Early-Childhood Social Reticence Predicts Brain Function in Preadolescent Youths During Distinct Forms of Peer Evaluation

Social reticence is expressed as shy, anxiously avoidant behavior in early childhood. With development, overt signs of social reticence may diminish but could still manifest themselves in neural responses to peers. We obtained measures of social reticence across 2 to 7 years of age. At age 11, preadolescents previously characterized as high (n = 30) or low (n = 23) in social reticence completed a novel functional-MRI-based peer-interaction task that quantifies neural responses to the anticipation and receipt of distinct forms of social evaluation. High (but not low) social reticence in early childhood predicted greater activity in dorsal anterior cingulate cortex and left and right insula, brain regions implicated in processing salience and distress, when participants anticipated unpredictable compared with predictable feedback. High social reticence was also associated with negative functional connectivity between insula and ventromedial prefrontal cortex, a region commonly implicated in affect regulation. Finally, among participants with high social reticence, negative evaluation was associated with increased amygdala activity, but only during feedback from unpredictable peers.

[1]  E. Nelson,et al.  Social re-orientation and brain development: An expanded and updated view , 2015, Developmental Cognitive Neuroscience.

[2]  Jorge Moll,et al.  Self-blame-Selective Hyperconnectivity Between Anterior Temporal and Subgenual Cortices and Prediction of Recurrent Depressive Episodes. , 2015, JAMA psychiatry.

[3]  C. Büchel,et al.  The brain’s response to reward anticipation and depression in adolescence: dimensionality, specificity and longitudinal predictions in a community-based sample , 2015 .

[4]  Adrienne L. Romer,et al.  Forgetting the best when predicting the worst: Preliminary observations on neural circuit function in adolescent social anxiety , 2015, Developmental Cognitive Neuroscience.

[5]  L. Uddin.  Salience processing and insular cortical function and dysfunction , 2014, Nature Reviews Neuroscience.

[6]  Steffi Weidt,et al.  Neuroimaging in social anxiety disorder—A meta-analytic review resulting in a new neurofunctional model , 2014, Neuroscience & Biobehavioral Reviews.

[7]  Ellen Leibenluft,et al.  Applications of multivariate modeling to neuroimaging group analysis: A comprehensive alternative to univariate general linear model , 2014, NeuroImage.

[8]  A. Reiss,et al.  Reward processing in healthy offspring of parents with bipolar disorder. , 2014, JAMA psychiatry.

[9]  N. Fox,et al.  Longitudinal trajectories of social reticence with unfamiliar peers across early childhood. , 2014, Developmental psychology.

[10]  J. O'Doherty,et al.  Anterior Insula Activity Reflects the Effects of Intentionality on the Anticipation of Aversive Stimulation , 2014, The Journal of Neuroscience.

[11]  D. Bannerman,et al.  Aversive Prediction Error Signals in the Amygdala , 2014, The Journal of Neuroscience.

[12]  P. Dayan,et al.  Action versus valence in decision making , 2014, Trends in Cognitive Sciences.

[13]  L. Somerville,et al.  Adolescent-specific patterns of behavior and neural activity during social reinforcement learning , 2014, Cognitive, affective & behavioral neuroscience.

[14]  N. Fox,et al.  Lasting associations between early-childhood temperament and late-adolescent reward-circuitry response to peer feedback , 2014, Development and Psychopathology.

[15]  Todd A. Hare,et al.  Early developmental emergence of human amygdala–prefrontal connectivity after maternal deprivation , 2013, Proceedings of the National Academy of Sciences.

[16]  E. Leibenluft,et al.  Neuroimaging studies of pediatric social anxiety: paradigms, pitfalls and a new direction for investigating the neural mechanisms , 2013, Biology of Mood & Anxiety Disorders.

[17]  D. Grupe,et al.  Uncertainty and anticipation in anxiety: an integrated neurobiological and psychological perspective , 2013, Nature Reviews Neuroscience.

[18]  E. Leibenluft,et al.  The neural correlates of emotion-based cognitive control in adults with early childhood behavioral inhibition , 2013, Biological Psychology.

[19]  John Jonides,et al.  The Neural Basis of Difficulties Disengaging From Negative Irrelevant Material in Major Depression , 2013, Psychological science.

[20]  E. Crone,et al.  Understanding adolescence as a period of social–affective engagement and goal flexibility , 2012, Nature Reviews Neuroscience.

[21]  Sterling C. Johnson,et al.  A generalized form of context-dependent psychophysiological interactions (gPPI): A comparison to standard approaches , 2012, NeuroImage.

[22]  E. Wagenmakers,et al.  Erroneous analyses of interactions in neuroscience: a problem of significance , 2011, Nature Neuroscience.

[23]  E. Nelson,et al.  The development of the ventral prefrontal cortex and social flexibility , 2011, Developmental Cognitive Neuroscience.

[24]  Jason P. Mitchell,et al.  Medial prefrontal cortex subserves diverse forms of self-reflection , 2011, Social neuroscience.

[25]  R. Davidson,et al.  The integration of negative affect, pain and cognitive control in the cingulate cortex , 2011, Nature Reviews Neuroscience.

[26]  Bregtje Gunther Moor,et al.  Please Scroll down for Article Social Neuroscience Do You like Me? Neural Correlates of Social Evaluation and Developmental Trajectories Do You like Me? Neural Correlates of Social Evaluation and Developmental Trajectories Neural Correlates of Peer Evaluation , 2022 .

[27]  S. Petersen,et al.  The “Task B problem” and other considerations in developmental functional neuroimaging , 2010, Human brain mapping.

[28]  N. Fox,et al.  Neural Correlates of Reward Processing in Adolescents With a History of Inhibited Temperament , 2009, Psychological science.

[29]  C. Carter,et al.  Optimizing the Design and Analysis of Clinical Functional Magnetic Resonance Imaging Research Studies , 2008, Biological Psychiatry.

[30]  Erin B. McClure-Tone,et al.  Amygdala and ventrolateral prefrontal cortex function during anticipated peer evaluation in pediatric social anxiety. , 2008, Archives of general psychiatry.

[31]  C. Kennard,et al.  Functional role of the supplementary and pre-supplementary motor areas , 2008, Nature Reviews Neuroscience.

[32]  N. Fox,et al.  Printed in the United States of America DOI: 10.1017/S0954579407000363 Behavioral inhibition and anxiety disorders: Multiple levels of a resilience process , 2022 .

[33]  Michael G. Hardin,et al.  Attention alters neural responses to evocative faces in behaviorally inhibited adolescents , 2007, NeuroImage.

[34]  T. Heatherton,et al.  Anterior cingulate cortex responds differentially to expectancy violation and social rejection , 2006, Nature Neuroscience.

[35]  Olga V. Demler,et al.  Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the National Comorbidity Survey Replication. , 2005, Archives of general psychiatry.

[36]  S. Rauch,et al.  Inhibited and Uninhibited Infants "Grown Up": Adult Amygdalar Response to Novelty , 2003, Science.

[37]  H. Merckelbach,et al.  The Screen for Child Anxiety Related Emotional Disorders (SCARED) and traditional childhood anxiety measures. , 1998, Journal of behavior therapy and experimental psychiatry.

[38]  N. Ryan,et al.  Schedule for Affective Disorders and Schizophrenia for School-Age Children-Present and Lifetime Version (K-SADS-PL): initial reliability and validity data. , 1997, Journal of the American Academy of Child and Adolescent Psychiatry.

[39]  Peter Dayan,et al.  A Neural Substrate of Prediction and Reward , 1997, Science.

[40]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[41]  Kenneth H. Rubin,et al.  Being alone, playing alone, and acting alone: distinguishing among reticence and passive and active solitude in young children. , 1994, Child development.

[42]  A. Petersen,et al.  A self-report measure of pubertal status: Reliability, validity, and initial norms , 1988, Journal of youth and adolescence.

[43]  Kenneth H. Rubin,et al.  Social withdrawal in childhood. , 2009, Annual review of psychology.

[44]  A. Craig,et al.  How do you feel — now? The anterior insula and human awareness , 2009, Nature Reviews Neuroscience.

[45]  M. Rothbart,et al.  Revision of the Early Adolescent Temperament Questionnaire , 2006 .

[46]  Kenneth H. Rubin,et al.  Continuity and discontinuity of behavioral inhibition and exuberance: psychophysiological and behavioral influences across the first four years of life. , 2001, Child development.

[47]  W. Mischel,et al.  A cognitive-affective system theory of personality: reconceptualizing situations, dispositions, dynamics, and invariance in personality structure. , 1995, Psychological review.

[48]  K. Dodge,et al.  A review and reformulation of social information-processing mechanisms in children's social adjustment. , 1994 .