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Understanding adolescence as a period of social–affective engagement and goal flexibility

Nature Reviews Neuroscience volume 13, pages 636–650 (2012)Cite this article

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Key Points

  • Adolescence is a time of marked improvements in cognitive abilities, such as abstract reasoning, problem solving and creative thought. More generally, it is also an important developmental period for maturational advancements in cognitive, affective and social capacities.

  • At the same time, adolescence is characterized by increased risk-taking, sensation-seeking and sensitivity to social evaluation, and these contribute to a wide range of serious health consequences in adolescence, including substance use, accidents, violence and suicide.

  • Several established models of adolescent brain development have suggested that these serious health problems emerging in adolescence can be explained by a relative immaturity in regions of the prefrontal cortex (which is thought to be important for the regulation of behaviour and emotions) in the face of rapid maturation of limbic brain regions (leading to intensification of emotions).

  • Using a meta-analysis of functional MRI data, we examined the evidence for these changes in brain function in relation to cognitive control, social–affective processing and social–cognitive reasoning over the course of adolescent development.

  • We conclude that the neuroimaging evidence for a slow maturation of cognitive control regions across adolescence is relatively inconsistent, with some studies reporting increases and others finding decreases in activation.

  • We found more consistent evidence for increased limbic responses to affective stimuli such as rewards, emotional faces and social feedback, peaking in mid-adolescence.

  • Brain regions involved in understanding others' intentions in social reasoning, such as the anterior medial prefrontal cortex and temporoparietal junction, show changes in relative contributions over the course of adolescent development.

  • On the basis of the meta-analysis and new insights from other research, we present a heuristic model that views adolescent brain development as a period of social and affective engagement and a time of learning and flexibility in adjusting goals and priorities. A key component of this model focuses on the impact of puberty on social–affective development.

Abstract

Research has demonstrated that extensive structural and functional brain development continues throughout adolescence. A popular notion emerging from this work states that a relative immaturity in frontal cortical neural systems could explain adolescents' high rates of risk-taking, substance use and other dangerous behaviours. However, developmental neuroimaging studies do not support a simple model of frontal cortical immaturity. Rather, growing evidence points to the importance of changes in social and affective processing, which begin around the onset of puberty, as crucial to understanding these adolescent vulnerabilities. These changes in social–affective processing also may confer some adaptive advantages, such as greater flexibility in adjusting one's intrinsic motivations and goal priorities amidst changing social contexts in adolescence.

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Figure 1: Meta-analysis of functional MRI studies in adolescents.
Figure 2: Interactive decision-making paradigms to examine social reasoning.
Figure 3: A model of adolescent brain development.

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References

  1. Dahl, R. E. & Gunnar, M. R. Heightened stress responsiveness and emotional reactivity during pubertal maturation: implications for psychopathology. Dev. Psychopathol. 21, 1–6 (2009).

    Article  PubMed  Google Scholar 

  2. Steinberg, L. A. Social neuroscience perspective on adolescent risk-taking. Dev. Rev. 28, 78–106 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  3. Blakemore, S. J., Burnett, S. & Dahl, R. E. The role of puberty in the developing adolescent brain. Hum. Brain Mapp. 31, 926–933 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  4. Arnett, J. J. Adolescence and Emerging Adulthood: A Cultural Approach (Prentice Hall, 2004).

    Google Scholar 

  5. Dahl, R. E. & Vanderschuren, L. J. The feeling of motivation in the developing brain. Dev. Cogn. Neurosci. 1, 361–363 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  6. Gladwin, T. E., Figner, B., Crone, E. A. & Wiers, R. W. Addiction, adolescence, and the integration of control and motivation. Dev. Cogn. Neurosci. 1, 364–376 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  7. Somerville, L. H., Jones, R. M. & Casey, B. J. A time of change: behavioral and neural correlates of adolescent sensitivity to appetitive and aversive environmental cues. Brain Cogn. 72, 124–133 (2010). An influential paper that describes the dual processing model, suggesting that adolescence is characterized by faster maturation of subcortical brain regions relative to frontal cortical regions.

    Article  PubMed  Google Scholar 

  8. Ernst, M. & Fudge, J. L. A developmental neurobiological model of motivated behavior: anatomy, connectivity and ontogeny of the triadic nodes. Neurosci. Biobehav. Rev. 33, 367–382 (2009).

    Article  PubMed  Google Scholar 

  9. Steinberg, L. et al. Age differences in sensation seeking and impulsivity as indexed by behavior and self-report: evidence for a dual systems model. Dev. Psychol. 44, 1764–1778 (2008).

    Article  PubMed  Google Scholar 

  10. Nelson, E. E., Leibenluft, E., McClure, E. B. & Pine, D. S. The social re-orientation of adolescence: a neuroscience perspective on the process and its relation to psychopathology. Psychol. Med. 35, 163–174 (2005).

    Article  PubMed  Google Scholar 

  11. Nelson, E. E. & Guyer, A. E. The development of the ventral prefrontal cortex and social flexibility. Dev. Cogn. Neurosci. 1, 233–245 (2011). A very interesting paper that focuses on the role of ventral prefrontal circuitry and social flexibility in adolescent development.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Pfeifer, J. H. & Allen, N. B. Arrested development? Reconsidering dual-systems models of brain function in adolescence and disorders. Trends Cogn. Sci. 16, 322–329 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  13. Asato, M. R., Sweeney, J. A. & Luna, B. Cognitive processes in the development of TOL performance. Neuropsychologia 44, 2259–2269 (2006).

    Article  PubMed  Google Scholar 

  14. Huizinga, M., Dolan, C. V. & van der Molen, M. W. Age-related change in executive function: developmental trends and a latent variable analysis. Neuropsychologia 44, 2017–2036 (2006).

    Article  PubMed  Google Scholar 

  15. Case, R. The Mind's Staircase: Exploring the Conceptual Underpinnings of Children's Thought and Knowledge (Erlbaum, 1992).

    Google Scholar 

  16. Zelazo, P. D., Craik, F. I. & Booth, L. Executive function across the life span. Acta Psychol. (Amst.) 115, 167–183 (2004).

    Article  Google Scholar 

  17. Zelazo, P. D. The development of conscious control in childhood. Trends Cogn. Sci. 8, 12–17 (2004).

    Article  PubMed  Google Scholar 

  18. Miyake, A. et al. The unity and diversity of executive functions and their contributions to complex “Frontal Lobe” tasks: a latent variable analysis. Cogn. Psychol. 41, 49–100 (2000).

    Article  CAS  PubMed  Google Scholar 

  19. Miller, E. K. & Cohen, J. D. An integrative theory of prefrontal cortex function. Annu. Rev. Neurosci. 24, 167–202 (2001).

    Article  CAS  PubMed  Google Scholar 

  20. Kwon, H., Reiss, A. L. & Menon, V. Neural basis of protracted developmental changes in visuo-spatial working memory. Proc. Natl Acad. Sci. USA 99, 13336–13341 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Klingberg, T., Forssberg, H. & Westerberg, H. Increased brain activity in frontal and parietal cortex underlies the development of visuospatial working memory capacity during childhood. J. Cogn. Neurosci. 14, 1–10 (2002).

    Article  PubMed  Google Scholar 

  22. Schweinsburg, A. D., Nagel, B. J. & Tapert, S. F. fMRI reveals alteration of spatial working memory networks across adolescence. J. Int. Neuropsychol. Soc. 11, 631–644 (2005).

    Article  PubMed  PubMed Central  Google Scholar 

  23. Scherf, K. S., Sweeney, J. A. & Luna, B. Brain basis of developmental change in visuospatial working memory. J. Cogn. Neurosci. 18, 1045–1058 (2006).

    Article  PubMed  Google Scholar 

  24. Crone, E. A., Wendelken, C., Donohue, S., van Leijenhorst, L. & Bunge, S. A. Neurocognitive development of the ability to manipulate information in working memory. Proc. Natl Acad. Sci. USA 103, 9315–9320 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Ciesielski, K. T., Lesnik, P. G., Savoy, R. L., Grant, E. P. & Ahlfors, S. P. Developmental neural networks in children performing a Categorical N-Back Task. Neuroimage 33, 980–990 (2006).

    Article  PubMed  Google Scholar 

  26. Olesen, P. J., Macoveanu, J., Tegner, J. & Klingberg, T. Brain activity related to working memory and distraction in children and adults. Cereb. Cortex 17, 1047–1054 (2007).

    Article  PubMed  Google Scholar 

  27. Thomason, M. E. et al. Development of spatial and verbal working memory capacity in the human brain. J. Cogn. Neurosci. 21, 316–332 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  28. O'Hare, E. D., Lu, L. H., Houston, S. M., Bookheimer, S. Y. & Sowell, E. R. Neurodevelopmental changes in verbal working memory load-dependency: an fMRI investigation. Neuroimage 42, 1678–1685 (2008).

    Article  PubMed  Google Scholar 

  29. Jolles, D. D., Kleibeuker, S. W., Rombouts, S. A. & Crone, E. A. Developmental differences in prefrontal activation during working memory maintenance and manipulation for different memory loads. Dev. Sci. 14, 713–724 (2011).

    Article  PubMed  Google Scholar 

  30. Wendelken, C., Baym, C. L., Gazzaley, A. & Bunge, S. A. Neural indices of improved attentional modulation over middle childhood. Dev. Cogn. Neurosci. 1, 175–186 (2011).

    Article  CAS  PubMed  Google Scholar 

  31. Adleman, N. E. et al. A developmental fMRI study of the Stroop color-word task. Neuroimage 16, 61–75 (2002).

    Article  PubMed  Google Scholar 

  32. Bunge, S. A., Dudukovic, N. M., Thomason, M. E., Vaidya, C. J. & Gabrieli, J. D. Immature frontal lobe contributions to cognitive control in children: evidence from fMRI. Neuron 33, 301–311 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Casey, B. J., Thomas, K. M., Davidson, M. C., Kunz, K. & Franzen, P. L. Dissociating striatal and hippocampal function developmentally with a stimulus–response compatibility task. J. Neurosci. 22, 8647–8652 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Marsh, R. et al. A developmental fMRI study of self-regulatory control. Hum. Brain Mapp. 27, 848–863 (2006).

    Article  PubMed  PubMed Central  Google Scholar 

  35. Rubia, K. et al. Progressive increase of frontostriatal brain activation from childhood to adulthood during event-related tasks of cognitive control. Hum. Brain Mapp. 27, 973–993 (2006).

    Article  PubMed  PubMed Central  Google Scholar 

  36. Rubia, K., Smith, A. B., Taylor, E. & Brammer, M. Linear age-correlated functional development of right inferior fronto-striato-cerebellar networks during response inhibition and anterior cingulate during error-related processes. Hum. Brain Mapp. 28, 1163–1177 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  37. Casey, B. J. et al. Early development of subcortical regions involved in non-cued attention switching. Dev. Sci. 7, 534–542 (2004).

    Article  CAS  PubMed  Google Scholar 

  38. Christakou, A. et al. Sex-dependent age modulation of frontostriatal and temporoparietal activation during cognitive control. Neuroimage 48, 223–236 (2009).

    Article  PubMed  Google Scholar 

  39. Crone, E. A., Donohue, S. E., Honomichl, R., Wendelken, C. & Bunge, S. A. Brain regions mediating flexible rule use during development. J. Neurosci. 26, 11239–11247 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Bunge, S. A. & Wright, S. B. Neurodevelopmental changes in working memory and cognitive control. Curr. Opin. Neurobiol. 17, 243–250 (2007).

    Article  CAS  PubMed  Google Scholar 

  41. Geier, C. F., Garver, K., Terwilliger, R. & Luna, B. Development of working memory maintenance. J. Neurophysiol. 101, 84–99 (2009).

    Article  PubMed  Google Scholar 

  42. Brahmbhatt, S. B., McAuley, T. & Barch, D. M. Functional developmental similarities and differences in the neural correlates of verbal and nonverbal working memory tasks. Neuropsychologia 46, 1020–1031 (2008).

    Article  PubMed  Google Scholar 

  43. Libertus, M. E., Brannon, E. M. & Pelphrey, K. A. Developmental changes in category-specific brain responses to numbers and letters in a working memory task. Neuroimage 44, 1404–1414 (2009).

    Article  PubMed  Google Scholar 

  44. Tamm, L., Menon, V. & Reiss, A. L. Maturation of brain function associated with response inhibition. J. Am. Acad. Child Adolesc. Psychiatry 41, 1231–1238 (2002).

    Article  PubMed  Google Scholar 

  45. Durston, S. et al. A shift from diffuse to focal cortical activity with development. Dev. Sci. 9, 1–8 (2006).

    Article  PubMed  Google Scholar 

  46. Booth, J. R. et al. Neural development of selective attention and response inhibition. Neuroimage 20, 737–751 (2003).

    Article  PubMed  Google Scholar 

  47. Velanova, K., Wheeler, M. E. & Luna, B. The maturation of task set-related activation supports late developmental improvements in inhibitory control. J. Neurosci. 29, 12558–12567 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Cohen, J. R. et al. Decoding developmental differences and individual variability in response inhibition through predictive analyses across individuals. Front. Hum. Neurosci. 4, 47 (2010).

    PubMed  PubMed Central  Google Scholar 

  49. Konrad, K. et al. Development of attentional networks: an fMRI study with children and adults. Neuroimage 28, 429–439 (2005).

    Article  PubMed  Google Scholar 

  50. Morton, J. B., Bosma, R. & Ansari, D. Age-related changes in brain activation associated with dimensional shifts of attention: an fMRI study. Neuroimage 46, 249–256 (2009).

    Article  PubMed  Google Scholar 

  51. Luna, B. et al. Maturation of widely distributed brain function subserves cognitive development. Neuroimage 13, 786–793 (2001).

    Article  CAS  PubMed  Google Scholar 

  52. Brahmbhatt, S. B., White, D. A. & Barch, D. M. Developmental differences in sustained and transient activity underlying working memory. Brain Res. 1354, 140–151 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Johnson, M. H., Grossmann, T. & Cohen Kadosh, K. Mapping functional brain development: building a social brain through interactive specialization. Dev. Psychol. 45, 151–159 (2009).

    Article  PubMed  Google Scholar 

  54. Luna, B., Padmanabhan, A. & O'Hearn, K. What has fMRI told us about the development of cognitive control through adolescence? Brain Cogn. 72, 101–113 (2010).

    Article  PubMed  Google Scholar 

  55. Crone, E. A., Zanolie, K., Van Leijenhorst, L., Westenberg, P. M. & Rombouts, S. A. Neural mechanisms supporting flexible performance adjustment during development. Cogn. Affect. Behav. Neurosci. 8, 165–177 (2008).

    Article  PubMed  Google Scholar 

  56. Cohen, J. R. et al. A unique adolescent response to reward prediction errors. Nature Neurosci. 13, 669–671 (2010). One of the first studies investigating the development of the prediction error in adolescents. It describes how this may underpin some changes in risk-taking in adolescence.

    Article  CAS  PubMed  Google Scholar 

  57. van den Bos, W., Guroglu, B., van den Bulk, B. G., Rombouts, S. A. & Crone, E. A. Better than expected or as bad as you thought? The neurocognitive development of probabilistic feedback processing. Front. Hum. Neurosci. 3, 52 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  58. van Duijvenvoorde, A. C., Zanolie, K., Rombouts, S. A., Raijmakers, M. E. & Crone, E. A. Evaluating the negative or valuing the positive? Neural mechanisms supporting feedback-based learning across development. J. Neurosci. 28, 9495–9503 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Velanova, K., Wheeler, M. E. & Luna, B. Maturational changes in anterior cingulate and frontoparietal recruitment support the development of error processing and inhibitory control. Cereb. Cortex 18, 2505–2522 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  60. Dumontheil, I., Houlton, R., Christoff, K. & Blakemore, S. J. Development of relational reasoning during adolescence. Dev. Sci. 13, F15–F24 (2010).

    Article  PubMed  Google Scholar 

  61. Dumontheil, I., Hassan, B., Gilbert, S. J. & Blakemore, S. J. Development of the selection and manipulation of self-generated thoughts in adolescence. J. Neurosci. 30, 7664–7671 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Wright, S. B., Matlen, B. J., Baym, C. L., Ferrer, E. & Bunge, S. A. Neural correlates of fluid reasoning in children and adults. Front. Hum. Neurosci. 1, 8 (2007).

    PubMed  Google Scholar 

  63. Crone, E. A. et al. Neurocognitive development of relational reasoning. Dev. Sci. 12, 55–66 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  64. Fuligni, A. J. in Research on Minority Adolescents: Conceptual, Theoretical, and Methodological Issues (eds McLoyd, V. & Steinberg, L.) 127–143 (Erlbaum, 1998).

    Google Scholar 

  65. Finn, A. S., Sheridan, M. A., Kam, C. L., Hinshaw, S. & D'Esposito, M. Longitudinal evidence for functional specialization of the neural circuit supporting working memory in the human brain. J. Neurosci. 30, 11062–11067 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Koolschijn, P. C., Schel, M. A., de Rooij, M., Rombouts, S. A. & Crone, E. A. A three-year longitudinal functional magnetic resonance imaging study of performance monitoring and test-retest reliability from childhood to early adulthood. J. Neurosci. 31, 4204–4212 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Jolles, D. D., van Buchem, M. A., Rombouts, S. A. & Crone, E. A. Practice effects in the developing brain: a pilot study. Dev. Cogn. Neurosci. 2 (Suppl. 1), 180–191 (2012).

    Article  Google Scholar 

  68. Jolles, D. D., van Buchem, M. A., Crone, E. A. & Rombouts, S. A. A comprehensive study of whole-brain functional connectivity in children and young adults. Cereb. Cortex 21, 385–391 (2011).

    Article  PubMed  Google Scholar 

  69. Fair, D. A. et al. Development of distinct control networks through segregation and integration. Proc. Natl Acad. Sci. USA 104, 13507–13512 (2007). A thoughtful analysis of the development of resting state networks from childhood through adolescence.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Jolles, D. D., van Buchem, M. A., Crone, E. A. & Rombouts, S. A. Functional brain connectivity at rest changes after working memory training. Hum. Brain Mapp. 11 Nov 2011 (doi:10.1002/hbm.21444).

    Article  PubMed  PubMed Central  Google Scholar 

  71. Haber, S. N. & Knutson, B. The reward circuit: linking primate anatomy and human imaging. Neuropsychopharmacology 35, 4–26 (2010).

    Article  PubMed  Google Scholar 

  72. Ernst, M. et al. Amygdala and nucleus accumbens in responses to receipt and omission of gains in adults and adolescents. Neuroimage 25, 1279–1291 (2005).

    Article  PubMed  Google Scholar 

  73. Van Leijenhorst, L. et al. Adolescent risky decision-making: neurocognitive development of reward and control regions. Neuroimage 51, 345–355 (2010).

    Article  PubMed  Google Scholar 

  74. Van Leijenhorst, L. et al. What motivates the adolescent? Brain regions mediating reward sensitivity across adolescence. Cereb. Cortex 20, 61–69 (2010).

    Article  PubMed  Google Scholar 

  75. Galvan, A. et al. Earlier development of the accumbens relative to orbitofrontal cortex might underlie risk-taking behavior in adolescents. J. Neurosci. 26, 6885–6892 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Geier, C. F., Terwilliger, R., Teslovich, T., Velanova, K. & Luna, B. Immaturities in reward processing and its influence on inhibitory control in adolescence. Cereb. Cortex 20, 1613–1629 (2010). One of the first studies to demonstrate that incentives appear to have a particularly pronounced effect on cognitive control in adolescents.

    Article  CAS  PubMed  Google Scholar 

  77. Chein, J., Albert, D., O'Brien, L., Uckert, K. & Steinberg, L. Peers increase adolescent risk taking by enhancing activity in the brain's reward circuitry. Dev. Sci. 14, F1–F10 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  78. Smith, A. B., Halari, R., Giampetro, V., Brammer, M. & Rubia, K. Developmental effects of reward on sustained attention networks. Neuroimage 56, 1693–1704 (2011).

    Article  PubMed  Google Scholar 

  79. Christakou, A., Brammer, M. & Rubia, K. Maturation of limbic corticostriatal activation and connectivity associated with developmental changes in temporal discounting. Neuroimage 54, 1344–1354 (2011).

    Article  PubMed  Google Scholar 

  80. Padmanabhan, A., Geier, C. F., Ordaz, S. J., Teslovich, T. & Luna, B. Developmental changes in brain function underlying the influence of reward processing on inhibitory control. Dev. Cogn. Neurosci. 1, 517–529 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  81. Bjork, J. M. et al. Incentive-elicited brain activation in adolescents: similarities and differences from young adults. J. Neurosci. 24, 1793–1802 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Bjork, J. M., Smith, A. R., Chen, G. & Hommer, D. W. Adolescents, adults and rewards: comparing motivational neurocircuitry recruitment using fMRI. PLoS ONE 5, e11440 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Forbes, E. E. & Dahl, R. E. Pubertal development and behavior: hormonal activation of social and motivational tendencies. Brain Cogn. 72, 66–72 (2010).

    Article  PubMed  Google Scholar 

  84. Krain, A. L. et al. An fMRI examination of developmental differences in the neural correlates of uncertainty and decision-making. J. Child Psychol. Psychiatry 47, 1023–1030 (2006).

    Article  PubMed  Google Scholar 

  85. Eshel, N., Nelson, E. E., Blair, R. J., Pine, D. S. & Ernst, M. Neural substrates of choice selection in adults and adolescents: development of the ventrolateral prefrontal and anterior cingulate cortices. Neuropsychologia 45, 1270–1279 (2007).

    Article  PubMed  Google Scholar 

  86. Bjork, J. M., Smith, A. R., Danube, C. L. & Hommer, D. W. Developmental differences in posterior mesofrontal cortex recruitment by risky rewards. J. Neurosci. 27, 4839–4849 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Van den Bos, W., Cohen, M. X., Kahnt, T. & Crone, E. A. Striatum–medial prefrontal cortex connectivity predicts developmental differences in reinforcement learning. Cereb. Cortex 22, 1247–1255 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  88. Sugam, J. A., Day, J. J., Wightman, R. M. & Carelli, R. M. Phasic nucleus accumbens dopamine encodes risk-based decision-making behavior. Biol. Psychiatry 71, 199–205 (2012).

    Article  CAS  PubMed  Google Scholar 

  89. Killgore, W. D., Oki, M. & Yurgelun-Todd, D. A. Sex-specific developmental changes in amygdala responses to affective faces. Neuroreport 12, 427–433 (2001).

    Article  CAS  PubMed  Google Scholar 

  90. Monk, C. S. et al. Adolescent immaturity in attention-related brain engagement to emotional facial expressions. Neuroimage 20, 420–428 (2003).

    Article  PubMed  Google Scholar 

  91. Williams, L. M. et al. The mellow years?: neural basis of improving emotional stability over age. J. Neurosci. 26, 6422–6430 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Guyer, A. E. et al. A developmental examination of amygdala response to facial expressions. J. Cogn. Neurosci. 20, 1565–1582 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  93. Hare, T. A. et al. Biological substrates of emotional reactivity and regulation in adolescence during an emotional go-nogo task. Biol. Psychiatry 63, 927–934 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  94. Pfeifer, J. H. et al. Entering adolescence: resistance to peer influence, risky behavior, and neural changes in emotion reactivity. Neuron 69, 1029–1036 (2011). One of the first studies showing longitudinally that increases in striatum response may be adaptive.

    Article  CAS  PubMed  Google Scholar 

  95. Pine, D. S. et al. Cortical brain regions engaged by masked emotional faces in adolescents and adults: an fMRI study. Emotion 1, 137–147 (2001).

    Article  CAS  PubMed  Google Scholar 

  96. Thomas, K. M. et al. Amygdala response to facial expressions in children and adults. Biol. Psychiatry 49, 309–316 (2001).

    Article  CAS  PubMed  Google Scholar 

  97. Nelson, E. E. et al. Developmental differences in neuronal engagement during implicit encoding of emotional faces: an event-related fMRI study. J. Child Psychol. Psychiatry 44, 1015–1024 (2003).

    Article  PubMed  Google Scholar 

  98. Yurgelun-Todd, D. A. & Killgore, W. D. Fear-related activity in the prefrontal cortex increases with age during adolescence: a preliminary fMRI study. Neurosci. Lett. 406, 194–199 (2006).

    Article  CAS  PubMed  Google Scholar 

  99. Deeley, Q. et al. Changes in male brain responses to emotional faces from adolescence to middle age. Neuroimage 40, 389–397 (2008).

    Article  PubMed  Google Scholar 

  100. Somerville, L. H., Hare, T. & Casey, B. J. Frontostriatal maturation predicts cognitive control failure to appetitive cues in adolescents. J. Cogn. Neurosci. 23, 2123–2134 (2011).

    Article  PubMed  Google Scholar 

  101. Casey, B., Jones, R. M. & Somerville, L. H. Braking and accelerating of the adolescent brain. J. Res. Adolesc. 21, 21–33 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  102. Schaffer, H. R. Social Development (Blackwell,1996).

    Google Scholar 

  103. Steinberg, L. & Morris, A. S. Adolescent development. Annu. Rev. Psychol. 52, 83–110 (2001).

    Article  CAS  PubMed  Google Scholar 

  104. Burnett, S., Sebastian, C., Cohen Kadosh, K. & Blakemore, S. J. The social brain in adolescence: evidence from functional magnetic resonance imaging and behavioural studies. Neurosci. Biobehav. Rev. 35, 1654–1664 (2011).

    Article  PubMed  Google Scholar 

  105. Rilling, J. K. & Sanfey, A. G. The neuroscience of social decision-making. Annu. Rev. Psychol. 62, 23–48 (2011).

    Article  PubMed  Google Scholar 

  106. Blakemore, S. J. The social brain in adolescence. Nature Rev. Neurosci. 9, 267–277 (2008).

    Article  CAS  Google Scholar 

  107. Wang, A. T., Lee, S. S., Sigman, M. & Dapretto, M. Developmental changes in the neural basis of interpreting communicative intent. Soc. Cogn. Affect. Neurosci. 1, 107–121 (2006).

    Article  PubMed  PubMed Central  Google Scholar 

  108. Blakemore, S. J., den Ouden, H., Choudhury, S. & Frith, C. Adolescent development of the neural circuitry for thinking about intentions. Soc. Cogn. Affect. Neurosci. 2, 130–139 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  109. Moriguchi, Y., Ohnishi, T., Mori, T., Matsuda, H. & Komaki, G. Changes of brain activity in the neural substrates for theory of mind during childhood and adolescence. Psychiatry Clin. Neurosci. 61, 355–363 (2007).

    Article  PubMed  Google Scholar 

  110. Kobayashi, C., Glover, G. H. & Temple, E. Children's and adults' neural bases of verbal and nonverbal 'theory of mind'. Neuropsychologia 45, 1522–1532 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  111. Burnett, S., Bird, G., Moll, J., Frith, C. & Blakemore, S. J. Development during adolescence of the neural processing of social emotion. J. Cogn. Neurosci. 21, 1736–1750 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  112. Saxe, R. R., Whitfield-Gabrieli, S., Scholz, J. & Pelphrey, K. A. Brain regions for perceiving and reasoning about other people in school-aged children. Child Dev. 80, 1197–1209 (2009).

    Article  PubMed  Google Scholar 

  113. Gunther Moor, B. et al. Neurodevelopmental changes of reading the mind in the eyes. Soc. Cogn. Affect. Neurosci. 7, 44–52 (2012).

    Article  Google Scholar 

  114. Sebastian, C. L. et al. Neural processing associated with cognitive and affective Theory of Mind in adolescents and adults. Soc. Cogn. Affect. Neurosci. 7, 53–63 (2012).

    Google Scholar 

  115. Pfeifer, J. H., Lieberman, M. D. & Dapretto, M. “I know you are but what am I?!”: neural bases of self- and social knowledge retrieval in children and adults. J. Cogn. Neurosci. 19, 1323–1337 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  116. Pfeifer, J. H. et al. Neural correlates of direct and reflected self-appraisals in adolescents and adults: when social perspective-taking informs self-perception. Child Dev. 80, 1016–1038 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  117. Eisenberg, N. & Fabes, F. in Handbook of Child Psychology: Social, Emotional, and Personality Development (eds Damon, W., Eisenberg, N. & Lerner, R.) 646–718 (Wiley, 2006).

    Google Scholar 

  118. Newcomb, A. F., Bukowski, W. M. & Pattee, L. Children's peer relations: a meta-analytic review of popular, rejected, neglected, controversial, and average sociometric status. Psychol. Bull. 113, 99–128 (1993).

    Article  CAS  PubMed  Google Scholar 

  119. Güth, W., Schmittberger, R. & Schwarze, B. An experimental analysis of ultimatum bargaining. J. Econom. Behav. Organiz. 3, 367 (1982).

    Article  Google Scholar 

  120. Berg, J., Dickhaut, J. & McCabe, K. Trust, reciprocity, and social history. Games Econom. Behav. 10, 122–142 (1995).

    Article  Google Scholar 

  121. Guroglu, B., van den Bos, W. & Crone, E. A. Fairness considerations: increasing understanding of intentionality during adolescence. J. Exp. Child Psychol. 104, 398–409 (2009).

    Article  PubMed  Google Scholar 

  122. van den Bos, W., Westenberg, M., van Dijk, E. & Crone, E. A. Development of trust and reciprocity in adolescence. Cogn. Dev. 25, 90–102 (2010).

    Article  Google Scholar 

  123. Steinbeis, N., Bernhardt, B. C. & Singer, T. Impulse control and underlying functions of the left DLPFC mediate age-related and age-independent individual differences in strategic social behavior. Neuron 73, 1040–1051 (2012).

    Article  CAS  PubMed  Google Scholar 

  124. Van Overwalle, F. Social cognition and the brain: a meta-analysis. Hum. Brain Mapp. 30, 829–858 (2009).

    Article  PubMed  Google Scholar 

  125. van den Bos, W., van Dijk, E., Westenberg, M., Rombouts, S. A. & Crone, E. A. What motivates repayment? Neural correlates of reciprocity in the Trust Game. Soc. Cogn. Affect. Neurosci. 4, 294–304 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  126. Guroglu, B., van den Bos, W., Rombouts, S. A. & Crone, E. A. Unfair? It depends: neural correlates of fairness in social context. Soc. Cogn. Affect. Neurosci. 5, 414–423 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  127. Guroglu, B., van den Bos, W., van Dijk, E., Rombouts, S. A. & Crone, E. A. Dissociable brain networks involved in development of fairness considerations: understanding intentionality behind unfairness. Neuroimage 57, 634–641 (2011).

    Article  PubMed  Google Scholar 

  128. van den Bos, W., van Dijk, E., Westenberg, M., Rombouts, S. A. & Crone, E. A. Changing brains, changing perspectives: the neurocognitive development of reciprocity. Psychol. Sci. 22, 60–70 (2011). A social interaction study that shows, using a neuroeconomics approach, a transition from self-referential processing to other-referential processing in adolescence.

    Article  PubMed  Google Scholar 

  129. Cillessen, A. H. & Rose, A. J. Understanding popularity in the peer system. Curr. Direct. Psychol. Sci. 14, 102–105 (2005).

    Article  Google Scholar 

  130. Decety, J. & Michalska, K. J. Neurodevelopmental changes in the circuits underlying empathy and sympathy from childhood to adulthood. Dev. Sci. 13, 886–899 (2010).

    Article  PubMed  Google Scholar 

  131. Gunther Moor, B., van Leijenhorst, L., Rombouts, S. A., Crone, E. A. & Van der Molen, M. W. Do you like me? Neural correlates of social evaluation and developmental trajectories. Soc. Neurosci. 5, 461–482 (2010).

    Article  PubMed  Google Scholar 

  132. Guyer, A. E., McClure-Tone, E. B., Shiffrin, N. D., Pine, D. S. & Nelson, E. E. Probing the neural correlates of anticipated peer evaluation in adolescence. Child Dev. 80, 1000–1015 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  133. Sebastian, C. L. et al. Effects of age and MAOA genotype on the neural processing of social rejection. Genes Brain Behav. 9, 628–637 (2010).

    CAS  PubMed  Google Scholar 

  134. Sebastian, C. L. et al. Developmental influences on the neural bases of responses to social rejection: implications of social neuroscience for education. Neuroimage 57, 686–694 (2011).

    Article  PubMed  Google Scholar 

  135. Gunther Moor, B. et al. Social exclusion and punishment of excluders: neural correlates and developmental trajectories. Neuroimage 59, 708–717 (2012). On the basis of a wide age range of participants, this is one of the first studies showing that social rejection in adolescence leads to subsequent punishment of excluders.

    Article  Google Scholar 

  136. Masten, C. L. et al. Neural correlates of social exclusion during adolescence: understanding the distress of peer rejection. Soc. Cogn. Affect. Neurosci. 4, 143–157 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  137. Masten, C. L., Telzer, E. H., Fuligni, A. J., Lieberman, M. D. & Eisenberger, N. I. Time spent with friends in adolescence relates to less neural sensitivity to later peer rejection. Soc. Cogn. Affect. Neurosci. 7, 106–114 (2012).

    Article  PubMed  Google Scholar 

  138. Masten, C. L. et al. Subgenual anterior cingulate responses to peer rejection: a marker of adolescents' risk for depression. Dev. Psychopathol. 23, 283–292 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  139. Angold, A., Costello, E. J. & Worthman, C. M. Puberty and depression: the roles of age, pubertal status, and pubertal timing. Psychol. Med. 28, 51–61 (1998).

    Article  CAS  PubMed  Google Scholar 

  140. Dahl, R. E. Adolescent brain development: a period of vulnerabilities and opportunities. Ann. NY Acad. Sci. 1021, 1–22 (2004).

    Article  PubMed  Google Scholar 

  141. Galvan, A. Adolescent development of the reward system. Front. Hum. Neurosci. 4, 6 (2010).

    PubMed  PubMed Central  Google Scholar 

  142. Steinberg, L. The Science of Adolescent Risk-Taking. (Washington, 2011).

    Google Scholar 

  143. Figner, B., Mackinlay, R. J., Wilkening, F. & Weber, E. U. Affective and deliberative processes in risky choice: age differences in risk taking in the Columbia Card Task. J. Exp. Psychol. Learn. Mem. Cogn. 35, 709–730 (2009).

    Article  PubMed  Google Scholar 

  144. Kleibeuker, S. W., De Dreu, C. K. W. & Crone, E. A. The development of creative cognition across adolescence: distinct trajectories for insight and divergent thinking. Dev. Sci. (in the press).

  145. Jacobs, E. & D'Esposito, M. Estrogen shapes dopamine-dependent cognitive processes: implications for women's health. J. Neurosci. 31, 5286–5293 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Gordon, I., Martin, C., Feldman, R. & Leckman, J. F. Oxytocin and social motivation. Dev. Cogn. Neurosci. 1, 471–493 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  147. Bos, P. A., Panksepp, J., Bluthe, R. M. & van Honk, J. Acute effects of steroid hormones and neuropeptides on human social–emotional behavior: a review of single administration studies. Front. Neuroendocrinol. 33, 17–35 (2012).

    Article  CAS  PubMed  Google Scholar 

  148. Eisenegger, C., Haushofer, J. & Fehr, E. The role of testosterone in social interaction. Trends Cogn. Sci. 15, 263–271 (2010). A compelling review on the influence of testosterone as a social hormone that influences social information processing and motivation.

    Article  CAS  Google Scholar 

  149. Carney, D. & Mason, M. F. Decision making and testosterone: when the ends justify the means. J. Exp. Social Psychol. 46, 668–671 (2010).

    Article  Google Scholar 

  150. Cooke, B. M. & Shukla, D. Double helix: Reciprocity between juvenile play and brain development. Dev. Cogn. Neurosci. 1, 459–470 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  151. Van Wingen, G., Mattern, C., Verkes, R. J., Buitelaar, J. & Fernandez, G. Testosterone reduces amygdala–orbitofrontal cortex coupling. Psychoneuroendocrinology 35, 105–113 (2010).

    Article  CAS  PubMed  Google Scholar 

  152. Forbes, E. E. et al. Healthy adolescents' neural response to reward: associations with puberty, positive affect, and depressive symptoms. J. Am. Acad. Child Adolesc. Psychiatry 49, 162–172 (2010).

    Google Scholar 

  153. Op de Macks, Z. et al. Testosterone levels correspond with increased ventral striatum activation in response to monetary rewards in adolescents. Dev. Cogn. Neurosci. 1, 506–516 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  154. Bramen, J. E. et al. Sex matters during adolescence: testosterone-related cortical thickness maturation differs between boys and girls. PLoS ONE 7, e33850 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  155. Schlegel, A. & Barry, H. Adolescence: An Anthropological Inquiry (Free Press, 1991).

    Google Scholar 

  156. Ross, J., Roeltgen, D. & Zinn, A. Cognition and the sex chromosomes: studies in Turner syndrome. Horm. Res. 65, 47–56 (2006).

    CAS  PubMed  Google Scholar 

  157. Sowell, E. R. et al. Longitudinal mapping of cortical thickness and brain growth in normal children. J. Neurosci. 24, 8223–8231 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  158. Gogtay, N. et al. Dynamic mapping of human cortical development during childhood through early adulthood. Proc. Natl Acad. Sci. USA 101, 8174–8179 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  159. Giedd, J. N. Structural magnetic resonance imaging of the adolescent brain. Ann. NY Acad. Sci. 1021, 77–85 (2004).

    Article  PubMed  Google Scholar 

  160. Lenroot, R. K. & Giedd, J. N. Brain development in children and adolescents: insights from anatomical magnetic resonance imaging. Neurosci. Biobehav. Rev. 30, 718–729 (2006).

    Article  PubMed  Google Scholar 

  161. Ostby, Y. et al. Heterogeneity in subcortical brain development: a structural magnetic resonance imaging study of brain maturation from 8 to 30 years. J. Neurosci. 29, 11772–11782 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  162. Spear, L. P. Heightened stress responsivity and emotional reactivity during pubertal maturation: implications for psychopathology. Dev. Psychopathol. 21, 87–97 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  163. Sisk, C. L. & Zehr, J. L. Pubertal hormones organize the adolescent brain and behavior. Front. Neuroendocrinol. 26, 163–174 (2005).

    Article  CAS  PubMed  Google Scholar 

  164. Galvan, A. Neural plasticity of development and learning. Hum. Brain Mapp. 31, 879–890 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  165. Wahlstrom, D., White, T. & Luciana, M. Neurobehavioral evidence for changes in dopamine system activity during adolescence. Neurosci. Biobehav. Rev. 34, 631–648 (2010).

    Article  CAS  PubMed  Google Scholar 

  166. Johnson, C. & Wilbrecht, L. Juvenile mice show greater flexibility in multiple choice reversal learning than adults. Dev. Cogn. Neurosci. 1, 540–551 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  167. Olesen, P. J., Nagy, Z., Westerberg, H. & Klingberg, T. Combined analysis of DTI and fMRI data reveals a joint maturation of white and grey matter in a fronto-parietal network. Brain Res. Cogn. Brain Res. 18, 48–57 (2003).

    Article  PubMed  Google Scholar 

  168. Durston, S. et al. A neural basis for the development of inhibitory control. Dev. Sci. 5, F9–F16 (2002).

    Article  Google Scholar 

  169. May, J. C. et al. Event-related functional magnetic resonance imaging of reward-related brain circuitry in children and adolescents. Biol. Psychiatry 55, 359–366 (2004).

    Article  PubMed  Google Scholar 

  170. Guyer, A. E. et al. Amygdala and ventrolateral prefrontal cortex function during anticipated peer evaluation in pediatric social anxiety. Arch. Gen. Psychiatry 65, 1303–1312 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  171. Decety, J., Michalska, K. J. & Kinzler, K. D. The contribution of emotion and cognition to moral sensitivity: a neurodevelopmental study. Cereb. Cortex 22, 209–220 (2012).

    Article  PubMed  Google Scholar 

  172. Harenski, C. L., Harenski, K. A., Shane, M. S. & Kiehl, K. A. Neural development of mentalizing in moral judgment from adolescence to adulthood. Dev. Cogn. Neurosci. 2, 162–173 (2012).

    Article  PubMed  Google Scholar 

  173. Church, J. A., Petersen, S. E. & Schlaggar, B. L. The “Task B problem” and other considerations in developmental functional neuroimaging. Hum. Brain Mapp. 31, 852–862 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

E.A.C. is supported by grants from the European Research Counsil (ERC), the Netherlands Science Foundation (NWO) and the Young Academy of the Royal Netherlands Academy of Arts and Sciences. R.E.D is supported by grants from the National Institute of Mental Health, National Institute of Drug Abuse, National Institute of Child Health and Human Development and National Institute on Alcohol Abuse and Alcoholism.

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  1. Eveline A. Crone and Ronald E. Dahl: All authors contributed equally to this work.

Authors and Affiliations

  1. Department of Psychology, Leiden University, Wassenaarseweg 52, 2333AK, The Netherlands

    Eveline A. Crone

  2. Institute of Human Development, University of California, Berkeley, 94707, California, USA

    Ronald E. Dahl

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Supplementary information S1 (table)

Developmental neuroimaging studies in the domains of cognitive control, emotion and social reasoning conducted between 2001 and 2011. (PDF 245 kb)

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Glossary

Cognitive control

A set of neurocognitive processes that are important for achieving short- and long-term goals, particularly when individuals are required to adjust their thoughts and actions adaptively in response to changing environmental demands in order to achieve their goal.

Relational reasoning

An essential component of fluid intelligence that requires a number of verbal or spatial dimensions to be considered simultaneously to reach a correct solution.

Social–cognitive development

Changes in cognitive skills and knowledge that facilitate understanding social situations, such as mentalizing and perspective-taking abilities.

Social–affective development

Changes in motivational and emotional aspects of social processing (such as empathy, increases in the salience of obtaining status, admiration and affiliation from peers) and the development of affective skills that support social competence.

Mentalizing

The ability to infer mental states of others, such as one's intentions, beliefs and desires — a key dimension of social–cognitive development in adolescence.

Self-oriented thoughts

Concern for outcomes that benefit one's own gains, such as in economic exchange when benefits for self and benefits for others are often conflicting.

Other-oriented thoughts

Concern for outcomes that benefit others, even when this is at the expense of gains for self, such as when evaluating what is fair for two parties.

Trust Game

Two-person interaction game that requires perspective-taking and relies on feelings of fairness and concern for others.

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Crone, E., Dahl, R. Understanding adolescence as a period of social–affective engagement and goal flexibility. Nat Rev Neurosci 13, 636–650 (2012). https://doi.org/10.1038/nrn3313

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