Longitudinally mapping the influence of sex and androgen signaling on the dynamics of human cortical maturation in adolescence

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 39, 2010, Pages 16988-16993

  Raznahan, Armin ^a,b   Lee, Yohan ^a   Stidd, Reva ^a   Long, Robert ^a   Greenstein, Dede ^a   Clasen, Liv ^a   Addington, Anjene ^a   Gogtay, Nitin ^a   Rapoport, Judith L ^a   Giedd, Jay N ^a  

^a NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^b KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Androgen receptor; Brain; Cortex; Development; Sex differences

Indexed keywords

ANDROGEN RECEPTOR; ANDROGEN;

ADOLESCENCE; ADOLESCENT; ADULT; ALLELE; ARTICLE; BRAIN CORTEX; BRAIN DEVELOPMENT; BRAIN REGION; CHILD; COGNITION; DEVELOPMENTAL STAGE; FEMALE; HUMAN; MALE; NEUROIMAGING; PRIORITY JOURNAL; SCHOOL CHILD; SEX DIFFERENCE; ADOLESCENT BEHAVIOR; ADOLESCENT DEVELOPMENT; ANATOMY AND HISTOLOGY; ANIMAL; BRAIN MAPPING; GENETIC VARIABILITY; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; SEXUAL DEVELOPMENT; SIGNAL TRANSDUCTION;

RODENTIA;

ADOLESCENT; ADOLESCENT BEHAVIOR; ADOLESCENT DEVELOPMENT; ANDROGENS; ANIMALS; BRAIN MAPPING; CEREBRAL CORTEX; FEMALE; GENETIC VARIATION; HUMANS; MALE; RECEPTORS, ANDROGEN; SEX CHARACTERISTICS; SEX FACTORS; SIGNAL TRANSDUCTION;

EID: 78049277844     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1006025107     Document Type: Article

References (53)

1. Forum on Child and Family Statistics (2009) America's Children: Key National Indicators of Well-Being (US Government Printing Office, Washington, DC).
2. Green HM, Meltzer A, Ford H, Goodman TR (2004) Mental Health of Children and Young People in Great Britain, 2004 (Palgrave Macmillan, Baskingstoke, UK).
3. Halpern DF (2000) Sex Differences in Cognitive Abilities (Lawrence Erlbaum, Mahwah, NJ), 3rd Ed.
4. Stokes SF, Klee T (2009) Factors that influence vocabulary development in two-year-old children. J Child Psychol Psychiatry 50:498-505.
5. Voyer D, Voyer S, Bryden MP (1995) Magnitude of sex differences in spatial abilities: A meta-analysis and consideration of critical variables. Psychol Bull 117:250-270.
6. Machin S, Pekkarinen T (2008) Assessment. Global sex differences in test score variability. Science 322:1331-1332.
7. Hines M (2008) Early androgen influences on human neural and behavioural development. Early Hum Dev 84:805-807.
8. Aristotle (1862) History of Animals, trans Cresswell R (Henry G Bohn, London).
9. Morris JA, Jordan CL, Breedlove SM (2004) Sexual differentiation of the vertebrate nervous system. Nat Neurosci 7:1034-1039. (Pubitemid 41184441)
10. Wallen K (2005) Hormonal influences on sexually differentiated behavior in nonhuman primates. Front Neuroendocrinol 26:7-26.
11. Clark AS, MacLusky NJ, Goldman-Rakic PS (1988) Androgen binding and metabolism in the cerebral cortex of the developing rhesus monkey. Endocrinology 123:932-940.
12. Zuloaga DG, Puts DA, Jordan CL, Breedlove SM (2008) The role of androgen receptors in the masculinization of brain and behavior: What we've learned from the testicular feminization mutation. Horm Behav 53:613-626.
13. van Wingen G, Mattern C, Verkes RJ, Buitelaar J, Fernández G (2010) Testosterone reduces amygdala-orbitofrontal cortex coupling. Psychoneuroendocrinology 35:105-113.
14. T'Sjoen G, et al. (2010) Male gender identity in complete androgen insensitivity syndrome. Arch Sex Behav, 10.1007/s10508-010-9624-1.
15. Wisniewski AB, et al. (2000) Complete androgen insensitivity syndrome: Long-term medical, surgical, and psychosexual outcome. J Clin Endocrinol Metab 85:2664-2669.
16. Imperato-McGinley J, Pichardo M, Gautier T, Voyer D, Bryden MP (1991) Cognitive abilities in androgen-insensitive subjects: Comparison with control males and females from the same kindred. Clin Endocrinol (Oxf) 34:341-347.
17. Gogtay N, et al. (2004) Dynamic mapping of human cortical development during childhood through early adulthood. Proc Natl Acad Sci USA 101:8174-8179. (Pubitemid 38698073)
18. Lenroot RK, et al. (2007) Sexual dimorphism of brain developmental trajectories during childhood and adolescence. Neuroimage 36:1065-1073.
19. Brambilla DJ, O'Donnell AB, Matsumoto AM, McKinlay JB (2007) Intraindividual variation in levels of serum testosterone and other reproductive and adrenal hormones in men. Clin Endocrinol (Oxf) 67:853-862.
20. Neufang S, et al. (2009) Sex differences and the impact of steroid hormones on the developing human brain. Cereb Cortex 19:464-473.
21. 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.
22. Peper JS, et al. (2009) Sex steroids and brain structure in pubertal boys and girls. Psychoneuroendocrinology 34:332-342.
23. Perrin JS, et al. (2008) Growth of white matter in the adolescent brain: Role of testosterone and androgen receptor. J Neurosci 28:9519-9524.
24. Paus T, et al. (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.
25. Lerch JP, Evans AC (2005) Cortical thickness analysis examined through power analysis and a population simulation. Neuroimage 24:163-173.
26. Shaw P, et al. (2008) Neurodevelopmental trajectories of the human cerebral cortex. J Neurosci 28:3586-3594.
27. Buchanan G, et al. (2004) Structural and functional consequences of glutamine tract variation in the androgen receptor. Hum Mol Genet 13:1677-1692. (Pubitemid 39173438)
28. Chamberlain NL, Driver ED, Miesfeld RL (1994) The length and location of CAG trinucleotide repeats in the androgen receptor N-terminal domain affect transactivation function. Nucleic Acids Res 22:3181-3186.
29. Irvine RA, et al. (2000) Inhibition of p160-mediated coactivation with increasing androgen receptor polyglutamine length. Hum Mol Genet 9:267-274.
30. Tut TG, Ghadessy FJ, Trifiro MA, Pinsky L, Yong EL (1997) Long polyglutamine tracts in the androgen receptor are associated with reduced trans-activation, impaired sperm production, and male infertility. J Clin Endocrinol Metab 82:3777-3782. (Pubitemid 27509371)
31. Kazemi-Esfarjani P, Trifiro MA, Pinsky L (1995) Evidence for a repressive function of the long polyglutamine tract in the human androgen receptor: possible pathogenetic relevance for the (CAG)n-expanded neuronopathies. Hum Mol Genet 4:523-527.
32. Albertelli MA, Scheller A, Brogley M, Robins DM (2006) Replacing the mouse androgen receptor with human alleles demonstrates glutamine tract length-dependent effects on physiology and tumorigenesis in mice. Mol Endocrinol 20:1248-1260. (Pubitemid 43801229)
33. Zitzmann M (2009) The role of the CAG repeat androgen receptor polymorphism in andrology. Front Horm Res 37:52-61.
34. Van Nieuwerburgh F, et al. (2008) Shorter CAG repeats in the androgen receptor gene may enhance hyperandrogenicity in polycystic ovary syndrome. Gynecol Endocrinol 24:669-673.
35. Ferk P, Perme MP, Teran N, Gersak K (2008) Androgen receptor gene (CAG)n polymorphism in patients with polycystic ovary syndrome. Fertil Steril 90:860-863.
36. Westberg L, Eriksson E (2008) Sex steroid-related candidate genes in psychiatric disorders. J Psychiatry Neurosci 33:319-330. (Pubitemid 351977158)
37. Lyon MF (1961) Gene action in the X-chromosome of the mouse (Mus musculus L.). Nature 190:372-373.
38. Im K, et al. (2008) Brain size and cortical structure in the adult human brain. Cereb Cortex 18:2181-2191.
39. Galvan A, et al. (2006) Earlier development of the accumbens relative to orbitofrontal cortex might underlie risk-taking behavior in adolescents. J Neurosci 26:6885-6892. (Pubitemid 44315249)
40. Steinberg L (2005) Cognitive and affective development in adolescence. Trends Cogn Sci 9:69-75.
41. Yang Y, Raine A (2009) Prefrontal structural and functional brain imaging findings in antisocial, violent, and psychopathic individuals: Ameta-analysis. Psychiatry Res 174:81-88.
42. Zacks JM (2008) Neuroimaging studies of mental rotation: A meta-analysis and review. J Cogn Neurosci 20:1-19.
43. Christakou A, et al. (2009) Sex-dependent age modulation of frontostriatal and temporo-parietal activation during cognitive control. Neuroimage 48:223-236.
44. Lenroot RK, Giedd JN(2010) Sex differences in the adolescent brain. Brain Cogn 72:46-55.
45. Fernández-Guasti A, Kruijver FP, Fodor M, Swaab DF (2000) Sex differences in the distribution of androgen receptors in the human hypothalamus. J Comp Neurol 425: 422-435. (Pubitemid 30659207)
46. Garcés C, et al. (2008) Hormone levels in 12- to 15-year-old boys and girls in Spain and their relationship with anthropometric variables. Clin Biochem 41:621-624.
47. Garagorri JM, et al. (2008) Reference levels for 17-hydroxyprogesterone, 11- desoxycortisol, cortisol, testosterone, dehydroepiandrosterone sulfate and androstenedione in infants from birth to six months of age. Eur J Pediatr 167:647-653.
48. Giedd JN, et al. (1999) Brain development during childhood and adolescence: A longitudinal MRI study. Nat Neurosci 2:861-863. (Pubitemid 30602596)
49. Shaw P, et al. (2006) Intellectual ability and cortical development in children and adolescents. Nature 440:676-679.
50. Hollingshead AB (1975) Four-Factor Index for Social Status (Yale Univ Press, New Haven, CT).
51. Zijdenbos AP, Forghani R, Evans AC (2002) Automatic "pipeline" analysis of 3-D MRI data for clinical trials: Application to multiple sclerosis. IEEE Trans Med Imaging 21: 1280-1291.
52. MacDonald D, Kabani N, Avis D, Evans AC (2000) Automated 3-D extraction of inner and outer surfaces of cerebral cortex from MRI. Neuroimage 12:340-356.
53. Pinheiro J, Bates DM (2000) Mixed-effects models in S and S-PLUS (Springer, New York).