Attention alters neural responses to evocative faces in behaviorally inhibited adolescents

Behavioral inhibition (BI) is a risk factor for anxiety disorders. While the two constructs bear behavioral similarities, previous work has not extended these parallels to the neural level. This study examined amygdala reactivity during a task previously used with clinically anxious adolescents. Adolescents were selected for enduring patterns of BI or non-inhibition (BN). We examined amygdala response to evocative emotion faces in BI (N=10, mean 12.8 years) and BN (N=17, mean 12.5 years) adolescents while systematically manipulating attention. Analyses focused on amygdala response during subjective ratings of internal fear (constrained attention) and passive viewing (unconstrained attention) during the presentation of emotion faces (Happy, Angry, Fearful, and Neutral). BI adolescents, relative to BN adolescents, showed exaggerated amygdala response during subjective fear ratings and deactivation during passive viewing, across all emotion faces. In addition, the BI group showed an abnormally high amygdala response to a task condition marked by novelty and uncertainty (i.e., rating fear state to a Happy face). Perturbations in amygdala function are evident in adolescents temperamentally at risk for anxiety. Attention state alters the underlying pattern of neural processing, potentially mediating the observed behavioral patterns across development. BI adolescents also show a heightened sensitivity to novelty and uncertainty, which has been linked to anxiety. These patterns of reactivity may help sustain early temperamental biases over time and contribute to the observed relation between BI and anxiety.

[1]  M. D’Esposito,et al.  A Trial-Based Experimental Design for fMRI , 1997, NeuroImage.

[2]  J. Stevenson-Hinde,et al.  Behavioral inhibition, heart period, and respiratory sinus arrhythmia in young children. , 1998, Developmental psychobiology.

[3]  F. Castellanos,et al.  An fMRI examination of developmental differences in the neural correlates of uncertainty and decision-making. , 2006, Journal of child psychology and psychiatry, and allied disciplines.

[4]  D. Pine.  Pathophysiology of childhood anxiety disorders , 1999, Biological Psychiatry.

[5]  H. Goldsmith,et al.  Linking temperamental fearfulness and anxiety symptoms: a behavior–genetic perspective , 2000, Biological Psychiatry.

[6]  Israel Liberzon,et al.  Corticolimbic blood flow during nontraumatic emotional processing in posttraumatic stress disorder. , 2006, Archives of general psychiatry.

[7]  Robert Ladouceur,et al.  The Role of Intolerance of Uncertainty in Etiology and Maintenance. , 2004 .

[8]  P. Whalen.  Fear, Vigilance, and Ambiguity , 1998 .

[9]  M Ashtari,et al.  Orbital frontal and amygdala volume reductions in obsessive-compulsive disorder. , 1999, Archives of general psychiatry.

[10]  J. Kagan,et al.  The Long Shadow of Temperament , 2004 .

[11]  D. Amaral.  Amygdalohippocampal and amygdalocortical projections in the primate brain. , 1986, Advances in experimental medicine and biology.

[12]  M Ingvar,et al.  A PET activation study of dynamic mechanical allodynia in patients with mononeuropathy , 1999, PAIN®.

[13]  Ellen Leibenluft,et al.  Adolescent immaturity in attention-related brain engagement to emotional facial expressions , 2003, NeuroImage.

[14]  Younglim Lee,et al.  Amygdala and bed nucleus of the stria terminalis: differential roles in fear and anxiety measured with the acoustic startle reflex. , 1997, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[15]  Nathan A. Fox,et al.  Conceptual, biological, and behavioral distinctions among different categories of shy children. , 1999 .

[16]  Karl J. Friston,et al.  Detecting Activations in PET and fMRI: Levels of Inference and Power , 1996, NeuroImage.

[17]  Michael Davis,et al.  The amygdala: vigilance and emotion , 2001, Molecular Psychiatry.

[18]  Richard G. Heimberg,et al.  Generalized anxiety disorder: Advances in research and practice. , 2004 .

[19]  K. E. Nichols,et al.  Behavioral inhibition: linking biology and behavior within a developmental framework. , 2005, Annual review of psychology.

[20]  Lisa M Shin,et al.  Neuroimaging Studies of Amygdala Function in Anxiety Disorders , 2003, Annals of the New York Academy of Sciences.

[21]  Karl Magnus Petersson,et al.  Context-dependent Deactivation of the Amygdala during Pain , 2004, Journal of Cognitive Neuroscience.

[22]  E. Murray,et al.  Control of Response Selection by Reinforcer Value Requires Interaction of Amygdala and Orbital Prefrontal Cortex , 2000, The Journal of Neuroscience.

[23]  Karl J. Friston,et al.  A unified statistical approach for determining significant signals in images of cerebral activation , 1996, Human brain mapping.

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

[25]  Lars R. Bergman,et al.  Methods and models for studying the individual. , 1998 .

[26]  E. Leibenluft,et al.  Limbic hyperactivation during processing of neutral facial expressions in children with bipolar disorder. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[27]  N. Fox,et al.  Behavioral and physiological antecedents of inhibited and uninhibited behavior. , 1996, Child development.

[28]  P. Vokonas,et al.  Prospective study of posttraumatic stress disorder symptoms and coronary heart disease in the Normative Aging Study. , 2007, Archives of general psychiatry.

[29]  D. Pine,et al.  Face-emotion processing in offspring at risk for panic disorder. , 2005, Journal of the American Academy of Child and Adolescent Psychiatry.

[30]  J. Kagan,et al.  Temperamental contributions to the affect family of anxiety. , 2001, The Psychiatric clinics of North America.

[31]  S. Geisser,et al.  An Extension of Box's Results on the Use of the $F$ Distribution in Multivariate Analysis , 1958 .

[32]  Francesco Fera,et al.  The Amygdala Response to Emotional Stimuli: A Comparison of Faces and Scenes , 2002, NeuroImage.

[33]  P. Ekman.  Pictures of Facial Affect , 1976 .

[34]  Leslie G. Ungerleider,et al.  Neural processing of emotional faces requires attention , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[35]  J. Kagan,et al.  Behavioral inhibition in young children. , 1984 .

[36]  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.

[37]  Michael G. Hardin,et al.  Reward and punishment sensitivity in shy and non-shy adults: Relations between social and motivated behavior. , 2006, Personality and individual differences.

[38]  J. Kagan.  Temperament and the reactions to unfamiliarity. , 1997, Child development.

[39]  J. Kagan,et al.  Inhibited and uninhibited types of children. , 1989, Child development.

[40]  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.

[41]  N. Fox,et al.  Mismatch negativity in socially withdrawn children , 2003, Biological Psychiatry.

[42]  Monique Ernst,et al.  Abnormal attention modulation of fear circuit function in pediatric generalized anxiety disorder. , 2007, Archives of general psychiatry.

[43]  Karl J. Friston,et al.  Generalisability, Random Effects & Population Inference , 1998, NeuroImage.

[44]  J. Kagan.  Temperamental contributions to affective and behavioral profiles in childhood. , 2001 .

[45]  N. Fox,et al.  Temperament and anxiety disorders. , 2005, Child and adolescent psychiatric clinics of North America.

[46]  Michael G. Hardin,et al.  Striatal Functional Alteration in Adolescents Characterized by Early Childhood Behavioral Inhibition , 2006, The Journal of Neuroscience.

[47]  Louis A. Schmidt,et al.  Extreme fear, shyness, and social phobia : origins, biological mechanisms, and clinical outcomes , 1999 .

[48]  J. Kagan,et al.  Behavioral inhibition to the unfamiliar. , 1984 .

[49]  E. Murray,et al.  The amygdala and reward , 2002, Nature Reviews Neuroscience.

[50]  S. Hofmann,et al.  From Social Anxiety to Social Phobia: Multiple Perspectives , 2000 .

[51]  J. Kagan,et al.  Behavioral inhibition in children of parents with panic disorder and agoraphobia. A controlled study. , 1988, Archives of general psychiatry.

[52]  B. J. Casey,et al.  Amygdala response to fearful faces in anxious and depressed children. , 2001, Archives of general psychiatry.

[53]  J. Kagan,et al.  Childhood derivatives of inhibition and lack of inhibition to the unfamiliar. , 1988, Child development.

[54]  Kenneth H. Rubin,et al.  Frontal activation asymmetry and social competence at four years of age. , 1995, Child development.

[55]  Thomas M. Moerland,et al.  Fate of unattended fearful faces in the amygdala is determined by both attentional resources and cognitive modulation , 2005, NeuroImage.

[56]  Kenneth H. Rubin,et al.  Behavioral and neuroendocrine responses in shy children. , 1997, Developmental psychobiology.

[57]  Sheri R. Levy,et al.  The role of children's lay theories about the malleability of human attributes in beliefs about and volunteering for disadvantaged groups. , 2004, Child development.

[58]  John E Richards,et al.  Familiarization, attention, and recognition memory in infancy: an event-related potential and cortical source localization study. , 2005, Developmental psychology.

[59]  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.

[60]  Kenneth H. Rubin,et al.  Psychophysiological and behavioral evidence for varying forms and functions of nonsocial behavior in preschoolers. , 2004, Child development.

[61]  N. Logothetis,et al.  Negative functional MRI response correlates with decreases in neuronal activity in monkey visual area V1 , 2006, Nature Neuroscience.

[62]  J. Kagan,et al.  Stable behavioral inhibition and its association with anxiety disorder. , 1992, Journal of the American Academy of Child and Adolescent Psychiatry.

[63]  S. Taylor,et al.  Corticolimbic blood flow in posttraumatic stress disorder during script-driven imagery , 2005, Biological Psychiatry.

[64]  Christopher S. Monk,et al.  Increased Amygdala Activity During Successful Memory Encoding in Adolescent Major Depressive Disorder: An fMRI Study , 2006, Biological Psychiatry.