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Lasting associations between early-childhood temperament and late-adolescent reward-circuitry response to peer feedback

  • Amanda E. Guyer (a1), Brenda Benson (a2), Victoria R. Choate (a3), Yair Bar-Haim (a4), Koraly Perez-Edgar (a5), Johanna M. Jarcho (a2), Daniel S. Pine (a2), Monique Ernst (a2), Nathan A. Fox (a6) and Eric E. Nelson (a2)...

Abstract

Behavioral inhibition, a temperament identifiable in infancy, is associated with heightened withdrawal from social encounters. Prior studies raise particular interest in the striatum, which responds uniquely to monetary gains in behaviorally inhibited children followed into adolescence. Although behavioral manifestations of inhibition are expressed primarily in the social domain, it remains unclear whether observed striatal alterations to monetary incentives also extend to social contexts. In the current study, imaging data were acquired from 39 participants (17 males, 22 females; ages 16–18 years) characterized since infancy on measures of behavioral inhibition. A social evaluation task was used to assess neural response to anticipation and receipt of positive and negative feedback from novel peers, classified by participants as being of high or low interest. As with monetary rewards, striatal response patterns differed during both anticipation and receipt of social reward between behaviorally inhibited and noninhibited adolescents. The current results, when combined with prior findings, suggest that early-life temperament predicts altered striatal response in both social and nonsocial contexts and provide support for continuity between temperament measured in early childhood and neural response to social signals measured in late adolescence and early adulthood.

Copyright

Corresponding author

Address correspondence and reprint requests to: Amanda E. Guyer, Department of Human Ecology, Center for Mind and Brain, University of California, Davis, 267 Cousteau Place, Davis, CA 95618; E-mail: aeguyer@ucdavis.edu.

References

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Adolphs, R. (2001). The neurobiology of social cognition. Current Opinion in Neurobiology, 11, 231239. doi:10.1016/S0959-4388(00)00202-6
Allen, J. P., Porter, M. R., McFarland, F. C., Marsh, P., & McElhaney, K. B. (2005). The two faces of adolescents' success with peers: Adolescent popularity, social adaptation, and deviant behavior. Child Development, 76, 747760. doi:10.1111/j.1467-8624.2005.00875.x
Almas, A. N., Phillips, D. A., Henderson, H. A., Hane, A. A., Degnan, K. A., Moas, O. L., et al. (2011). The relations between infant negative reactivity, nonmaternal childcare, and children's interactions with familiar and unfamiliar peers. Social Development, 20, 718740. doi:10.1111/j.1467-9507.2011.00605.x
Asendorpf, J. B., & Meier, G. H. (1993). Personality effects on children's speech in everyday life: Sociability-mediated exposure and shyness-mediated reactivity to social situations. Journal of Personality and Social Psychology, 64, 10721083. doi:10.1037/0022-3514.64.6.1072
Atallah, H. E., Lopez-Paniagua, D., Rudy, J. W., & O'Reilly, R. C. (2007). Separate neural substrates for skill learning and performance in the ventral and dorsal striatum. Nature Neuroscience, 10, 126131. doi:10.1038/nn1817
Bar-Haim, Y., Fox, N. A., Benson, B., Guyer, A. E., Williams, A., Nelson, E. E., et al. (2009). Neural correlates of reward processing in adolescents with a history of inhibited temperament. Psychological Science, 20, 10091018. doi:10.1111/j.1467-9280.2009.02401.x
Beesdo, K., Bittner, A., Pine, D. S., Stein, M. B., Höfler, M., Lieb, R., et al. (2007). Incidence of social anxiety disorder and the consistent risk for secondary depression in the first three decades of life. Archives of General Psychiatry, 64, 903912. doi:10.1001/archpsyc.64.8.903
Birmaher, B., Khetarpal, S., Brent, D., Cully, M., Balach, L., Kaufman, J., et al. (1997). The Screen for Child Anxiety Related Emotional Disorders (SCARED): Scale construction and psychometric characteristics. Journal of the American Academy of Child & Adolescent Psychiatry, 36, 545553. doi:10.1097/00004583-199704000-00018
Blakemore, S. J. (2008). The social brain in adolescence. Nature Reviews Neuroscience, 9, 267277. doi:10.1038/nrn2353
Boivin, M., Hymel, S., & Burkowski, W. M. (1995). The roles of social withdrawal, peer rejection, and victimization by peers in predicting loneliness and depressed mood in childhood. Development and Psychopathology, 7, 765785. doi:10.1017/S0954579400006830
Brown, B. B. (2004). Adolescents' relationships with peers. In Lerner, R. M. & Steinberg, L. (Eds.), Handbook of adolescent psychology (2nd ed., pp. 363394). Hoboken, NJ: Wiley.
Burgess, K. B., Wojslawowicz, J. C., Rubin, K. H., Rose-Krasnor, L., & Booth-LaForce, C. (2006). Social information processing and coping strategies of shy/withdrawn and aggressive children: Does friendship matter? Child Development, 77, 371383. doi:10.1111/j.1467-8624.2006.00876.x
Chen, X., DeSouza, A. T., Chen, H., & Wang, L. (2006). Reticent behavior and experiences in peer interactions in Chinese and Canadian children. Developmental Psychology, 42, 656665. doi:10.1037/0012-1649.42.4.656
Chronis-Tuscano, A., Degnan, K. A., Pine, D. S., Perez-Edgar, K., Henderson, H. A., Diaz, Y., et al. (2009). Stable early maternal report of behavioral inhibition predicts lifetime social anxiety disorder in adolescence. Journal of the American Academy of Child & Adolescent Psychiatry, 48, 928935. doi:10.1097/CHI.0b013e3181ae09df
Cicchetti, D., & Rogosch, F. A. (2002). A developmental psychopathology perspective on adolescence. Journal of Consulting and Clinical Psychology, 70, 620. doi:10.1037/0022-006X.70.1.6
Cicchetti, D., & Thomas, K. M. (2008). Imaging brain systems in normality and psychopathology. Development and Psychopathology, 20, 10231027. doi:10.1017/S0954579408000485
Cicchetti, D., & Tucker, D. (1994). Development and self-regulatory structures of the mind. Development and Psychopathology, 6, 533549. doi:10.1017/S0954579400004673
Coplan, R. J., Rubin, K. H., Fox, N. A., Calkins, S. D., & Stewart, S. L. (1994). Being alone, playing alone, and acting alone: Distinguishing among reticence and passive and active solitude among children. Child Development, 65, 129137.
Cox, R. W. (1996). AFNI: Software for analysis and visualization of functional magnetic resonance neuroimages. Computers and Biomedical Research, 29, 162173. doi:10.1006/cbmr.1996.0014
Degnan, K. A., & Fox, N. A. (2007). Behavioral inhibition and anxiety disorders: Multiple levels of a resilience process. Development and Psychopathology, 19, 729746. doi:10.1017/S0954579407000363
Di Martino, A., Scheres, A., Margulies, D. S., Kelly, A. M., Uddin, L. Q., Shehzad, Z., et al. (2008). Functional connectivity of human striatum: A resting state fMRI study. Cerebral Cortex, 18, 27352747. doi:10.1093/cercor/bhn041
Egger, H. L., Pine, D. S., Nelson, E. E., Leibenluft, E., Ernst, M., Towbin, K., et al. (2011). The NIMH Child Emotional Faces Picture Set (NIMH-ChEFS): A new set of children's facial emotion stimuli. International Journal of Methods in Psychiatric Research, 20, 145156. doi:10.1002/mpr.343
Ernst, M., & Fudge, J. L. (2009). A developmental neurobiological model of motivated behavior: Anatomy, connectivity and ontogeny of the triadic nodes. Neuroscience & Biobehavioral Reviews, 33, 367382. doi:10.1016/j.neubiorev.2008.10.009
Fox, N. A., Henderson, H. A., Marshall, P. J., Nichols, K. E., & Ghera, M. M. (2005). Behavioral inhibition: Linking biology and behavior within a developmental framework. Annual Review of Psychology, 56, 235262. doi:10.1146/annurev.psych.55.090902.141532
Fox, N. A., Henderson, H. A., Rubin, K. H., Calkins, S. D., & Schmidt, L. A. (2001). Continuity and discontinuity of behavioral inhibition and exuberance: Psychophysiological and behavioral influences across the first four years of life. Child Development, 72, 121. doi:10.1111/1467-8624.00262
Goldsmith, H. H. (1996). Studying temperament via construction of the Toddler Behavior Assessment Questionnaire. Child Development, 67, 218235. doi:10.1111/j.1467-8624.1996.tb01730
Gunther Moor, B., van Leijenhorst, L., Rombouts, S. A., Crone, E. A., & Van der Molen, M. W. (2010). Do you like me? Neural correlates of social evaluation and developmental trajectories. Social Neuroscience, 5, 461482. doi:10.1080/17470910903526155
Guyer, A. E., Choate, V. R., Detloff, A., Benson, B., Nelson, E. E., Perez-Edgar, K., et al. (2012). Striatal functional alteration during incentive anticipation in pediatric anxiety disorders. American Journal of Psychiatry, 169, 205212. doi:10.1176/appi.ajp.2011.11010006
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, 8192. doi:10.1093/scan/nsr043
Guyer, A. E., Lau, J. Y., McClure-Tone, E. B., Parrish, J., Shiffrin, N. D., Reynolds, R. C., et al. (2008). Amygdala and ventrolateral prefrontal cortex function during anticipated peer evaluation in pediatric social anxiety. Archives of General Psychiatry, 65, 13031312. doi:10.1001/archpsyc.65.11.1303
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, 10001015. doi:10.1111/j.1467-8624.2009.01313.x
Guyer, A. E., Nelson, E. E., Perez-Edgar, K., Hardin, M. G., Roberson-Nay, R., Monk, C. S., et al. (2006). Striatal functional alteration in adolescents characterized by early childhood behavioral inhibition. Journal of Neuroscience, 26, 63996405. doi:10.1523/jneurosci.0666-06.2006
Haber, S. N., & Knutson, B. (2010). The reward circuit: Linking primate anatomy and human imaging. Neuropsychopharmacology, 35, 426. doi:10.1038/npp.2009.129
Hanish, L. D., & Guerra, N. G. (2000). Predictors of peer victimization among urban youth. Social Development, 9, 521543. doi:10.1111/1467-9507.00141
Haruno, M., & Kawato, M. (2006). Different neural correlates of reward expectation and reward expectation error in the putamen and caudate nucleus during stimulus–action–reward association learning. Journal of Neurophysiology, 95, 948959. doi:10.1152/jn.00382.2005
Haxby, J. V., Hoffman, E. A., & Gobbini, M. I. (2000). The distributed human neural system for face perception. Trends in Cognitive Science, 4, 223233. doi:10.1016/S1364-6613(00)01482–0
Hazy, T. E., Frank, M. J., & O'Reilly, R. C. (2010). Neural mechanisms of acquired phasic dopamine responses in learning. Neuroscience & Biobehavioral Reviews, 34, 701720. doi:10.1016/j.neubiorev.2009.11.019
Helfinstein, S. M., Benson, B., Perez-Edgar, K., Bar-Haim, Y., Detloff, A., Pine, D. S., et al. (2011). Striatal responses to negative monetary outcomes differ between temperamentally inhibited and noninhibited adolescents. Neuropsychologia, 49, 479485. doi:10.1016/j.neuropsychologia.2010.12.015
Helfinstein, S. M., Fox, N. A., & Pine, D. S. (2012). Approach–withdrawal and the role of the striatum in the temperament of behavioral inhibition. Developmental Psychology, 48, 815826. doi:10.1037/a0026402
Howarth, G. Z., Guyer, A. E., & Perez-Edgar, K. (2013). Young children's affective responses to acceptance and rejection from peers: A computer-based task sensitive to variation in temperamental shyness and gender. Social Development, 22, 146162. doi:10.1111/sode.12006
Izuma, K., Saito, D. N., & Sadato, N. (2008). Processing of social and monetary rewards in the human striatum. Neuron, 58, 284294. doi:10.1016/j.neuron.2008.03.020
Jarcho, J. M., Fox, N. A., Pine, D. S., Etkin, A., Leibenluft, E., Shechner, T., et al. (2012). The neural correlates of emotion-based cognitive control in adults with early childhood behavioral inhibition. Biological Psychology, 92, 306314. doi:10.1016/j.biopsycho.2012.09.008
Jones, R. M., Somerville, L. H., Li, J., Ruberry, E. J., Libby, V., Glover, G., et al. (2011). Behavioral and neural properties of social reinforcement learning. Journal of Neuroscience, 31, 1303913045. doi:10.1523/JNEUROSCI.2972-11.2011
Kagan, J. (1997). Galen's prophecy: Temperament in human nature. Boulder, CO: Westview Press.
Kagan, J., & Fox, N. A. (2007). Biology, culture, and temperamental biases. Handbook of child psychology. Hoboken, NJ: Wiley. doi:10.1002/9780470147658.chpsy0304
Kampe, K. K., Frith, C. D., Dolan, R. J., & Frith, U. (2001). Reward value of attractiveness and gaze. Nature, 413, 589. doi:10.1038/35098149
Kaufman, J., Birmaher, B., Brent, D., Rao, U., Flynn, C., Moreci, P., et al. (1997). Schedule for Affective Disorders and Schizophrenia for School-Age Children—Present and Lifetime Version (K-SADS-PL): Initial reliability and validity data. Journal of the American Academy of Child & Adolescent Psychiatry, 36, 980988. doi:10.1097/00004583-199707000-00021
La Greca, A. M., & Lopez, N. (1998). Social anxiety among adolescents: Linkages with peer relations and friendships. Journal of Abnormal Child Psychology, 26, 8394. doi:10.1023/A:1022684520514
Lau, J. Y., Guyer, A. E., Tone, E. B., Jenness, J., Parrish, J., Pine, D. S., et al. (2011). Neural responses to peer rejection in anxious adolescents: Contributions from the amygdala–hippocampal complex. International Journal of Behavioral Development. doi:10.1177/0165025411406854
Lorberbaum, J. P., Kose, S., Johnson, M. R., Arana, G. W., Sullivan, L. K., Hamner, M. B., et al. (2004). Neural correlates of speech anticipatory anxiety in generalized social phobia. NeuroReport, 15, 27012705.
Marshall, P. J., Reeb, B. C., & Fox, N. A. (2009). Electrophysiological responses to auditory novelty in temperamentally different 9-month-old infants. Developmental Science, 12, 568582. doi:10.1111/j.1467-7687.2008.00808.x
Mattfeld, A. T., Gluck, M. A., & Stark, C. E. (2011). Functional specialization within the striatum along both the dorsal/ventral and anterior/posterior axes during associative learning via reward and punishment. Learning & Memory, 18, 703711. doi:10.1101/lm.022889.111
McClure, E. B., Monk, C. S., Nelson, E. E., Parrish, J. M., Adler, A., Blair, R. J., et al. (2007). Abnormal attention modulation of fear circuit function in pediatric generalized anxiety disorder. Archives of General Psychiatry, 64, 97106. doi:10.1001/archpsyc.64.1.97
Muranishi, M., Inokawa, H., Yamada, H., Ueda, Y., Matsumoto, N., Nakagawa, M., et al. (2011). Inactivation of the putamen selectively impairs reward history-based action selection. Experimental Brain Research, 209, 235246. doi:10.1007/s00221-011-2545-y
Muris, P., Meesters, C., Merckelbach, H., Sermon, A., & Zwakhalen, S. (1998). Worry in normal children. Journal of the American Academy of Child & Adolescent Psychiatry, 37, 703710. doi:10.1097/00004583-199807000-00009
Nelson, E. E., Leibenluft, E., McClure, E. B., & Pine, D. S. (2005). The social re-orientation of adolescence: A neuroscience perspective on the process and its relation to psychopathology. Psychological Medicine, 35, 163174. doi:10.1017/S0033291704003915
Perez-Edgar, K., Bar-Haim, Y., McDermott, J. M., Chronis-Tuscano, A., Pine, D. S., & Fox, N. A. (2010). Attention biases to threat and behavioral inhibition in early childhood shape adolescent social withdrawal. Emotion, 10, 349357. doi:10.1037/a0018486
Perez-Edgar, K., & Fox, N. A. (2005). Temperament and anxiety disorders. Child and Adolescent Psychiatric Clinics of North America, 14, 681706. doi:10.1016/j.chc.2005.05.008
Perez-Edgar, K., Hardee, J. E., Guyer, A. E., Benson, B. E., Nelson, E. E., Gorodetsky, E., et al. (2013). DRD4 and striatal modulation of the link between childhood behavioral inhibition and adolescent anxiety. Social Cognitive and Affective Neuroscience. doi:10.1093/scan/nst001
Perez-Edgar, K., Roberson-Nay, R., Hardin, M. G., Poeth, K., Guyer, A. E., Nelson, E. E., et al. (2007). Attention alters neural responses to evocative faces in behaviorally inhibited adolescents. Neuroimage, 35, 15381546. doi:10.1016/j.neuroimage.2007.02.006
Peters, J., & Buchel, C. (2010). Neural representations of subjective reward value. Behavioural Brain Research, 213, 135141. doi:10.1016/j.bbr.2010.04.031
Pfeifer, J. H., Lieberman, M. D., & Dapretto, M. (2007). “I know you are but what am I?!” Neural bases of self- and social knowledge retrieval in children and adults. Journal of Cognitive Neuroscience, 19, 13231337. doi:10.1162/jocn.2007.19.8.1323
Pine, D. S. (1999). Pathophysiology of childhood anxiety disorders. Biological Psychiatry, 46, 15551566. doi:10.1016/S0006-3223(99)00115–8
Redcay, E. (2008). The superior temporal sulcus performs a common function for social and speech perception: Implications for the emergence of autism. Neuroscience Biobehavioral Reviews, 32, 123142. doi:10.1016/j.neubiorev.2007.06.004
Rimm-Kaufman, S. E., & Kagan, J. (2005). Infant predictors of kindergarten behavior: The contribution of inhibited and uninhibited temperament types. Behavioral Disorders, 30, 331347. doi:10.1016/S0193-3973(02)00128–4
Rowe, D. C., & Plomin, R. (1977). Temperament in early childhood. Journal of Personality Assessment, 41, 150156. doi:10.1207/s15327752jpa4102_5
Rubin, K. H. (1989). The Play Observation Scale (POS). University of Waterloo.
Rubin, K. H., Bukowski, W. M., & Parker, J. G. (2006). Peer interactions, relationships, and groups. In Eisenberg, N. E., Damon, W. E., & Lerner, R. M. E. (Eds.), Handbook of child psychology: Vol. 3. Emotional, and personality development (6th ed., pp. 571645). Hoboken, NJ: Wiley.
Rubin, K. H., Coplan, R. J., & Bowker, J. C. (2009). Social withdrawal in childhood. Annual Review of Psychology, 60, 141171. doi:10.1146/annurev.psych.60.110707.163642
Saxe, R. (2006). Uniquely human social cognition. Current Opinion in Neurobiology, 16, 235239. doi:10.1016/j.conb.2006.03.001
Schneier, F. R., Abi-Dargham, A., Martinez, D., Slifstein, M., Hwang, D. R., Liebowitz, M. R., et al. (2009). Dopamine transporters, D2 receptors, and dopamine release in generalized social anxiety disorder. Depression and Anxiety, 26, 411418. doi:10.1002/da.20543
Schneier, F. R., Liebowitz, M. R., Abi-Dargham, A., Zea-Ponce, Y., Lin, S. H., & Laruelle, M. (2000). Low dopamine D(2) receptor binding potential in social phobia. American Journal of Psychiatry, 157, 457459. doi:10.1176/appi.ajp.157.3.457
Schultz, W. (2006). Behavioral theories and the neurophysiology of reward. Annual Review of Psychology, 57, 87115. doi:10.1146/annurev.psych.56.091103.070229
Schwartz, C. E., Wright, C. I., Shin, L. M., Kagan, J., & Rauch, S. L. (2003). Inhibited and uninhibited infants “grown up”: Adult amygdalar response to novelty. Science, 300, 19521953. doi:10.1126/science.1083703
Silverman, W. K., La Greca, A. M., & Wasserstein, S. (1995). What do children worry about? Worries and their relation to anxiety. Child Development, 66, 671686. doi:10.1111/j.1467-8624.1995.tb00897.x
Spreckelmeyer, K. N., Krach, S., Kohls, G., Rademacher, L., Irmak, A., Konrad, K., et al. (2009). Anticipation of monetary and social reward differently activates mesolimbic brain structures in men and women. Social Cognitive and Affective Neuroscience, 4, 158165. doi:10.1093/scan/nsn051
Tarullo, A. R., Mliner, S., & Gunnar, M. R. (2011). Inhibition and exuberance in preschool classrooms: Associations with peer social experiences and changes in cortisol across the preschool year. Developmental Psycholology, 47, 13741388. doi:10.1037/a0024093
Tiihonen, J., Kuikka, J., Bergström, K., Lepola, U., Koponen, H., & Leinonen, E. (1997). Dopamine reuptake site densities in patients with social phobia. American Journal of Psychiatry, 154, 239242.
Trainor, B. C. (2011). Stress responses and the mesolimbic dopamine system: Social contexts and sex differences. Hormones and Behavior, 60, 457469. doi:10.1016/j.yhbeh.2011.08.013
van Leijenhorst, L., Crone, E. A., & Bunge, S. A. (2006). Neural correlates of developmental differences in risk estimation and feedback processing. Neuropsychologia, 44, 21582170. doi:10.1016/j.neuropsychologia.2006.02.002
Voorn, P., Vanderschuren, L. J., Groenewegen, H. J., Robbins, T. W., & Pennartz, C. M. (2004). Putting a spin on the dorsal–ventral divide of the striatum. Trends in Neurosciences, 27, 468474. doi:10.1016/j.tins.2004.06.006

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