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.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$189.00 per year
only $15.75 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Dahl, R. E. & Gunnar, M. R. Heightened stress responsiveness and emotional reactivity during pubertal maturation: implications for psychopathology. Dev. Psychopathol. 21, 1–6 (2009).
Steinberg, L. A. Social neuroscience perspective on adolescent risk-taking. Dev. Rev. 28, 78–106 (2008).
Blakemore, S. J., Burnett, S. & Dahl, R. E. The role of puberty in the developing adolescent brain. Hum. Brain Mapp. 31, 926–933 (2010).
Arnett, J. J. Adolescence and Emerging Adulthood: A Cultural Approach (Prentice Hall, 2004).
Dahl, R. E. & Vanderschuren, L. J. The feeling of motivation in the developing brain. Dev. Cogn. Neurosci. 1, 361–363 (2011).
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).
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.
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).
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).
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).
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.
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).
Asato, M. R., Sweeney, J. A. & Luna, B. Cognitive processes in the development of TOL performance. Neuropsychologia 44, 2259–2269 (2006).
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).
Case, R. The Mind's Staircase: Exploring the Conceptual Underpinnings of Children's Thought and Knowledge (Erlbaum, 1992).
Zelazo, P. D., Craik, F. I. & Booth, L. Executive function across the life span. Acta Psychol. (Amst.) 115, 167–183 (2004).
Zelazo, P. D. The development of conscious control in childhood. Trends Cogn. Sci. 8, 12–17 (2004).
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).
Miller, E. K. & Cohen, J. D. An integrative theory of prefrontal cortex function. Annu. Rev. Neurosci. 24, 167–202 (2001).
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).
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).
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).
Scherf, K. S., Sweeney, J. A. & Luna, B. Brain basis of developmental change in visuospatial working memory. J. Cogn. Neurosci. 18, 1045–1058 (2006).
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).
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).
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).
Thomason, M. E. et al. Development of spatial and verbal working memory capacity in the human brain. J. Cogn. Neurosci. 21, 316–332 (2009).
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).
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).
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).
Adleman, N. E. et al. A developmental fMRI study of the Stroop color-word task. Neuroimage 16, 61–75 (2002).
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).
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).
Marsh, R. et al. A developmental fMRI study of self-regulatory control. Hum. Brain Mapp. 27, 848–863 (2006).
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).
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).
Casey, B. J. et al. Early development of subcortical regions involved in non-cued attention switching. Dev. Sci. 7, 534–542 (2004).
Christakou, A. et al. Sex-dependent age modulation of frontostriatal and temporoparietal activation during cognitive control. Neuroimage 48, 223–236 (2009).
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).
Bunge, S. A. & Wright, S. B. Neurodevelopmental changes in working memory and cognitive control. Curr. Opin. Neurobiol. 17, 243–250 (2007).
Geier, C. F., Garver, K., Terwilliger, R. & Luna, B. Development of working memory maintenance. J. Neurophysiol. 101, 84–99 (2009).
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).
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).
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).
Durston, S. et al. A shift from diffuse to focal cortical activity with development. Dev. Sci. 9, 1–8 (2006).
Booth, J. R. et al. Neural development of selective attention and response inhibition. Neuroimage 20, 737–751 (2003).
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).
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).
Konrad, K. et al. Development of attentional networks: an fMRI study with children and adults. Neuroimage 28, 429–439 (2005).
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).
Luna, B. et al. Maturation of widely distributed brain function subserves cognitive development. Neuroimage 13, 786–793 (2001).
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).
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).
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).
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).
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.
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).
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).
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).
Dumontheil, I., Houlton, R., Christoff, K. & Blakemore, S. J. Development of relational reasoning during adolescence. Dev. Sci. 13, F15–F24 (2010).
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).
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).
Crone, E. A. et al. Neurocognitive development of relational reasoning. Dev. Sci. 12, 55–66 (2009).
Fuligni, A. J. in Research on Minority Adolescents: Conceptual, Theoretical, and Methodological Issues (eds McLoyd, V. & Steinberg, L.) 127–143 (Erlbaum, 1998).
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).
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).
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).
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).
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.
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).
Haber, S. N. & Knutson, B. The reward circuit: linking primate anatomy and human imaging. Neuropsychopharmacology 35, 4–26 (2010).
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).
Van Leijenhorst, L. et al. Adolescent risky decision-making: neurocognitive development of reward and control regions. Neuroimage 51, 345–355 (2010).
Van Leijenhorst, L. et al. What motivates the adolescent? Brain regions mediating reward sensitivity across adolescence. Cereb. Cortex 20, 61–69 (2010).
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).
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.
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).
Smith, A. B., Halari, R., Giampetro, V., Brammer, M. & Rubia, K. Developmental effects of reward on sustained attention networks. Neuroimage 56, 1693–1704 (2011).
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).
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).
Bjork, J. M. et al. Incentive-elicited brain activation in adolescents: similarities and differences from young adults. J. Neurosci. 24, 1793–1802 (2004).
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).
Forbes, E. E. & Dahl, R. E. Pubertal development and behavior: hormonal activation of social and motivational tendencies. Brain Cogn. 72, 66–72 (2010).
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).
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).
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).
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).
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).
Killgore, W. D., Oki, M. & Yurgelun-Todd, D. A. Sex-specific developmental changes in amygdala responses to affective faces. Neuroreport 12, 427–433 (2001).
Monk, C. S. et al. Adolescent immaturity in attention-related brain engagement to emotional facial expressions. Neuroimage 20, 420–428 (2003).
Williams, L. M. et al. The mellow years?: neural basis of improving emotional stability over age. J. Neurosci. 26, 6422–6430 (2006).
Guyer, A. E. et al. A developmental examination of amygdala response to facial expressions. J. Cogn. Neurosci. 20, 1565–1582 (2008).
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).
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.
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).
Thomas, K. M. et al. Amygdala response to facial expressions in children and adults. Biol. Psychiatry 49, 309–316 (2001).
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).
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).
Deeley, Q. et al. Changes in male brain responses to emotional faces from adolescence to middle age. Neuroimage 40, 389–397 (2008).
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).
Casey, B., Jones, R. M. & Somerville, L. H. Braking and accelerating of the adolescent brain. J. Res. Adolesc. 21, 21–33 (2011).
Schaffer, H. R. Social Development (Blackwell,1996).
Steinberg, L. & Morris, A. S. Adolescent development. Annu. Rev. Psychol. 52, 83–110 (2001).
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).
Rilling, J. K. & Sanfey, A. G. The neuroscience of social decision-making. Annu. Rev. Psychol. 62, 23–48 (2011).
Blakemore, S. J. The social brain in adolescence. Nature Rev. Neurosci. 9, 267–277 (2008).
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).
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).
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).
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).
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).
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).
Gunther Moor, B. et al. Neurodevelopmental changes of reading the mind in the eyes. Soc. Cogn. Affect. Neurosci. 7, 44–52 (2012).
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).
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).
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).
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).
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).
Güth, W., Schmittberger, R. & Schwarze, B. An experimental analysis of ultimatum bargaining. J. Econom. Behav. Organiz. 3, 367 (1982).
Berg, J., Dickhaut, J. & McCabe, K. Trust, reciprocity, and social history. Games Econom. Behav. 10, 122–142 (1995).
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).
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).
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).
Van Overwalle, F. Social cognition and the brain: a meta-analysis. Hum. Brain Mapp. 30, 829–858 (2009).
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).
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).
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).
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.
Cillessen, A. H. & Rose, A. J. Understanding popularity in the peer system. Curr. Direct. Psychol. Sci. 14, 102–105 (2005).
Decety, J. & Michalska, K. J. Neurodevelopmental changes in the circuits underlying empathy and sympathy from childhood to adulthood. Dev. Sci. 13, 886–899 (2010).
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).
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).
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).
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).
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.
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).
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).
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).
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).
Dahl, R. E. Adolescent brain development: a period of vulnerabilities and opportunities. Ann. NY Acad. Sci. 1021, 1–22 (2004).
Galvan, A. Adolescent development of the reward system. Front. Hum. Neurosci. 4, 6 (2010).
Steinberg, L. The Science of Adolescent Risk-Taking. (Washington, 2011).
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).
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).
Jacobs, E. & D'Esposito, M. Estrogen shapes dopamine-dependent cognitive processes: implications for women's health. J. Neurosci. 31, 5286–5293 (2011).
Gordon, I., Martin, C., Feldman, R. & Leckman, J. F. Oxytocin and social motivation. Dev. Cogn. Neurosci. 1, 471–493 (2011).
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).
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.
Carney, D. & Mason, M. F. Decision making and testosterone: when the ends justify the means. J. Exp. Social Psychol. 46, 668–671 (2010).
Cooke, B. M. & Shukla, D. Double helix: Reciprocity between juvenile play and brain development. Dev. Cogn. Neurosci. 1, 459–470 (2011).
Van Wingen, G., Mattern, C., Verkes, R. J., Buitelaar, J. & Fernandez, G. Testosterone reduces amygdala–orbitofrontal cortex coupling. Psychoneuroendocrinology 35, 105–113 (2010).
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).
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).
Bramen, J. E. et al. Sex matters during adolescence: testosterone-related cortical thickness maturation differs between boys and girls. PLoS ONE 7, e33850 (2012).
Schlegel, A. & Barry, H. Adolescence: An Anthropological Inquiry (Free Press, 1991).
Ross, J., Roeltgen, D. & Zinn, A. Cognition and the sex chromosomes: studies in Turner syndrome. Horm. Res. 65, 47–56 (2006).
Sowell, E. R. et al. Longitudinal mapping of cortical thickness and brain growth in normal children. J. Neurosci. 24, 8223–8231 (2004).
Gogtay, N. et al. Dynamic mapping of human cortical development during childhood through early adulthood. Proc. Natl Acad. Sci. USA 101, 8174–8179 (2004).
Giedd, J. N. Structural magnetic resonance imaging of the adolescent brain. Ann. NY Acad. Sci. 1021, 77–85 (2004).
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).
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).
Spear, L. P. Heightened stress responsivity and emotional reactivity during pubertal maturation: implications for psychopathology. Dev. Psychopathol. 21, 87–97 (2009).
Sisk, C. L. & Zehr, J. L. Pubertal hormones organize the adolescent brain and behavior. Front. Neuroendocrinol. 26, 163–174 (2005).
Galvan, A. Neural plasticity of development and learning. Hum. Brain Mapp. 31, 879–890 (2010).
Wahlstrom, D., White, T. & Luciana, M. Neurobehavioral evidence for changes in dopamine system activity during adolescence. Neurosci. Biobehav. Rev. 34, 631–648 (2010).
Johnson, C. & Wilbrecht, L. Juvenile mice show greater flexibility in multiple choice reversal learning than adults. Dev. Cogn. Neurosci. 1, 540–551 (2011).
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).
Durston, S. et al. A neural basis for the development of inhibitory control. Dev. Sci. 5, F9–F16 (2002).
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).
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).
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).
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).
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).
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.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Supplementary information
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)
Related links
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.
Rights and permissions
About this article
Cite this article
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
Published:
Issue Date:
DOI: https://doi.org/10.1038/nrn3313