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Current Behavioral Neuroscience Reports

, Volume 4, Issue 2, pp 99–106 | Cite as

Attention Processes Underlying Risk and Resilience in Behaviorally Inhibited Children

  • Heather A. HendersonEmail author
  • McLennon J.G. Wilson
Child and Developmental Psychiatry (K Fitzgerald, Section Editor)
Part of the following topical collections:
  1. Topical Collection on Child and Developmental Psychiatry

Abstract

Purpose of Review

We briefly review the literature on behavioral inhibition (BI) in childhood and its associated social and emotional outcomes. We review the interplay of automatic and controlled attention processes in BI children and outline the relations between childhood BI and two components of effortful control (EC): response inhibition and attention switching.

Recent Findings

Contemporary research in cognitive and behavioral neuroscience indicates that components of EC differentially impact developmental risk for BI children. Response inhibition may inflate the risk of anxiety issues by promoting the inefficient deployment of attentional resources in social contexts, while attention shifting may serve as a protective factor by supporting dynamic social information processing.

Summary

The attentional processes subsumed under EC have diverse implications for the developmental trajectory of BI. Further research is necessary to identify the exact mechanisms by which the components of EC affect the manifestation of BI across development, and how this knowledge can guide early intervention efforts.

Keywords

Behavioral inhibition Executive attention Effortful control Response inhibition Attention shifting Affective flexibility 

Notes

Compliance with Ethical Standards

Conflict of Interest

Dr. Heather Henderson declares grants from Social Sciences and Humanities Research Council of Canada (Grant number: 435-2016-0494). McLennon Wilson declares that he has no conflicts of interest.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

References

Papers of particular interest, published recently, have been highlighted as: • Of importance

  1. 1.
    Fox NA, Henderson HA, Marshall PJ, Nichols KE, Ghera MM. Behavioral inhibition: linking biology and behavior within a developmental framework. Annu Rev Psychol. 2005;56:235–62. doi: 10.1146/annurev.psych.55.090902.141532.CrossRefPubMedGoogle Scholar
  2. 2.
    Kagan J, Reznick JS, Clarke C, Snidman N, Garcia-Coll C, Steven J. Behavioral inhibition to the unfamiliar. Child Dev. 1984;55:2212–25. doi: 10.2307/1129793.CrossRefGoogle Scholar
  3. 3.
    Rubin KH, Coplan RJ, Bowker JC. Social withdrawal in childhood. Annu Rev Psychol. 2009;60:141–71. doi: 10.1146/annurev.psych.60.110707.163642.Social.CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Ladd GW, Kochenderfer-Ladd B, Eggum ND, Kochel KP, McConnell EM. Characterizing and comparing the friendships of anxious-solitary and unsociable preadolescents. Child Dev. 2011;82:1434–53. doi: 10.1111/j.1467-8624.2011.01632.x.CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Rudasill KM, Rimm-Kaufman SE. Teacher-child relationship quality: the roles of child temperament and teacher-child interactions. Early Child Res Q. 2009;24:107–20. doi: 10.1016/j.ecresq.2008.12.003.CrossRefGoogle Scholar
  6. 6.
    Valiente C, Swanson J, Lemery-Chalfant K. Kindergartners’ temperament, classroom engagement, and student-teacher relationship: moderation by effortful control. Soc Dev. 2012;21:558–76.CrossRefGoogle Scholar
  7. 7.
    Karevold E, Ystrom E, Coplan RJ, Sanson AV, Mathiesen KS. A prospective longitudinal study of shyness from infancy to adolescence: stability, age-related changes, and prediction of socio-emotional functioning. J Abnorm Child Psychol. 2012;40:1167–77. doi: 10.1007/s10802-012-9635-6.CrossRefPubMedGoogle Scholar
  8. 8.
    Chronis-Tuscano A, Degnan KA, Pine DS, Perez-Edgar K, Henderson HA, Diaz Y, et al. Stable early maternal report of behavioral inhibition predicts lifetime social anxiety disorder in adolescence. J Am Acad Child Adolesc Psychiatry. 2009;48:928–35. doi: 10.1097/CHI.0b013e3181ae09df.CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Clauss J, Blackford J. Behavioral inhibition and risk for developing social anxiety disorder: a meta-analytic study. J Am Acad Child Adolesc Psychiatry. 2012;51:1–13. doi: 10.1016/j.jaac.2012.08.002.Behavioral.CrossRefGoogle Scholar
  10. 10.
    Degnan KA, Almas AN, Henderson HA, Hane AA, Walker OL, Fox NA. Longitudinal trajectories of social reticence with unfamiliar peers across early childhood. Dev Psychol. 2014;50:2311–23. doi: 10.1037/a0037751.CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    • Eggum-Wilkens ND, Reichenberg RE, Eisenberg N, Spinrad TL. Components of effortful control and their relations to children’s shyness. Int J Behav Dev. 2016;40:544–54. doi: 10.1177/0165025415597792. An empirical example of how different components of parent-reported effortful control relate to developmental trajectories of shyness across childhood CrossRefPubMedGoogle Scholar
  12. 12.
    Tang A, Van Lieshout RJ, Lahat A, Duku E, Boyle MH, Saigal S, et al. Shyness trajectories across the first four decades predict mental health outcomes. J Abnorm Child Psychol. 2017; doi: 10.1007/s10802-017-0265-x.Google Scholar
  13. 13.
    Grady JS, Karraker K, Metzger A. Shyness trajectories in slow-to-warm-up infants: relations with child sex and maternal parenting. J Appl Dev Psychol. 2012;33:91–101.CrossRefGoogle Scholar
  14. 14.
    Shell MD, Gazelle H, Faldowski RA. Anxious solitude and the middle school transition: a diathesis x stress model of peer exclusion and victimization trajectories. Dev Psychol. 2014;50:1569–83. doi: 10.1016/j.appdev.2011.11.002.CrossRefPubMedGoogle Scholar
  15. 15.
    Markovic A, Bowker J. Friends also matter: Examining friendship adjustment indices as moderators of anxious withdrawal and trajectories of change in psychological maladjustment. Dev Psychol. Forthcoming 2017.Google Scholar
  16. 16.
    • Henderson HA, Pine DS, Fox NA. Behavioral inhibition and developmental risk: a dual-processing perspective. Neuropsychopharmacology. 2015;40:207–24. doi: 10.1038/npp.2014.189. A theoretical model describing the impact of automatic and controlled processing on developmental outcomes of BI children CrossRefPubMedGoogle Scholar
  17. 17.
    Davis M. Pharmacological and anatomical analysis of fear conditioning using the fear-potentiated startle paradigm. Behav Neurosci. 1986;100:814–24. doi: 10.1037/0735-7044.100.6.814.CrossRefPubMedGoogle Scholar
  18. 18.
    LeDoux JE, Iwata J, Cicchetti P, Reis DJ. Different projections of the central amygdaloid nucleus mediate autonomic and behavioral correlates of conditioned fear. J Neurosci. 1988;8:2517–29.PubMedGoogle Scholar
  19. 19.
    Barker TV, Reeb-Sutherland BC, Fox NA. Individual differences in fear potentiated startle in behaviorally inhibited children. Dev Psychobiol. 2014;56:133–41. doi: 10.1002/dev.21096.CrossRefPubMedGoogle Scholar
  20. 20.
    Guyer AE, Caouette JD, Lee CC, Ruiz SK. Will they like me? Adolescents’ emotional responses to peer evaluation. Int J Behav Dev. 2014;38:155–63. doi: 10.1177/0165025413515627.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Jarcho JM, Davis MM, Shechner T, Degnan KA, Henderson HA, Stoddard J, et al. Early-childhood social reticence predicts brain function in preadolescent youths during distinct forms of peer evaluation. Psychol Sci. 2016;27:821–35. doi: 10.1177/0956797616638319.CrossRefPubMedGoogle Scholar
  22. 22.
    Pérez-Edgar K, Bar-Haim Y, McDermott JM, Chronis-Tuscano A, Pine DS, Fox NA. Attention biases to threat and behavioral inhibition in early childhood shape adolescent social withdrawal. Emotion. 2010;10:349–57. doi: 10.1037/a0018486.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Helfinstein SM, Benson B, Perez-Edgar K, Bar-Haim Y, Detloff A, Pine DS, et al. Striatal responses to negative monetary outcomes differ between temperamentally inhibited and non-inhibited adolescents. Neuropsychologia. 2011;49:479–85. doi: 10.1016/j.neuropsychologia.2010.12.015.CrossRefPubMedGoogle Scholar
  24. 24.
    Guyer AE, Benson B, Choate VR, Bar-Haim Y, Perez-Edgar K, Jarcho JM, et al. Lasting associations between early-childhood temperament and late-adolescent reward-circuitry response to peer feedback. Dev Psychopathol. 2014;26:229–43. doi: 10.1017/S0954579413000941.CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Guyer AE, Nelson EE, Perez-Edgar K, Hardin MG, Roberson-Nay R, Monk CS, et al. Striatal functional alteration in adolescents characterized by early childhood behavioral inhibition. J Neurosci. 2006;26:6399–405. doi: 10.1523/JNEUROSCI.0666-06.2006.CrossRefPubMedGoogle Scholar
  26. 26.
    Bar-Haim Y, Fox NA, Benson B, Guyer AE, Williams A, Nelson EE, et al. Neural correlates of reward processing in adolescents with a history of inhibited temperament. Psychol Sci. 2009;20:1009–18. doi: 10.1111/j.1467-9280.2009.02401.x.CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    White LK, Degnan KA, Henderson HA, Pérez-Edgar K, Walker OL, Shechner T, et al. Developmental relations among behavioral inhibition, anxiety, and attention biases to threat and positive information. Child Dev. 2017;88:141–55. doi: 10.1111/cdev.12696.CrossRefPubMedGoogle Scholar
  28. 28.
    Hardee JE, Benson BE, Bar-Haim Y, Mogg K, Bradley BP, Chen G, et al. Patterns of neural connectivity during an attention bias task moderates associations between early childhood temperament and internalizing symptoms in young adulthood. Biol Psychiatry. 2013;74:273–9. doi: 10.1016/j.biopsych.2013.01.036.CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Kokin J, Younger A, Gosselin P, Vaillancourtb T. Biased facial expression interpretation in shy children. Infant Child Dev. 2006;3:3–5. doi: 10.1002/icd.Google Scholar
  30. 30.
    Rothbart M, Derryberry D. Development of individual differences in temperament. In: Lamb ME, Brown AL, editors. Advances in developmental psychology. Hillsdale, NJ: Erlbaum; 1981.Google Scholar
  31. 31.
    Rothbart MK, Bates JE. Temperament. In: Damon W, Lerner RM, Eisenberg N, editors. Handbook of child psychology: Vol 3: social, emotional, and personality development. New York: Wiley; 2006.Google Scholar
  32. 32.
    Rothbart MK, Ahadi SA, Hershey KL, Fisher P. Investigations of temperament at three to seven years: the children’s behavior questionnaire. Child Dev. 2001;72:1394–408.CrossRefPubMedGoogle Scholar
  33. 33.
    Posner MI, Rothbart MK. Research on attention networks as a model for the integration of psychological science. Annu Rev Psychol. 2007;58:1–23. doi: 10.1146/annurev.psych.58.110405.085516.CrossRefPubMedGoogle Scholar
  34. 34.
    Eisenberg N, Smith CL, Sadovsky A, Spinrad TL. Effortful control: relations with emotion regulation, adjustment, and socialization in childhood. In: Baumeister RF, Vohs KD, editors. Handbook of self-regulation: research, theory, and application. New York: Guilford Press; 2004.Google Scholar
  35. 35.
    Kochanska G, Knaack A. Effortful control as a personality characteristic of young children: antecedents, correlates, and consequences. J Pers. 2003;71:1087–112. doi: 10.1111/1467-6494.7106008.CrossRefPubMedGoogle Scholar
  36. 36.
    Spinrad TL, Stifter CA, Donelan-McCall N, Turner L. Mothers’ regulation strategies in response to toddlers’ affect: links to later emotion self-regulation. Soc Dev. 2004;13:40–55. doi: 10.1111/j.1467-9507.2004.00256.x.CrossRefGoogle Scholar
  37. 37.
    Morales S, Fu X, Pérez-Edgar KE. A developmental neuroscience perspective on affect-biased attention. Accid Anal Prev. 2016;21:26–41. doi: 10.1016/j.dcn.2016.08.001.Google Scholar
  38. 38.
    Eysenck MW, Derakshan N, Santos R, Calvo MG. Anxiety and cognitive performance: attentional control theory. Emotion. 2007;7(2):336–53.CrossRefPubMedGoogle Scholar
  39. 39.
    Eysenck MW, Calvo MG. Anxiety and performance: the processing efficiency theory. Cogn Emot. 1992;6:409–34. doi: 10.1080/02699939208409696.CrossRefGoogle Scholar
  40. 40.
    Derryberry D, Reed MA. Anxiety-related attentional biases and their regulation by attentional control. J Abnorm Psychol. 2002;111:225–36. doi: 10.1037/0021-843X.111.2.225.CrossRefPubMedGoogle Scholar
  41. 41.
    Gagne JR, Miller MM, Goldsmith HH. Early-but modest-gender differences in focal aspects of childhood temperament. Pers Individ Dif. 2013;55:95–100. doi: 10.1016/j.paid.2013.02.006.CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Simonds J, Rothbart M. The temperament in middle childhood questionnaire (TMCQ): A computerized self-report instrument for ages 7–10. Poster presented at the Occasional Temperament Conference, Athens, GA. 2004.Google Scholar
  43. 43.
    White LK, McDermott JM, Degnan KA, Henderson HA, Fox NA. Behavioral inhibition and anxiety: the moderating roles of inhibitory control and attention shifting. J Abnorm Child Psychol. 2011;39:735–47. doi: 10.1007/s10802-011-9490-x.CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    • Wolfe CD, Bell MA. Brain electrical activity of shy and non-shy preschool-aged children during executive function tasks. Infant Child Dev. 2014;23:259–72. doi: 10.1002/icd.1858. An empirical example of how shyness relates to cortical activation, in the absence of performance benefits, for shy preschool-aged children CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Henderson HA. Electrophysiological correlates of cognitive control and the regulation of shyness in children. Dev Neuropsychol. 2010;35:177–93. doi: 10.1080/87565640903526538.CrossRefPubMedGoogle Scholar
  46. 46.
    van Veen V, Carter CS. The timing of action-monitoring processes in the anterior cingulate cortex. J Cogn Neurosci. 2002;14:593–602. doi: 10.1162/08989290260045837.CrossRefPubMedGoogle Scholar
  47. 47.
    • Fu X, Taber-Thomas BC, Perez-Edgar K. Frontolimbic functioning during threat-related attention: relations to early behavioral inhibition and anxiety in children. Biol Psychol. 2017;122:98–109. doi: 10.1016/j.biopsycho.2015.08.010. An fMRI study showing that engagement of the dlPFC when orienting away from threat predicts increased anxiety in BI children, suggesting that executive attention is recruited as a compensatory, but not necessarily effective, strategy in BI children CrossRefPubMedGoogle Scholar
  48. 48.
    Miyake A, Friedman NP, Emerson MJ, Witzki AH, Howerter A, Wager TD. The unity and diversity of executive functions and their contributions to complex “frontal lobe” tasks: a latent variable analysis. Cogn Psychol. 2000;41:49–100. doi: 10.1006/cogp.1999.0734.CrossRefPubMedGoogle Scholar
  49. 49.
    Eisenberg N, Shepard SA, Fabes RA, Murphy BC, Guthrie IK. Shyness and children’s emotionality, regulation, and coping: contemporaneous, longitudinal, and across-context relations. Child Dev. 1998;69:767–90. doi: 10.2307/1132203.CrossRefPubMedGoogle Scholar
  50. 50.
    Wolfe CD, Zhang J, Kim-Spoon J, Ann BM. A longitudinal perspective on the association between cognition and temperamental shyness. Int J Behav Dev. 2014;38:266–76. doi: 10.1177/0165025413516257.CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Eisenberg N, Fabes RA, Murphy BC. Relations of shyness and low sociability to regulation and emotionality. J Pers Soc Psychol. 1995;68:505–17. doi: 10.1037/0022-3514.68.3.505.CrossRefPubMedGoogle Scholar
  52. 52.
    Eastwood JD, Smilek D, Merikle PM. Differential attentional guidance by unattended faces expressing positive and negative emotion. Percept Psychophys. 2001;63:1004–13. doi: 10.3758/BF03194519.CrossRefPubMedGoogle Scholar
  53. 53.
    Fox E, Russo R, Bowles R, Dutton K. Do threatening stimuli draw or hold visual attention in subclinical anxiety? J Exp Psychol Gen. 2001;130:681–700. doi: 10.1037/0096-3445.130.4.681.CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Vuilleumier P. How brains beware: neural mechanisms of emotional attention. Trends in Cogn Sci. 2005;9:585–94. doi: 10.1016/j.tics.2005.10.011.CrossRefGoogle Scholar
  55. 55.
    Fox E. Processing emotional facial expressions: the role of anxiety and awareness. Cogn Affect Behav Neurosci. 2002;2:52–63. doi: 10.1080/02699930143000527.CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Lobue V, Pérez-Edgar K. Sensitivity to social and non-social threats in temperamentally shy children at-risk for anxiety. Dev Sci. 2014;17:239–47. doi: 10.1111/desc.12110.CrossRefPubMedGoogle Scholar
  57. 57.
    Reeck C, Egner T. Emotional task management: neural correlates of switching between affective and non-affective task-sets. Soc Cogn Affect Neurosci [Internet]. 2015;10:1045–53. doi: 10.1093/scan/nsu153.CrossRefGoogle Scholar
  58. 58.
    Malooly AM, Genet JJ, Siemer M. Individual differences in reappraisal effectiveness: the role of affective flexibility. Emotion. 2013;13:302–13. doi: 10.1037/a0029980.CrossRefPubMedGoogle Scholar
  59. 59.
    • Marcus O, Stanciu O, MacLeod C, Liebregts H, Visu-Petra L. A FISTful of emotion: individual differences in trait anxiety and cognitive-affective flexibility during preadolescence. J Abnorm Child Psychol. 2016;44:1231–42. doi: 10.1037/a0029980. An empirical study demonstrating that trait anxiety is associated with deficits in the ability to flexibly engage with and disengage from the affective dimension of human facial stimuli in a matching task CrossRefPubMedGoogle Scholar
  60. 60.
    Mocan O, Stanciu O, Visu-Petra L. Relating individual differences in internalizing symptoms to emotional attention set-shifting in children. Anxiety Stress Coping. 2014;27:509–26. doi: 10.1080/10615806.2014.888419.CrossRefPubMedGoogle Scholar
  61. 61.
    De Lissnyder E, Koster EHW, Derakhshan N, De Raedt R. The association between depressive symptoms and executive control impairments in response to emotional and non-emotional information. Cogn Emot. 2010;24:264–80. doi: 10.1080/02699930903378354.CrossRefGoogle Scholar
  62. 62.
    Genet JJ, Malooly AM, Siemer M. Flexibility is not always adaptive: affective flexibility and inflexibility predict rumination use in everyday life. Cogn Emot. 2013;27:1–11. doi: 10.1080/02699931.2012.733351.CrossRefGoogle Scholar
  63. 63.
    Evans DE, Rothbart MK. Developing a model for adult temperament. J Res Pers. 2007;41:868–88. doi: 10.1016/j.jrp.2006.11.002.CrossRefGoogle Scholar
  64. 64.
    Eisenberg N, Eggum ND, Sallquist J, Edwards A. Relations of self-regulatory/control capacities to maladjustment, social competence, and emotionality. In: Hoyle RH, editor. Handbook of personality and self-regulation. New York: Wiley; 2010.Google Scholar
  65. 65.
    Chu BC, Crocco ST, Esseling P, Areizaga MJ, Lindner AM, Skriner LC. Transdiagnostic group behavioral activation and exposure therapy for youth anxiety and depression: initial randomized controlled trial. Behav Res Ther. 2016;76:65–75. doi: 10.1016/j.brat.2015.11.005.CrossRefPubMedGoogle Scholar
  66. 66.
    Susa G, Benga O, Pitica I, Miclea M. Child temperamental reactivity and self-regulation effects on attentional biases. Front Psychol. 2014;5(922):1–11. doi: 10.3389/fpsyg.2014.00922.Google Scholar
  67. 67.
    Bishop SR, Lau M, Shapiro S, Carlson L, Anderson ND, Carmody J, et al. Mindfulness: a proposed operational definition. Clin Psychol Sci Pract. 2004;11:230–41. doi: 10.1093/clipsy/bph077.CrossRefGoogle Scholar
  68. 68.
    Flook L, Smalley SL, Kitil MJ, Galla BM, Kaiser-Greenland S, Locke J, et al. Effects of mindful awareness practices on executive functions in elementary school children. J Appl Sch Psychol. 2010;26:70–95. doi: 10.1080/15377900903379125.CrossRefGoogle Scholar
  69. 69.
    Napoli M, Krech PR, Holley LC. Mindfulness training for elementary school students: the attention academy. J Appl Sch Psychol. 2005;21:99–125. doi: 10.1300/J008v21n01_05.CrossRefGoogle Scholar
  70. 70.
    Mendelson T, Greenberg MT, Dariotis JK, Gould LF, Rhoades BL, Leaf PJ. Feasibility and preliminary outcomes of a school-based mindfulness intervention for urban youth. J Abnorm Child Psychol. 2010;38:985–94. doi: 10.1007/s10802-010-9418-x.CrossRefPubMedGoogle Scholar
  71. 71.
    Nadler R, Cordy M, Stengel J, Segal Z V., Hayden EP. A brief mindfulness practice increases self-reported calmness in young children: A pilot study. Mindfulness. 2017;8:1–8. Doi:10.1007/s12671–017–0685-2Google Scholar

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© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Department of PsychologyUniversity of WaterlooWaterlooCanada

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