Sex Differences in White Matter Microstructure in the Human Brain Predominantly Reflect Differences in Sex Hormone Exposure

Cerebral Cortex

Volumn 27, Issue 5, 2017, Pages 2994-3001

  Van Hemmen, J ^a,b   Saris, I M J ^c   Cohen Kettenis, P T ^b   Veltman, D J ^b   Pouwels, P J W ^b   Bakker, J ^a,b,d  

^a NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^c VU University Medical Center ^*  (Netherlands)

^d UNIVERSITY OF LIÈGE   (Belgium)

Author keywords

Androgens; CAIS; DTI; Sexual differentiation, white matter

Indexed keywords

SEX HORMONE;

ADULT; ARTICLE; COMPLETE ANDROGEN INSENSITIVITY SYNDROME; DIFFUSION TENSOR IMAGING; FEMALE; FRACTIONAL ANISOTROPY; HUMAN; KARYOTYPE 46,XX; KARYOTYPE 46,XY; MAJOR CLINICAL STUDY; MALE; MICROMORPHOLOGY; NEUROANATOMY; PRIORITY JOURNAL; SEX CHROMOSOME; SEX DIFFERENCE; WHITE MATTER; ADOLESCENT; ANDROGEN INSENSITIVITY SYNDROME; ANISOTROPY; BRAIN MAPPING; DIAGNOSTIC IMAGING; DRUG EFFECTS; IMAGE PROCESSING; NONPARAMETRIC TEST; PATHOLOGY; SEXUAL CHARACTERISTICS; XY GONADAL DYSGENESIS; YOUNG ADULT;

ADOLESCENT; ADULT; ANDROGEN-INSENSITIVITY SYNDROME; ANISOTROPY; BRAIN MAPPING; DIFFUSION TENSOR IMAGING; FEMALE; GONADAL DYSGENESIS, 46,XY; GONADAL STEROID HORMONES; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MALE; SEX CHARACTERISTICS; STATISTICS, NONPARAMETRIC; WHITE MATTER; YOUNG ADULT;

EID: 85019152743     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhw156     Document Type: Article

References (50)

1. Basser PJ, Mattiello J, LeBihan D. (1994). MR diffusion tensor spectroscopy and imaging. Biophys J. 66: 259-267.
2. Baum M. (1979). Differentiation of coital behavior in mammals: a comparative analysis. Neurosci Biobehav Rev. 3: 265-284.
3. Baum MJ. (2006). Mammalian animal models of psychosexual differentiation: when is translation to the human situation possible?. Horm Behav. 50: 579-588.
4. Brock O, Baum MJ, Bakker J. (2011). The development of female sexual behavior requires prepubertal estradiol. J Neurosci. 31: 5574-5578.
5. Chou K-H, Cheng Y, Chen I-Y, Lin C-P, Chu W-C. (2011). Sex-linked white matter microstructure of the social and analytic brain. NeuroImage. 54: 725-733.
6. Cohen-Bendahan CCC, Van De Beek C, Berenbaum SA. (2005). Prenatal sex hormone effects on child and adult sex-Typed behavior: methods and findings. Neurosci Biobehav Rev. 29: 353-384.
7. DeLisi LE, Maurizio AM, Svetina C, Ardekani B, Szulc K, Nierenberg J, Leonard J, Harvey PD. (2005). Klinefelter s syndrome (XXY) as a genetic model for psychotic disorders. Am J Med Genet B Neuropsychiatr Genet. 135B: 15-23.
8. Den Braber A, Van t Ent D, Stoffers D, Linkenkaer-Hansen K, Boomsma DI, De Geus EJC. (2013). Sex differences in gray and white matter structure in age-matched unrelated males and females and opposite-sex siblings. Int J Psychol Res. 6: 7-21.
9. Doehnert U, Bertelloni S, Werner R, Dati E, Hiort O. (2015). Characteristic features of reproductive hormone profiles in late adolescent and adult females with complete androgen insensitivity syndrome. Sex Dev. 9: 69-74.
10. Hamann S, Stevens J, Vick JH, Bryk K, Quigley CA, Berenbaum SA, Wallen K. (2014). Brain responses to sexual images in 46, XY women with complete androgen insensitivity syndrome are female-Typical. Horm Behav. 66: 724-730.
11. Herting MM, Maxwell EC, Irvine C, Nagel BJ. (2011). The impact of sex, puberty, and hormones on white matter microstructure in adolescents. Cereb Cortex. 22: 1979-1992.
12. Hines M, Ahmed SF, Hughes IA. (2003). Psychological outcomes and gender-related development in complete androgen insensitivity syndrome. Arch Sex Behav. 32: 93-101.
13. Holzapfel M, Barnea-Goraly N, Eckert MA, Kesler SR, Reiss AL. (2006). Selective alterations of white matter associated with visuospatial and sensorimotor dysfunction in Turner syndrome. J Neurosci. 26: 7007-7013.
14. Hong DS, Reiss AL. (2014). Cognitive and neurological aspects of sex chromosome aneuploidies. Lancet Neurol. 13: 306-318.
15. Hughes IA, Davies JD, Bunch TI, Pasterski V, Mastroyannopoulou K, MacDougall J. (2012). Androgen insensitivity syndrome. Lancet. 380: 1419-1428.
16. Inano S, Takao H, Hayashi N, Abe O, Ohtomo K. (2011). Effects of age and gender on white matter integrity. AJNR Am J Neuroradiol. 32: 2103-2109.
17. Jones DK, Knösche TR, Turner R. (2013). White matter integrity, fiber count, and other fallacies: the do s and don ts of diffusion MRI. NeuroImage. 73: 239-254.
18. Kanaan RA, Chaddock C, Allin M, Picchioni MM, Daly E, Shergill SS, McGuire PK. (2014). Gender influence on white matter microstructure: a tract-based spatial statistics analysis. PLoS One. 9: e91109.
19. Kranz GS, Hahn A, Kaufmann U, Küblböck M, Hummer A, Ganger S, Seiger R, Winkler D, Swaab DF, Windischberger C, et al. (2014). White matter microstructure in transsexuals and controls investigated by diffusion tensor imaging. J Neurosci. 34: 15466-15475.
20. Lombardo MV, Ashwin E, Auyeung B, Chakrabarti B, Taylor K, Hackett G, Bullmore ET, Baron-Cohen S. (2012). Fetal testosterone influences sexually dimorphic gray matter in the human brain. J Neurosci. 32: 674-680.
21. Masica DN, Money J, Ehrhardt AA. (1971). Fetal feminization and female gender identity in the testicular feminizing syndrome of androgen insensitivity. Arch Sex Behav. 1: 131-142.
22. McCarthy MM, Arnold AP. (2011). Reframing sexual differentiation of the brain. Nat Neurosci. 14: 677-683.
23. Melo KFS, Mendonca BB, Billerbeck AEC, Costa EMF, Inácio M, Silva FAQ, Leal AMO, Latronico AC, Arnhold IJP. (2003). Clinical, hormonal, behavioral, and genetic characteristics of androgen insensitivity syndrome in a Brazilian cohort: five novel mutations in the androgen receptor gene. J Clin Endocrinol Metab. 88: 3241-3250.
24. Menzler K, Belke M, Wehrmann E, Krakow K, Lengler U, Jansen A, Hamer HM, Oertel WH, Rosenow F, Knake S. (2011). Men and women are different: diffusion tensor imaging reveals sexual dimorphism in the microstructure of the thalamus, corpus callosum and cingulum. NeuroImage. 54: 2557-2562.
25. Molko N, Cachia A, Riviere D, Mangin JF, Bruandet M, LeBihan D, Cohen L, Dehaene S. (2004). Brain anatomy in Turner syndrome: evidence for impaired social and spatial-numerical networks. Cereb Cortex. 14: 840-850.
26. Mueller SC, Merke DP, Leschek EW, Fromm S, VanRyzin C, Ernst M. (2011). 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.
27. Mueller SC, Verwilst T, Van Branteghem A, T Sjoen G, Cools M. (2016). The contribution of the androgen receptor (AR) in human spatial learning and memory: a study in women with complete androgen insensitivity syndrome (CAIS). Horm Behav. 78: 121-126.
28. Oakes MB, Eyvazzadeh AD, Quint E, Smith YR. (2008). Complete androgen insensitivity syndrome-A review. J Pediatr Adolesc Gynecol. 21: 305-310.
29. Peper JS, Mandl RCW, Braams BR, de Water E, Heijboer AC, Koolschijn PCMP, Crone EA. (2013). Delay discounting and frontostriatal fiber tracts: a combined DTI and MTR study on impulsive choices in healthy young adults. Cereb Cortex. 23: 1695-1702.
30. Perrin JS, Hervé P-Y, Leonard G, Perron M, Pike GB, Pitiot A, Richer L, Veillette S, Pausova Z, Paus T. (2008). Growth of white matter in the adolescent brain: role of testosterone and androgen receptor. J Neurosci. 28: 9519-9524.
31. 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.
32. Pierpaoli C, Basser PJ. (1996). Toward a quantitative assessment of diffusion anisotropy. Magn Reson Med. 36: 893-906.
33. Rametti G, Carrillo B, Gomez-Gil E, Junque C, Segovia S, Gomez Á, Guillamon A. (2011). White matter microstructure in female to male transsexuals before cross-sex hormonal treatment. A diffusion tensor imaging study. J Psychiatr Res. 45: 199-204.
34. Ruigrok ANV, Salimi-Khorshidi G, Lai M-C, Baron-Cohen S, Lombardo MV, Tait RJ, Suckling J. (2014). A meta-Analysis of sex differences in human brain structure. Neurosci Biobehav Rev. 39: 34-50.
35. Sarkey S, Azcoitia I, Garcia-Segura LM, Garcia-Ovejero D, DonCarlos LL. (2008). Classical androgen receptors in nonclassical sites in the brain. Horm Behav. 53: 753-764.
36. Savic I. (2012). Advances in research on the neurological and neuropsychiatric phenotype of Klinefelter syndrome. Curr Opin Neurol. 25: 138-143.
37. Schoonheim MM, Vigeveno RM, Rueda Lopes FC, Pouwels PJW, Polman CH, Barkhof F, Geurts JJG. (2014). Sex-specific extent and severity of white matter damage in multiple sclerosis: implications for cognitive decline. HumBrainMapp. 35: 2348-2358.
38. Schulz KM, Molenda-Figueira HA, Sisk CL. (2009). Back to the future: the organizational-Activational hypothesis adapted to puberty and adolescence. Horm Behav. 55: 597-604.
39. Sisk CL, Zehr JL. (2005). Pubertal hormones organize the adolescent brain and behavior. Front Neuroendocrinol. 26: 163-174.
40. Smith SM, Jenkinson M, Johansen-Berg H, Rueckert D, Nichols TE, Mackay CE, Watkins KE, Ciccarelli O, Cader MZ, Matthews PM, et al. (2006). Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. NeuroImage. 31: 1487-1505.
41. Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TE, Johansen-Berg H, Bannister PR, De Luca M, Drobnjak I, Flitney DE, et al. (2004). Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage. 23(Suppl 1): S208-S219.
42. Smith SM, Nichols TE. (2009). Threshold-free cluster enhancement: addressing problems ofsmoothing, threshold dependence and localisation in cluster inference. NeuroImage. 44: 83-98.
43. Takao H, Hayashi N, Ohtomo K. (2014). Sex dimorphism in the white matter: fractional anisotropy and brain size. J Magn Reson Imaging. 39: 917-923.
44. van Hemmen J, Veltman DJ, Hoekzema E, Cohen-Kettenis PT, Dessens AB, Bakker J. (2016). Neural activation during mental rotation in complete androgen insensitivity syndrome: the influence of sex hormones and sex chromosomes. Cereb Cortex. 26: 1036-1045.
45. van Strien JW. (1992). Classificatie van links- en rechtshandige proefpersonen [Classification of left-handed and righthanded test subjects]. Ned Tijdschr Psychol. 47: 88-92.
46. Villalon-Reina J, Jahanshad N, Beaton E, Toga AW, Thompson PM, Simon TJ. (2013). White matter microstructural abnormalities in girls with chromosome 22q11.2 deletion syndrome, Fragile X or Turner syndrome as evidenced by diffusion tensor imaging. NeuroImage. 81: 441-454.
47. Wallen K. (2005). Hormonal influences on sexually differentiated behavior in nonhuman primates. Front Neuroendocrinol. 26: 7-26.
48. Winkler AM, Ridgway GR, Webster MA, Smith SM, Nichols TE. (2014). Permutation inference for the general linear model. NeuroImage. 92: 381-397.
49. Wisniewski AB, Migeon CJ, Meyer-Bahlburg HF, Gearhart JP, Berkovitz GD, Brown TR, Money J. (2000). Complete androgen insensitivity syndrome: long-Term medical, surgical, and psychosexual outcome. J Clin Endocrinol Metab. 85: 2664-2669.
50. Yamagata B, Barnea-Goraly N, Marzelli MJ, Park Y, Hong DS, Mimura M, Reiss AL. (2012). White matter aberrations in prepubertal estrogen-naive girls with monosomic Turner syndrome. Cereb Cortex. 22: 2761-2768.