CoChat
Sign Up
Cited by 437Neural and Behavioral Psychology StudiesChild and Adolescent Psychosocial and Emotional DevelopmentHypothalamic control of reproductive hormones

Puberty and the human brain: insights into adolescent development

Open access
Vijayakumar, Nandita, Op de Macks, Zdena, Shirtcliff, Elizabeth A., Pfeifer, Jennifer H.·2018·Neuroscience & Biobehavioral Reviews
DOI 10.1016/j.neubiorev.2018.06.004PMC PMC6234123
Open this paper in CoChat — free account

Abstract

Alongside the exponential flourish of research on age-related trajectories of human brain development during childhood and adolescence in the past two decades, there has been an increase in the body of work examining the association between pubertal development and brain maturation. This review systematically examines empirical research on puberty-related structural and functional brain development in humans, with the aim of identifying convergent patterns of associations. We emphasize longitudinal studies, and discuss pervasive but oft-overlooked methodological issues that may be contributing to inconsistent findings and hindering progress (e.g., conflating distinct pubertal indices and different measurement instruments). We also briefly evaluate support for prominent models of adolescent neurodevelopment that hypothesize puberty-related changes in brain regions involved in affective and motivational processes. For the field to progress, replication studies are needed to help resolve current inconsistencies and gain a clearer understanding of pubertal associations with brain development in humans, knowledge that is crucial to make sense of the changes in psychosocial functioning, risk behavior, and mental health during adolescence.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1016/j.neubiorev.2018.06.004

Cites

39 of 39 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • The increase in sex hormones at puberty plays a role in brain development, social outcomes, and mental health.

    “Evidence suggests that the increase in sex hormones at puberty plays a role in brain development, 114-117 social outcomes, 118 and mental health. 119-121”

    From The Lancet Psychiatry Commission on youth mental health (2024) · cites this paper as [115]

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 152

  1. Abdelgadir SE, Roselli CE, Choate JV, Resko JA, 1999 Androgen receptor messenger ribonucleic acid in brains and pituitaries of male rhesus monkeys: studies on distribution, hormonal control, and relationship to luteinizing hormone secretion. Biol. Reprod 60, 1251– 1256. 10208992
  2. Ahmed EI, Zehr JL, Schulz KM, Lorenz BH, DonCarlos LL, Sisk CL, 2008 Pubertal hormones modulate the addition of new cells to sexually dimorphic brain regions. Nat. Neurosci 11, 995– 997. 19160494 PMC2772186
  3. Alarcon G, Cservenka A, Fair DA, Nagel BJ, 2014 Sex differences in the neural substrates of spatial working memory during adolescence are not mediated by endogenous testosterone. Brain Res 1593, 40– 54. 25312831 PMC4252582
  4. Alarcón G, Cservenka A, Nagel BJ, 2017 Adolescent neural response to reward is related to participant sex and task motivation. Brain Cogn 111, 51– 62. 10.1016/j.bandc.2016.10.003 27816780 PMC5698908 · DOI
  5. Alexander-Bloch A, Giedd JN, Bullmore E, 2013 Imaging structural co-variance between human brain regions. Nat. Rev. Neurosci 14, 322– 336. 10.1038/nrn3465 23531697 PMC4043276 · DOI · Paper page
  6. Antonio Mun˜oz-Cueto J, Miguel Garci´a-Segura L, Ruiz-Marcos A, 1990 Developmental sex differences and effect of ovariectomy on the number of cortical pyramidal cell dendritic spines. Brain Res 515, 64– 68. 10.1016/00068993(90)90577-X 2357578 · DOI
  7. Apter D, Vihko R, 1985 Premenarcheal endocrine changes in relation to age at menarche. Clin. Endocrinol. (Oxf.) 22, 753– 760. 3160508
  8. Asato MR, Sweeney JA, Luna B, 2006 Cognitive processes in the development of TOL performance. Neuropsychologia 44, 2259– 2269. 10.1016/j.neuropsychologia.2006.05.010 16797612 · DOI · Paper page
  9. Asato MR, Terwilliger R, Woo J, Luna B, 2010 White matter development in adolescence: a DTI study. Cereb. Cortex, 20, 2122– 2131. 20051363 PMC2923214
  10. Barendse MEA, Simmons JG, Byrne ML, Seal ML, Patton G, Mundy L, Wood SJ, Olsson CA, Allen NB, Whittle S, 2018 Brain structural connectivity during adrenarche: Associations between hormone levels and white matter microstructure. Psychoneuroendocrinology 88, 70– 77. 10.1016/j.psyneuen.2017.11.009 29175736 · DOI
  11. Barkovich AJ, 2000 Concepts of myelin and myelination in neuroradiology. Am. J. Neuroradiol 21, 1099– 1109. 10871022 PMC7973874
  12. Bava S, Boucquey V, Goldenberg D, Thayer RE, Ward M, Jacobus J, Tapert SF, 2011 Sex differences in adolescent white matter architecture. Brain Res 1375, 41– 48. 21172320 PMC3035918
  13. Berenbaum SA, Beltz AM, Corley R, 2015 The importance of puberty for adolescent development: conceptualization and measurement. Adv. Child Dev. Behav 48, 53– 92. 10.1016/bs.acdb.2014.11.002 25735941 · DOI
  14. Biro FM, Pinney SM, Huang B, Baker ER, Walt Chandler D, Dorn LD, 2014 Hormone changes in peripubertal girls. J. Clin. Endocrinol. Metab 99, 3829– 3835. 10.1210/jc.2013-4528 25029416 PMC4184081 · DOI
  15. Blanton RE, Cooney RE, Joormann J, Eugene F, Glover GH, Gotlib IH, 2012 Pubertal stage and brain anatomy in girls. Neuroscience 217, 105– 112. 22569152 PMC4584426
  16. Bramen JE, Hranilovich JA, Dahl RE, Chen J, Rosso C, Forbes EE, Dinov ID, Worthman CM, Sowell ER, 2012 Sex matters during adolescence: testosterone-related cortical thickness maturation differs between boys and girls. PLoS ONE 7, e33850. 22479458 PMC3315517
  17. Brouwer RM, Koenis MMG, Schnack HG, van Baal GC, van Soelen ILC, Boomsma DI, Hulshoff Pol HE, 2015 Longitudinal development of hormone levels and grey matter density in 9 and 12-year-old twins. Behav. Genet 45, 313– 323. 25656383 PMC4422848
  18. Buvat J, Buvat-Herbaut M, 1981 Changes in the gonadotrophins, in the prolactin and in the sexual steroid levels throughout the normal menstrual cycle. J. Gynecol. Obstet. Biol. Reprod 10, 99– 108. 6792269
  19. Byrne ML, Whittle S, Vijayakumar N, Dennison M, Simmons JG, Allen NB, 2017 A systematic review of adrenarche as a sensitive period in neurobiological development and mental health. Dev. Cogn. Neurosci, Sensitive periods across development 25, 12– 28. 10.1016/j.dcn.2016.12.004 28077245 PMC6987793 · DOI · Paper page
  20. Casey BJ, Galván A, Somerville LH, 2016 Beyond simple models of adolescence to an integrated circuit-based account: A commentary. Dev. Cogn. Neurosci 17, 128– 130. 10.1016/j.dcn.2015.12.006 26739434 PMC6987976 · DOI · Paper page
  21. Casey BJ, Jonrd RM, Hare TA, 2008 The adolescent brain. Ann. N. Y. Acad. Sci 1124, 111– 126. 18400927 PMC2475802
  22. Chenn A, Walsh CA, 2002 Regulation of cerebral cortical size by control of cell cycle exit in neural precursors. Science 297, 365– 369. 10.1126/science.1074192 12130776 · DOI · Paper page
  23. Choudhury S, 2010 Culturing the adolescent brain: what can neuroscience learn from anthropology? Soc. Cogn. Affect. Neurosci 5, 159– 167. 10.1093/scan/nsp030 19959484 PMC2894667 · DOI
  24. Cooke BM, Woolley CS, 2005 Gonadal hormone modulation of dendrites in the mammalian CNS. J. Neurobiol 64, 34– 46. 10.1002/neu.20143 15884004 · DOI
  25. Cservenka A, Stroup ML, Etkin A, Nagel BJ, 2015 The effects of age, sex, and hormones on emotional conflict-related brain response during adolescence. Brain Cogn 99, 135– 150. 26175008 PMC4555000
  26. Cunningham RL, Claiborne BJ, McGinnis MY, 2007 Pubertal exposure to anabolic androgenic steroids increases spine densities on neurons in the limbic system of male rats. Neuroscience 150, 609– 615. 10.1016/j.neuroscience.2007.09.038 17980492 PMC2981146 · DOI
  27. Davey CG, Yücel M, Allen NB, 2008 The emergence of depression in adolescence: development of the prefrontal cortex and the representation of reward. Neurosci. Biobehav. Rev 32, 1– 19. 10.1016/j.neubiorev.2007.04.016 17570526 · DOI · Paper page
  28. De Lorme KC, Schulz KM, Salas-Ramirez KY, Sisk CL, 2012 Pubertal testosterone organizes regional volume and neuronal number within the medial amygdala of adult male Syrian hamsters. Brain Res 1460, 33– 40. 10.1016/j.brainres.2012.04.035 22578470 PMC3367452 · DOI
  29. Deardorff J, Hoyt LT, Carter R, Shirtcliff EA (in press). Exploring the complexity of puberty: Understudied populations and processes. Journal of Research on Adolescence PMC6827435 30869847
  30. Demir A, Alfthan H, Stenman UH, Voutilainen R, 1994 A clinically useful method for detecting gonadotropins in children: assessment of luteinizing hormone and follicle-stimulating hormone from urine as an alternative to serum by ultrasensitive time-resolved immunofluorometric assays. Pediatr. Res 36, 221– 226. 10.1203/00006450-199408000-00014 7970938 · DOI
  31. Di Luigi L, Baldari C, Gallotta MC, Perroni F, Romanelli F, Lenzi A, Guidetti L, 2006 Salivary steroids at rest and after a training load in young male athletes: relationship with chronological age and pubertal development. Int. J. Sports Med 27, 709– 717. 10.1055/s-2005-872931 16944399 · DOI
  32. Dorn LD, Biro FM, 2011 Puberty and its measurement: A decade in review. J.Res. Adolesc 21, 180– 195. 10.1111/j.1532-7795.2010.00722.x · DOI · Paper page
  33. Dorn LD, Dahl RE, Woodward HR, Biro F, 2006 Defining the boundaries of early adolescence: A user’s guide to assessing pubertal status and pubertal timing in research with adolescents. Appl. Dev. Sci 10, 30– 56. 10.1207/s1532480xads1001_3 · DOI · Paper page
  34. Ducharme S, Albaugh MD, Nguyen T-V, Hudziak JJ, Mateos-Pérez JM, Labbe A, Evans AC, Karama S, 2016 Trajectories of cortical thickness maturation in normal brain development — The importance of quality control procedures. NeuroImage 125, 267– 279. 10.1016/j.neuroimage.2015.10.010 26463175 PMC4691414 · DOI · Paper page
  35. Ducharme S, Albaugh MD, Nguyen T-V, Hudziak JJ, Mateos-Pérez JM, Labbe A, Evans AC, Karama S, 2015 Trajectories of cortical surface area and cortical volume maturation in normal brain development. Data Brief 5, 929– 938. 10.1016/j.dib.2015.10.044 26702424 PMC4669480 · DOI
  36. Dumontheil I, Houlton R, Christoff K, Blakemore S-J, 2010 Development of relational reasoning during adolescence. Dev. Sci 13, F15– F24. 10.1111/j.1467-7687.2010.01014.x 20977551 · DOI
  37. Eatough EM, Shirtcliff EA, Hanson JL, Pollak SD, 2009 Hormonal reactivity to MRI scanning in adolescents. Psychoneuroendocrinology 34, 1242– 1246. 19346079 PMC2747582
  38. Fareri DS, Gabard-Durnam L, Goff B, Flannery J, Gee DG, Lumian DS, Caldera C, Tottenham N, 2015 Normative development of ventral striatal resting state connectivity in humans. NeuroImage 118, 422– 437. 26087377 PMC5553607
  39. Feldstein Ewing SW, Hudson KA, Caouette J, Mayer AR, Thayer RE, Ryman SG, Bryan AD (2018). Sexual risk-taking and subcortical brain volume in adolescence. Ann. Behav. Med 52, 393– 405. 29659656 PMC6360948
  40. Ferri J, Bress JN, Eaton NR, Proudfit GH, 2014 The impact of puberty and social anxiety on amygdala activation to faces in adolescence. Dev. Neurosci 36, 239– 249. 25034314 PMC4152317
  41. Forbes EE, Phillips ML, Silk JS, Ryan ND, Dahl RE, 2011 Neural systems of threat processing in adolescents: role of pubertal maturation and relation to measures of negative affect. Dev. Neuropsychol 36, 429– 452. 21516542 PMC3085008
  42. Forbes EE, Ryan ND, Phillips ML, Manuck SB, Worthman CM, Moyles DL, Tarr JA, Sciarrillo SR, Dahl RE, 2010 Healthy adolescents’ neural response to reward: associations with puberty, positive affect, and depressive symptoms. JAAC 49, 162– 72. e1–5. PMC2837556 20215938
  43. Frith U, Frith CD, 2003 Development and neurophysiology of mentalizing. Philos. Trans. R. Soc. Lond. B. Biol. Sci 358, 459– 473. 10.1098/rstb.2002.1218 12689373 PMC1693139 · DOI · Paper page
  44. Galvan A, 2010 Adolescent development of the reward system. Front. Hum. Neurosci 4 10.3389/neuro.09.006.2010 PMC2826184 20179786 · DOI · Paper page
  45. Goddings A-L, Burnett Heyes S, Bird G, Viner RM, Blakemore S-J, 2012 The relationship between puberty and social emotion processing. Dev. Sci 15, 801– 811. 23106734 PMC3795450
  46. Goddings A-L, Mills KL, Clasen LS, Giedd JN, Viner RM, Blakemore SJ, 2014 The influence of puberty on subcortical brain development. NeuroImage 88, 242– 251. 24121203 PMC3991320
  47. Guyer AE, Monk CS, McClure-Tone EB, Nelson EE, Roberson-Nay R, Adler AD, Fromm SJ, Leibenluft E, Pine DS, Ernst M, 2008 A developmental examination of amygdala response to facial expressions. J. Cogn. Neurosci 20, 1565– 1582. 10.1162/jocn.2008.20114 18345988 PMC2902865 · DOI · Paper page
  48. Harden KP, Mendle J, 2012 Gene-environment interplay in the association between pubertal timing and delinquency in adolescent girls. J. Abnorm. Psychol 121, 73– 87. 10.1037/a0024160 21668078 PMC4079281 · DOI
  49. Harden KP, Mendle J, Kretsch N, 2012 Environmental and genetic pathways between early pubertal timing and dieting in adolescence: distinguishing between objective and subjective timing. Psychol. Med 42, 183– 193. 10.1017/S0033291711000961 21676282 · DOI
  50. Hare TA, Tottenham N, Galvan A, Voss HU, Glover GH, Casey BJ, 2008 Biological substrates of emotional reactivity and regulation in adolescence during an emotional go-nogo task. Biol. Psychiatry 63, 927– 934. 10.1016/j.biopsych.2008.03.015015 18452757 PMC2664095 · DOI
  51. Havelock JC, Auchus RJ, Rainey WE, 2004 The rise in adrenal androgen biosynthesis: adrenarche. Semin. Reprod. Med 22, 337– 347. 10.1055/s-2004-861550 15635501 · DOI
  52. Hebbard PC, King RR, Malsbury CW, Harley CW, 2003 Two organizational effects of pubertal testosterone in male rats: transient social memory and a shift away from long-term potentiation following a tetanus in hippocampal CA1. Exp. Neurol 182, 470– 475. 12895458
  53. Herting MM, Gautam P, Spielberg JM, Dahl RE, Sowell ER, 2015 A longitudinal study: changes in cortical thickness and surface area during pubertal maturation. PLoS ONE 10, e0119774. 25793383 PMC4368209
  54. Herting MM, Gautam P, Spielberg JM, Kan E, Dahl RE, Sowell ER, 2014 The role of testosterone and estradiol in brain volume changes across adolescence: a longitudinal structural MRI study. Hum. Brain Mapp 35, 5633– 5645. 10.1002/hbm.22575 24977395 PMC4452029 · DOI · Paper page
  55. Herting MM, Kim R, Uban KA, Kan E, Binley A, Sowell ER, 2017 Longitudinal changes in pubertal maturation and white matter microstructure. Psychoneuroendocrinology 81, 70– 79. 10.1016/j.psyneuen.2017.03.017 28419914 PMC5612361 · DOI
  56. Herting MM, Maxwell EC, Irvine C, Nagel BJ, 2012 The impact of sex, puberty, and hormones on white matter microstructure in adolescents. Cereb. Cortex 22, 1979– 1992. 22002939 PMC3412439
  57. Herting MM, Sowell ER, 2017 Puberty and structural brain development in humans. Front. Neuroendocrinol 44, 122– 137. 10.1016/j.yfrne.2016.12.003 28007528 PMC5612369 · DOI
  58. Hervé P-Y, Leonard G, Perron M, Pike B, Pitiot A, Richer L, Veillette S, Pausova Z, Paus T, 2009 Handedness, motor skills and maturation of the corticospinal tract in the adolescent brain. Hum. Brain Mapp 30, 3151– 3162. 19235881 PMC6870659
  59. Hofman LF, 2001 Human saliva as a diagnostic specimen. J. Nutr 131, 1621S– 5S. 11340128
  60. Holder MK, Blaustein JD, 2014 Puberty and adolescence as a time of vulnerability to stressors that alter neurobehavioral processes. Front. Neuroendocrinol 35, 89– 110. 10.1016/j.yfrne.2013.10.004 24184692 PMC3946873 · DOI · Paper page
  61. Hu S, Pruessner JC, Coupé P, Collins DL, 2013 Volumetric analysis of medial temporal lobe structures in brain development from childhood to adolescence. NeuroImage 74, 276– 287. 23485848
  62. Huizinga M, Dolan CV, van der Molen MW, 2006 Age-related change in executive function: developmental trends and a latent variable analysis. Neuropsychologia 44, 2017– 2036. 10.1016/j.neuropsychologia.2006.01.010 16527316 · DOI · Paper page
  63. Jankowski KF, Moore WE, Merchant JS, Kahn LE, Pfeifer JH, 2014 But do you think I’m cool? Developmental differences in striatal recruitment during direct and reflected social self-evaluations. Accid. Anal. Prev 8, 40– 54. PMC4422645 24582805
  64. Juraska JM, Willing J, 2017 Pubertal onset as a critical transition for neural development and cognition. Brain Res 1654, 87– 94. 10.1016/j.brainres.2016.04.012 27060769 PMC5053848 · DOI
  65. Kashon ML, Sisk CL, 1994 Pubertal maturation is associated with an increase in the number of androgen receptor-immunoreactive cells in the brains of male ferrets. Brain Res. Dev. Brain Res 78, 237– 242. 8026077
  66. Kilford EJ, Garrett E, Blakemore S-J, 2016 The development of social cognition in adolescence: An integrated perspective. Neurosci. Biobehav. Rev 70, 106– 120. 10.1016/j.neubiorev.2016.08.016 27545755 · DOI · Paper page
  67. Kim JH, Juraska JM, 1997 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, 77– 85. 9298236
  68. Klapwijk ET, Goddings A-L, Burnett Heyes S, Bird G, Viner RM, Blakemore S-J, 2013 Increased functional connectivity with puberty in the mentalising network involved in social emotion processing. Horm. Behav 64, 314– 322. 23998674 PMC4540076
  69. Klauser P, Whittle S, Simmons JG, Byrne ML, Mundy LK, Patton GC, Fornito A, Allen NB, 2015 Reduced frontal white matter volume in children with early onset of adrenarche. Psychoneuroendocrinology 52, 111– 118. 25459897
  70. Koolschijn PCMP, Peper JS, Crone EA, 2014 The influence of sex steroids on structural brain maturation in adolescence. PLoS ONE 9, e83929. 24416184 PMC3885531
  71. Koss WA, Lloyd MM, Sadowski RN, Wise LM, Juraska JM, 2015 Gonadectomy before puberty increases the number of neurons and glia in the medial prefrontal cortex of female, but not male, rats. Dev. Psychobiol 57, 305– 312. 10.1002/dev.21290 25782706 PMC4380816 · DOI · Paper page
  72. Kraemer HC, Yesavage JA, Taylor JL, Kupfer D, 2000 How can we learn about developmental processes from cross-sectional studies, or can we? Am. J. Psychiatry 157, 163– 171. 10.1176/appi.ajp.157.2.163 10671382 · DOI · Paper page
  73. LeMoult J, Colich NL, Sherdell L, Hamilton JP, Gotlib IH, 2015 Influence of menarche on the relation between diurnal cortisol production and ventral striatum activity during reward anticipation. Soc. Cogn. Affect. Neurosci 10, 1244– 1250. 25678549 PMC4560950
  74. Lenroot RK, Gogtay N, Greenstein DK, Wells EM, Wallace GL, Clasen LS, Blumenthal JD, Lerch J, Zijdenbos AP, Evans AC, Thompson PM, Giedd JN, 2007 Sexual dimorphism of brain developmental trajectories during childhood and adolescence. NeuroImage 36, 1065– 1073. 10.1016/j.neuroimage.2007.03.053 17513132 PMC2040300 · DOI · Paper page
  75. Liening SH, Stanton SJ, Saini EK, Schultheiss OC, 2010 Salivary testosterone, cortisol, and progesterone: two-week stability, interhormone correlations, and effects of time of day, menstrual cycle, and oral contraceptive use on steroid hormone levels. Physiol. Behav 99, 8– 16. 10.1016/j.physbeh.2009.10.001 19833145 · DOI
  76. Luna B, 2009 Developmental changes in cognitive control through adolescence. Adv. Child Dev. Behav 37, 233– 278. 19673164 PMC2782527
  77. Marceau K, Dorn LD, Susman EJ, 2012 Stress and puberty-related hormone reactivity, negative emotionality, and parent–adolescent relationships. Psychoneuroendocrinology 37, 1286– 1298. 10.1016/j.psyneuen.2012.01.001 22284540 · DOI
  78. Matchock RL, Dorn LD, Susman EJ, 2007 Diurnal and seasonal cortisol, testosterone, and DHEA rhythms in boys and girls during puberty. Chronobiol. Int 24, 969– 990. 10.1080/07420520701649471 17994350 · DOI
  79. Menzies L, Goddings A-L, Whitaker KJ, Blakemore S-J, Viner RM, 2015 The effects of puberty on white matter development in boys. Dev. Cogn. Neurosci 11, 116– 128. 25454416 PMC4352899
  80. Mills KL, Tamnes CK, 2014 Methods and considerations for longitudinal structural brain imaging analysis across development. Dev. Cogn. Neurosci 9, 172– 190. 10.1016/j.dcn.2014.04.004 24879112 PMC6989768 · DOI
  81. Monk CS, McClure EB, Nelson EE, Zarahn E, Bilder RM, Leibenluft E, Charney DS, Ernst M, Pine DS, 2003 Adolescent immaturity in attention-related brain engagement to emotional facial expressions. NeuroImage 20, 420– 428. 14527602
  82. Moore WE 3rd, Pfeifer JH, Masten CL, Mazziotta JC, Iacoboni M, Dapretto M, 2012 Facing puberty: associations between pubertal development and neural responses to affective facial displays. Soc. Cogn. Affect. Neurosci 7, 35– 43. 22228752 PMC3252633
  83. Morgan JK, Olino TM, McMakin DL, Ryan ND, Forbes EE, 2013 Neural response to reward as a predictor of increases in depressive symptoms in adolescence. Neurobiol. Dis 52, 66– 74. 22521464 PMC3430834
  84. Murray CR, Simmons JG, Allen NB, Byrne ML, Mundy LK, Seal ML, Patton GC, Olsson CA, Whittle S, 2016 Associations between dehydroepiandrosterone (DHEA) levels, pituitary volume, and social anxiety in children. Psychoneuroendocrinology 64, 31– 39. 10.1016/j.psyneuen.2015.11.004 26600008 · DOI
  85. Nelson E, Leibenluft E, McClure E, Pine D, 2005 The social re-orientation of adolescence: a neuroscience perspective on the process and its relation to psychopathology. Psychol. Med 35, 163– 174. 15841674
  86. Neufang S, Specht K, Hausmann M, Güntürkün O, Herpertz-Dahlmann B, Fink GR, Konrad K, 2009 Sex differences and the impact of steroid hormones on the developing human brain. Cereb. Cortex 19, 464– 473. 18550597
  87. Nguyen T-V, Gower P, Albaugh MD, Botteron KN, Hudziak JJ, Fonov VS, Collins L, Ducharme S, McCracken JT, 2016a The developmental relationship between DHEA and visual attention is mediated by structural plasticity of cortico-amygdalar networks. Psychoneuroendocrinology 70, 122– 133. 10.1016/j.psyneuen.2016.05.003 27236606 PMC4907862 · DOI
  88. Nguyen T-V, Lew J, Albaugh MD, Botteron KN, Hudziak JJ, Fonov VS, Collins DL, Ducharme S, McCracken JT, 2017 Sex-specific associations of testosterone with prefrontal-hippocampal development and executive function. Psychoneuroendocrinology 76, 206– 217. 10.1016/j.psyneuen.2016.12.005 27984812 PMC5272813 · DOI
  89. Nguyen T-V, McCracken J, Ducharme S, Botteron KN, Mahabir M, Johnson W, Israel M, Evans AC, Karama S, for the Brain Development Cooperative Group, 2012 Testosterone-related cortical maturation across childhood and adolescence. Cereb. Cortex 23, 1424– 1432. 22617851 PMC3643718
  90. Nguyen T-V, McCracken JT, Albaugh MD, Botteron KN, Hudziak JJ, Ducharme S, 2016b A testosterone-related structural brain phenotype predicts aggressive behavior from childhood to adulthood. Psychoneuroendocrinology 63, 109– 118. 10.1016/j.psyneuen.2015.09.021 26431805 PMC4695305 · DOI
  91. Nguyen T-V, McCracken JT, Ducharme S, Cropp BF, Botteron KN, Evans AC, Karama S, 2013 Interactive effects of dehydroepiandrosterone and testosterone on cortical thickness during early brain development. J. Neurosci 33, 10840– 10848. 23804104 PMC3693059
  92. Ojeda SR, Lomniczi A, Mastronardi C, Heger S, Roth C, Parent A-S, Matagne V, Mungenast AE, 2006 Minireview: the neuroendocrine regulation of puberty: is the time ripe for a systems biology approach? Endocrinology 147, 1166– 1174. 10.1210/en.2005-1136 16373420 · DOI
  93. Op de Macks ZA, Bunge SA, Bell ON, Kriegsfeld LJ, Kayser AS, Dahl RE, 2016a The effect of social rank feedback on risk taking and associated reward processes in adolescent girls. Soc. Cogn. Affect. Neurosci 12, 240– 250. PMC5390714 27614768
  94. Op de Macks ZA, Bunge SA, Bell ON, Wilbrecht L, Kriegsfeld LJ, Kayser AS, Dahl RE, 2016b Risky decision-making in adolescent girls: The role of pubertal hormones and reward circuitry. Psychoneuroendocrinology 74, 77– 91. 27591399
  95. Padmanabhan A, Lynn A, Foran W, Luna B, O’Hearn K, 2013 Age related changes in striatal resting state functional connectivity in autism. Front. Hum. Neurosci 7 10.3389/fnhum.2013.00814 PMC3842522 24348363 · DOI
  96. Palmert MR, Hayden DL, Mansfield MJ, Crigler JF, Crowley WF, Chandler DW, Boepple PA, 2001 The longitudinal study of adrenal maturation during gonadal suppression: evidence that adrenarche is a gradual process. J. Clin. Endocrinol. Metab 86, 4536– 4542. 10.1210/jcem.86.9.7863 11549704 · DOI
  97. Pangelinan MM, Leonard G, Perron M, Pike GB, Richer L, Veillette S, Pausova Z, Paus T, 2016 Puberty and testosterone shape the corticospinal tract during male adolescence. Brain Struct. Funct 221, 1083– 1094. 25503450
  98. Pantsiotou S, Papadimitriou A, Douros K, Priftis K, Nicolaidou P, Fretzayas A, 2008 Maturational tempo differences in relation to the timing of the onset of puberty in girls. Acta Paediatr. Oslo Nor 1992 97, 217– 220. 10.1111/j.1651-2227.2007.00598.x 18177444 · DOI
  99. Patton GC, Viner R, 2007 Pubertal transitions in health. Lancet Lond. Engl 369, 1130– 1139. 10.1016/S0140-6736(07)60366-3 17398312 · DOI
  100. Peper JS, Brouwer RM, Schnack HG, van Baal GC, van Leeuwen M, van den Berg SM, Delemarre-Van de Waal HA, Boomsma DI, Kahn RS, Hulshoff Pol HE, 2009a Sex steroids and brain structure in pubertal boys and girls. Psychoneuroendocrinology 34, 332– 342. 18980810
  101. Peper JS, Brouwer RM, Schnack HG, Van Baal GCM, van Leeuwen M, van den Berg SM, Delemarre-Van de Waal HA, Janke AL, Collins DL, Evans AC, Boomsma DI, Kahn RS, Hulshoff Pol HE, 2008 Cerebral white matter in early puberty is associated with luteinizing hormone concentrations. Psychoneuroendocrinology 33, 909– 915. 18640784
  102. Peper JS, de Reus MA, van den Heuvel MP, Schutter DJLG, 2015 Short fused? associations between white matter connections, sex steroids, and aggression across adolescence. Hum. Brain Mapp 36, 1043– 1052. 10.1002/hbm.22684 25359710 PMC6869636 · DOI
  103. Peper JS, Schnack HG, Brouwer RM, Van Baal GCM, Pjetri E, Székely E, van Leeuwen M, van den Berg SM, Collins DL, Evans AC, Boomsma DI, Kahn RS, Hulshoff Pol HE, 2009b Heritability of regional and global brain structure at the onset of puberty: a magnetic resonance imaging study in 9-year-old twin pairs. Hum. Brain Mapp 30, 2184– 2196. 19294640 PMC6870645
  104. Perrin JS, Leonard G, Perron M, Pike GB, Pitiot A, Richer L, Veillette S, Pausova Z, Paus T, 2009 Sex differences in the growth of white matter during adolescence. NeuroImage 45, 1055– 1066. 10.1016/j.neuroimage.2009.01.023 19349224 · DOI · Paper page
  105. Peters S, Braams BR, Raijmakers MEJ, Koolschijn PCMP, Crone EA, 2014 The neural coding of feedback learning across child and adolescent development. Cogn. Neurosci. J. Of 26, 1705– 1720. 24564463
  106. Peters S, Jolles DJ, van Duijvenvoorde ACK, Crone EA, Peper JS, 2015 The link between testosterone and amygdala-orbitofrontal cortex connectivity in adolescent alcohol use. Psychoneuroendocrinology 53, 117– 126. 25618591
  107. Petersen AC, Crockett L, Richards M, Boxer A, 1988 A self-report measure of pubertal status: Reliability, validity, and initial norms. J. Youth Adolesc 17, 117– 133. 10.1007/BF01537962 24277579 · DOI · Paper page
  108. Pfefferbaum A, Rohlfing T, Pohl KM, Lane B, Chu W, Kwon D, Nolan Nichols B, Brown SA, Tapert SF, Cummins K, Thompson WK, Brumback T, Meloy MJ, Jernigan TL, Dale A, Colrain IM, Baker FC, Prouty D, De Bellis MD, Voyvodic JT, Clark DB, Luna B, Chung T, Nagel BJ, Sullivan EV, 2015 Adolescent development of cortical and white matter structure in the NCANDA sample: Role of sex, ethnicity, puberty, and alcohol drinking. Cereb. Cortex 26, 4101– 4121. 26408800 PMC5027999
  109. Pfeifer JH, Allen NB, 2016 The audacity of specificity: Moving adolescent developmental neuroscience towards more powerful scientific paradigms and translatable models. Dev. Cogn. Neurosci 17, 131– 137. 10.1016/j.dcn.2015.12.012 26754460 PMC4826651 · DOI
  110. Pfeifer JH, Masten CL, Moore WE 3rd, Oswald TM, Mazziotta JC, Iacoboni M, Dapretto M, 2011 Entering adolescence: resistance to peer influence, risky behavior, and neural changes in emotion reactivity. Neuron 69, 1029– 1036. 10.1016/j.neuron.2011.02.019 21382560 PMC3840168 · DOI · Paper page
  111. Pfeifer JH, Peake SJ, 2012 Self-development: integrating cognitive, socioemotional, and neuroimaging perspectives. Dev. Cogn. Neurosci 2, 55– 69. 10.1016/j.dcn.2011.07.012 22682728 PMC6987679 · DOI
  112. Plant TM, Barker-Gibb ML, 2004 Neurobiological mechanisms of puberty in higher primates. Hum. Reprod. Update 10, 67– 77. 15005465
  113. Richmond S, Johnson KA, Seal ML, Allen NB, Whittle S, 2016 Development of brain networks and relevance of environmental and genetic factors: A systematic review. Neurosci. Biobehav. Rev 71, 215– 239. 10.1016/j.neubiorev.2016.08.024 27590832 · DOI · Paper page
  114. Romeo RD, Sisk CL, 2001 Pubertal and seasonal plasticity in the amygdala. Brain Res 889, 71– 77. 11166688
  115. Sato SM, Schulz KM, Sisk CL, Wood RI, 2008 Adolescents and androgens, receptors and rewards. Horm. Behav 53, 647– 658. 10.1016/j.yhbeh.2008.01.010 18343381 PMC2435368 · DOI
  116. Satterthwaite TD, Vandekar S, Wolf DH, Ruparel K, Roalf DR, Jackson C, Elliott MA, Bilker WB, Calkins ME, Prabhakaran K, Davatzikos C, Hakonarson H, Gur RE, Gur RC, 2014 Sex differences in the effect of puberty on hippocampal morphology. JAAC 53, 341– 50. e1. PMC3935178 24565361
  117. Schriber RA, Guyer AE, 2016 Adolescent neurobiological susceptibility to social context. Dev. Cogn. Neurosci 19, 1– 18. 10.1016/j.dcn.2015.12.009 26773514 PMC4912893 · DOI · Paper page
  118. Schweinsburg AD, Nagel BJ, Tapert SF, 2005 fMRI reveals alteration of spatial working memory networks across adolescence. J. Int. Neuropsychol. Soc 11, 631– 644. 10.1017/S1355617705050757 16212691 PMC2270702 · DOI · Paper page
  119. Shaw P, Kabani NJ, Lerch JP, Eckstrand K, Lenroot R, Gogtay N, Greenstein D, Clasen L, Evans A, Rapoport JL, Giedd JN, Wise SP, 2008 Neurodevelopmental trajectories of the human cerebral cortex. J. Neurosci 28, 3586– 3594. 18385317 PMC6671079
  120. Shimony JS, McKinstry RC, Akbudak E, Aronovitz JA, Snyder AZ, Lori NF, Cull TS, Conturo TE, 1999 Quantitative diffusion-tensor anisotropy brain MR imaging: normative human data and anatomic analysis. Radiology 212, 770– 784. 10.1148/radiology.212.3.r99au51770 10478246 · DOI
  121. Shirtcliff EA, Dahl RE, Pollak SD, 2009 Pubertal development: correspondence between hormonal and physical development. Child Dev 80, 327– 337. 10.1111/j.1467-8624.2009.01263.x 19466995 PMC2727719 · DOI · Paper page
  122. Silverman MH, Jedd K, Luciana M, 2015 Neural networks involved in adolescent reward processing: An activation likelihood estimation meta-analysis of functional neuroimaging studies. NeuroImage 122, 427– 439. 10.1016/j.neuroimage.2015.07.083 26254587 PMC4618189 · DOI · Paper page
  123. Södergård R, Bäckström T, Shanbhag V, Carstensen H, 1982 Calculation of free and bound fractions of testosterone and estradiol-17 beta to human plasma proteins at body temperature. J. Steroid Biochem 16, 801– 810. 7202083
  124. Sodian B, 2011 Theory of mind in infancy. Child Dev. Perspect 5, 39– 43. 10.1111/j.1750-8606.2010.00152.x · DOI
  125. Soliman A, De Sanctis V, Elalaily R, 2014 Nutrition and pubertal development. Indian J. Endocrinol. Metab 18, S39– S47. 10.4103/2230-8210.145073 25538876 PMC4266867 · DOI
  126. Somerville LH, Casey BJ, 2010 Developmental neurobiology of cognitive control and motivational systems. Curr. Opin. Neurobiol 20, 236– 241. 20167473 PMC3014528
  127. Spielberg JM, Forbes EE, Ladouceur CD, Worthman CM, Olino TM, Ryan ND, Dahl RE, 2015 Pubertal testosterone influences threat-related amygdalaorbitofrontal cortex coupling. Soc. Cogn. Affect. Neurosci 10, 408– 415. 24795438 PMC4350481
  128. Steen RG, Hamer RM, Lieberman JA, 2007 Measuring brain volume by MR imaging: Impact of measurement precision and natural variation on sample size requirements. Am. J. Neuroradiol 28, 1119– 1125. 10.3174/ajnr.A0537 17569971 PMC8134133 · DOI
  129. Steinberg L, 2008 A social neuroscience perspective on adolescent risk-taking. Dev. Rev. DR 28, 78– 106. 18509515 PMC2396566
  130. Tanner JM, 1962 Growth at Adolescence (2nd edition). Blackwell Publishing, Oxford.
  131. Telzer EH, Flannery J, Humphreys KL, Goff B, Gabard-Durman L, Gee DG, Tottenham N, 2015 “The Cooties Effect”: Amygdala reactivity to opposite- versus same-sex faces declines from childhood to adolescence. J. Cogn. Neurosci 27, 1685– 1696. 25848681 PMC5723398
  132. Tung Y-C, Lee J-S, Tsai W-Y, Hsiao P-H, 2004 Physiological changes of adrenal androgens in childhood. J. Formos. Med. Assoc. Taiwan Yi Zhi 103, 921– 924. 15624041
  133. Tyborowska A, Volman I, Smeekens S, Toni I, Roelofs K, 2016 Testosterone during puberty shifts emotional control from pulvinar to anterior prefrontal cortex. J. Neurosci 36, 6156– 6164. 27277794 PMC6604884
  134. Ubuka T, Tsutsui K, 2014 Review: neuroestrogen regulation of socio-sexual behavior of males. Front. Neurosci 8, 323 10.3389/fnins.2014.00323 25352775 PMC4195287 · DOI
  135. Urosevic S, Collins P, Muetzel R, Lim KO, Luciana M, 2014 Pubertal status associations with reward and threat sensitivities and subcortical brain volumes during adolescence. Brain Cogn 89, 15– 26. 24512818 PMC4125562
  136. van den Bos W, Eppinger B, 2016 Developing developmental cognitive neuroscience: From agenda setting to hypothesis testing. Dev. Cogn. Neurosci 17, 138– 144. 10.1016/j.dcn.2015.12.011 26797489 PMC6987973 · DOI
  137. van Duijvenvoorde ACK, Op de Macks ZA, Overgaauw S, Gunther Moor B, Dahl RE, Crone EA, 2014 A cross-sectional and longitudinal analysis of rewardrelated brain activation: effects of age, pubertal stage, and reward sensitivity. Brain Cogn 89, 3– 14. 24512819
  138. Veldhuis JD, 1996 Neuroendocrine mechanisms mediating awakening of the human gonadotropic axis in puberty. Pediatr. Nephrol. Berl. Ger 10, 304– 317. 8792395
  139. Vesper HW, Botelho JC, 2010 Standardization of testosterone measurements in humans. J. Steroid Biochem. Mol. Biol 121, 513– 519. 10.1016/j.jsbmb.2010.03.032 20302935 · DOI · Paper page
  140. Vesper HW, Botelho JC, Shacklady C, Smith A, Myers GL, 2008 CDC project on standardizing steroid hormone measurements. Steroids 73, 1286– 1292. 10.1016/j.steroids.2008.09.008 18834895 · DOI
  141. Vesper HW, Botelho JC, Wang Y, 2014 Challenges and improvements in testosterone and estradiol testing. Asian J. Androl 16, 178– 184. 10.4103/1008-682X.122338 24407184 PMC3955326 · DOI
  142. Vijayakumar N, Allen NB, Youssef G, Dennison M, Yücel M, Simmons JG, Whittle S, 2016 Brain development during adolescence: A mixed-longitudinal investigation of cortical thickness, surface area, and volume. Hum. Brain Mapp 37, 2027– 2038. 10.1002/hbm.23154 26946457 PMC6867680 · DOI
  143. Virta A, Barnett A, Pierpaoli C, 1999 Visualizing and characterizing white matter fiber structure and architecture in the human pyramidal tract using diffusion tensor MRI. Magn. Reson. Imaging 17, 1121– 1133. 10499674
  144. Wallen K, Baum MJ, 2002 Masculinization and defeminization in altricial and precocial mammals: comparative aspects of steroid hormone action, in: Pfaff DW, Arnold AP, Fahrbach SE, Etgen AM, Rubin RT (Eds.), Hormones, Brain and Behavior Academic Press, San Diego, pp. 385– 423. 10.1016/B978-012532104-4/50071-8 · DOI
  145. Weil LG, Fleming SM, Dumontheil I, Kilford EJ, Weil RS, Rees G, Dolan RJ, Blakemore S-J, 2013 The development of metacognitive ability in adolescence. Conscious. Cogn 22, 264– 271. 10.1016/j.concog.2013.01.004 23376348 PMC3719211 · DOI · Paper page
  146. Westberry JM, Wilson ME, 2012 Regulation of estrogen receptor alpha gene expression in the mouse prefrontal cortex during early postnatal development. Neurogenetics 13, 159– 167. 10.1007/s10048-012-0323-z 22457017 · DOI
  147. Whittle S, Yücel M, Lorenzetti V, Byrne ML, Simmons JG, Wood SJ, Pantelis C, Allen NB, 2012 Pituitary volume mediates the relationship between pubertal timing and depressive symptoms during adolescence. Psychoneuroendocrinology 37, 881– 891. 22071452
  148. Wierenga LM, Langen M, Oranje B, Durston S, 2014 Unique developmental trajectories of cortical thickness and surface area. NeuroImage 87, 120– 126. 10.1016/j.neuroimage.2013.11.010 24246495 · DOI
  149. Wong AP-Y, Pipitone J, Park MTM, Dickie EW, Leonard G, Perron M, Pike BG, Richer L, Veillette S, Chakravarty MM, Pausova Z, Paus T, 2014 Estimating volumes of the pituitary gland from T1- weighted magnetic-resonance images: effects of age, puberty, testosterone, and estradiol. NeuroImage 94, 216– 221. 24632090
  150. Zehr JL, Nichols LR, Schulz KM, Sisk CL, 2008 Adolescent development of neuron structure in dentate gyrus granule cells of male Syrian hamsters. Dev. Neurobiol 68, 1517– 1526. 10.1002/dneu.20675 18792070 PMC2676582 · DOI
  151. Zehr JL, Todd BJ, Schulz KM, McCarthy MM, Sisk CL, 2006 Dendritic pruning of the medial amygdala during pubertal development of the male Syrian hamster. J. Neurobiol 66, 578– 590. 10.1002/neu.20251 16555234 · DOI · Paper page
  152. Zielinski BA, Gennatas ED, Zhou J, Seeley WW, 2010 Network-level structural covariance in the developing brain. Proc. Natl. Acad. Sci 107, 18191– 18196. 10.1073/pnas.1003109107 20921389 PMC2964249 · DOI · Paper page

Cited by

Sorted by citations

Authors
Vijayakumar, N., Op de Macks, Z., Shirtcliff, E. A., & Pfeifer, J. H.
Affiliations
  • University of Oregon (US)
  • Iowa State University (US)
Corresponding author
Vijayakumar, Nandita
ORCID
Venue
Neuroscience & Biobehavioral Reviews
Publisher
Elsevier BV
Published
2018-09
Volume
92
Pages
417-436
ISSN
0149-7634 (ISSN-L)
DOI
10.1016/j.neubiorev.2018.06.004
PMC
PMC6234123
OpenAlex
W2810098278
Cited by
437
References
39
Citations by year
2026: 56 · 2025: 76 · 2024: 57 · 2023: 74 · 2022: 60 · 2021: 46 · 2020: 45 · 2019: 22 · 2018: 1
FWCI
3.81
Type
journal article
Language
en
Open access
Licence
Locations
  • Neuroscience & Biobehavioral Reviews (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
  • Figshare (submittedVersion, cc-by)
Funders
National Institute of Health (P50 DA035763, R01 MH107418)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
  • Social Sciences › Psychology › Clinical Psychology › Child and Adolescent Psychosocial and Emotional Development
  • Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
Keywords
puberty, adolescent brain development, brain maturation, structural brain development, functional brain development, emotional processing, motivational processes, replication
MeSH terms
Adolescent, Brain, Humans, Puberty, Adolescent Development

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review