Adolescent-specific patterns of behavior and neural activity during social reinforcement learning

Cognitive, Affective and Behavioral Neuroscience

Volumn 14, Issue 2, 2014, Pages 683-697

  Jones, Rebecca M ^a   Somerville, Leah H ^b   Li, Jian ^c   Ruberry, Erika J ^a   Powers, Alisa ^a   Mehta, Natasha ^a   Dyke, Jonathan ^a   Casey, B J ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b HARVARD UNIVERSITY   (United States)

^c PEKING UNIVERSITY   (China)

Author keywords

Adolescence; Brain; fMRI; Peers; Reinforcement; Social acceptance

Indexed keywords

OXYGEN;

ADOLESCENT; ADOLESCENT BEHAVIOR; ADULT; AGE; ASSOCIATION; BLOOD; BRAIN; BRAIN MAPPING; CHILD; FEMALE; HUMAN; IMAGE PROCESSING; MALE; MOTIVATION; NEUROPSYCHOLOGICAL TEST; PHOTOSTIMULATION; PHYSIOLOGY; REINFORCEMENT; SEX DIFFERENCE; VASCULARIZATION; YOUNG ADULT;

ADOLESCENT; ADOLESCENT BEHAVIOR; ADULT; AGE FACTORS; BRAIN; BRAIN MAPPING; CHILD; CUES; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MALE; MOTIVATION; NEUROPSYCHOLOGICAL TESTS; OXYGEN; PHOTIC STIMULATION; REINFORCEMENT, SOCIAL; SEX FACTORS; YOUNG ADULT;

EID: 84904406204     PISSN: 15307026     EISSN: None     Source Type: Journal    
DOI: 10.3758/s13415-014-0257-z     Document Type: Article

References (73)

1. Alexander, G. E., & Crutcher, M. D. (1990). Preparation for movement: Neural representations of intended direction in three motor areas of the monkey. Journal of Neurophysiology, 64(1), 133-150.
2. Bhanji, J. P., & Delgado, M. R. (2013). The social brain and reward: Social information processing in the human striatum. WIREs Cognitive Science, 5(1), 61-73.
3. Bishop, J. A., & Inderbitzen, H. M. (1995). Peer acceptance and friendship: An investigation of their relation to self-esteem. The Journal of Early Adolescence, 15(4), 476-489.
4. Blakemore, S. J., & Mills, K. L. (2013). Is adolescence a sensitive period for sociocultural processing? Annual Review of Psychology, 65, 187-207.
5. Bray, S., & O'Doherty, J. (2007). Neural coding of reward-prediction error signals during classical conditioning with attractive faces. Journal of Neurophysiology, 97(4), 3036-3045.
6. Cauffman, E., Shulman, E. P., Steinberg, L., Claus, E., Banich, M. T., Graham, S., & Woolard, J. (2010). Age differences in affective decision making as indexed by performance on the Iowa Gambling Task. Developmental Psychology, 46(1), 193-207.
7. Caze, R. D., & van der Meer, M. A. (2013). Adaptive properties of differential learning rates for positive and negative outcomes. Biological Cybernetics, 107(6), 711-719.
8. 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.
9. Chen, L. H., Baker, S. P., Braver, E. R., & Li, G. (2000). Carrying passengers as a risk factor for crashes fatal to 16- and 17-year-old drivers. JAMA, 283(12), 1578-1582.
10. Christakou, A., Gershman, S. J., Niv, Y., Simmons, A., Brammer, M., & Rubia, K. (2013). Neural and psychological maturation of decision-making in adolescence and young adulthood. Journal of Cognitive Neuroscience, 25(11), 1807-1823.
11. Church, J. A., Petersen, S. E., & Schlaggar, B. L. (2010). The Task B problem and other considerations in developmental functional neuroimaging. Human Brain Mapping, 31(6), 852-862.
12. Cohen, J. R., Asarnow, R. F., Sabb, F. W., Bilder, R. M., Bookheimer, S. Y., Knowlton, B. J., & Poldrack, R. A. (2010). A unique adolescent response to reward prediction errors. Nature Neuroscience, 13(6), 669-671.
13. Collins, W. A., & Steinberg, L. (2007). Adolescent development in interpersonal context. In Handbook of Child Psychology. Hoboken, NJ: John Wiley & Sons, Inc.
14. Craig, A. D. (2009). How do you feel-now? The anterior insula and human awareness. Nature Review Neuroscience, 10(1), 59-70.
15. Critchley, H. D., Wiens, S., Rotshtein, P., Ohman, A., & Dolan, R. J. (2004). Neural systems supporting interoceptive awareness. Nature Neuroscience, 7(2), 189-195.
16. Crone, E. A., & Dahl, R. E. (2012). Understanding adolescence as a period of social-affective engagement and goal flexibility. Nature Review Neuroscience, 13(9), 636-650.
17. Cunnington, R., Windischberger, C., Deecke, L., & Moser, E. (2002). The preparation and execution of self-initiated and externally-triggered movement: A study of event-related fMRI. NeuroImage, 15(2), 373-385.
18. Damasio, A. (2003). Feelings of emotion and the self. Annals of the New York Academy of Sciences, 1001, 253-261.
19. Dodge, K. A., Lansford, J. E., Burks, V. S., Bates, J. E., Pettit, G. S., Fontaine, R., & Price, J. M. (2003). Peer rejection and social information-processing factors in the development of aggressive behavior problems in children. Child Development, 74(2), 374-393.
20. Downar, J., Crawley, A. P., Mikulis, D. J., & Davis, K. D. (2001). The effect of task relevance on the cortical response to changes in visual and auditory stimuli: An event-related fMRI study. NeuroImage, 14(6), 1256-1267.
21. Eisenberger, N. I., Lieberman, M. D., & Williams, K. D. (2003). Does rejection hurt? An FMRI study of social exclusion. Science, 302(5643), 290-292.
22. Engelmann, J. B., Moore, S., Monica Capra, C., & Berns, G. S. (2012). Differential neurobiological effects of expert advice on risky choice in adolescents and adults. Social Cognitive and Affective Neuroscience, 7(5), 557-567.
23. Fareri, D. S., Niznikiewicz, M. A., Lee, V. K., & Delgado, M. R. (2012). Social network modulation of reward-related signals. Journal of Neuroscience, 32(26), 9045-9052.
24. Fiorillo, C. D., Tobler, P. N., & Schultz, W. (2003). Discrete coding of reward probability and uncertainty by dopamine neurons. Science, 299(5614), 1898-1902.
25. Galvan, 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. Journal of Neuroscience, 26(25), 6885-6892.
26. 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.
27. Geier, C. F., Terwilliger, R., Teslovich, T., Velanova, K., & Luna, B. (2010). Immaturities in reward processing and its influence on inhibitory control in adolescence. Cerebral Cortex, 20(7), 1613-1629.
28. Glover, G. H., & Thomason, M. E. (2004). Improved combination of spiral-in/out images for BOLD fMRI. Magnetic Resonance in Medicine, 51(4), 863-868.
29. Guyer, A. E., Choate, V. R., Pine, D. S., & Nelson, E. E. (2012). Neural circuitry underlying affective response to peer feedback in adolescence. Social Cognitive and Affective Neuroscience, 7(1), 81-92.
30. Guyer, A. E., McClure-Tone, E. B., Shiffrin, N. D., Pine, D. S., & Nelson, E. E. (2009). Probing the neural correlates of anticipated peer evaluation in adolescence. Child Development, 80(4), 1000-1015.
31. Herrmann, E., Call, J., Hernandez-Lloreda, M. V., Hare, B., & Tomasello, M. (2007). Humans have evolved specialized skills of social cognition: The cultural intelligence hypothesis. Science, 317(5843), 1360-1366.
32. Izuma, K., Saito, D. N., & Sadato, N. (2008). Processing of social and monetary rewards in the human striatum. Neuron, 58(2), 284-294.
33. Johnstone, T., Somerville, L. H., Alexander, A. L., Oakes, T. R., Davidson, R. J., Kalin, N. H., & Whalen, P. J. (2005). Stability of amygdala BOLD response to fearful faces over multiple scan sessions. NeuroImage, 25(4), 1112-1123.
34. Jones, R. M., Somerville, L. H., Li, J., Ruberry, E. J., Libby, V., Glover, G.,. Casey, B. J. (2011). Behavioral and neural properties of social reinforcement learning. Journal of Neuroscience, 31(37), 13039-13045.
35. Kahnt, T., Park, S. Q., Cohen, M. X., Beck, A., Heinz, A., & Wrase, J. (2009). Dorsal striatal-midbrain connectivity in humans predicts how reinforcements are used to guide decisions. Journal of Cognitive Neuroscience, 21(7), 1332-1345.
36. Kohls, G., Peltzer, J., Herpertz-Dahlmann, B., & Konrad, K. (2009). Differential effects of social and non-social reward on response inhibition in children and adolescents. Developmental Science, 12(4), 614-625.
37. La Greca, A. M., Prinstein, M. J., & Fetter, M. D. (2001). Adolescent peer crowd affiliation: Linkages with health-risk behaviors and close friendships. Journal of Pediatric Psychology, 26(3), 131-143.
38. Laird, R. D., Jordan, K. Y., Dodge, K. A., Pettit, G. S., & Bates, J. E. (2001). Peer rejection in childhood, involvement with antisocial peers in early adolescence, and the development of externalizing behavior problems. Development and Psychopathology, 13(2), 337-354.
39. Lamm, C., Batson, C. D., & Decety, J. (2007). The neural substrate of human empathy: Effects of perspective-taking and cognitive appraisal. Journal of Cognitive Neuroscience, 19(1), 42-58.
40. Lamm, C., & Singer, T. (2010). The role of anterior insular cortex in social emotions. Brain Structure and Function, 214(5-6), 579-591.
41. Larson, R., & Richards, M. H. (1991). Daily companionship in late childhood and early adolescence: Changing developmental contexts. Child Development, 62(2), 284-300.
42. Lin, A., Adolphs, R., & Rangel, A. (2012). Social and monetary reward learning engage overlapping neural substrates. Social Cognitive and Affective Neuroscience, 7(3), 274-281.
43. Luthar, S. S., & D'Avanzo, K. (1999). Contextual factors in substance use: A study of suburban and inner-city adolescents. Development and Psychopathology, 11(4), 845-867.
44. Masten, C. L., Eisenberger, N. I., Borofsky, L. A., Pfeifer, J. H., McNealy, K., Mazziotta, J. C., & Dapretto, M. (2009). Neural correlates of social exclusion during adolescence: Understanding the distress of peer rejection. Social Cognitive and Affective Neuroscience, 4(2), 143-157.
45. Masten, C. L., Telzer, E. H., Fuligni, A. J., Lieberman, M. D., & Eisenberger, N. I. (2012). Time spent with friends in adolescence relates to less neural sensitivity to later peer rejection. Social Cognitive and Affective Neuroscience, 7, 106-114.
46. Meshi, D., Morawetz, C., & Heekeren, H. R. (2013). Nucleus accumbens response to gains in reputation for the self relative to gains for others predicts social media use. Frontiers in Human Neuroscience, 7, 439.
47. O'Doherty, J. P., Buchanan, T. W., Seymour, B., & Dolan, R. J. (2006). Predictive neural coding of reward preference involves dissociable responses in human ventral midbrain and ventral striatum. Neuron, 49(1), 157-166.
48. Pfeifer, J. H., & Blakemore, S. J. (2012). Adolescent social cognitive and affective neuroscience: Past, present, and future. Social Cognitive and Affective Neuroscience, 7(1), 1-10.
49. Prinstein, M. J., & Aikins, J. W. (2004). Cognitive moderators of the longitudinal association between peer rejection and adolescent depressive symptoms. Journal of Abnormal Child Psychology, 32(2), 147-158.
50. Prinstein, M. J., Boergers, J., & Spirito, A. (2001). Adolescents' and their friends' health-risk behavior: Factors that alter or add to peer influence. Journal of Pediatric Psychology, 26(5), 287-298.
51. Rademacher, L., Krach, S., Kohls, G., Irmak, A., Grunder, G., & Spreckelmeyer, K. N. (2010). Dissociation of neural networks for anticipation and consumption of monetary and social rewards. NeuroImage, 49(4), 3276-3285.
52. Rescorla, R. A., & Wagner, A. R. (1972). A theory of Pavlovian conditioning: Variations in the effectiveness of reinforcement and nonreinforcement. In A. H. Black & W. F. Prokasy (Eds.), Classical conditioning II: Current research and theory (pp. 64-99). New York: Appleton Century Crofts.
53. Rudolph, K. D., Caldwell, M. S., & Conley, C. S. (2005). Need for approval and children's well-being. Child Development, 76(2), 309-323.
54. Schultz, W., Dayan, P., & Montague, P. R. (1997). A neural substrate of prediction and reward. Science, 275(5306), 1593-1599.
55. Seymour, B., O'Doherty, J. P., Dayan, P., Koltzenburg, M., Jones, A. K., Dolan, R. J.,. Frackowiak, R. S. (2004). Temporal difference models describe higher-order learning in humans. Nature, 429(6992), 664-667.
56. Silk, J. S., Stroud, L. R., Siegle, G. J., Dahl, R. E., Lee, K. H., & Nelson, E. E. (2012). Peer acceptance and rejection through the eyes of youth: Pupillary, eyetracking and ecological data from the Chatroom Interact task. Social Cognitive and Affective Neuroscience, 7, 93-105.
57. Singer, T., Critchley, H. D., & Preuschoff, K. (2009). A common role of insula in feelings, empathy and uncertainty. Trends in Cognitive Science, 13(8), 334-340.
58. Somerville, L. H. (2013). The teenage brain: Sensitivity to social evaluation. Current Directions in Psychological Science, 22(2), 121-127.
59. Somerville, L. H., Jones, R. M., Ruberry, E. J., Dyke, J. P., Glover, G., & Casey, B. J. (2013). The medial prefrontal cortex and the emergence of self-conscious emotion in adolescence. Psychological Science, 24(8), 1554-1562.
60. Steinberg, L. (2008). A social neuroscience perspective on adolescent risk-taking. Developmental Review, 28, 78-106.
61. Talairach, J., & Tournoux, P. (1988). Co-planar stereotaxic atlas of the human brain. New York, NY: Thieme Medical Publishers.
62. Teslovich, T., Mulder, M., Franklin, N. T., Ruberry, E. J., Millner, A., Somerville, L. H., et al. (2014). Adolescents let sufficient evidence accumulate before making a decision when large incentives are at stake. Developmental Science, 17(1), 59-70.
63. van den Bos, W., Cohen, M. X., Kahnt, T., & Crone, E. A. (2012). Striatum-medial prefrontal cortex connectivity predicts developmental changes in reinforcement learning. Cerebral Cortex, 22(6), 1247-1255.
64. van den Bos, W., McClure, S. M., Harris, L. T., Fiske, S. T., & Cohen, J. D. (2007). Dissociating affective evaluation and social cognitive processes in the ventral medial prefrontal cortex. Cognitive, Affective, & Behavioral Neuroscience, 7(4), 337-346.
65. van Duijvenvoorde, A. C., Zanolie, K., Rombouts, S. A., Raijmakers, M. E., & Crone, E. A. (2008). Evaluating the negative or valuing the positive? Neural mechanisms supporting feedback-based learning across development. Journal of Neuroscience, 28(38), 9495-9503.
66. Van Leijenhorst, L., Zanolie, K., Van Meel, C. S., Westenberg, P. M., Rombouts, S. A., & Crone, E. A. (2010). What motivates the adolescent? Brain regions mediating reward sensitivity across adolescence. Cerebral Cortex, 20(1), 61-69.
67. Vanhalst, J., Luyckx, K., Scholte, R. H., Engels, R. C., & Goossens, L. (2013). Low self-esteem as a risk factor for loneliness in adolescence: Perceived - but not actual - social acceptance as an underlying mechanism. Journal of Abnormal Child Psychology, 41(7), 1067-1081.
68. Veronneau, M. H., Vitaro, F., Brendgen, M., Dishion, T. J., & Tremblay, R. E. (2010). Transactional analysis of the reciprocal links between peer experiences and academic achievement from middle childhood to early adolescence. Developmental Psychology, 46(4), 773-790.
69. Wechsler, D. (1999). Wechsler abbreviated scale of intelligence. San Antonio, TX: The Psychological Corporation.
70. Weigard, A., Chein, J., Albert, D., Smith, A., & Steinberg, L. (2014). Effects of anonymous peer observation on adolescents' preference for immediate rewards. Developmental Science, 17(1), 71-78.
71. Wentzel, K. R., & Caldwell, K. (1997). Friendships, peer acceptance, and group membership: relations to academic achievement in middle school. Child Development, 68(6), 1198-1209.
72. White, B. A., & Kistner, J. A. (2011). Biased self-perceptions, peer rejection, and aggression in children. Journal of Abnormal Child Psychology, 39(5), 645-656.
73. Wiese, H., Stude, P., Nebel, K., de Greiff, A., Forsting, M., Diener, H. C., & Keidel, M. (2004). Movement preparation in self-initiated versus externally triggered movements: An event-related fMRI-study. Neuroscience Letters, 371(2-3), 220-225.