Journal of Abnormal Child Psychology

, Volume 43, Issue 5, pp 863–874 | Cite as

Temperament and Parenting Styles in Early Childhood Differentially Influence Neural Response to Peer Evaluation in Adolescence

  • Amanda E. GuyerEmail author
  • Johanna M. Jarcho
  • Koraly Pérez-Edgar
  • Kathryn A. Degnan
  • Daniel S. Pine
  • Nathan A. Fox
  • Eric E. Nelson


Behavioral inhibition (BI) is a temperament characterized by social reticence and withdrawal from unfamiliar or novel contexts and conveys risk for social anxiety disorder. Developmental outcomes associated with this temperament can be influenced by children’s caregiving context. The convergence of a child’s temperamental disposition and rearing environment is ultimately expressed at both the behavioral and neural levels in emotional and cognitive response patterns to social challenges. The present study used functional neuroimaging to assess the moderating effects of different parenting styles on neural response to peer rejection in two groups of adolescents characterized by their early childhood temperament (M age = 17.89 years, N = 39, 17 males, 22 females; 18 with BI; 21 without BI). The moderating effects of authoritarian and authoritative parenting styles were examined in three brain regions linked with social anxiety: ventrolateral prefrontal cortex (vlPFC), striatum, and amygdala. In youth characterized with BI in childhood, but not in those without BI, diminished responses to peer rejection in vlPFC were associated with higher levels of authoritarian parenting. In contrast, all youth showed decreased caudate response to peer rejection at higher levels of authoritative parenting. These findings indicate that BI in early life relates to greater neurobiological sensitivity to variance in parenting styles, particularly harsh parenting, in late adolescence. These results are discussed in relation to biopsychosocial models of development.


Behavioral inhibition Social anxiety Parenting Peer rejection Brain function 



This research was supported by the Intramural Research Program of the National Institute of Mental Health (NIMH), an NIMH Seymour S. Kety Memorial Award (AEG), and NIMH grants MH080076 (AEG) and MH074454 (NAF). The authors thank all of the families who participated in the study.

Ethical Standards

All persons gave their informed consent prior to their inclusion in the study.

Conflict of Interest

The authors declare that they have no conflicts of interest.


  1. 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, 483–492. doi: 10.1007/s10578-013-0418-2.PubMedCrossRefGoogle Scholar
  2. 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, 1009–1018. doi: 10.1111/j.1467 9280.2009.02401.x.PubMedCentralPubMedCrossRefGoogle Scholar
  3. Baumrind, D. (1991). The influence of parenting styles on adolescent competence and substance use. The Journal of Early Adolescence, 11, 56–95.CrossRefGoogle Scholar
  4. Behrens, T. E., Hunt, L. T., & Rushworth, M. F. (2009). The computation of social behavior. Science, 324, 1160–1164.PubMedCrossRefGoogle Scholar
  5. Belsky, J., & Pluess, M. (2009). Beyond diathesis stress: differential susceptibility to environmental influences. Psychological Bulletin, 135, 885–908. doi: 10.1037/A0017376.PubMedCrossRefGoogle Scholar
  6. Boyce, W. T., & Ellis, B. J. (2005). Biological sensitivity to context: I. An evolutionary-developmental theory of the origins and functions of stress reactivity. Development and Psychopathology, 17, 271–301. doi: 10.1017/S0954579405050145.PubMedCrossRefGoogle Scholar
  7. Bunge, S. A. (2004). How we use rules to select actions: a review of evidence from cognitive neuroscience. Cognitive, Affective and Behavioral Neuroscience, 4, 564–579.PubMedCrossRefGoogle Scholar
  8. Casement, M. D., Guyer, A. E., Hipwell, A. E., McAloon, R. L., Hoffmann, A. M., Keenan, K. E., & Forbes, E. E. (2014). Girls’ challenging social experiences in early adolescence predict neural response to rewards and depressive symptoms. Developmental Cognitive Neuroscience, 8, 18–27. doi: 10.1016/j.dcn.2013.12.003.PubMedCentralPubMedCrossRefGoogle Scholar
  9. 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 and Adolescent Psychiatry, 48, 928–935. doi: 10.1097/CHI.0b013e3181ae09df.PubMedCentralPubMedCrossRefGoogle Scholar
  10. 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(1066–1075), e1061. doi: 10.1016/j.jaac.2012.08.002.Google Scholar
  11. Cox, R. W. (1996). AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Computers and Biomedical Research, 29, 162–173. doi: 10.1006/cbmr.1996.0014.PubMedCrossRefGoogle Scholar
  12. Darling, N., & Steinberg, L. (1993). Parenting style as context: an integrative model. Psychological Bulletin, 113, 487–496. doi: 10.1037/0033-2909.113.3.487.CrossRefGoogle Scholar
  13. Degnan, K. A., Almas, A. N., & Fox, N. A. (2010). Temperament and the environment in the etiology of childhood anxiety. Journal of Child Psychology and Psychiatry, 51, 497–517. doi: 10.1111/j.1469-7610.2010.02228.x.PubMedCentralPubMedCrossRefGoogle Scholar
  14. Degnan, K. A., & Fox, N. A. (2007). Behavioral inhibition and anxiety disorders: multiple levels of a resilience process. Development and Psychopathology, 19, 729–746. doi: 10.1017/S0954579407000363.PubMedCrossRefGoogle Scholar
  15. Delgado, M. R. (2007). Reward-related responses in the human striatum. Annals of the New York Academy of Sciences, 1104, 70–88.PubMedCrossRefGoogle Scholar
  16. Egger, H. L., Pine, D. S., Nelson, E. E., Leibenluft, E., Ernst, M., Towbin, K., & Angold, A. (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, 145–156. doi: 10.1002/mpr.343.PubMedCentralPubMedGoogle Scholar
  17. Eisenberger, N. I., Lieberman, M. D., & Williams, K. D. (2003). Does rejection hurt? An FMRI study of social exclusion. Science, 302, 290–292.PubMedCrossRefGoogle Scholar
  18. Ellis, B. J., Boyce, W. T., Belsky, J., Bakermans-Kranenburg, M. J., & van Ijzendoorn, M. H. (2011). Differential susceptibility to the environment: an evolutionary–neurodevelopmental theory. Development and Psychopathology, 23, 7–28. doi: 10.1017/S0954579410000611.PubMedCrossRefGoogle Scholar
  19. 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. doi: 10.1146/annurev.psych.55.090902.141532.PubMedCrossRefGoogle Scholar
  20. 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, 1–21. doi: 10.1111/1467-8624.00262.PubMedCrossRefGoogle Scholar
  21. Gershoff, E. T. (2013). Spanking and child development: we know enough now to stop hitting our children. Child Development Perspectives, 7, 133–137. doi: 10.1111/cdep.12038.PubMedCentralPubMedCrossRefGoogle Scholar
  22. Goldsmith, H. H. (1996). Studying temperament via construction of the toddler behavior assessment questionnaire. Child Development, 67, 218–235. doi: 10.1111/j.1467-8624.1996.tb01730.PubMedCrossRefGoogle Scholar
  23. Guyer, A. E., Benson, B., Choate, V. R., Bar-Haim, Y., Perez-Edgar, K., Jarcho, J. M., et al. (2014). Lasting associations between early-childhood temperament and late-adolescent reward-circuitry response to peer feedback. Development and Psychopathology, 26, 229–243. doi: 10.1017/S0954579413000941.PubMedCentralPubMedCrossRefGoogle Scholar
  24. Guyer, A. E., Choate, V. R., Detloff, A., Benson, B., Nelson, E. E., Perez-Edgar, K., et al. (2012a). Striatal functional alteration during incentive anticipation in pediatric anxiety disorders. American Journal of Psychiatry, 169, 205–212. doi: 10.1176/appi.ajp.2011.11010006.PubMedCentralPubMedCrossRefGoogle Scholar
  25. Guyer, A. E., Choate, V. R., Pine, D. S., & Nelson, E. E. (2012b). Neural circuitry underlying affective response to peer feedback in adolescence. Social Cognitive and Affective Neuroscience, 7, 81–92. doi: 10.1093/scan/nsr043.PubMedCentralPubMedCrossRefGoogle Scholar
  26. 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. Archvies of General Psychiatry, 65, 1303–1312. doi: 10.1001/archpsyc.65.11.1303.CrossRefGoogle Scholar
  27. 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, 1000–1015. doi: 10.1111/j.1467-8624.2009.01313.x.PubMedCentralPubMedCrossRefGoogle Scholar
  28. 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, 6399–6405. doi: 10.1523/JNEUROSCI. 0666-06.2006.PubMedCrossRefGoogle Scholar
  29. Hankin, B. L., & Abela, J. R. Z. (2006). Development of psychopathology: A vulnerability-stress perspective. Thousand Oaks: Sage.Google Scholar
  30. Hastings, P. D., Sullivan, C., McShane, K. E., Coplan, R. J., Utendale, W. T., & Vyncke, J. D. (2008). Parental socialization, vagal regulation, and preschoolers’ anxious difficulties: direct mothers and moderated fathers. Child Development, 79, 45–64. doi: 10.1111/j.1467-8624.2007.01110.x.PubMedCrossRefGoogle Scholar
  31. 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, 306–314. doi: 10.1016/j.biopsycho.2012.09.008.PubMedCentralPubMedCrossRefGoogle Scholar
  32. Kaufman, J., Birmaher, B., Brent, D., Rao, U., Flynn, C., Moreci, P., & Ryan, N. (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 and Adolescent Psychiatry, 36, 980–988. doi: 10.1097/00004583-199707000-00021.PubMedCrossRefGoogle Scholar
  33. Kertes, D. A., Donzella, B., Talge, N. M., Garvin, M. C., Van Ryzin, M. J., & Gunnar, M. R. (2009). Inhibited temperament and parent emotional availability differentially predict young children’s cortisol responses to novel social and nonsocial events. Development Psychobiology, 51, 521–532. doi: 10.1002/dev.20390.CrossRefGoogle Scholar
  34. Kiff, C. J., Lengua, L. J., & Zalewski, M. (2011). Nature and nurturing: parenting in the context of child temperament. Clinical Child and Family Psychology Review, 14, 251–301. doi: 10.1007/s10567-011-0093-4.PubMedCentralPubMedCrossRefGoogle Scholar
  35. Lau, J. Y., Guyer, A. E., Tone, E. B., Jenness, J., Parrish, J., Pine, D. S., & Nelson, E. E. (2011). Neural responses to peer rejection in anxious adolescents: contributions from the amygdala-hippocampal complex. International Journal of Behavioral Development, 36, 36–44. doi: 10.1177/0165025411406854.CrossRefGoogle Scholar
  36. LeDoux, J. E. (2000). Emotion circuits in the brain. Annual Review of Neuroscience, 23, 155–184. doi: 10.1146/annurev.neuro.23.1.155.PubMedCrossRefGoogle Scholar
  37. Levy, B. J., & Wagner, A. D. (2011). Cognitive control and right ventrolateral prefrontal cortex: reflexive reorienting, motor inhibition, and action updating. Annals of the New York Academy of Sciences, 1224, 40–62. doi: 10.1111/j.1749-6632.2011.05958.x.PubMedCentralPubMedCrossRefGoogle Scholar
  38. Maslowsky, J., Mogg, K., Bradley, B. P., McClure-Tone, E., Ernst, M., Pine, D. S., & Monk, C. S. (2010). A preliminary investigation of neural correlates of treatment in adolescents with generalized anxiety disorder. Journal of Child and Adolescent Psychopharmacology, 20, 105–111. doi: 10.1089/cap.2009.0049.PubMedCentralPubMedCrossRefGoogle Scholar
  39. 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, 143–157. doi: 10.1093/scan/nsp007.PubMedCentralPubMedCrossRefGoogle Scholar
  40. Monk, C. S., Nelson, E. E., McClure, E. B., Mogg, K., Bradley, B. P., Leibenluft, E., et al. (2006). Ventrolateral prefrontal cortex activation and attentional bias in response to angry faces in adolescents with generalized anxiety disorder. American Journal of Psychiatry, 163, 1091–1097.PubMedCrossRefGoogle Scholar
  41. Nelson, E. E., & Guyer, A. E. (2011). The development of the ventral prefrontal cortex and social flexibility. Developmental Cognitive Neuroscience, 1, 233–245. doi: 10.1016/j.dcn.2011.01.002.PubMedCentralPubMedCrossRefGoogle Scholar
  42. Perez-Edgar, K., Hardee, J. E., Guyer, A. E., Benson, B. E., Nelson, E. E., Gorodetsky, E., et al. (2014). DRD4 and striatal modulation of the link between childhood behavioral inhibition and adolescent anxiety. Social Cognitive and Affective Neuroscience, 9, 445–453. doi: 10.1093/scan/nst001.PubMedCentralPubMedCrossRefGoogle Scholar
  43. 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, 1538–1546. doi: 10.1016/j.neuroimage.2007.02.006.PubMedCentralPubMedCrossRefGoogle Scholar
  44. Phillips, D., Crowell, N. A., Gunnar, M., Fox, N. A., Sussman, A. L., Hane, A. A., & Bisgaier, J. (2012). Reactive temperament and sensitivity to context in child care. Social Development, 21, 628–643.CrossRefGoogle Scholar
  45. Price, J. L. (2007). Definition of the orbital cortex in relation to specific connections with limbic and visceral structures and other cortical regions. Annals of the New York Academy of Sciences, 1121, 54–71. doi: 10.1196/annals.1401.008.PubMedCrossRefGoogle Scholar
  46. Robinson, C. C., Mandelco, B., Olsen, S. F., & Hart, C. H. (2001). Parenting styles and dimensions questionnaire. In B. F. Perlmutter, J. Touliatos, & G. W. Holdem (Eds.), Handbook of family measurement techniques: Instruments and index. Thousand Oaks: Sage.Google Scholar
  47. Rowe, D. C., & Plomin, R. (1977). Temperament in early childhood. Journal of Personality Assessment, 41, 150–156. doi: 10.1207/s15327752jpa4102_5.PubMedCrossRefGoogle Scholar
  48. Rubin, K. H. (1989). The play observation scale (POS). Canada: University of Waterloo.Google Scholar
  49. Rubin, K. H., Burgess, K. B., Dwyer, K. M., & Hastings, P. D. (2003). Predicting preschoolers’ externalizing behaviors from toddler temperament, conflict, and maternal negativity. Developmental Psychology, 39, 164–176.PubMedCrossRefGoogle Scholar
  50. Rubin, K. H., Burgess, K. B., & Hastings, P. D. (2002). Stability and social-behavioral consequences of toddlers’ inhibited temperament and parenting behaviors. Child Development, 73, 483–495.PubMedCrossRefGoogle Scholar
  51. Sakagami, M., & Pan, X. (2007). Functional role of the ventrolateral prefrontal cortex in decision making. Current Opinions in Neurobiology, 17, 228–233. doi: 10.1016/j.conb.2007.02.008.CrossRefGoogle Scholar
  52. 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, 1952–1953. doi: 10.1126/science.1083703.PubMedCrossRefGoogle Scholar
  53. Silk, J. S., Siegle, G. J., Lee, K. H., Nelson, E. E., Stroud, L. R., & Dahl, R. E. (2014). Increased neural response to peer rejection associated with adolescent depression and pubertal development. Social Cognitive Affective Neuroscience, 9, 1798–1807. doi: 10.1093/scan/nst175.PubMedCrossRefGoogle Scholar
  54. Steinberg, L. (2001). We know some things: adolescent-parent relationships in retrospect and prospect. Journal of Research on Adolescence, 11, 1–19.CrossRefGoogle Scholar
  55. Steinberg, L., & Morris, A. S. (2001). Adolescent development. Annual Review of Psychology, 52, 83–110.PubMedCrossRefGoogle Scholar
  56. Tan, P. Z., Lee, K. H., Dahl, R. E., Nelson, E. E., Stroud, L. J., Siegle, G. J., et al. (2014). Associations between maternal negative affect and adolescent’s neural response to peer evaluation. Developmental Cognitive Neuroscience, 8, 28–39. doi: 10.1016/j.dcn.2014.01.006.PubMedCrossRefGoogle Scholar
  57. Taylor, S. E., Eisenberger, N. I., Saxbe, D., Lehman, B. J., & Lieberman, M. D. (2006). Neural responses to emotional stimuli are associated with childhood family stress. Biological Psychiatry, 60, 296–301. doi: 10.1016/j.biopsych.2005.09.027.PubMedCrossRefGoogle Scholar
  58. van der Voort, A., Linting, M., Juffer, F., Bakermans-Kranenburg, M. J., Schoenmaker, C., & van Ijzendoorn, M. H. (2014). The development of adolescents’ internalizing behavior: longitudinal effects of maternal sensitivity and child inhibition. Journal of Youth and Adolescence, 43, 528–540. doi: 10.1007/s10964-013-9976-7.PubMedCrossRefGoogle Scholar
  59. Whittle, S., Yap, M. B., Yucel, M., Sheeber, L., Simmons, J. G., Pantelis, C., & Allen, N. B. (2009). Maternal responses to adolescent positive affect are associated with adolescents’ reward neuroanatomy. Social Cognitive and Affective Neuroscience, 4, 247–256. doi: 10.1093/scan/nsp012.PubMedCentralPubMedCrossRefGoogle Scholar
  60. Whittle, S., Yucel, M., Forbes, E. E., Davey, C. G., Harding, I. H., Sheeber, L., et al. (2012). Adolescents’ depressive symptoms moderate neural responses to their mothers’ positive behavior. Social Cognitive and Affective Neuroscience, 7, 23–34. doi: 10.1093/scan/nsr049.PubMedCentralPubMedCrossRefGoogle Scholar
  61. Williams, L. R., Degnan, K. A., Perez-Edgar, K. E., Henderson, H. A., Rubin, K. H., Pine, D. S., et al. (2009). Impact of behavioral inhibition and parenting style on internalizing and externalizing problems from early childhood through adolescence. Journal of Abnormal Child Psychology, 37, 1063–1075. doi: 10.1007/s10802-009-9331-3.PubMedCentralPubMedCrossRefGoogle Scholar
  62. Yap, M. B., Whittle, S., Yucel, M., Sheeber, L., Pantelis, C., Simmons, J. G., & Allen, N. B. (2008). Interaction of parenting experiences and brain structure in the prediction of depressive symptoms in adolescents. Archives of General Psychiatry, 65, 1377–1385. doi: 10.1001/archpsyc.65.12.1377.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Amanda E. Guyer
    • 1
    Email author
  • Johanna M. Jarcho
    • 2
  • Koraly Pérez-Edgar
    • 3
  • Kathryn A. Degnan
    • 4
  • Daniel S. Pine
    • 2
  • Nathan A. Fox
    • 4
  • Eric E. Nelson
    • 2
  1. 1.Department of Human Ecology, Center for Mind and BrainUniversity of California DavisDavisUSA
  2. 2.Section on Development and Affective Neuroscience, Intramural Program of Research, National Institute of Mental HealthNational Institutes of HealthBethesdaUSA
  3. 3.Department of PsychologyThe Pennsylvania State UniversityUniversity ParkUSA
  4. 4.Department of Human Development and Quantitative MethodologyUniversity of MarylandCollege ParkUSA

Personalised recommendations