Sex steroids and brain structure in pubertal boys and girls

Psychoneuroendocrinology

Volumn 34, Issue 3, 2009, Pages 332-342

  Peper, Jiska S ^a   Brouwer, Rachel M ^a   Schnack, Hugo G ^a   van Baal, G Caroline ^a   van Leeuwen, Marieke ^b   van den Berg, Stéphanie M ^b   Delemarre Van de Waal, Henriëtte A ^c   Boomsma, Dorret I ^b   Kahn, René S ^a   Hulshoff Pol, Hilleke E ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b VU UNIVERSITY AMSTERDAM   (Netherlands)

^c VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Brain structure; Estradiol; MRI; Puberty; Sex differences; Testosterone

Indexed keywords

ESTRADIOL; TESTOSTERONE;

ADOLESCENT; ARTICLE; BRAIN DEVELOPMENT; BRAIN SIZE; CHILD; ESTRADIOL BLOOD LEVEL; FEMALE; GRAY MATTER; HUMAN; MALE; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; OCCIPITAL CORTEX; PARIETAL LOBE; PREFRONTAL CORTEX; PRIORITY JOURNAL; PUBERTY; SCHOOL CHILD; SEX DIFFERENCE; TEMPORAL CORTEX; TESTOSTERONE BLOOD LEVEL; WHITE MATTER;

ADOLESCENT; AGE FACTORS; BRAIN; CHILD; ESTRADIOL; FEMALE; HUMANS; MALE; PUBERTY; SALIVA; SEX CHARACTERISTICS; TESTOSTERONE;

EID: 59249100857     PISSN: 03064530     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2008.09.012     Document Type: Article

References (53)

1. Barker J.M., and Galea L.A. Repeated estradiol administration alters different aspects of neurogenesis and cell death in the hippocampus of female, but not male, rats. Neuroscience 152 (2008) 888-902
2. Blakemore S.J. The social brain in adolescence. Nat. Rev. Neurosci. 9 (2008) 267-277
3. Boccardi M., Ghidoni R., Govoni S., Testa C., Benussi L., Bonetti M., Binetti G., and Frisoni G.B. Effects of hormone therapy on brain morphology of healthy postmenopausal women: a voxel-based morphometry study. Menopause 13 (2006) 584-591
4. Bu{combining double acute accent}defeld T., Grgurevic N., Tobet S.A., and Majdic G. Sex differences in brain developing in the presence or absence of gonads. Dev. Neurobiol. 68 (2008) 981-995
5. Butler G.E., Walker R.F., Walker R.V., Teague P., Riad-Fahmy D., and Ratcliffe S.G. Salivary testosterone levels and the progress of puberty in the normal boy. Clin. Endocrinol. (Oxf.) 30 (1989) 587-596
6. Chen X., Sachdev P.S., Wen W., and Anstey K.J. Sex differences in regional gray matter in healthy individuals aged 44-48 years: a voxel-based morphometric study. Neuroimage 36 (2007) 691-699
7. Collaer M.L., and Hines M. Human behavioral sex differences: a role for gonadal hormones during early development?. Psychol. Bull. 118 (1995) 55-107
8. Collins D.L., Holmes C.J., Peters T.M., and Evans A.C. Automatic 3-D model-based neuroanatomical segmentation. Hum. Brain Mapp. 4 (1995) 190-208
9. De Vries G.J., Rissman E.F., Simerly R.B., Yang L.Y., Scordalakes E.M., Auger C.J., Swain A., Lovell-Badge R., Burgoyne P.S., and Arnold A.P. A model system for study of sex chromosome effects on sexually dimorphic neural and behavioral traits. J. Neurosci. 22 (2002) 9005-9014
10. De Vries G.J. Minireview: sex differences in adult and developing brains: compensation, compensation, compensation. Endocrinology 145 (2004) 1063-1068
11. Demir A., Voutilainen R., Juul A., Dunkel L., Alfthan H., Skakkebaek N.E., and Stenman U.H. Increase in first morning voided urinary luteinizing hormone levels precedes the physical onset of puberty. J. Clin. Endocrinol. Metab. 81 (1996) 2963-2967
12. Durston S., Hulshoff Pol H.E., Casey B.J., Giedd J.N., Buitelaar J.K., and van Engeland H. Anatomical MRI of the developing human brain: what have we learned?. J. Am. Acad. Child Adolesc. Psychiatry. 40 (2001) 1012-1020
13. Eberling J.L., Wu C., Haan M.N., Mungas D., Buonocore M., and Jagust W.J. Preliminary evidence that estrogen protects against age-related hippocampal atrophy. Neurobiol. Aging 24 (2003) 725-732
14. Finley S.K., and Kritzer M.F. Immunoreactivity for intracellular androgen receptors in identified subpopulations of neurons, astrocytes and oligodendrocytes in primate prefrontal cortex. J. Neurobiol. 40 (1999) 446-457
15. Genovese C.R., Lazar N.A., and Nichols T. Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuroimage 15 (2002) 870-878
16. Giedd J.N., Castellanos F.X., Rajapakse J.C., Vaituzis A.C., and Rapoport J.L. Sexual dimorphism of the developing human brain. Prog. Neuropsychopharmacol. Biol. Psychiatry 21 (1997) 1185-1201
17. Giedd J.N., Blumenthal J., Jeffries N.O., Castellanos F.X., Liu H., Zijdenbos A., Paus T., Evans A.C., and Rapoport J.L. Brain development during childhood and adolescence: a longitudinal MRI study. Nat. Neurosci. 2 (1999) 861-863
18. Giedd J.N., Clasen L.S., Lenroot R., Greenstein D., Wallace G.L., Ordaz S., Molloy E.A., Blumenthal J.D., Tossell J.W., Stayer C., Samango-Sprouse C.A., Shen D., Davatzikos C., Merke D., and Chrousos G.P. Puberty-related influences on brain development. Mol. Cell Endocrinol. 254-255 (2006) 154-162
19. Gilmore J.H., Lin W., Prastawa M.W., Looney C.B., Vetsa Y.S., Knickmeyer R.C., Evans D.D., Smith J.K., Hamer R.M., Lieberman J.A., and Gerig G. Regional gray matter growth, sexual dimorphism, and cerebral asymmetry in the neonatal brain. J. Neurosci. 27 (2007) 1255-1260
20. Gogtay N., Giedd J.N., Lusk L., Hayashi K.M., Greenstein D., Vaituzis A.C., Nugent T.F., Herman D.H., Clasen L.S., Toga A.W., Rapoport J.L., and Thompson P.M. Dynamic mapping of human cortical development during childhood through early adulthood. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 8174-8179
21. Goldstein J.M., Seidman L.J., Horton N.J., Makris N., Kennedy D.N., Caviness Jr. V.S., Faraone S.V., and Tsuang M.T. Normal sexual dimorphism of the adult human brain assessed by in vivo magnetic resonance imaging. Cereb. Cortex 11 (2001) 490-497
22. Good C.D., Johnsrude I., Ashburner J., Henson R.N., Friston K.J., and Frackowiak R.S. 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 (2001) 685-700
23. Grabner G., Janke A.L., Budge M.M., Smith D., Pruessner J., and Collins D.L. Symmetric atlasing and model based segmentation: an application to the hippocampus in older adults. Med. Image Comput. Comput. Assist. Interv. Int. Conf. Med. Image Comput. Comput. Assist. Interv. 9 (2006) 58-66
24. Grumbach M.M., and Styne D.M. Puberty ontogeny, neuroendocrinology, physiology, and disorders. In: Larsen P.R., Kronenberg H.M., Melmed S., and Polonski K.S. (Eds). Williams Textbook of Endocrinology. 10th ed. (2003), Elsevier, New York 1115-1286
25. Hulshoff Pol H.E., Cohen-Kettenis P.T., Van Haren N.E.M., Peper J.S., Brans R.G.H., Cahn W., Schnack H.G., Gooren L.J.G., and Kahn R.S. Changing your sex changes your brain: influences of testosterone and estrogen on adult human brain structure. Eur. J. Endocrinol. 155 (2006) s107-s114
26. Jernigan T.L., Trauner D.A., Hesselink J.R., and Tallal P.A. Maturation of human cerebrum observed in vivo during adolescence. Brain 114 Pt 5 (1991) 2037-2049
27. Lenroot R.K., Gogtay N., Greenstein D.K., Wells E.M., Wallace G.L., Clasen L.S., Blumenthal J.D., Lerch J., Zijdenbos A.P., Evans A.C., Thompson P.M., and Giedd J.N. Sexual dimorphism of brain developmental trajectories during childhood and adolescence. Neuroimage 36 (2007) 1065-1073
28. Lord C., Buss C., Lupien S.J., and Pruessner J.C. Hippocampal volumes are larger in postmenopausal women using estrogen therapy compared to past users, never users and men: a possible window of opportunity effect. Neurobiol. Aging 29 (2008) 95-101
29. Maes F., Collignon A., Vandermeulen D., Marchal G., and Suetens P. Multimodality image registration by maximization of mutual information. IEEE Trans. Med. Imaging 16 (1997) 187-198
30. Marshall W.A., and Tanner J.M. Variations in pattern of pubertal changes in girls. Arch. Dis. Child. 44 (1969) 291-303
31. Marshall W.A., and Tanner J.M. Variations in the pattern of pubertal changes in boys. Arch. Dis. Child. 45 (1970) 13-23
32. McEwen B.S., Biegon A., Davis P.G., Krey L.C., Luine V.N., McGinnis M.Y., Paden C.M., Parsons B., and Rainbow T.C. Steroid hormones: humoral signals which alter brain cell properties and functions. Recent Prog. Horm. Res. 38 (1982) 41-92
33. McEwen B.S. In: Ellendorff F., Gluckman P.D., and Parvizi N. (Eds). Gonadal Hormone Receptors in Developing and Adult Brain: Relationship to the Regulatory Phenotype (1984), Perinatology Press, New York 149-159
34. Neufang, S., Specht, K., Hausmann, M., Gunturkun, O., Herpertz-Dahlmann, B., Fink G.R., Konrad, K., in press. Sex differences and the impact of steroid hormones on the developing human brain. Cereb. Cortex, doi:10.1093/cercor/bhn100.
35. Paus T., Zijdenbos A., Worsley K., Collins D.L., Blumenthal J., Giedd J.N., Rapoport J.L., and Evans A.C. Structural maturation of neural pathways in children and adolescents: in vivo study. Science 283 (1999) 1908-1911
36. Paus T. Mapping brain maturation and cognitive development during adolescence. Trends Cogn. Sci. 9 (2005) 60-68
37. Peper J.S., Brouwer R.M., Schnack H.G., van Baal G.C.M., Van Leeuwen M., Van den Berg S.M., Delemarre-Van de Waal H.A., Janke A.L., Collins D.L., Evans A.C., Boomsma D.I., Kahn R.S., and Hulshoff Pol H.E. Cerebral white matter in early puberty is associated with luteinizing hormone concentrations. Psychoneuroendocrinology 33 (2008) 909-915
38. Peper, J.S., Schnack, H.G., Brouwer, R.M., van Baal, G.C.M., Pjetri, E., Székely, E., Van Leeuwen, M., Van den Berg, S.M., Collins, D.L., Evans, A.C., Boomsma, D.I., Kahn, R.S., Hulshoff Pol, H.E., in press. Heritability of global and regional brain structure at the onset of puberty: a magnetic resonance imaging study in 9-year old twin-pairs. Hum. Brain Mapp.
39. Pilgrim C., and Hutchison J.B. Developmental regulation of sex differences in the brain: can the role of gonadal steroids be redefined?. Neuroscience 60 (1994) 843-855
40. Protopopescu X., Butler T., Pan H., Root J., Altemus M., Polanecsky M., McEwen B., Silbersweig D., and Stern E. Hippocampal structural changes across the menstrual cycle. Hippocampus (2008) 10.1002/hipo.20468
41. Romeo R.D. Puberty: a period of both organizational and activational effects of steroid hormones on neurobehavioural development. J. Neuroendocrinol. 15 (2003) 1185-1192
42. Romeo R.D., and McEwen B.S. Sex differences in steroid-induced synaptic plasticity. In: Miller V.M., and Hay M. (Eds). Advances in Molecular and Cellular Biology: Principles of Sex-based Differences in Physiology (2004), Elsevier Science, London 247-258
43. Schnack H.G., Hulshoff Pol H.E., Baare W.F., Staal W.G., Viergever M.A., and Kahn R.S. Automated separation of gray and white matter from MR images of the human brain. Neuroimage 13 (2001) 230-237
44. Schwarz J.M., and McCarthy M.M. Steroid-induced sexual differentiation of the developing brain: multiple pathways, one goal. J. Neurochem. 105 (2008) 1561-1572
45. Simerly R.B., Chang C., Muramatsu M., and Swanson L.W. Distribution of androgen and estrogen receptor mRNA-containing cells in the rat brain: an in situ hybridization study. J. Comp. Neurol. 294 (1990) 76-95
46. Sisk C.L., and Zehr J.L. Pubertal hormones organize the adolescent brain and behavior. Front. Neuroendocrinol. 26 (2005) 163-174
47. Sowell E.R., Trauner D.A., Gamst A., and Jernigan T.L. Development of cortical and subcortical brain structures in childhood and adolescence: a structural MRI study. Dev. Med. Child Neurol. 44 (2002) 4-16
48. Sowell E.R., Thompson P.M., Leonard C.M., Welcome S.E., Kan E., and Toga A.W. Longitudinal mapping of cortical thickness and brain growth in normal children. J. Neurosci. 24 (2004) 8223-8231
49. Talairach J., and Tournoux P. Co-planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging (1988), Thieme, New York
50. van Leeuwen M., Van den Berg S.M., and Boomsma D.I. A twin-family study of general IQ. Learn. Indiv. Diff. 18 (2008) 76-88
51. Wang J., Cheng C.M., Zhou J., Smith A., Weickert C.S., Perlman W.R., Becker K.G., Powell D., and Bondy C.A. Estradiol alters transcription factor gene expression in primate prefrontal cortex. J. Neurosci. Res. 76 (2004) 306-314
52. Wilke M., Krageloh-Mann I., and Holland S.K. Global and local development of gray and white matter volume in normal children and adolescents. Exp. Brain Res. 178 (2007) 296-307
53. Woolley C.S. Effects of estrogen in the CNS. Curr. Opin. Neurobiol. 9 (1999) 349-354