Abstract
Unfamiliar people, places, and objects often elicit wariness and distress in behaviorally inhibited infants. As behaviorally inhibited infants mature through childhood and become adolescents, peer-based social situations become the driving source of this wariness. The conflict between a desire for positive social interactions and fear of negative evaluation interferes with one of the primary “jobs” of adolescence: learning to successfully navigate an increasingly complex social world. Neural networks involved in social information processing, social learning, and social competence contribute to the maladaptive approach and avoidance response patterns and tendencies associated with behavioral inhibition. In the present chapter, we review the neural networks involved in social competence and social cognition, discuss key links between altered neural function and social cognition associated with behavioral inhibition, and highlight gaps in the field. Finally, we propose future directions to advance our understanding of the neural mechanisms that underlie behaviors and cognition elicited in novel social contexts for behaviorally inhibited youth.
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References
Affrunti, N. W., Geronimi, E. M., & Woodruff-Borden, J. (2014). Temperament, peer victimization, and nurturing parenting in child anxiety: A moderated mediation model. Child Psychiatry and Human Development, 45(4), 483–492. https://doi.org/10.1007/s10578-013-0418-2
Albert, D., Chein, J., & Steinberg, L. (2013). Peer influences on adolescent decision making. Current Directions in Psychological Science, 22(2), 114–120. https://doi.org/10.1177/0963721412471347
Alcala-Lopez, D., Smallwood, J., Jefferies, E., Van Overwalle, F., Vogeley, K., Mars, R. B., … Bzdok, D. (2017). Computing the social brain Connectome across systems and states. Cerebral Cortex, 1–26. https://doi.org/10.1093/cercor/bhx121
Bar-Haim, Y., Fox, N. A., Benson, B., Guyer, A. E., Williams, A., Nelson, E. E., … Ernst, M. (2009). Neural correlates of reward processing in adolescents with a history of inhibited temperament. Psychological Science, 20(8), 1009–1018. https://doi.org/10.1111/j.1467-9280.2009.02401.x
Barrett, L. F., & Satpute, A. B. (2013). Large-scale brain networks in affective and social neuroscience: Towards an integrative functional architecture of the brain. Current Opinion in Neurobiology, 23(3), 361–372. https://doi.org/10.1016/j.conb.2012.12.012
Baxter, M. G., Parker, A., Lindner, C. C. C., Izquierdo, A. D., & Murray, E. A. (2000). Control of response selection by reinforcer value requires interaction of amygdala and orbital prefrontal cortex. Journal of Neuroscience, 20(11), 4311–4319.
Becker, M. P., Nitsch, A. M., Hewig, J., Miltner, W. H., & Straube, T. (2016). Parametric modulation of reward sequences during a reversal task in ACC and VMPFC but not amygdala and striatum. NeuroImage, 143, 50–57. https://doi.org/10.1016/j.neuroimage.2016.09.022
Beesdo, K., Pine, D. S., Lieb, R., & Wittchen, H. U. (2010). Incidence and risk patterns of anxiety and depressive disorders and categorization of generalized anxiety disorder. Archives of General Psychiatry, 67(1), 47–57. https://doi.org/10.1001/archgenpsychiatry.2009.177
Bick, J., Zhu, T., Stamoulis, C., Fox, N. A., Zeanah, C., & Nelson, C. A. (2015). Effect of early institutionalization and foster care on long-term white matter development: A randomized clinical trial. JAMA Pediatrics, 169(3), 211–219. https://doi.org/10.1001/jamapediatrics.2014.3212
Bickart, K. C., Hollenbeck, M. C., Barrett, L. F., & Dickerson, B. C. (2012). Intrinsic amygdala-cortical functional connectivity predicts social network size in humans. Journal of Neuroscience, 32(42), 14729–14741. https://doi.org/10.1523/JNEUROSCI.1599-12.2012
Blackford, J. U., Allen, A. H., Cowan, R. L., & Avery, S. N. (2013). Amygdala and hippocampus fail to habituate to faces in individuals with an inhibited temperament. Social Cognitive and Affective Neuroscience, 8(2), 143–150. https://doi.org/10.1093/scan/nsr078
Blackford, J. U., Avery, S. N., Cowan, R. L., Shelton, R. C., & Zald, D. H. (2011). Sustained amygdala response to both novel and newly familiar faces characterizes inhibited temperament. Social Cognitive and Affective Neuroscience, 6(5), 621–629. https://doi.org/10.1093/scan/nsq073
Blackford, J. U., Avery, S. N., Shelton, R. C., & Zald, D. H. (2009). Amygdala temporal dynamics: Temperamental differences in the timing of amygdala response to familiar and novel faces. BMC Neuroscience, 10, 145. https://doi.org/10.1186/1471-2202-10-145
Blackford, J. U., Clauss, J. A., Avery, S. N., Cowan, R. L., Benningfield, M. M., & VanDerKlok, R. M. (2014). Amygdala-cingulate intrinsic connectivity is associated with degree of social inhibition. Biological Psychology, 99, 15–25. https://doi.org/10.1016/j.biopsycho.2014.02.003
Blakemore, S. J. (2008). The social brain in adolescence. Nature Reviews Neuroscience, 9(4), 267–277. https://doi.org/10.1038/nrn2353
Botvinick, M. M., Cohen, J. D., & Carter, C. S. (2004). Conflict monitoring and anterior cingulate cortex: An update. Trends in Cognitive Sciences, 8(12), 539–546. https://doi.org/10.1016/j.tics.2004.10.003
Braams, B. R., & Crone, E. A. (2017). Peers and parents: A comparison between neural activation when winning for friends and mothers in adolescence. Social Cognitive and Affective Neuroscience, 12(3), 417–426. https://doi.org/10.1093/scan/nsw136
Brown, B. B., Bakken, J. P., Ameringer, S. W., & Mahon, S. D. (2008). A comprehensive conceptualization of the peer influence process in adolescence. Understanding Peer Influence in Children and Adolescents, 17–44.
Brown, B. B., & Larson, J. (2009). Peer relationships in adolescence. In L. Steinberg & R. M. Lerner (Eds.), Handbook of adolescent psychology, Volume 2: Contextual influences on adolescent development (Vol. 2, p. 74). Hoboken, NJ: John Wiley & Sons.
Buhle, J. T., Silvers, J. A., Wager, T. D., Lopez, R., Onyemekwu, C., Kober, H., … Ochsner, K. N. (2014). Cognitive reappraisal of emotion: A meta-analysis of human neuroimaging studies. Cerebral Cortex, 24(11), 2981–2990. https://doi.org/10.1093/cercor/bht154
Buss, K. A. (2011). Which fearful toddlers should we worry about? Context, fear regulation, and anxiety risk. Developmental Psychology, 47(3), 804–819. https://doi.org/10.1037/a0023227
Buss, K. A., Davis, E. L., Kiel, E. J., Brooker, R. J., Beekman, C., & Early, M. C. (2013). Dysregulated fear predicts social wariness and social anxiety symptoms during kindergarten. Journal of Clinical Child and Adolescent Psychology, 42(5), 603–616. https://doi.org/10.1080/15374416.2013.769170
Cabeleira, C. M., Steinman, S. A., Burgess, M. M., Bucks, R. S., MacLeod, C., Melo, W., & Teachman, B. A. (2014). Expectancy bias in anxious samples. Emotion, 14(3), 588.
Calvo, M. G., & Nummenmaa, L. (2016). Perceptual and affective mechanisms in facial expression recognition: An integrative review. Cognition & Emotion, 30(6), 1081–1106. https://doi.org/10.1080/02699931.2015.1049124
Caouette, J. D., & Guyer, A. E. (2014). Gaining insight into adolescent vulnerability for social anxiety from developmental cognitive neuroscience. Developmental Cognitive Neuroscience, 8, 65–76.
Caspi, A., Moffitt, T. E., Newman, D. L., & Silva, P. A. (1996). Behavioral observations at age 3 years predict adult psychiatric disorders – longitudinal evidence from a birth cohort. Archives of General Psychiatry, 53(11), 1033–1039.
Chronis-Tuscano, A., Degnan, K. A., Pine, D. S., Perez-Edgar, K., Henderson, H. A., Diaz, Y., … Fox, N. A. (2009). Stable early maternal report of behavioral inhibition predicts lifetime social anxiety disorder in adolescence. Journal of the American Academy of Child and Adolescent Psychiatry, 48(9), 928–935. https://doi.org/10.1097/CHI.0b013e3181ae09df
Cisler, J. M., & Koster, E. H. (2010). Mechanisms of attentional biases towards threat in anxiety disorders: An integrative review. Clinical Psychology Review, 30(2), 203–216. https://doi.org/10.1016/j.cpr.2009.11.003
Clauss, J. A., Avery, S. N., VanDerKlok, R. M., Rogers, B. P., Cowan, R. L., Benningfield, M. M., & Blackford, J. U. (2014). Neurocircuitry underlying risk and resilience to social anxiety disorder. Depression and Anxiety, 31(10), 822–833. https://doi.org/10.1002/da.22265
Clauss, J. A., & Blackford, J. U. (2012). Behavioral inhibition and risk for developing social anxiety disorder: A meta-analytic study. Journal of the American Academy of Child and Adolescent Psychiatry, 51(10), 1066–1075 e1061. https://doi.org/10.1016/j.jaac.2012.08.002
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 in young-children. Child Development, 65(1), 129–137. https://doi.org/10.1111/j.1467-8624.1994.tb00739.x
Damoiseaux, J. S., & Greicius, M. D. (2009). Greater than the sum of its parts: A review of studies combining structural connectivity and resting-state functional connectivity. Brain Structure & Function, 213(6), 525–533. https://doi.org/10.1007/s00429-009-0208-6
Deater-Deckard, K. (2001). Annotation: Recent research examining the role of peer relationships in the development of psychopathology. Journal of Child Psychology and Psychiatry and Allied Disciplines, 42(5), 565–579. https://doi.org/10.1111/1469-7610.00753
Degnan, K. A., Almas, A. N., Henderson, H. A., Hane, A. A., Walker, O. L., & Fox, N. A. (2014). Longitudinal trajectories of social reticence with unfamiliar peers across early childhood. Developmental Psychology, 50(10), 2311–2323. https://doi.org/10.1037/a0037751
Dunbar, R. I., & Shultz, S. (2007). Understanding primate brain evolution. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 362(1480), 649–658. https://doi.org/10.1098/rstb.2006.2001
Ellis, B. J., Del Giudice, M., Dishion, T. J., Figueredo, A. J., Gray, P., Griskevicius, V., … Wilson, D. S. (2012). The evolutionary basis of risky adolescent behavior: Implications for science, policy, and practice. Developmental Psychology, 48(3), 598–623. https://doi.org/10.1037/a0026220
Etkin, A., Egner, T., & Kalisch, R. (2011). Emotional processing in anterior cingulate and medial prefrontal cortex. Trends in Cognitive Sciences, 15(2), 85–93. https://doi.org/10.1016/j.tics.2010.11.004
Feng, P., Zheng, Y., & Feng, T. Y. (2016). Resting-state functional connectivity between amygdala and the ventromedial prefrontal cortex following fear reminder predicts fear extinction. Social Cognitive and Affective Neuroscience, 11(6), 991–1001. https://doi.org/10.1093/scan/nsw031
Fox, A. S., & Kalin, N. H. (2014). A translational neuroscience approach to understanding the development of social anxiety disorder and its pathophysiology. The American Journal of Psychiatry, 171(11), 1162–1173. https://doi.org/10.1176/appi.ajp.2014.14040449
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, 235–262.
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(1), 1–21.
Frith, C. D., & Frith, U. (2006). The neural basis of mentalizing. Neuron, 50(4), 531–534. https://doi.org/10.1016/j.neuron.2006.05.001
Frith, U., & Frith, C. D. (2003). Development and neurophysiology of mentalizing. Philosophical Transactions of the Royal Society B-Biological Sciences, 358(1431), 459–473. https://doi.org/10.1098/rstb.2002.1218
Fu, X., Taber-Thomas, B. C., & Perez-Edgar, K. (2017). Frontolimbic functioning during threat-related attention: Relations to early behavioral inhibition and anxiety in children. Biological Psychology, 122, 98–109. https://doi.org/10.1016/j.biopsycho.2015.08.010
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. https://doi.org/10.1523/Jneurosci.1062-06.2006
Gazelle, H., & Rudolph, K. D. (2004). Moving toward and away from the world: Social approach and avoidance trajectories in anxious solitary youth. Child Development, 75(3), 829–849. https://doi.org/10.1111/j.1467-8624.2004.00709.x
Gobbini, M. I., & Haxby, J. V. (2007). Neural systems for recognition of familiar faces. Neuropsychologia, 45(1), 32–41. https://doi.org/10.1016/j.neuropsychologia.2006.04.015
Goffman, E. (2009). Stigma: Notes on the management of spoiled identity. Simon and Schuster. New York
Gold, A. L., Morey, R. A., & McCarthy, G. (2015). Amygdala-prefrontal cortex functional connectivity during threat-induced anxiety and goal distraction. Biological Psychiatry, 77(4), 394–403. https://doi.org/10.1016/j.biopsych.2014.03.030
Grabenhorst, F., & Rolls, E. T. (2011). Value, pleasure and choice in the ventral prefrontal cortex. Trends in Cognitive Sciences, 15(2), 56–67. https://doi.org/10.1016/j.tics.2010.12.004
Gunnar, M. R., & Hostinar, C. E. (2015). The social buffering of the hypothalamic-pituitary-adrenocortical axis in humans: Developmental and experiential determinants. Social Neuroscience, 10(5), 479–488. https://doi.org/10.1080/17470919.2015.1070747
Guyer, A. E., Benson, B., Choate, V. R., Bar-Haim, Y., Perez-Edgar, K., Jarcho, J. M., … Nelson, E. E. (2014). Lasting associations between early-childhood temperament and late-adolescent reward-circuitry response to peer feedback. Development and Psychopathology, 26(1), 229–243. https://doi.org/10.1017/S0954579413000941
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. https://doi.org/10.1093/scan/nsr043
Guyer, A. E., & Jarcho, J. M. (2018). Neuroscience and peer relations. In W. Bukowski, B. Laursen, & K. H. Rubin (Eds.), Handbook of peer interactions, relationships, and groups (2nd ed.). New York, NY: Guilford Press.
Guyer, A. E., Jarcho, J. M., Perez-Edgar, K., Degnan, K. A., Pine, D. S., Fox, N. A., & Nelson, E. E. (2015). Temperament and parenting styles in early childhood differentially influence neural response to peer evaluation in adolescence. Journal of Abnormal Child Psychology, 43(5), 863–874. https://doi.org/10.1007/s10802-015-9973-2
Guyer, A. E., Lau, J. Y., McClure-Tone, E. B., Parrish, J., Shiffrin, N. D., Reynolds, R. C., … Nelson, E. E. (2008). Amygdala and ventrolateral prefrontal cortex function during anticipated peer evaluation in pediatric social anxiety. Archives of General Psychiatry, 65(11), 1303–1312. https://doi.org/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(4), 1000–1015.
Guyer, A. E., Nelson, E. E., Perez-Edgar, K., Hardin, M. G., Roberson-Nay, R., Monk, C. S., … Ernst, M. (2006). Striatal functional alteration in adolescents characterized by early childhood behavioral inhibition. Journal of Neuroscience, 26(24), 6399–6405.
Hampton, A. N., Adolphs, R., Tyszka, M. J., & O'Doherty, J. P. (2007). Contributions of the amygdala to reward expectancy and choice signals in human prefrontal cortex. Neuron, 55(4), 545–555. https://doi.org/10.1016/j.neuron.2007.07.022
Hanish, L. D., & Guerra, N. G. (2004). Aggressive victims, passive victims, and bullies: Developmental continuity or developmental change? Merrill-Palmer Quarterly-Journal of Developmental Psychology, 50(1), 17–38. https://doi.org/10.1353/mpq.2004.0003
Hardee, J. E., Benson, B. E., Bar-Haim, Y., Mogg, K., Bradley, B. P., Chen, G., … Perez-Edgar, K. (2013). Patterns of neural connectivity during an attention Bias task moderate associations between early childhood temperament and internalizing symptoms in young adulthood. Biological Psychiatry, 74(4), 273–279. https://doi.org/10.1016/j.biopsych.2013.01.036
Hasenfratz, L., Benish-Weisman, M., Steinberg, T., & Knafo-Noam, A. (2015). Temperament and peer problems from early to middle childhood: Gene-environment correlations with negative emotionality and sociability. Development and Psychopathology, 27(4 Pt 1), 1089–1109. https://doi.org/10.1017/S095457941500070X
Haxby, J. V., Hoffman, E. A., & Gobbini, M. I. (2000). The distributed human neural system for face perception. Trends in Cognitive Sciences, 4(6), 223–233. https://doi.org/10.1016/S1364-6613(00)01482-0
Heimberg, R. G., Brozovich, F. A., & Rapee, R. M. (2010). A cognitive behavioral model of social anxiety disorder: Update and extension. In Social anxiety (2nd ed., pp. 395–422). San Diego, CA: Academic Press.
Helfinstein, S. M., Benson, B., Perez-Edgar, K., Bar-Haim, Y., Detloff, A., Pine, D. S., … Ernst, M. (2011). Striatal responses to negative monetary outcomes differ between temperamentally inhibited and non-inhibited adolescents. Neuropsychologia, 49(3), 479–485. https://doi.org/10.1016/j.neuropsychologia.2010.12.015
Henderson, H. A., Marshall, P. J., Fox, N. A., & Rubin, K. H. (2004). Psychophysiological and behavioral evidence for varying forms and functions of nonsocial behavior in preschoolers. Child Development, 75(1), 251–263. https://doi.org/10.1111/j.1467-8624.2004.00667.x
Holt-Lunstad, J., Smith, T. B., & Layton, J. B. (2010). Social relationships and mortality risk: A meta-analytic review. PLoS Medicine, 7(7), e1000316. https://doi.org/10.1371/journal.pmed.1000316
Howard, J. D., Gottfried, J. A., Tobler, P. N., & Kahnt, T. (2015). Identity-specific coding of future rewards in the human orbitofrontal cortex. Proceedings of the National Academy of Sciences of the United States of America, 112(16), 5195–5200. https://doi.org/10.1073/pnas.1503550112
Jarcho, J. M., Davis, M. M., Shechner, T., Degnan, K. A., Henderson, H. A., Stoddard, J., … Nelson, E. E. (2016). Early-childhood social reticence predicts brain function in preadolescent youths during distinct forms of peer evaluation. Psychological Science, 27(6), 821–835. https://doi.org/10.1177/0956797616638319
Jarcho, J. M., Fox, N. A., Pine, D. S., Etkin, A., Leibenluft, E., Shechner, T., & Ernst, M. (2013). The neural correlates of emotion-based cognitive control in adults with early childhood behavioral inhibition. Biological Psychology, 92(2), 306–314. https://doi.org/10.1016/j.biopsycho.2012.09.008
Jarcho, J. M., Fox, N. A., Pine, D. S., Leibenluft, E., Shechner, T., Degnan, K. A., … Ernst, M. (2014). Enduring influence of early temperament on neural mechanisms mediating attention-emotion conflict in adults. Depression and Anxiety, 31(1), 53–62. https://doi.org/10.1002/da.22140
Jarcho, J. M., Leibenluft, E., Walker, O. L., Fox, N. A., Pine, D. S., & Nelson, E. E. (2013). Neuroimaging studies of pediatric social anxiety: Paradigms, pitfalls and a new direction for investigating the neural mechanisms. Biol Mood Anxiety Disord, 3, 14. https://doi.org/10.1186/2045-5380-3-14
Jarcho, J. M., Romer, A. L., Shechner, T., Galvan, A., Guyer, A. E., Leibenluft, E., … Nelson, E. E. (2015). Forgetting the best when predicting the worst: Preliminary observations on neural circuit function in adolescent social anxiety. Developmental Cognitive Neuroscience, 13, 21–31. https://doi.org/10.1016/j.dcn.2015.03.002
Jenkins, A. C., & Mitchell, J. P. (2011). Medial prefrontal cortex subserves diverse forms of self-reflection. Social Neuroscience, 6(3), 211–218. https://doi.org/10.1080/17470919.2010.507948
Kagan, J. (2012). The biography of behavioral inhibition. In M. Zentner & R. L. Shiner (Eds.), Handbook of temperament (pp. 69–82). New York, NY: Guilford Press.
Kagan, J., & Snidman, N. (1991). Infant predictors of inhibited and uninhibited profiles. Psychological Science, 2(1), 40–44. https://doi.org/10.1111/j.1467-9280.1991.tb00094.x
Kanwisher, N., McDermott, J., & Chun, M. M. (1997). The fusiform face area: A module in human extrastriate cortex specialized for face perception. Journal of Neuroscience, 17(11), 4302–4311.
Kennedy, D. P., & Adolphs, R. (2012). The social brain in psychiatric and neurological disorders. Trends in Cognitive Sciences, 16(11), 559–572. https://doi.org/10.1016/j.tics.2012.09.006
Knudsen, E. I. (2004). Sensitive periods in the development of the brain and behavior. Journal of Cognitive Neuroscience, 16(8), 1412–1425. https://doi.org/10.1162/0898929042304796
Knutson, B., Adams, C. M., Fong, G. W., & Hommer, D. (2001). Anticipation of increasing monetary reward selectively recruits nucleus accumbens. Journal of Neuroscience, 21(16), RC159.
Knutson, B., Fong, G. W., Bennett, S. M., Adams, C. M., & Hommer, D. (2003). A region of mesial prefrontal cortex tracks monetarily rewarding outcomes: Characterization with rapid event-related fMRI. NeuroImage, 18(2), 263–272.
Kochenderfer-Ladd, B. (2003). Identification of aggressive and asocial victims and the stability of their peer victimization. Merrill-Palmer Quarterly-Journal of Developmental Psychology, 49(4), 401–425. https://doi.org/10.1353/mpq.2003.0022
Lahat, A., Benson, B. E., Pine, D. S., Fox, N. A., & Ernst, M. (2016). Neural responses to reward in childhood: Relations to early behavioral inhibition and social anxiety. Social Cognitive and Affective Neuroscience. https://doi.org/10.1093/scan/nsw122
Lahat, A., Perez-Edgar, K., Degnan, K. A., Guyer, A. E., Lejuez, C. W., Ernst, M., … Fox, N. A. (2012). Early childhood temperament predicts substance use in young adults. Translational Psychiatry, 2, e157. https://doi.org/10.1038/tp.2012.87
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. https://doi.org/10.1093/scan/nsr006
Lombardo, M. V., Chakrabarti, B., Bullmore, E. T., Wheelwright, S. J., Sadek, S. A., Suckling, J., … Consortium, M. A. (2010). Shared neural circuits for mentalizing about the self and others. Journal of Cognitive Neuroscience, 22(7), 1623–1635. https://doi.org/10.1162/jocn.2009.21287
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(1), 106–114. https://doi.org/10.1093/scan/nsq098
Mathews, A., & MacLeod, C. (2005). Cognitive vulnerability to emotional disorders. Annual Review of Clinical Psychology, 1, 167–195. https://doi.org/10.1146/annurev.clinpsy.1.102803.143916
McLaughlin, K. A., Sheridan, M. A., Winter, W., Fox, N. A., Zeanah, C. H., & Nelson, C. A. (2014). Widespread reductions in cortical thickness following severe early-life deprivation: A neurodevelopmental pathway to attention-deficit/hyperactivity disorder. Biological Psychiatry, 76(8), 629–638. https://doi.org/10.1016/j.biopsych.2013.08.016
Metereau, E., & Dreher, J. C. (2015). The medial orbitofrontal cortex encodes a general unsigned value signal during anticipation of both appetitive and aversive events. Cortex, 63, 42–54. https://doi.org/10.1016/j.cortex.2014.08.012
Meyer, M. L., & Lieberman, M. D. (2012). Social working memory: Neurocognitive networks and directions for future research. Frontiers in Psychology, 3, 571. https://doi.org/10.3389/fpsyg.2012.00571
Miranda, R., & Mennin, D. S. (2007). Depression, generalized anxiety disorder, and certainty in pessimistic predictions about the future. Cognitive Therapy and Research, 31(1), 71–82.
Moor, B. G., van Leijenhorst, L., Rombouts, S. A. R. B., Crone, E. A., & Van der Molen, M. W. (2010). Do you like me? Neural correlates of social evaluation and developmental trajectories. Social Neuroscience, 5(5-6), 461–482.
Morales, S., Fu, X., & Perez-Edgar, K. E. (2016). A developmental neuroscience perspective on affect-biased attention. Developmental Cognitive Neuroscience, 21, 26–41. https://doi.org/10.1016/j.dcn.2016.08.001
Morales, S., Taber-Thomas, B. C., & Perez-Edgar, K. E. (2017). Patterns of attention to threat across tasks in behaviorally inhibited children at risk for anxiety. Developmental Science, 20(2). https://doi.org/10.1111/desc.12391
Morrison, R. G., & Nottebohm, F. (1993). Role of a telencephalic nucleus in the delayed song learning of socially isolated zebra finches. Journal of Neurobiology, 24(8), 1045–1064. https://doi.org/10.1002/neu.480240805
Murphy, N. A., Hall, J. A., Schmid Mast, M., Ruben, M. A., Frauendorfer, D., Blanch-Hartigan, D., … Nguyen, L. (2015). Reliability and validity of nonverbal thin slices in social interactions. Personality and Social Psychology Bulletin, 41(2), 199–213. https://doi.org/10.1177/0146167214559902
Narr, R. K., Allen, J. P., Tan, J. S., & Loeb, E. L. (2017). Close friendship strength and broader peer group desirability as differential predictors of adult mental health. Child Development. https://doi.org/10.1111/cdev.12905
Nelson, C. A., Zeanah, C. H., Fox, N. A., Marshall, P. J., Smyke, A. T., & Guthrie, D. (2007). Cognitive recovery in socially deprived young children: The Bucharest early intervention project. Science, 318(5858), 1937–1940. https://doi.org/10.1126/science.1143921
Nelson, C. A., Westerlund, A., McDermott, J. M., Zeanah, C. H., & Fox, N. A. (2013). Emotion recognition following early psychosocial deprivation. Development and Psychopathology, 25(2), 517–525. https://doi.org/10.1017/S0954579412001216
Nelson, E. E., & Guyer, A. E. (2011). The development of the ventral prefrontal cortex and social flexibility. Developmental Cognitive Neuroscience, 1(3), 233–245. https://doi.org/10.1016/j.dcn.2011.01.002
Nelson, E. E., Jarcho, J. M., & Guyer, A. E. (2016). Social re-orientation and brain development: An expanded and updated view. Developmental Cognitive Neuroscience, 17, 118–127. https://doi.org/10.1016/j.dcn.2015.12.008
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(2), 163–174.
Newcomb, A. F., Bukowski, W. M., & Pattee, L. (1993). Children’s peer relations: A meta-analytic review of popular, rejected, neglected, controversial, and average sociometric status. Psychological Bulletin, 113(1), 99–128.
O’Doherty, J., Dayan, P., Schultz, J., Deichmann, R., Friston, K. J., & Dolan, R. J. (2004). Dissociable roles of ventral and dorsal striatum in instrumental conditioning. Science, 304(5669), 452–454. https://doi.org/10.1126/science.1094285
O'Doherty, J., Kringelbach, M. L., Rolls, E. T., Hornak, J., & Andrews, C. (2001). Abstract reward and punishment representations in the human orbitofrontal cortex. Nature Neuroscience, 4(1), 95–102. https://doi.org/10.1038/82959
Ormel, J., Raven, D., van Oort, F., Hartman, C. A., Reijneveld, S. A., Veenstra, R., … Oldehinkel, A. J. (2015). Mental health in Dutch adolescents: A TRAILS report on prevalence, severity, age of onset, continuity and co-morbidity of DSM disorders. Psychological Medicine, 45(2), 345–360. https://doi.org/10.1017/S0033291714001469
Pedersen, S., Vitaro, F., Barker, E. D., & Borge, A. I. (2007). The timing of middle-childhood peer rejection and friendship: Linking early behavior to early-adolescent adjustment. Child Development, 78(4), 1037–1051. https://doi.org/10.1111/j.1467-8624.2007.01051.x
Perez-Edgar, K., Hardee, J. E., Guyer, A. E., Benson, B. E., Nelson, E. E., Gorodetsky, E., … Ernst, M. (2014). DRD4 and striatal modulation of the link between childhood behavioral inhibition and adolescent anxiety. Social Cognitive and Affective Neuroscience, 9(4), 445–453. https://doi.org/10.1093/scan/nst001
Perez-Edgar, K., Roberson-Nay, R., Hardin, M. G., Poeth, K., Guyer, A. E., Nelson, E. E., … Ernst, M. (2007). Attention alters neural responses to evocative faces in behaviorally inhibited adolescents. NeuroImage, 35(4), 1538–1546. https://doi.org/10.1016/j.neuroimage.2007.02.006
Powell, J., Lewis, P. A., Roberts, N., Garcia-Finana, M., & Dunbar, R. I. (2012). Orbital prefrontal cortex volume predicts social network size: An imaging study of individual differences in humans. Proceedings of the Biological Sciences, 279(1736), 2157–2162. https://doi.org/10.1098/rspb.2011.2574
Rapee, R. M., & Spence, S. H. (2004). The etiology of social phobia: Empirical evidence and an initial model. Clinical Psychology Review, 24(7), 737–767. https://doi.org/10.1016/j.cpr.2004.06.004
Rilling, J. K., & Sanfey, A. G. (2011). The neuroscience of social decision-making. Annual Review of Psychology, 62, 23–48. https://doi.org/10.1146/annurev.psych.121208.131647
Rodriguez, P. F., Aron, A. R., & Poldrack, R. A. (2006). Ventral-striatal/nucleus-accumbens sensitivity to prediction errors during classification learning. Human Brain Mapping, 27(4), 306–313. https://doi.org/10.1002/hbm.20186
Rothbart, M. K. (2012). Advances in temperament: History, concepts, and measures. In M. Zentner & R. L. Shiner (Eds.), Handbook of temperament (pp. 3–20). New York, NY: Guilford Press.
Roy, A. K., Benson, B. E., Degnan, K. A., Perez-Edgar, K., Pine, D. S., Fox, N. A., & Ernst, M. (2014). Alterations in amygdala functional connectivity reflect early temperament. Biological Psychology, 103, 248–254. https://doi.org/10.1016/j.biopsycho.2014.09.007
Rubin, K. H., & Burgess, K. B. (2001). Social withdrawal and anxiety. The Developmental Psychopathology of Anxiety, 407–434, New York, NY: Oxford University Press.
Rubin, K. H., Coplan, R. J., & Bowker, J. C. (2009). Social withdrawal in childhood. Annual Review of Psychology, 60, 141–171. https://doi.org/10.1146/annurev.psych.60.110707.163642
Rubin, K. H., Hymel, S., Mills, R. S., & Rose-Krasnor, L. (1991). Conceptualizing different developmental pathways to and from social isolation in childhood. In D. Cicchetti & S. L. Toth (Eds.), Internalizing and externalizing expressions of dysfunction (Vol. 2, pp. 91–122) New York, NY: Psychology Press.
Ruff, C. C., & Fehr, E. (2014). The neurobiology of rewards and values in social decision making. Nature Reviews Neuroscience, 15(8), 549–562. https://doi.org/10.1038/nrn3776
Saxbe, D., Del Piero, L., Immordino-Yang, M. H., Kaplan, J., & Margolin, G. (2015). Neural correlates of adolescents’ viewing of parents’ and peers’ emotions: Associations with risk-taking behavior and risky peer affiliations. Social Neuroscience, 10(6), 592–604. https://doi.org/10.1080/17470919.2015.1022216
Schultz, W. (2004). Neural coding of basic reward terms of animal learning theory, game theory, microeconomics and behavioural ecology. Current Opinion in Neurobiology, 14(2), 139–147. https://doi.org/10.1016/j.conb.2004.03.017
Schultz, W., Dayan, P., & Montague, P. R. (1997). A neural substrate of prediction and reward. Science, 275(5306), 1593–1599. https://doi.org/10.1126/science.275.5306.1593
Schwartz, C. E., Kunwar, P. S., Greve, D. N., Kagan, J., Snidman, N. C., & Bloch, R. B. (2012). A phenotype of early infancy predicts reactivity of the amygdala in male adults. Molecular Psychiatry, 17(10), 1042–1050. https://doi.org/10.1038/mp.2011.96
Schwartz, C. E., Kunwar, P. S., Greve, D. N., Moran, L. R., Viner, J. C., Covino, J. M., … Wallace, S. R. (2010). Structural differences in adult orbital and ventromedial prefrontal cortex predicted by infant temperament at 4 months of age. Archives of General Psychiatry, 67(1), 78–84. https://doi.org/10.1001/archgenpsychiatry.2009.171
Schwartz, C. E., Kunwar, P. S., Hirshfeld-Becker, D. R., Henin, A., Vangel, M. G., Rauch, S. L., … Rosenbaum, J. F. (2015). Behavioral inhibition in childhood predicts smaller hippocampal volume in adolescent offspring of parents with panic disorder. Translational Psychiatry, 5, e605. https://doi.org/10.1038/tp.2015.95
Schwartz, C. E., Snidman, N., & Kagan, J. (1999). Adolescent social anxiety as an outcome of inhibited temperament in childhood. Journal of the American Academy of Child and Adolescent Psychiatry, 38(8), 1008–1015. https://doi.org/10.1097/00004583-199908000-00017
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(5627), 1952–1953. https://doi.org/10.1126/science.1083703
Shenhav, A., & Greene, J. D. (2014). Integrative moral judgment: Dissociating the roles of the amygdala and ventromedial prefrontal cortex. Journal of Neuroscience, 34(13), 4741–4749. https://doi.org/10.1523/Jneurosci.3390-13.2014
Sheridan, M. A., Fox, N. A., Zeanah, C. H., McLaughlin, K. A., & Nelson, C. A. (2012). Variation in neural development as a result of exposure to institutionalization early in childhood. Proceedings of the National Academy of Sciences of the United States of America, 109(32), 12927–12932. https://doi.org/10.1073/pnas.1200041109
Silverman, M. H., Jedd, K., & Luciana, M. (2015). Neural networks involved in adolescent reward processing: An activation likelihood estimation meta-analysis of functional neuroimaging studies. NeuroImage, 122, 427–439. https://doi.org/10.1016/j.neuroimage.2015.07.083
Smetana, J. G., Campione-Barr, N., & Metzger, A. (2006). Adolescent development in interpersonal and societal contexts. Annual Review of Psychology, 57, 255–284. https://doi.org/10.1146/annurev.psych.57.102904.190124
Spielberg, J. M., Jarcho, J. M., Dahl, R. E., Pine, D. S., Ernst, M., & Nelson, E. E. (2015). Anticipation of peer evaluation in anxious adolescents: Divergence in neural activation and maturation. Social Cognitive and Affective Neuroscience, 10(8), 1084–1091. https://doi.org/10.1093/scan/nsu165
Sporns, O., Chialvo, D. R., Kaiser, M., & Hilgetag, C. C. (2004). Organization, development and function of complex brain networks. Trends in Cognitive Sciences, 8(9), 418–425. https://doi.org/10.1016/j.tics.2004.07.008
Stamoulis, C., Vanderwert, R. E., Zeanah, C. H., Fox, N. A., & Nelson, C. A. (2017). Neuronal networks in the developing brain are adversely modulated by early psychosocial neglect. Journal of Neurophysiology, 118(4), 2275–2288. https://doi.org/10.1152/jn.00014.2017
Steinberg, L., & Morris, A. S. (2001). Adolescent development. Annual Review of Psychology, 52, 83–110. https://doi.org/10.1146/annurev.psych.52.1.83
Sugimura, N., & Rudolph, K. D. (2012). Temperamental differences in Children’s reactions to peer victimization. Journal of Clinical Child and Adolescent Psychology, 41(3), 314–328. https://doi.org/10.1080/15374416.2012.656555
Suway, J. G., Degnan, K. A., Sussman, A. L., & Fox, N. A. (2012). The relations among theory of mind, Behavioral inhibition, and peer interactions in early childhood. Social Development, 21(2), 331–342. https://doi.org/10.1111/j.1467-9507.2011.00634.x
Sylvester, C. M., Barch, D. M., Harms, M. P., Belden, A. C., Oakberg, T. J., Gold, A. L., … Pine, D. S. (2016). Early childhood Behavioral inhibition predicts cortical thickness in adulthood. Journal of the American Academy of Child and Adolescent Psychiatry, 55(2), 122–129. https://doi.org/10.1016/j.jaac.2015.11.007
Taber-Thomas, B. C., Morales, S., Hillary, F. G., & Perez-Edgar, K. E. (2016a). Altered topography of intrinsic functional connectivity in childhood risk for social anxiety. Depression and Anxiety, 33(11), 995–1004. https://doi.org/10.1002/da.22508
Taber-Thomas, B. C., Morales, S., Hillary, F. G., & Perez-Edgar, K. E. (2016b). Altered topography of intrinsic functional connectivity in childhood risk for social anxiety. Depression and Anxiety. https://doi.org/10.1002/da.22508
Tobler, P. N., Fiorillo, C. D., & Schultz, W. (2005). Adaptive coding of reward value by dopamine neurons. Science, 307(5715), 1642–1645. https://doi.org/10.1126/science.1105370
Tremblay, S., Sharika, K. M., & Platt, M. L. (2017). Social decision-making and the brain: A comparative perspective. Trends in Cognitive Sciences, 21(4), 265–276. https://doi.org/10.1016/j.tics.2017.01.007
Troller-Renfree, S., McDermott, J. M., Nelson, C. A., Zeanah, C. H., & Fox, N. A. (2015). The effects of early foster care intervention on attention biases in previously institutionalized children in Romania. Developmental Science, 18(5), 713–722. https://doi.org/10.1111/desc.12261
Troller-Renfree, S., Nelson, C. A., Zeanah, C. H., & Fox, N. A. (2016). Deficits in error monitoring are associated with externalizing but not internalizing behaviors among children with a history of institutionalization. Journal of Child Psychology and Psychiatry, 57(10), 1145–1153. https://doi.org/10.1111/jcpp.12604
Uddin, L. Q. (2015). Salience processing and insular cortical function and dysfunction. Nature Reviews. Neuroscience, 16(1), 55–61. https://doi.org/10.1038/nrn3857
Vuilleumier, P., & Pourtois, G. (2007). Distributed and interactive brain mechanisms during emotion face perception: Evidence from functional neuroimaging. Neuropsychologia, 45(1), 174–194. https://doi.org/10.1016/j.neuropsychologia.2006.06.003
Wessa, M., Heissler, J., Schonfelder, S., & Kanske, P. (2013). Goal-directed behavior under emotional distraction is preserved by enhanced task-specific activation. Social Cognitive and Affective Neuroscience, 8(3), 305–312. https://doi.org/10.1093/scan/nsr098
Williams, L. R., Fox, N. A., Lejuez, C. W., Reynolds, E. K., Henderson, H. A., Perez-Edgar, K. E., … Pine, D. S. (2010). Early temperament, propensity for risk-taking and adolescent substance-related problems: A prospective multi-method investigation. Addictive Behaviors, 35(12), 1148–1151. https://doi.org/10.1016/j.addbeh.2010.07.005
Yacubian, J., Sommer, T., Schroeder, K., Glascher, J., Braus, D. F., & Buchel, C. (2007). Subregions of the ventral striatum show preferential coding of reward magnitude and probability. NeuroImage, 38(3), 557–563. https://doi.org/10.1016/j.neuroimage.2007.08.007
Zaki, J., Hennigan, K., Weber, J., & Ochsner, K. N. (2010). Social cognitive conflict resolution: Contributions of domain-general and domain-specific neural systems. Journal of Neuroscience, 30(25), 8481–8488. https://doi.org/10.1523/JNEUROSCI.0382-10.2010
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Jarcho, J.M., Guyer, A.E. (2018). The Neural Mechanisms of Behavioral Inhibition. In: Pérez-Edgar, K., Fox, N. (eds) Behavioral Inhibition. Springer, Cham. https://doi.org/10.1007/978-3-319-98077-5_4
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