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Cited by 219Neural and Behavioral Psychology StudiesFunctional Brain Connectivity StudiesHypothalamic control of reproductive hormones

Understanding the role of puberty in structural and functional development of the adolescent brain

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Goddings, Anne‐Lise, Beltz, Adriene, Peper, Jiska S., Crone, Eveline A., Braams, Barbara R.·2019·Journal of Research on Adolescence
DOI 10.1111/jora.12408
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Abstract

Over the past two decades, there has been a tremendous increase in our understanding of structural and functional brain development in adolescence. However, understanding the role of puberty in this process has received much less attention. This review examines this relationship by summarizing recent research studies where the role of puberty was investigated in relation to brain structure, connectivity, and task‐related functional magnetic resonance imaging (fMRI). The studies together suggest that puberty may contribute to adolescent neural reorganization and maturational advancement, and sex differences also emerge in puberty. The current body of work shows some mixed results regarding impact and exact direction of pubertal influence. We discuss several limitations of current studies and propose future directions on how to move the field forward.

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  • 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 [117]

  • Puberty is characterized by cortical and subcortical reorganization.

    “Puberty is a key developmental stage characterized by changes in physiological stress responses (16) as well as cortical and subcortical reorganization (17–19).”

    From Sexual differentiation of neural mechanisms of stress sensitivity during puberty (2023) · cites this paper as [17]

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  1. Abdelgadir, S. E., Roselli, C. E., Choate, J. V., & Resko, J. A. (1999). Androgen receptor messenger ribonucleic acid in brains and pituitaries of male rhesus monkeys: Studies on distribution, hormonal control, and relation- ship to luteinizing hormone secretion. Biology of Repro- duction, 60, 1251-1256. https://doi.org/10.1095/ biolreprod60.5.1251 · DOI · Paper page
  2. Ahmed, E. I., Zehr, J. L., Schulz, K. M., Lorenz, B. H., DonCarlos, L. L., & Sisk, C. L. (2008). Pubertal hor- mones modulate the addition of new cells to sexually dimorphic brain regions. Nature Neuroscience, 11, 995- 997. https://doi.org/10.1038/nn.2178 · DOI · Paper page
  3. Asato, M. R., Terwilliger, R., Woo, J., & Luna, B. (2010). White matter development in adolescence: A DTI study. Cerebral Cortex, 20, 2122-2131. https://doi.org/ 10.1093/cercor/bhp282 · DOI · Paper page
  4. Bava, S., Thayer, R., Jacobus, J., Ward, M., Jernigan, T. L., & Tapert, S. F. (2010). Longitudinal characterization of white matter maturation during adolescence. Brain Research, 1327, 38-46. https://doi.org/10.1016/j.brainre s.2010.02.066 · DOI
  5. Beltz, A. M., Blakemore, J. E. O., & Berenbaum, S. A. (2013). Sex differences in brain and behavioral devel- opment. In J. Rubenstein & P. Rakic (Eds.), Comprehen- sive developmental neuroscience: Neural circuit development and function in the heathy and diseased brain (pp. 467- 501). Amsterdam, The Netherlands: Elsevier.
  6. Berenbaum, S. A., Beltz, A. M., & Corley, R. (2015). The importance of puberty for adolescent development: Conceptualization and measurement. Advances in Child Development and Behavior, 48, 53-92. https://doi.org/ 10.1016/bs.acdb.2014.11.002 · DOI
  7. Bishop, K. M., & Wahlsten, D. (1997). Sex differences in the human corpus callosum: Myth or reality? Neuroscience and Biobehavioral Reviews, 21, 581-601. https://doi.org/10.1016/S0149-7634(96)00049-8 · DOI
  8. Biswal, B. B., Mennes, M., Zuo, X. N., Gohel, S., Kelly, C., Smith, S. M., . . . Milham, M. P. (2010). Toward PUBERTY AND THE ADOLESCENT BRAIN 47 discovery science of human brain function. Proceedings of the National Academy of Sciences of the United States of America, 107, 4734-4739. https://doi.org/10.1073/pnas. 0911855107 · DOI · Paper page
  9. Bohlken, M. M., Brouwer, R. M., Mandl, R. C. W., Van den Heuvel, M. P., Hedman, A. M., De Hert, M., . . . Hulshoff Pol, H. E. (2016). Structural brain connectivity as a genetic marker for schizophrenia. JAMA Psychia- try, 73(1), 11-19. https://doi.org/10.1001/jamapsychi atry.2015.1925 · DOI
  10. Bos, P. A., Hofman, D., Hermans, E. J., Montoya, E. R., Baron-Cohen, S., & van Honk, J. (2016). Testosterone reduces functional connectivity during the Reading the Mind in the Eyes test. Psychoneuroendocrinology, 68, 194- 201. https://doi.org/10.1016/j.psyneuen.2016.03.006 · DOI
  11. Brock, O., Baum, M. J., & Bakker, J. (2011). The develop- ment of female sexual behavior requires prepubertal estradiol. Journal of Neuroscience, 31, 5574-5578. https://doi.org/10.1523/JNEUROSCI.0209-11.2011 · DOI
  12. Brouwer, R. M., Koenis, M. M., Schnack, H. G., van Baal, G. C., van Soelen, I. L., Boomsma, D. I., & Hulshoff Pol, H. E. (2015). Longitudinal development of hor- mone levels and grey matter density in 9 and 12-year- old twins. Behavior Genetics, 45, 313-323. https://doi. org/10.1007/s10519-015-9708-8 · DOI
  13. Bullmore, E., & Sporns, O. (2009). Complex brain net- works: Graph theoretical analysis of structural and functional systems. Nature Reviews Neuroscience, 10, 186-198. https://doi.org/10.1038/nrn2575 · DOI · Paper page
  14. Casey, B. J. (2015). Beyond simple models of self-control to circuit-based accounts of adolescent behavior. Annual Review of Psychology, 66, 295-319. https://doi. org/10.1146/annurev-psych-010814-015156 · DOI · Paper page
  15. Clark, A. S., MacLusky, N. J., & Goldman-Rakic, P. S. (1988). Androgen binding and metabolism in the cere- bral cortex of the developing rhesus monkey. Endocrinology, 123, 932-940. https://doi.org/10.1210/ endo-123-2-932 · DOI
  16. Cosgrove, K. P., Mazure, C. M., & Staley, J. K. (2007). Evolving knowledge of sex differences in brain structure, function, and chemistry. Biological Psychiatry, 62, 847-855. https://doi.org/10.1016/j.biopsych.2007. 03.001 · DOI · Paper page
  17. Crone, E. A., & Elzinga, B. M. (2015). Changing brains: How longitudinal functional magnetic resonance imag- ing studies can inform us about cognitive and social- affective growth trajectories. Wiley Interdisciplinary Reviews-Cognitive Science, 6(1), 53-63. https://doi.org/ 10.1002/wcs.1327 · DOI
  18. Cservenka, A., Stroup, M. L., Etkin, A., & Nagel, B. J. (2015). The effects of age, sex, and hormones on emo- tional conflict-related brain response during adoles- cence. Brain and Cognition, 99, 135-150. https://doi. org/10.1016/j.bandc.2015.06.002 · DOI
  19. Cui, J., Shen, Y., & Li, R. (2013). Estrogen synthesis and signaling pathways during aging: From periphery to brain. Trends in Molecular Medicine, 19, 197-209. https://doi.org/10.1016/j.molmed.2012.12.007 · DOI
  20. Dahl, R. E. (2008). Biological, developmental, and neu- robehavioral factors relevant to adolescent driving risks. American Journal of Preventive Medicine, 35, S278- S284. https://doi.org/10.1016/j.amepre.2008.06.013 · DOI
  21. Dalgleish, T., Walsh, N. D., Mobbs, D., Schweizer, S., van Harmelen, A. L., Dunn, B., . . . Stretton, J. (2017). Social pain and social gain in the adolescent brain: A common neural circuitry underlying both positive and nega- tive social evaluation. Scientific Reports, 7, p42010. https://doi.org/ARTN 42010/10.1038/srep42010 · DOI · Paper page
  22. De Lorme, K. C., Schulz, K. M., Salas-Ramirez, K. Y., & Sisk, C. L. (2012). Pubertal testosterone organizes regional volume and neuronal number within the medial amygdala of adult male Syrian hamsters. Brain Research, 1460, 33-40. https://doi.org/10.1016/j.brainre s.2012.04.035 · DOI
  23. Dennison, M., Whittle, S., Yucel, M., Vijayakumar, N., Kline, A., Simmons, J., & Allen, N. B. (2013). Mapping subcortical brain maturation during adolescence: Evi- dence of hemisphere-and sex-specific longitudinal changes. Developmental Science, 16, 772-791. https://doi. org/10.1111/desc.12057 · DOI · Paper page
  24. Dorn, L. D., & Biro, F. M. (2011). Puberty and its mea- surement: A decade in review. Journal of Research on Adolescence, 21, 180-195. https://doi.org/10.1111/j. 1532-7795.2010.00722.x · DOI · Paper page
  25. Dorn, L. D., Dahl, R. E., Woodward, H. R., & Biro, F. (2006). Defining the boundaries of early adolescence: A user's guide to assessing pubertal status and pubertal timing in research with adolescents. Applied Develop- mental Science, 10(1), 30-56. https://doi.org/10.1207/ s1532480xads1001_3 · DOI · Paper page
  26. Dubb, A., Gur, R., Avants, B., & Gee, J. (2003). Character- ization of sexual dimorphism in the human corpus cal- losum. NeuroImage, 20, 512-519. https://doi.org/10. 1016/S1053-8119(03)00313-6 · DOI
  27. Ferri, J., Bress, J. N., Eaton, N. R., & Proudfit, G. H. (2014). The impact of puberty and social anxiety on amygdala activation to faces in adolescence. Develop- mental Neuroscience, 36, 239-249. https://doi.org/10. 1159/000363736 · DOI
  28. Filippi, M., van den Heuvel, M. P., Fornito, A., He, Y., Pol, H. E. H., Agosta, F., . . . Rocca, M. A. (2013). Assessment of system dysfunction in the brain through MRI-based connectomics. Lancet Neurology, 12, 1189- 1199. https://doi.org/10.1016/S1474-4422(13)70144-3 · DOI
  29. Filkowski, M. M., Olsen, R. M., Duda, B., Wanger, T. J., & Sabatinelli, D. (2017). Sex differences in emotional perception: Meta analysis of divergent activation. NeuroImage, 147, 925-933. https://doi.org/10.1016/j.ne uroimage.2016.12.016 · DOI
  30. Forbes, E. E., Phillips, M. L., Silk, J. S., Ryan, N. D., & Dahl, R. E. (2011). Neural systems of threat processing in adolescents: Role of pubertal maturation and rela- tion to measures of negative affect. Developmental Neu- ropsychology, 36, 429-452. https://doi.org/10.1080/ 87565641.2010.550178 · DOI
  31. Forbes, E. E., Ryan, N. D., Phillips, M. L., Manuck, S. B., Worthman, C. M., Moyles, D. L., . . . Dahl, R. E. (2010). Healthy adolescents' neural response to reward: Asso- ciations with puberty, positive affect, and depressive symptoms. Journal of the American Academy of Child and Adolescent Psychiatry, 49, 162-172. https://doi.org/10. 1016/j.jaac.2009.11.006 · DOI
  32. Giedd, J. N., Blumenthal, J., Jeffries, N. O., Castellanos, F. X., Liu, H., Zijdenbos, A., . . . Rapoport, J. L. (1999). Brain development during childhood and adolescence: A longitudinal MRI study. Nature Neuroscience, 2, 861- 863. https://doi.org/10.1038/13158 · DOI · Paper page
  33. Giedd, J. N., & Denker, A. H. (2015). The adolescent brain: Insights from neuroimaging. In J.-P. Bour- guignon, J.-C. Carels & Y. Christen (Eds.), Brain cross- talk in puberty and adolescence (pp. 85-96). Cham, Switzerland: Springer.
  34. Goddings, A. L., Heyes, S. B., Bird, G., Viner, R. M., & Blakemore, S. J. (2012). The relationship between pub- erty and social emotion processing. Developmental Science, 15, 801-811. https://doi.org/10.1111/j.1467- 7687.2012.01174.x · DOI · Paper page
  35. Goddings, A. L., Mills, K. L., Clasen, L. S., Giedd, J. N., Viner, R. M., & Blakemore, S. J. (2014). The influence of puberty on subcortical brain development. Neuro- Image, 88, 242-251. https://doi.org/10.1016/j.neuroima ge.2013.09.073 · DOI
  36. Guyer, A. E., Monk, C. S., McClure-Tone, E. B., Nelson, E. E., Roberson-Nay, R., Adler, A. D., . . . Ernst, M. (2008). A developmental examination of amygdala response to facial expressions. Journal of Cognitive Neu- roscience, 20, 1565-1582. https://doi.org/10.1162/jocn. 2008.20114 · DOI · Paper page
  37. Halpern, D. F. (2013). Sex differences in cognitive abilities (4th ed.). London, UK: Psychology Press.
  38. Halpern, C. T., Kaestle, C. E., & Hallfors, D. D. (2007). Perceived physical maturity, age of romantic partner, and adolescent risk behavior. Prevention Science, 8(1), 1-10. https://doi.org/10.1007/s11121-006-0046-1 · DOI
  39. Herting, M. M., Gautam, P., Spielberg, J. M., Dahl, R. E., & Sowell, E. R. (2015). A longitudinal study: Changes in cortical thickness and surface area during pubertal maturation. PLoS ONE, 10, e0119774. https://doi.org/ 10.1371/journal.pone.0119774 · DOI · Paper page
  40. Herting, M. M., Gautam, P., Spielberg, J. M., Kan, E., Dahl, R. E., & Sowell, E. R. (2014). The role of testos- terone and estradiol in brain volume changes across adolescence: A longitudinal structural MRI study. Human Brain Mapping, 35, 5633-5645. https://doi.org/ 10.1002/hbm.22575 · DOI · Paper page
  41. Herting, M. M., Johnson, C., Mills, K. L., Vijayakumar, N., Dennison, M., Liu, C., . . . Tamnes, C. K. (2018). Development of subcortical volumes across adoles- cence in males and females: A multisample study of longitudinal changes. NeuroImage, 172, 194-205. https://doi.org/10.1016/j.neuroimage.2018.01.020 · DOI · Paper page
  42. Herting, M. M., Maxwell, E. C., Irvine, C., & Nagel, B. J. (2012). The impact of sex, puberty, and hormones on white matter microstructure in adolescents. Cerebral Cortex, 22, 1979-1992. https://doi.org/10.1093/cercor/ bhr246 · DOI
  43. Herting, M. M., & Sowell, E. R. (2017). Puberty and struc- tural brain development in humans. Frontiers in Neu- roendocrinology, 44, 122-137. https://doi.org/10.1016/j. yfrne.2016.12.003 · DOI
  44. Ho, A., Villacis, A. J., Svirsky, S. E., Foilb, A. R., & Romeo, R. D. (2012). The pubertal-related decline in cellular proliferation and neurogenesis in the dentate gyrus of male rats is independent of the pubertal rise in gonadal hormones. Developmental Neurobiology, 72, 743-752. https://doi.org/10.1002/dneu.20987 · DOI
  45. Holmes, M. M., Goldman, B. D., & Forger, N. G. (2008). Social status and sex independently influence andro- gen receptor expression in the eusocial naked mole-rat brain. Hormones and Behavior, 54, 278-285. https://doi. org/10.1016/j.yhbeh.2008.03.010 · DOI
  46. Huttenlocher, P. R. (1990). Morphometric study of human cerebral cortex development. Neuropsychologia, 28, 517- 527. https://doi.org/10.1016/0028-3932(90)90031-I · DOI · Paper page
  47. Jones, D. K. (2010). Precision and accuracy in diffusion tensor magnetic resonance imaging. Topics in Magnetic Resonance Imaging, 21, 87-99. https://doi.org/10.1097/ RMR.0b013e31821e56ac · DOI
  48. Juraska, J. M., & Willing, J. (2017). Pubertal onset as a critical transition for neural development and cogni- tion. Brain Research, 1654, 87-94. https://doi.org/10. 1016/j.brainres.2016.04.012 · DOI
  49. Kawata, M. (1995). Roles of steroid hormones and their receptors in structural organization in the nervous sys- tem. Neuroscience Research, 24(1), 1-46. https://doi.org/ 10.1016/0168-0102(96)81278-8 · DOI
  50. Klapwijk, E. T., Goddings, A. L., Burnett Heyes, S., Bird, G., Viner, R. M., & Blakemore, S. J. (2013). Increased functional connectivity with puberty in the mentalising network involved in social emotion processing. Hor- mones and Behavior, 64, 314-322. https://doi.org/10. 1016/j.yhbeh.2013.03.012 · DOI
  51. Koss, W. A., Lloyd, M. M., Sadowski, R. N., Wise, L. M., & Juraska, J. M. (2015). Gonadectomy before puberty increases the number of neurons and glia in the med- ial prefrontal cortex of female, but not male, rats. Developmental Psychobiology, 57, 305-312. https://doi. org/10.1002/dev.21290 · DOI · Paper page
  52. Kraemer, H. C., Yesavage, J. A., Taylor, J. L., & Kupfer, D. (2000). How can we learn about developmental pro- cesses from cross-sectional studies, or can we? Ameri- can Journal of Psychiatry, 157, 163-171. https://doi.org/ 10.1176/appi.ajp.157.2.163 · DOI · Paper page
  53. Ladouceur, C. D., Peper, J. S., Crone, E. A., & Dahl, R. E. (2012). White matter development in adolescence: The influence of puberty and implications for affective dis- orders. Developmental Cognitive Neuroscience, 2(1), 36- 54. https://doi.org/10.1016/j.dcn.2011.06.002 · DOI
  54. Le Bihan, D., & Johansen-Berg, H. (2012). Diffusion MRI at 25: Exploring brain tissue structure and function. NeuroImage, 61, 324-341. https://doi.org/10.1016/j.neu roimage.2011.11.006 · DOI · Paper page
  55. Lee, P. A., & Houk, C. P. (2006). Gonadotropin-releasing hormone analog therapy for central precocious puberty and other childhood disorders affecting growth and puberty. Treatments in Endocrinology, 5, 287-296. https://doi.org/10.2165/00024677-200605050-00003 · DOI
  56. Lenroot, R. K., Gogtay, N., Greenstein, D. K., Wells, E. M., Wallace, G. L., Clasen, L. S., . . . Giedd, J. N. (2007). Sex- ual dimorphism of brain developmental trajectories dur- ing childhood and adolescence. NeuroImage, 36, 1065- 1073. https://doi.org/10.1016/j.neuroimage.2007.03.053 · DOI · Paper page
  57. Leonard, C. M., Towler, S., Welcome, S., Halderman, L. K., Otto, R., Eckert, M. A., & Chiarello, C. (2008). Size matters: Cerebral volume influences sex differences in neuroanatomy. Cerebral Cortex, 18, 2920-2931. https://doi.org/10.1093/cercor/bhn052 · DOI
  58. Luders, E., Narr, K. L., Thompson, P. M., Rex, D. E., Jancke, L., Steinmetz, H., & Toga, A. W. (2004). Gender differences in cortical complexity. Nature Neuroscience, 7, 799-800. https://doi.org/10.1038/nn1277 · DOI
  59. Marshall, W. A., & Tanner, J. M. (1969). Variations in pattern of pubertal changes in girls. Archives of Disease in Childhood, 44, 291-303. https://doi.org/10.1136/adc. 44.235.291 · DOI · Paper page
  60. Masten, C. L., Eisenberger, N. I., Pfeifer, J. H., Colich, N. L., & Dapretto, M. (2013). Associations among pubertal development, empathic ability, and neural responses while witnessing peer rejection in adolescence. Child Development, 84, 1338-1354. https://doi.org/10.1111/ cdev.12056 · DOI
  61. Meindl, K., Windhager, S., Wallner, B., & Schaefer, K. (2012). Second-to-fourth digit ratio and facial shape in boys: The lower the digit ratio, the more robust the face. Proceedings of the Royal Society B-Biological Sciences, 279, 2457-2463. https://doi.org/10.1098/rspb.2011.2351 · DOI
  62. Melcangi, R. C., Magnaghi, V., Galbiati, M., & Martini, L. (2001). Glial cells: A target for steroid hormones. Pro- gress in Brain Research, 132, 31-40. https://doi.org/10. 1016/S0079-6123(01)32063-0 · DOI
  63. Mendle, J., Beltz, A., Carter, R., & Dorn, L. D. (2019). Under- standing puberty and its measurement: Ideas for research in a new generation of youth. Journal of Research on Ado- lescence, 29, 82-95. https://doi.org/10.1111/jora.12371 · DOI
  64. Mendle, J., Turkheimer, E., & Emery, R. E. (2007). Detri- mental psychological outcomes associated with early pubertal timing in adolescent girls. Developmental Review, 27, 151-171. https://doi.org/10.1016/j.dr.2006. 11.001 · DOI · Paper page
  65. Menzies, L., Goddings, A. L., Whitaker, K. J., Blakemore, S. J., & Viner, R. M. (2015). The effects of puberty on white matter development in boys. Developmental Cog- nitive Neuroscience, 11, 116-128. https://doi.org/10. 1016/j.dcn.2014.10.002 · DOI
  66. Meyer, G., Ferres-Torres, R., & Mas, M. (1978). The effects of puberty and castration on hippocampal den- dritic spines of mice. A golgi study. Brain Research, 155 (1), 108-112. https://doi.org/10.1016/0006-8993(78) 90309-8 · DOI
  67. Miller, G. A., & Chapman, J. P. (2001). Misunderstanding analysis of covariance. Journal of Abnormal Psychology, 110(1), 40-48. https://doi.org/10.1037//0021-843x.110. 1.40 · DOI · Paper page
  68. Moore, W. E., Pfeifer, J. H., Masten, C. L., Mazziotta, J. C., Iacoboni, M., & Dapretto, M. (2012). Facing puberty: Associations between pubertal development and neural responses to affective facial displays. Social Cognitive and Affective Neuroscience, 7(1), 35-43. https://doi.org/ 10.1093/scan/nsr066 · DOI · Paper page
  69. Murphy, D. D., & Segal, M. (1996). Regulation of den- dritic spine density in cultured rat hippocampal neu- rons by steroid hormones. Journal of Neuroscience, 16, 4059-4068. https://doi.org/10.1523/JNEUROSCI.16-13- 04059.1996 · DOI
  70. Narvacan, K., Treit, S., Camicioli, R., Martin, W., & Beau- lieu, C. (2017). Evolution of deep gray matter volume across the human lifespan. Human Brain Mapping, 38, 3771-3790. https://doi.org/10.1002/hbm.23604 · DOI
  71. Nguyen, T. V., Gower, P., Albaugh, M. D., Botteron, K. N., Hudziak, J. J., Fonov, V. S., . . . McCracken, J. T. (2016). The developmental relationship between DHEA and visual attention is mediated by structural plasticity of cortico-amygdalar networks. Psychoneuroendocrinol- ogy, 70, 122-133. https://doi.org/10.1016/j.psyneuen. 2016.05.003 · DOI
  72. Nguyen, T. V., McCracken, J. T., Albaugh, M. D., Botteron, K. N., Hudziak, J. J., & Ducharme, S. (2016). A testos- terone-related structural brain phenotype predicts aggressive behavior from childhood to adulthood. Psy- choneuroendocrinology, 63, 109-118. https://doi.org/10. 1016/j.psyneuen.2015.09.021 · DOI
  73. Nguyen, T. V., McCracken, J., Ducharme, S., Botteron, K. N., Mahabir, M., Johnson, W., . . . Grp, B. D. C. (2013). Testosterone-related cortical maturation across child- hood and adolescence. Cerebral Cortex, 23, 1424-1432. https://doi.org/10.1093/cercor/bhs125 · DOI
  74. Nguyen, T. V., McCracken, J. T., Ducharme, S., Cropp, B. F., Botteron, K. N., Evans, A. C., & Karama, S. (2013). Interactive effects of dehydroepiandrosterone and testosterone on cortical thickness during early brain development. Journal of Neuroscience, 33, 10840-10848. https://doi.org/10.1523/JNEUROSCI.5747-12.2013 · DOI
  75. Nunez, J. L., Sodhi, J., & Juraska, J. M. (2002). Ovarian hormones after postnatal day 20 reduce neuron num- ber in the rat primary visual cortex. Journal of Neurobi- ology, 52, 312-321. https://doi.org/10.1002/neu.10092 · DOI
  76. Op de Macks, Z. A., Bunge, S. A., Bell, O. N., Kriegsfeld, L. J., Kayser, A. S., & Dahl, R. E. (2017). The effect of social rank feedback on risk taking and associated reward processes in adolescent girls. Social Cognitive and Affective Neuroscience, 12, 240-250. https://doi.org/ 10.1093/scan/nsw125 · DOI
  77. Op de Macks, Z. A., Bunge, S. A., Bell, O. N., Wilbrecht, L., Kriegsfeld, L. J., Kayser, A. S., & Dahl, R. E. (2016). Risky decision-making in adolescent girls: The role of pubertal hormones and reward circuitry. Psychoneu- roendocrinology, 74, 77-91. https://doi.org/10.1016/j. psyneuen.2016.08.013 · DOI
  78. Paikoff, R. L., & Brooks-Gunn, J. (1991). Do parent-child relationships change during puberty? Psychological Bul- letin, 110(1), 47. https://doi.org/10.1037/0033-2909.110. 1.47 · DOI
  79. Pangelinan, M. M., Leonard, G., Perron, M., Pike, G. B., Richer, L., Veillette, S., . . . Paus, T. (2016). Puberty and testosterone shape the corticospinal tract during male adolescence. Brain Structure and Function, 221, 1083- 1094. https://doi.org/10.1007/s00429-014-0956-9 · DOI
  80. Paus, T., Keshavan, M., & Giedd, J. N. (2008). Why do many psychiatric disorders emerge during adoles- cence? Nature Reviews Neuroscience, 9, 947-957. https://doi.org/10.1038/nrn2513 · DOI · Paper page
  81. Paus, T., Wong, A. P. Y., Syme, C., & Pausova, Z. (2017). Sex differences in the adolescent brain and body: Find- ings from the Saguenay youth study. Journal of Neuro- science Research, 95, 362-370. https://doi.org/10.1002/ jnr.23825 · DOI
  82. Pellis, S. M. (2002). Sex differences in play fighting revis- ited: Traditional and nontraditional mechanisms of sexual differentiation in rats. Archives of Sexual Behav- ior, 31(1), 17-26. https://doi.org/10.1023/A: 1014070916047 · DOI · Paper page
  83. Peper, J. S., De Reus, M. A., Van Den Heuvel, M. P., & Schutter, D. J. (2015). Short fused? Associations between white matter connections, sex steroids, and aggression across adolescence. Human Brain Mapping, 36, 1043-1052. https://doi.org/10.1002/hbm.22684 · DOI
  84. Peper, J. S., Koolschijn, P. C., & Crone, E. A. (2013). Devel- opment of risk taking: Contributions from adolescent testosterone and the orbito-frontal cortex. Journal of Cognitive Neuroscience, 25, 2141-2150. https://doi.org/ 10.1162/jocn_a_00445 · DOI
  85. Peper, J. S., van den Heuvel, M. P., Mandl, R. C., Hul- shoff Pol, H. E., & van Honk, J. (2011). Sex steroids and connectivity in the human brain: A review of neu- roimaging studies. Psychoneuroendocrinology, 36, 1101- 1113. https://doi.org/10.1016/j.psyneuen.2011.05.004 · DOI
  86. Pesaresi, M., Soon-Shiong, R., French, L., Kaplan, D. R., Miller, F. D., & Paus, T. (2015). Axon diameter and axonal transport: In vivo and in vitro effects of andro- gens. NeuroImage, 115, 191-201. https://doi.org/10. 1016/j.neuroimage.2015.04.048 · DOI
  87. Peters, S., Jolles, D. J., Van Duijvenvoorde, A. C. K., Crone, E. A., & Peper, J. S. (2015). The link between testosterone and amygdala-orbitofrontal cortex connec- tivity in adolescent alcohol use. Psychoneuroendocrinol- ogy, 53, 117-126. https://doi.org/10.1016/j.psyneuen. 2015.01.004 · DOI · Paper page
  88. Petersen, A. C., Crockett, L., Richards, M., & Boxer, A. (1988). A self-report measure of pubertal status: Relia- bility, validity, and initial norms. Journal of Youth and Adolescence, 17, 117-133. https://doi.org/10.1007/ BF01537962 · DOI · Paper page
  89. Raznahan, A., Shaw, P. W., Lerch, J. P., Clasen, L. S., Green- stein, D., Berman, R., . . . Giedd, J. N. (2014). Longitudinal four-dimensional mapping of subcortical anatomy in human development. Proceedings of the National Academy of Sciences of the United States of America, 111, 1592-1597. https://doi.org/10.1073/pnas.1316911111 · DOI · Paper page
  90. Schmithorst, V. J., & Yuan, W. H. (2010). White matter development during adolescence as shown by diffusion MRI. Brain and Cognition, 72(1), 16-25. https://doi.org/ 10.1016/j.bandc.2009.06.005 · DOI · Paper page
  91. Schulz, K. M., & Sisk, C. L. (2006). Pubertal hormones, the adolescent brain, and the maturation of social behav- iors: Lessons from the Syrian hamster. Molecular and Cel- lular Endocrinology, 254-255, 120-126. https://doi.org/ 10.1016/j.mce.2006.04.025 · DOI
  92. Schutter, D. J., Peper, J. S., Koppeschaar, H. P., Kahn, R. S., & van Honk, J. (2005). Administration of testos- terone increases functional connectivity in a cortico- cortical depression circuit. Journal of Neuropsychiatry and Clinical Neurosciences, 17, 372-377. https://doi.org/ 10.1176/jnp.17.3.372 · DOI
  93. Shirtcliff, E. A., Dahl, R. E., & Pollak, S. D. (2009). Pubertal development: Correspondence between hor- monal and physical development. Child Development, 80, 327-337. https://doi.org/10.1111/j.1467-8624.2009. 01263.x · DOI · Paper page
  94. Sholl, S. A., & Kim, K. L. (1989). Estrogen receptors in the rhesus monkey brain during fetal development. Developmental Brain Research, 50, 189-196. https://doi. org/10.1016/0165-3806(89)90194-6 · DOI
  95. Shughrue, P. J., Lane, M. V., & Merchenthaler, I. (1997). Regulation of progesterone receptor messenger ribonu- cleic acid in the rat medial preoptic nucleus by estro- genic and antiestrogenic compounds: An in situ hybridization study. Endocrinology, 138, 5476-5484. https://doi.org/10.1210/endo.138.12.5595 · DOI
  96. Silk, J. S., Siegle, G. J., Lee, K. H., Nelson, E. E., Stroud, L. R., & Dahl, R. E. (2014). Increased neural response to peer rejection associated with adolescent depression and puber- tal development. Social Cognitive and Affective Neuroscience, 9, 1798-1807. https://doi.org/10.1093/scan/nst175 · DOI · Paper page
  97. Simmonds, D. J., Hallquist, M. N., Asato, M., & Luna, B. (2014). Developmental stages and sex differences of white matter and behavioral development through adolescence: A longitudinal diffusion tensor imaging (DTI) study. NeuroImage, 92, 356-368. https://doi.org/ 10.1016/j.neuroimage.2013.12.044 · DOI
  98. Spielberg, J. M., Forbes, E. E., Ladouceur, C. D., Worth- man, C. M., Olino, T. M., Ryan, N. D., & Dahl, R. E. (2015). Pubertal testosterone influences threat-related amygdala-orbitofrontal cortex coupling. Social Cognitive and Affective Neuroscience, 10, 408-415. https://doi.org/ 10.1093/scan/nsu062 · DOI
  99. Spreckelmeyer, K. N., Krach, S., Kohls, G., Rademacher, L., Irmak, A., Konrad, K., . . . Grunder, G. (2009). Anticipation of monetary and social reward differently activates mesolimbic brain structures in men and women. Social Cognitive and Affective Neuroscience, 4, 158-165. https://doi.org/10.1093/scan/nsn051 · DOI · Paper page
  100. Sripada, R. K., Swain, J. E., Evans, G. W., Welsh, R. C., & Liberzon, I. (2014). Childhood poverty and stress reactivity are associated with aberrant functional connectivity in default mode network. Neuropsychopharma- cology, 39, 2244-2251. https://doi.org/10.1038/npp.2014. · DOI
  101. Steen, R. G., Hamer, R. M., & Lieberman, J. A. (2007). Mea- suring brain volume by MR imaging: Impact of mea- surement precision and natural variation on sample size requirements. American Journal of Neuroradiology, 28, 1119-1125. https://doi.org/10.3174/ajnr.A0537 · DOI
  102. Stevens, J. S., & Hamann, S. (2012). Sex differences in brain activation to emotional stimuli: A meta-analysis of neuroimaging studies. Neuropsychologia, 50, 1578- 1593. https://doi.org/10.1016/j.neuropsychologia.2012. 03.011 · DOI · Paper page
  103. Tyborowska, A., Volman, I., Smeekens, S., Toni, I., & Roelofs, K. (2016). Testosterone during puberty shifts emotional control from pulvinar to anterior prefrontal cortex. Journal of Neuroscience, 36, 6156-6164. https://doi.org/10.1523/JNEUROSCI.3874-15.2016 · DOI · Paper page
  104. van den Bulk, B. G., Koolschijn, P. C. M., Meens, P. H., van Lang, N. D., van der Wee, N. J., Rombouts, S. A., . . . Crone, E. A. (2013). How stable is activation in the amygdala and prefrontal cortex in adolescence? A study of emotional face processing across three mea- surements. Developmental Cognitive Neuroscience, 4, 65- 76. https://doi.org/10.1016/j.dcn.2012.09.005 · DOI
  105. Van Duijvenvoorde, A. C. K., Achterberg, M., Braams, B. R., Peters, S., & Crone, E. A. (2016). Testing a dual-sys- tems model of adolescent brain development using resting-state connectivity analyses. NeuroImage, 124, 409-420. https://doi.org/10.1016/j.neuroimage.2015. 04.069 · DOI
  106. van Duijvenvoorde, A. C. K., Op de Macks, Z. A., Over- gaauw, S., Gunther Moor, B., Dahl, R. E., & Crone, E. A. (2014). A cross-sectional and longitudinal analysis of reward-related brain activation: Effects of age, pubertal stage, and reward sensitivity. Brain and Cognition, 89, 3- 14. https://doi.org/10.1016/j.bandc.2013.10.005 · DOI · Paper page
  107. van Leijenhorst, L., Zanolie, K., Van Meel, C. S., Westen- berg, P. M., Rombouts, S. A., & Crone, E. A. (2010). What motivates the adolescent? Brain regions mediat- ing reward sensitivity across adolescence. Cerebral Cor- tex, 20(1), 61-69. https://doi.org/10.1093/cercor/ bhp078 · DOI · Paper page
  108. van Wingen, G. A., Ossewaarde, L., Backstrom, T., Her- mans, E. J., & Fernandez, G. (2011). Gonadal hormone regulation of the emotion circuitry in humans. Neuroscience, 191, 38-45. https://doi.org/10.1016/j.neu roscience.2011.04.042 · DOI
  109. Verdonck, A., Gaethofs, M., Carels, C., & de Zegher, F. (1999). Effect of low-dose testosterone treatment on craniofacial growth in boys with delayed puberty. Euro- pean Journal of Orthodontics, 21, 137-143. https://doi. org/10.1093/ejo/21.2.137 · DOI
  110. V ertes, P. E., & Bullmore, E. T. (2015). Annual research review: Growth connectomics: The organization and reorganization of brain networks during normal and abnormal development. Journal of Child Psychology and Psychiatry, 56, 299-320. https://doi.org/10.1111/jcpp. 12365 · DOI · Paper page
  111. Walf, A. A., Koonce, C. J., & Frye, C. A. (2008). Estradiol or diarylpropionitrile decrease anxiety-like behavior of wildtype, but not estrogen receptor beta knockout, mice. Behavioral Neuroscience, 122, 974. https://doi.org/ 10.1037/a0012749 · DOI
  112. Wang, Y., Adamson, C., Yuan, W., Altaye, M., Rajagopal, A., Byars, A. W., & Holland, S. K. (2012). Sex differ- ences in white matter development during adoles- cence: A DTI study. Brain Research, 1478, 1-15. https://doi.org/10.1016/j.brainres.2012.08.038 · DOI
  113. Wierenga, L. M., Bos, M., Schreuders, E., Van de Kamp, F., Peper, J. S., Tamnes, C. K., & Crone, E. A. (2018). Unraveling age, puberty and testosterone effects on subcortical brain development across adolescence. Psy- choneuroendocrinology, 91, 105-114. https://doi.org/10. 1093/cercor/bhx154 · DOI
  114. Wierenga, L. M., Sexton, J. A., Laake, P., Giedd, J. N., & Tamnes, C. K. (2017). A key characteristic of sex differ- ences in the developing brain: Greater variability in brain structure of boys than girls. Cerebral Cortex. Advance online publication. https://doi.org/10.1093/cercor/ bhx154 · DOI
  115. Wierenga, L. M., van den Heuvel, M. P., van Dijk, S., Rijks, Y., de Reus, M. A., & Durston, S. (2016). The development of brain network architecture. Human Brain Mapping, 37, 717-729. https://doi.org/10.1002/ hbm.23062 · DOI
  116. Zehr, J. L., Nichols, L. R., Schulz, K. M., & Sisk, C. L. (2008). Adolescent development of neuron structure in dentate gyrus granule cells of male Syrian hamsters. Developmental Neurobiology, 68, 1517-1526. https://doi. org/10.1002/dneu.20675 · DOI
  117. Zeng, L. L., Shen, H., Liu, L., Wang, L. B., Li, B. J., Fang, P., . . . Hu, D. W. (2012). Identifying major depression using whole-brain functional connectivity: A multivari- ate pattern analysis. Brain, 135, 1498-1507. https://doi. org/10.1093/brain/aws059 · DOI · Paper page

Cited by

Sorted by citations

Authors
Goddings, A., Beltz, A., Peper, J. S., Crone, E. A., & Braams, B. R.
Affiliations
  • University College London (GB)
  • University of Michigan (US)
  • Leiden University (NL)
  • Harvard University (US)
Corresponding author
Goddings, Anne‐Lise
ORCID
Venue
Journal of Research on Adolescence
Publisher
Wiley
Published
2019-03
Volume
29
Issue
1
Pages
32-53
ISSN
  • 1050-8392 (ISSN-L)
  • 1532-7795
DOI
10.1111/jora.12408
OpenAlex
W2920817255
Cited by
219
References
26
Citations by year
2026: 26 · 2025: 24 · 2024: 27 · 2023: 55 · 2022: 32 · 2021: 20 · 2020: 20 · 2019: 14
FWCI
2.72
Type
journal article
Language
en
Open access
Licence
onlinelibrary.wiley.com/termsAndConditions#vor (vor, 13 d)
Locations
  • Journal of Research on Adolescence (publishedVersion)
  • PubMed (publishedVersion)
  • Leiden Repository (Leiden University) (submittedVersion)
  • Deep Blue (University of Michigan) (submittedVersion)
  • VU Research Portal (submittedVersion, other-oa)
  • Data Archiving and Networked Services (DANS) (submittedVersion)
  • Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
Funders
National Institute for Health and Care Research (CL-2016-18-007)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
  • Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
Keywords
puberty, adolescent brain development, structural brain development, brain reorganization, brain connectivity, sex differences, brain maturation
MeSH terms
Adolescent Health, Adolescent, Adolescent Behavior, Brain, Female, Humans, Magnetic Resonance Imaging, Male, Puberty, Sex Characteristics, Sexual Maturation, Social Behavior, Adolescent Development, Theory of Mind, Neuroimaging

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