The effects of puberty on white matter development in boys

Developmental Cognitive Neuroscience

Volumn 11, Issue , 2015, Pages 116-128

  Menzies, Lara ^a,b   Goddings, Anne Lise ^a,b   Whitaker, Kirstie J ^c   Blakemore, Sarah Jayne ^a   Viner, Russell M ^b  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c Brain Mapping Unit Department of Psychiatry Cambridge Biomedical Campus   (United Kingdom)

Author keywords

Adolescence; Brain development; Diffusion tensor imaging; Puberty; Structural magnetic resonance imaging; Testosterone; White matter

Indexed keywords

ESTRADIOL; PRASTERONE; TESTOSTERONE;

ADOLESCENT; ARTICLE; BRAIN REGION; BRAIN SIZE; CHILD; DIFFUSION TENSOR IMAGING; FRACTIONAL ANISOTROPY; GONAD DEVELOPMENT; HUMAN; MALE; MEAN DIFFUSIVITY; NERVOUS SYSTEM DEVELOPMENT; NEUROANATOMY; NEUROIMAGING; PHYSICAL PARAMETERS; PUBERTY; SEX DIFFERENCE; WHITE MATTER; AGING; ANISOTROPY; BRAIN; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGY; SALIVA; SEXUAL MATURATION; ULTRASTRUCTURE;

ADOLESCENT; AGING; ANISOTROPY; BRAIN; CHILD; DIFFUSION TENSOR IMAGING; HUMANS; MALE; NEUROIMAGING; PUBERTY; SALIVA; SEXUAL MATURATION; TESTOSTERONE; WHITE MATTER;

EID: 84922256489     PISSN: 18789293     EISSN: 18789307     Source Type: Journal    
DOI: 10.1016/j.dcn.2014.10.002     Document Type: Article

References (102)

1. J.L.R. Andersson, and M. Jenkinson Non-linear registration, aka spatial normalisation 2010
2. M.R. Asato, and R. Terwilliger White matter development in adolescence: a DTI study Cereb. Cortex 20 9 2010 2122 2131
3. M. Ashtari, and K.L. Cervellione White matter development during late adolescence in healthy males: a cross-sectional diffusion tensor imaging study Neuroimage 35 2 2007 501 510
4. W.S. Ball, and A.W. Byars Total and regional brain volumes in a population-based normative sample from 4 to 18 Years: the NIH MRI study of normal brain development Cereb. Cortex 22 1 2012 1 12
5. N. Barnea-Goraly, and V. Menon White matter development during childhood and adolescence: a cross-sectional diffusion tensor imaging study Cereb. Cortex 15 12 2005 1848 1854
6. P.J. Basser, and J. Mattiello Estimation of the effective self-diffusion tensor from the NMR spin-echo J. Magn. Reson. B 103 3 1994 247 254
7. P.J. Basser, and C. Pierpaoli Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI J. Magn. Reson. B 111 3 1996 209 219
8. S. Bava, and R. Thayer Longitidinal characterisation of white matter during adolescence Brain Res. 1327 2010 38 46
9. C. Beaulieu The basis of anisotropic water diffusion in the nervous system - a technical review NMR Biomed. 15 7-8 2002 435 455
10. D. Ben Bashat, and L. Ben Sira Normal white matter development from infancy to adulthood: comparing diffusion tensor and high b value diffusion weighted MR images J. Magn. Reson. Imaging 21 5 2005 503 511
11. F.M. Biro, and A.W. Lucky Pubertal staging in boys J. Pediatr. 127 1 1995 100 102
12. S.J. Blakemore, and S. Burnett The role of puberty in the developing adolescent brain Hum. Brain Mapp. 31 6 2010 926 933
13. T. Blumenfeld-Katzir, and O. Pasternak Diffusion MRI of structural brain plasticity induced by a learning and memory task PLoS ONE 6 6 2011 e20678
14. D. Bonekamp, and L.M. Nagae Diffusion tensor imaging in children and adolescents: reproducibility, hemispheric, and age-related differences Neuroimage 34 2 2007 733 742
15. K.P. Burnham, and D.R. Anderson Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach 2nd ed. 2002 Springer-Verlag ISBN 0-387-95364-7
16. L. Coleman, and J. Coleman The measurement of puberty: a review J. Adolesc. 25 5 2002 535 550
17. B.M. Cooke, and C.S. Woolley Gonadal hormone modulation of dendrites in the mammalian CNS J. Neurobiol. 64 1 2005 34 46
18. K.C. De Lorme, and K.M. Schulz Pubertal testosterone organizes regional volume and neuronal number within the medial amygdala of adult male Syrian hamsters Brain Res. 1460 2012 33 40
19. S. De Santis, and M. Drakesmith Why diffusion tensor MRI does well only some of the time: variance and covariance of white matter tissue microstructure attributes in the living human brain? Neuroimage 89 100 2014 35 44
20. S.C. Deoni, and B.K. Rutt Gleaning multicomponent T1 and T2 information from steady-state imaging data? Magn. Reson. Med. 60 6 2008 1372 1387
21. L.D. Dorn, and R.E. Dahl Defining boundaries of early adolescence: a user's guide to assessing pubertal status and pubertal timing in research with adolescents Appl. Dev. Sci. 10 2006 30 56
22. T.J. Eluvathingal, and K.M. Hasan Quantitative diffusion tensor tractography of association and projection fibers in normally developing children and adolescents Cereb. Cortex 17 12 2007 2760 2768
23. A. Fedorov, and R. Beichel 3D slicer as an image computing platform for the quantitative imaging network Magn. Reson. Imaging 30 9 2012 1323 1341
24. E.E. Forbes, and R.E. Dahl Pubertal development and behavior: hormonal activation of social and motivational tendencies Brain Cogn. 72 1 2010 66 72
25. L.M. Garcia-Segura, and R.C. Melcangi Steroids and glial cell function Glia 54 6 2006 485 498
26. J.N. Giedd, and J. Blumenthal Brain development during childhood and adolescence: a longitudinal MRI study Nat. Neurosci. 2 10 1999 861 863
27. A. Giorgio, and K.E. Watkins Longitudinal changes in grey and white matter during adolescence Neuroimage 49 1 2010 94 103
28. A. Giorgio, and K.E. Watkins Changes in white matter microstructure during adolescence Neuroimage 39 1 2008 52 61
29. A.L. Goddings, and S.B. Heyes The relationship between puberty and social emotion processing Dev. Sci. 15 6 2012 801 811
30. A.L. Goddings, and K.L. Mills The influence of puberty on subcortical brain development Neuroimage 88 2014 242 251
31. N. Gogtay, and J.N. Giedd Dynamic mapping of human cortical development during childhood through early adulthood Proc. Natl. Acad. Sci. U. S. A. 101 21 2004 8174 8179
32. S.M. Gold, and R.R. Voskuhl Estrogen and testosterone therapies in multiple sclerosis Progr. Brain Res. 175 2009 239 251
33. M.M. Herting, and E.C. Maxwell The impact of sex, puberty, and hormones on white matter microstructure in adolescents Cereb. Cortex 22 9 2012 1979 1992
34. M. Jenkinson Measuring transformation error by RMS deviation. FMRIB Technical report TR99MJ1 1999
35. C.L. Jordan, and T.J. Williams Testosterone regulates terminal Schwann cell number and junctional size during developmental synapse elimination Dev. Neurosci. 23 6 2001 441 451
36. J.M. Juraska, and C.L. Sisk Sexual differentiation of the adolescent rodent brain: hormonal influences and developmental mechanisms Horm. Behav. 64 2 2013 203 210
37. J.H. Kim, and J.M. Juraska Sex differences in the development of axon number in the splenium of the rat corpus callosum from postnatal day 15 through 60 Brain Res. Dev. Brain Res. 102 1 1997 77 85
38. T. Klingberg, and C.J. Vaidya Myelination and organization of the frontal white matter in children: a diffusion tensor MRI study Neuroreport 10 13 1999 2817 2821
39. C.D. Ladouceur, and J.S. Peper White matter development in adolescence: the influence of puberty and implications for affective disorders Dev. Cogn. Neurosci. 2 1 2012 36 54
40. D. Le Bihan, and J.F. Mangin Diffusion tensor imaging: concepts and applications J. Magn. Reson. Imaging 13 4 2001 534 546
41. C. Lebel, and C. Beaulieu Longitudinal development of human brain wiring continues from childhood into adulthood J. Neurosci. 31 30 2011 10937 10947
42. C. Lebel, and L. Walker Microstructural maturation of the human brain from childhood to adulthood Neuroimage 40 3 2008 1044 1055
43. P.A. Lee, and C.P. Houk Puberty and its disorders (Chapter 11) F. Lifshitz, Paediatric Endocrinology 2006 Informa Healthcare 2
44. R.K. Lenroot, and N. Gogtay Sexual dimorphism of brain developmental trajectories during childhood and adolescence Neuroimage 36 4 2007 1065 1073
45. E. Leonelli, and M. Ballabio Neuroactive steroids: a therapeutic approach to maintain peripheral nerve integrity during neurodegenerative events J. Mol. Neurosci. 28 1 2006 65 76
46. A. MacKay, and K. Whittall In vivo visualization of myelin water in brain by magnetic resonance Magn. Reson. Med.: Off. J. Soc. Magn. Reson. Med./Soc. Magn. Reson. Med. 31 6 1994 673 677
47. B.S. McEwen, and A. Biegon Steroid hormones: humoral signals which alter brain cell properties and functions Recent Prog. Horm. Res. 38 1982 41 92
48. K. Meindl, and S. Windhager Second-to-fourth digit ratio and facial shape in boys: the lower the digit ratio, the more robust the face Proc. Biol. Sci. 279 1737 2012 2457 2463
49. R.C. Melcangi, and V. Magnaghi Glial cells: a target for steroid hormones Progr. Brain Res. 132 2001 31 40
50. R.C. Melcangi, and A.G. Mensah-Nyagan Neuroprotective effects of neuroactive steroids in the spinal cord and peripheral nerves J. Mol. Neurosci. 28 1 2006 1 2
51. D.J. Miller, and T. Duka Prolonged myelination in human neocortical evolution Proc. Natl. Acad. Sci. U. S. A. 109 41 2012 16480 16485
52. V. Miskovic, and L.A. Schmidt Frontal brain oscillatory coupling among men who vary in salivary testosterone levels Neurosci. Lett. 464 3 2009 239 242
53. M.C. Morriss, and R.A. Zimmerman Changes in brain water diffusion during childhood Neuroradiology 41 12 1999 929 934
54. P. Mukherjee, and J.H. Miller Normal brain maturation during childhood: developmental trends characterized with diffusion-tensor imaging Radiology 221 2 2001 349 358
55. L.K. Mundy, and J.G. Simmons Study protocol: the Childhood to Adolescence Transition Study (CATS) BMC Pediatr. 13 2013 160
56. T.V. Nguyen, and M. Yao Androgens activate mitogen-activated protein kinase signaling: role in neuroprotection J. Neurochem. 94 6 2005 1639 1651
57. T.V. Nguyen, and J.T. McCracken Interactive effects of dehydroepiandrosterone and testosterone on cortical thickness during early brain development J. Neurosci. 33 26 2013 10840 10848
58. T.E. Nichols, and A.P. Holmes Nonparametric permutation tests for functional neuroimaging: a primer with examples Hum. Brain Mapp. 15 1 2002 1 25
59. R. Patel, and S. Moore Attenuation of corpus callosum axon myelination and remyelination in the absence of circulating sex hormones Brain Pathol. 23 4 2013 462 475
60. G.C. Patton, and R. Viner Pubertal transitions in health Lancet 369 9567 2007 1130 1139
61. T. Paus Growth of white matter in the adolescent brain: myelin or axon? Brain Cogn. 72 1 2010 26 35
62. T. Paus, and M. Keshavan Why do many psychiatric disorders emerge during adolescence? Nat. Rev. Neurosci. 9 12 2008 947 957
63. T. Paus, and I. Nawaz-Khan 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 1 2010 63 75
64. J.S. Peper, and M.P. van den Heuvel Sex steroids and connectivity in the human brain: a review of neuroimaging studies Psychoneuroendocrinology 36 8 2011 1101 1113
65. J.S. Perrin, and P.Y. Herve Growth of white matter in the adolescent brain: role of testosterone and androgen receptor J. Neurosci. 28 38 2008 9519 9524
66. J.S. Perrin, and G. Leonard Sex differences in the growth of white matter during adolescence Neuroimage 45 4 2009 1055 1066
67. A.C. Petersen, and L. Crockett A self-report measure of pubertal status: reliability, validity, and initial norms J. Youth Adolesc. 17 2 1988 117 133
68. D. Qiu, and L.H. Tan Diffusion tensor imaging of normal white matter maturation from late childhood to young adulthood: voxel-wise evaluation of mean diffusivity, fractional anisotropy, radial and axial diffusivities, and correlation with reading development Neuroimage 41 2 2008 223 232
69. A. Raznahan, and Y. Lee 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 39 2010 16988 16993
70. A. Raznahan, and J.P. Lerch Patterns of coordinated anatomical change in human cortical development: a longitudinal neuroimaging study of maturational coupling Neuron 72 5 2011 873 884
71. R.D. Romeo Puberty: a period of both organizational and activational effects of steroid hormones on neurobehavioural development J. Neuroendocrinol. 15 12 2003 1185 1192
72. D. Rueckert, and L.I. Sonoda Nonrigid registration using free-form deformations: application to breast MR images IEEE Trans. Med. Imaging 18 8 1999 712 721
73. Y. Sagi, and I. Tavor Learning in the fast lane: new insights into neuroplasticity Neuron 73 6 2012 1195 1203
74. S. Sarkey, and I. Azcoitia Classical androgen receptors in non-classical sites in the brain Horm. Behav. 53 5 2008 753 764
75. V.J. Schmithorst, and M. Wilke Correlation of white matter diffusivity and anisotropy with age during childhood and adolescence: a cross-sectional diffusion-tensor MR imaging study Radiology 222 1 2002 212 218
76. J.F. Schneider, and K.A. Il'yasov Fast quantitative diffusion-tensor imaging of cerebral white matter from the neonatal period to adolescence Neuroradiology 46 4 2004 258 266
77. J.S. Schneiderman, and M.S. Buchsbaum Diffusion tensor anisotropy in adolescents and adults Neuropsychobiology 55 2 2007 96 111
78. K.M. Schulz, and H.A. Molenda-Figueira Back to the future: the organizational-activational hypothesis adapted to puberty and adolescence Horm. Behav. 55 5 2009 597 604
79. K.M. Schulz, and C.L. Sisk Pubertal hormones, the adolescent brain, and the maturation of social behaviors: lessons from the Syrian hamster Mol. Cell Endocrinol. 254-255 2006 120 126
80. D.J. Schutter, and J. van Honk Decoupling of midfrontal delta-beta oscillations after testosterone administration Int. J. Psychophysiol. 53 1 2004 71 73
81. P. Shaw, and N.J. Kabani Neurodevelopmental trajectories of the human cerebral cortex J. Neurosci. 28 14 2008 3586 3594
82. E.A. Shirtcliff, and R.E. Dahl Pubertal development: correspondence between hormonal and physical development Child Dev. 80 2 2009 327 337
83. D.J. Simmonds, and M.N. Hallquist Developmental stages and sex differences of white matter and behavioral development through adolescence: a longitudinal diffusion tensor imaging (DTI) study Neuroimage 92C 2013 356 368
84. S.M. Smith Fast robust automated brain extraction Hum. Brain Mapp. 17 3 2002 143 155
85. S.M. Smith, and M. Jenkinson Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data Neuroimage 31 4 2006 1487 1505
86. S.M. Smith, and M. Jenkinson Advances in functional and structural MR image analysis and implementation as FSL Neuroimage 23 Suppl. 1 2004 S208L 219
87. S.M. Smith, and T.E. Nichols Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference Neuroimage 44 1 2009 83 98
88. L. Snook, and L.A. Paulson Diffusion tensor imaging of neuro development in children and young adults Neuroimage 26 4 2005 1164 1173
89. E.R. Sowell, and P.M. Thompson Longitudinal mapping of cortical thickness and brain growth in normal children J. Neurosci. 24 38 2004 8223 8231
90. E.R. Sowell, and D.A. Trauner Development of cortical and subcortical brain structures in childhood and adolescence: a structural MRI study Dev. Med. Child Neurol. 44 1 2002 4 16
91. L. Steinberg Risk taking in adolescence - new perspectives from brain and behavioral science Curr. Direct. Psychol. Sci. 16 2 2007 55 59
92. C.K. Tamnes, and Y. Ostby Brain maturation in adolescence and young adulthood: regional age-related changes in cortical thickness and white matter volume and microstructure Cereb. Cortex 20 3 2010 534 548
93. J.M. Tanner, and R.H. Whitehouse Clinical longitudinal standards for height, weight, height velocity, weight velocity, and stages of puberty Arch. Dis. Child 51 3 1976 170 179
94. S.J. Taylor, and P.H. Whincup Performance of a new pubertal self-assessment questionnaire: a preliminary study Paediatr. Perinat. Epidemiol. 15 1 2001 88 94
95. G. van Wingen, and C. Mattern Testosterone reduces amygdala-orbitofrontal cortex coupling Psychoneuroendocrinology 35 1 2010 105 113
96. A. Verdonck, and M. Gaethofs Effect of low-dose testosterone treatment on craniofacial growth in boys with delayed puberty Eur. J. Orthod. 21 2 1999 137 143
97. I. Volman, and I. Toni Endogenous testosterone modulates prefrontal-amygdala connectivity during social emotional behavior Cereb. Cortex 21 10 2011 2282 2290
98. D. Wechsler Wechsler Abbreviated Scale of Intelligence 1999 Harcourt Brace & Company New York, NY
99. A.M. Winkler, G.R. Ridgway, M.A. Webster, S.M. Smith, and T.E. Nichols Permutation inference for the general linear model NeuroImage 92 2014 381 397
100. M.W. Woolrich, and S. Jbabdi Bayesian analysis of neuroimaging data in FSL Neuroimage 45 1 (Suppl.) 2009 S173 S186
101. P. Yakovlev, and A.R. Lecours The myelogenetic cycles of regional maturation of the brain A. Minkowsky, Regional Development of the Brain in Early Life 1967 Blackwell Oxford 3 70
102. A. Yendiki, and K. Koldewyn Spurious group differences due to head motion in a diffusion MRI study Neuroimage 88C 2013 79 90