction for mentalizing and its association with social impairments in autism. Neuroimage 56:1832-1838
31. Lutchmaya S, Baron-Cohen S, Raggatt P (2002a) Foetal testosterone and vocabulary size in 18-and 24-month-old infants. Infant Behav Dev 24:418-424
32. Lutchmaya S, Baron-Cohen S, Raggatt P (2002b) Foetal testosterone and eye contact in 12-month-old human infants. Infant Behav Dev 25: 327-335
33. McCarthy MM, Arnold AP (2011) Reframing sexual differentiation of the brain. Nat Neurosci 14:677-683
34. McCarthy MM, Auger AP, Bale TL, De Vries GJ, Dunn GA, Forger NG, Murray EK, Nugent BM, Schwarz JM, Wilson ME (2009) The epigenetics of sex differences in the brain. J Neurosci 29:12815-12823
35. Moffitt TE, Caspi A, Rutter M, Silva PA (1998) Sex differences in antisocial behavior. Cambridge: Cambridge UP.
36. Nichols T, Brett M, Andersson J, Wager T, Poline JB (2005) Valid conjunction inference with the minimum statistic. Neuroimage 25:653-660
37. Nummenmaa L, Calder AJ (2009) Neural mechanisms of social attention. Trends Cogn Sci 13:135-143
38. Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97-113
39. Passamonti L, Fairchild G, Goodyer IM, Hurford G, Hagan CC, Rowe JB, Calder AJ (2010) Neural abnormalities in early-onset and adolescenceonset conduct disorder. Arch Gen Psychiatry 67:729-738
40. Paus T, Nawaz-Khan I, Leonard G, Perron M, Pike GB, Pitiot A, Richer L, Susman E, Veillette S, Pausova Z (2010) Sexual dimorphism in the adolescent brain: role of testosterone and androgen receptor in global and local volumes of grey and white matter. Horm Behav 57:63-75
41. Pelphrey KA, Morris JP, McCarthy G (2005) Neural basis of eye gaze processing deficits in autism. Brain 128:1038-1048
42. Phoenix CH, Goy RW, Gerall AA, Young WC (1959) Organizing action of prenatally administered testosterone propionate on the tissues mediating mating behavior in the female guinea pig. Endocrinology 65:369-382
43. Raine A, Yang Y, Narr KL, Toga AW (2011) Sex differences in orbitofrontal gray as a partial explanation for sex differences in antisocial personality. Mol Psychiatry 16:227-236
44. Raznahan A, Lee Y, Stidd R, Long R, Greenstein D, Clasen L, Addington A, Gogtay N, Rapoport JL, Giedd JN (2010) Longitudinally mapping the influence of sex and androgen signaling on the dynamics of human cortical maturation in adolescence. Proc Natl Acad Sci U S A 107:16988-16993
45. Redcay E, Courchesne E (2008) Deviant functional magnetic resonance imaging patterns of brain activity to speech in 2-3-year-old children with autism spectrum disorder. Biol Psychiatry 64:589-598
46. Reinius B, Jazin E (2009) Prenatal sex differences in the human brain. Mol Psychiatry 14:987-989
47. Rojas DC, Bawn SD, Benkers TL, Reite ML, Rogers SJ (2002) Smaller left hemisphere planum temporale in adults with autistic disorder. Neurosci Lett 328:237-240
48. Rutter M, Caspi A, Fergusson D, Horwood LJ, Goodman R, Maughan B, Moffitt TE, Meltzer H, Carroll J (2004) Sex differences in developmental reading disability: new findings from 4 epidemiological studies. JAMA 291:2007-2012
49. Sarkar P, Bergman K, Fisk NM, O'Connor TG, Glover V (2007) Amniotic fluid testosterone: relationship with cortisol and gestational age. Clin Endocrinol (Oxf) 67:743-747
50. Saxe R, Powell LJ (2006) It's the thought that counts: specific brain regions for one component of theory of mind. Psychol Sci 17:692-699
51. Shaywitz SE, Shaywitz BA, Pugh KR, Fulbright RK, Constable RT, Mencl WE, Shankweiler DP, Liberman AM, Skudlarski P, Fletcher JM, Katz L, Marchione KE, Lacadie C, Gatenby C, Gore JC (1998) Functional disruption in the organization of the brain for reading in dyslexia. Proc Natl Acad Sci U S A 95:2636-2641
52. Swaab DF, Fliers E (1985) Asexually dimorphic nucleus in the human brain. Science 228:1112-1115
53. Tardif CL, Collins DL, Pike GB (2010) Regional impact of field strength on voxel-based morphometry results. Hum Brain Mapp 31:943-957
54. van de Beek C, Thijssen JH, Cohen-Kettenis PT, van Goozen SH, Buitelaar JK (2004) Relationships between sex hormones assessed in amniotic fluid, and maternal and umbilical cord serum: what is the best source of information to investigate the effects of fetal hormonal exposure? Horm Behav 46:663-669
55. van Honk J, Schutter DJ, Bos PA, Kruijt AW, Lentjes EG, Baron-Cohen S (2011) Testosterone administration impairs cognitive empathy in women depending on second-to-fourth digit ratio. Proc Natl Acad Sci U S A 108:3448-3452
56. Wager TD, Keller MC, Lacey SC, Jonides J (2005) Increased sensitivity in neuroimaging analyses using robust regression. Neuroimage 26:99-113
57. Wilke M, Holland SK, Altaye M, Gaser C (2008) Template-O-matic: a toolbox for creating customized pediatric templates. Neuroimage 41:903-913
58. Worsley KJ, Marrett S, Neelin P, Vandal AC, Friston KJ, Evans AC (1996) A unified statistical approach for determining significant signals in images of cerebral activation. Hum Brain Mapp 4:58-73.