Peers influence adolescent reward processing, but not response inhibition

  • Ashley R. Smith
  • Gail M. Rosenbaum
  • Morgan A. Botdorf
  • Laurence Steinberg
  • Jason M. Chein
Article

Abstract

Most adolescent risk taking occurs in the presence of peers. Prior research suggests that peers alter adolescents’ decision making by increasing reward sensitivity and the engagement of regions involved in the processing of rewards, primarily the striatum. However, the potential influence of peers on the capacity for impulse control, and the associated recruitment of the brain’s control circuitry, has not yet been adequately examined. In the current study, adolescents underwent functional neuroimaging while they completed interleaved rounds of risk-taking and response-inhibition tasks. Social context was manipulated such that the participants believed they were either playing alone and unobserved, or watched by an anonymous peer. Compared to those who completed the tasks alone, adolescents in the peer condition took more risks during the risk-taking task and exhibited relatively heightened activation of the striatum. Activity within this striatal region also predicted individual differences in overall risk taking. In contrast, the presence of peers had no effect on behavioral response inhibition and had minimal impact on the engagement of typical cognitive control regions. In a subregion of the anterior insula engaged mutually by both tasks, activity was again found to be sensitive to social context during the risk-taking task, but not during the response-inhibition task. These findings extend the evidence that the presence of peers biases adolescents towards risk taking by increasing reward sensitivity rather than disrupting cognitive control.

Keywords

Adolescence Peer influence Risk taking Cognitive control 

References

  1. Albert, D., Chein, J., & Steinberg, L. (2013). The teenage brain: Peer influences on adolescent decision making. Current Directions in Psychological Science, 22(2), 114–120.  https://doi.org/10.1177/0963721412471347 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Botdorf, M., Rosenbaum, G. M., Patrianakos, J., Steinberg, L., & Chein, J. M. (2017). Adolescent risk-taking is predicted by individual differences in cognitive control over emotional, but not non-emotional, response conflict. Cognition and Emotion, 31(5), 972–979.CrossRefPubMedGoogle Scholar
  3. Boynton, G. M., Engel, S. A., Glover, G. H., & Heeger, D. J. (1996). Linear systems analysis of functional magnetic resonance imaging in human V1. Journal of Neuroscience, 16(13), 4207–4221.CrossRefPubMedGoogle Scholar
  4. Braams, B. R., Peters, S., Peper, J. S., Güroğlu, B., & Crone, E. A. (2014). Gambling for self, friends, and antagonists: Differential contributions of affective and social brain regions on adolescent reward processing. NeuroImage, 100, 281–289.CrossRefPubMedGoogle Scholar
  5. Cascio, C. N., Carp, J., O’Donnell, M. B., Tinney, F. J., Jr, Bingham, C. R., Shope, J. T., & Falk, E. B. (2014). Buffering social influence: neural correlates of response inhibition predict driving safety in the presence of a peer. Journal of Cognitive Neuroscience, 27(1), 83–95.CrossRefGoogle Scholar
  6. Casey, B. J. (2015). Beyond simple models of self-control to circuit-based accounts of adolescent behavior. Annual Review of Psychology, 66, 295–319.CrossRefPubMedGoogle Scholar
  7. Casey, B. J., Getz, S., & Galván, A. (2008). The adolescent brain. Developmental Review, 28(1), 62–77.  https://doi.org/10.1016/j.dr.2007.08.003 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Casey, B. J., Epstein, J., Buhle, J., Liston, C., Davidson, M. C., Tonev, S., . . . Glover, G. (2007). Frontostriatal connectivity and its role in cognitive control in parent-child dyads with ADHD. American Journal of Psychiatry, 164, 1729–1736.Google Scholar
  9. Chein, J., Albert, D., O’Brien, L., Uckert, K., & Steinberg, L. (2011). Peers increase adolescent risk-taking by enhancing activity in the brain’s reward circuitry. Developmental Science, 14(2), F1–F10.  https://doi.org/10.1111/j.1467-7687.2010.01035.x CrossRefPubMedPubMedCentralGoogle Scholar
  10. Cox, R. W. (1996). AFNI: Software for analysis and visualization of functional magnetic resonance neuroimages. Computers and Biomedical Research, 29, 162–173.CrossRefPubMedGoogle Scholar
  11. Cox, R. W., Chen, G., Glen, D. R., Reynolds, R. C., Taylor, P. A. (2017). FMRI clustering in AFNI: false-positive rates redux. Brain Connectivity, 7(3), 152–171CrossRefPubMedPubMedCentralGoogle Scholar
  12. Criaud, M., & Boulinguez, P. (2013). Have we been asking the right questions when assessing response inhibition in go/no-go tasks with fMRI? A meta-analysis and critical review. Neuroscience and Biobehavioral Reviews, 37, 11–23.CrossRefPubMedGoogle Scholar
  13. Crone, E. A., & Dahl, R. E. (2012). Understanding adolescence as a period of social–affective engagement and goal flexibility. Nature Reviews Neuroscience, 13(9), 636–650.CrossRefPubMedGoogle Scholar
  14. Ernst, M. (2015). The triadic model perspective for the study of adolescent motivated behavior. Brain and Cognition, 89, 104–111.CrossRefGoogle Scholar
  15. Eshel, N., Nelson, E. E., Blair, R. J., Pine, D. S., & Ernst, M. (2007). Neural substrates of choice selection in adults and adolescents: Development of the ventrolateral prefrontal and anterior cingulate cortices. Neuropsychologia, 45(6), 1270–1279.CrossRefPubMedGoogle Scholar
  16. Galván, A. (2010). Adolescent development of the reward system. Frontiers in Human Neuroscience.  https://doi.org/10.3389/neuro.09.006.2010
  17. Galván, A., Hare, T. A., Parra, C. E., Penn, J., Voss, H., Glover, G., & Casey, B. J. (2006). Earlier development of the accumbens relative to orbitofrontal cortex might underlie risk-taking behavior in adolescents. The Journal of Neuroscience, 26(25), 6885–6892.CrossRefPubMedGoogle Scholar
  18. Gardner, M., & Steinberg, L. (2005). Peer influence on risk-taking, risk preference, and risky decision-making in adolescence and adulthood: An experimental study. Developmental Psychology, 41(4), 625–635.  https://doi.org/10.1037/0012-1649.41.4.625 CrossRefPubMedGoogle Scholar
  19. Luciana, M., & Collins, P. F. (2012). Incentive motivation, cognitive control, and the adolescent brain: Is it time for a paradigm shift?. Child Development Perspectives, 6(4), 392-399.PubMedPubMedCentralGoogle Scholar
  20. Luna, B., & Wright, C. (2016). Adolescent brain development: Implications to the juvenile criminal justice system, In K. Heilbrun (Ed.), APA Handbook of Psychology and Juvenile Justice, Washington, DC: American Psychological Association.Google Scholar
  21. Menon, V., & Uddin, L. Q. (2010). Saliency, switching, attention and control: a network model of insula function. Brain Structure & Function, 214, 655–667.CrossRefGoogle Scholar
  22. O’Brien, L., Albert, D., Chein, J., & Steinberg, L. (2011). Adolescents prefer more immediate rewards when in the presence of their peers. Journal of Research on Adolescence, 21(4), 747–753.  https://doi.org/10.1111/j.1532-7795.2011.00738.x CrossRefGoogle Scholar
  23. Pfeifer, J. H., & Allen, N. B. (2012). Arrested development? Reconsidering dual-systems models of brain function in adolescence and disorders. Trends in Cognitive Sciences, 16, 322–329.CrossRefPubMedPubMedCentralGoogle Scholar
  24. Poldrack, R. A. (2015). Is “efficiency” a useful concept in cognitive neuroscience? Accident Analysis and Prevention, 11, 12–17.  https://doi.org/10.1016/j.dcn.2014.06.001 Google Scholar
  25. Segalowitz, S. J., Santesso, D. L., Willoughby, T., Reker, D. L., Campbell, K., Chalmers, H., & Rose-Krasnor, L. (2012). Adolescent peer interaction and trait surgency weaken medial prefrontal cortex responses to failure. Social Cognitive and Affective Neuroscience, 7(1), 115–124.  https://doi.org/10.1093/scan/nsq090 CrossRefPubMedGoogle Scholar
  26. Shulman, E. P., Smith, A. R., Silva, K., Icenogle, G., Duell, N., Chein, J., & Steinberg, L. (2016). The dual systems model: Review, reappraisal, and reaffirmation. Developmental Cognitive Neuroscience, 17(2015), 103–117.  https://doi.org/10.1016/j.dcn.2015.12.010 CrossRefPubMedGoogle Scholar
  27. Silva, K., Shulman, E., Chein, J., & Steinberg, L. (2015). Peers increase late adolescents’ exploratory behavior and sensitivity to positive and negative feedback. Journal of Research on Adolescence. Advance online publication.  https://doi.org/10.1111/jora.12219
  28. Smith, A. R., Chein, J., & Steinberg, L. (2013). Impact of socio-emotional context, brain development, and pubertal maturation on adolescent risk-taking. Hormones and Behavior, 64(2), 323–332.  https://doi.org/10.1016/j.yhbeh.2013.03.006 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Smith, A. R., Chein, J., & Steinberg, L. (2014a). Peers increase adolescent risk-taking even when the probabilities of negative outcomes are known. Developmental Psychology, 50(5), 1564–1568.  https://doi.org/10.1037/a0035696 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Smith, A.R., Steinberg, L. & Chein, J. (2014b). The role of the anterior insular cortex in adolescent decision-making. Developmental Neuroscience, 36, 196–209.CrossRefPubMedPubMedCentralGoogle Scholar
  31. Smith, A. R., Steinberg, L., Strang, N., & Chein, J. (2015). Age differences in the impact of peers on adolescents’ and adults’ neural response to reward. Developmental Cognitive Neuroscience, 11, 75–82.  https://doi.org/10.1016/j.dcn.2014.08.010 CrossRefPubMedGoogle Scholar
  32. Steinberg, L. (2008). A social neuroscience perspective on adolescent risk-taking. Developmental Review, 28(1), 78–106.  https://doi.org/10.1016/j.dr.2007.08.002 CrossRefPubMedPubMedCentralGoogle Scholar
  33. Steinberg, L. (2010). A dual systems model of adolescent risk-taking. Developmental Psychobiology, 52, 216–224.  https://doi.org/10.1002/dev.20445 PubMedGoogle Scholar
  34. Steinberg, L., Albert, D., Cauffman, E., Banich, M., Graham, S., & Woolard, J. (2008). Age differences in sensation seeking and impulsivity as indexed by behavior and self-report: Evidence for a dual systems model. Developmental Psychology, 44(6), 1764–78.  https://doi.org/10.1037/a0012955 CrossRefPubMedGoogle Scholar
  35. Van Leijenhorst, L., Moor, B. G., de Macks, Z. A. O., Rombouts, S. A., Westenberg, P. M., & Crone, E. A. (2010). Adolescent risky decision-making: Neurocognitive development of reward and control regions. NeuroImage, 51(1), 345–355.CrossRefPubMedGoogle Scholar
  36. Weigard, A., Chein, J., Albert, D., Smith, A., & Steinberg, L. (2013). Effects of anonymous peer observation on adolescents’ preference for immediate rewards. Developmental Science, 17(1), 71–78. 10.1111/desc.12099Google Scholar
  37. Zuckerman, M. (1994). Behavioral expressions and biosocial bases of sensation seeking. New York, NY: Cambridge University Press.Google Scholar

Copyright information

© Psychonomic Society, Inc. 2018

Authors and Affiliations

  • Ashley R. Smith
    • 1
  • Gail M. Rosenbaum
    • 1
  • Morgan A. Botdorf
    • 1
  • Laurence Steinberg
    • 1
  • Jason M. Chein
    • 1
  1. 1.Temple UniversityPhiladelphiaUSA

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