Sustained amygdala response to both novel and newly familiar faces characterizes inhibited temperament.

Previous theories have proposed that the amygdala is hyper-responsive to novel stimuli in persons with an inhibited temperament-a biologically based predisposition to respond to novelty with wariness or avoidance behavior. In the current study, we used functional magnetic resonance imaging (fMRI) to assess amygdala blood oxygenation level-dependent (BOLD) response when viewing novel or recently familiarized faces in persons with an extreme inhibited or uninhibited temperament. In persons with an inhibited temperament, the amygdala showed increased BOLD response when viewing both novel and recently familiarized faces. In contrast, in persons with an uninhibited temperament, BOLD response in the amygdala was increased only when viewing novel faces. These findings suggest that inhibited temperament is characterized not by a simple exaggerated response to novel faces, but rather by a sustained increase in amygdala response to faces even after the faces have become familiarized. In individuals with an inhibited temperament, this sustained response may be related to the wariness of social situations that persists beyond initial exposure.

[1]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[2]  N. Fox,et al.  Stable early maternal report of behavioral inhibition predicts lifetime social anxiety disorder in adolescence. , 2009, Journal of the American Academy of Child and Adolescent Psychiatry.

[3]  Paul J. Laurienti,et al.  An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets , 2003, NeuroImage.

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

[5]  J. Kagan,et al.  Biological bases of childhood shyness. , 1988, Science.

[6]  S. Rauch,et al.  Differential prefrontal cortex and amygdala habituation to repeatedly presented emotional stimuli , 2001, Neuroreport.

[7]  R. Gur,et al.  Computerized Neurocognitive Scanning: II. The Profile of Schizophrenia , 2001, Neuropsychopharmacology.

[8]  D. Zald.  The human amygdala and the emotional evaluation of sensory stimuli , 2003, Brain Research Reviews.

[9]  D L Newman,et al.  Behavioral observations at age 3 years predict adult psychiatric disorders. Longitudinal evidence from a birth cohort. , 1996, Archives of general psychiatry.

[10]  R. Turner,et al.  Event-Related fMRI: Characterizing Differential Responses , 1998, NeuroImage.

[11]  Jennifer Urbano Blackford,et al.  A unique role for the human amygdala in novelty detection , 2010, NeuroImage.

[12]  M. Höfler,et al.  Incidence of social anxiety disorder and the consistent risk for secondary depression in the first three decades of life. , 2007, Archives of general psychiatry.

[13]  Jerome Kagan,et al.  Differential amygdalar response to novel versus newly familiar neutral faces: a functional MRI probe developed for studying inhibited temperament , 2003, Biological Psychiatry.

[14]  M. Windle,et al.  Adolescent temperament and lifetime psychiatric and substance abuse disorders assessed in young adulthood , 2006 .

[15]  J. Steven Reznick,et al.  Retrospective and concurrent self-report of behavioral inhibition and their relation to adult mental health , 1992, Development and Psychopathology.

[16]  Jean-Luc Anton,et al.  Region of interest analysis using an SPM toolbox , 2010 .

[17]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[18]  N. Ramsey,et al.  Amygdala responses to positively and negatively valenced baby faces in healthy female volunteers: Influences of individual differences in harm avoidance , 2009, Brain Research.

[19]  M. First,et al.  The Structured Clinical Interview for DSM-III-R (SCID). I: History, rationale, and description. , 1992, Archives of general psychiatry.

[20]  J. Kagan,et al.  Early childhood temperament as a determinant of externalizing behavior in adolescence , 1996, Development and Psychopathology.

[21]  S. Rauch,et al.  Response and Habituation of the Human Amygdala during Visual Processing of Facial Expression , 1996, Neuron.

[22]  R. Shelton,et al.  Amygdala temporal dynamics: temperamental differences in the timing of amygdala response to familiar and novel faces , 2009, BMC Neuroscience.

[23]  Godfrey Pearlson,et al.  An adaptive reflexive processing model of neurocognitive function: supporting evidence from a large scale (n = 100) fMRI study of an auditory oddball task , 2005, NeuroImage.

[24]  J. Kagan,et al.  Adolescent social anxiety as an outcome of inhibited temperament in childhood. , 1999, Journal of the American Academy of Child and Adolescent Psychiatry.

[25]  R. Gur,et al.  Computerized Neurocognitive Scanning: I. Methodology and Validation in Healthy People , 2001, Neuropsychopharmacology.

[26]  J. Kagan,et al.  Further evidence of association between behavioral inhibition and social anxiety in children. , 2001, The American journal of psychiatry.

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

[28]  Jessica Turner,et al.  Sex-related hemispheric lateralization of amygdala function in emotionally influenced memory: an FMRI investigation. , 2004, Learning & memory.

[29]  N. Fox,et al.  Startle response in behaviorally inhibited adolescents with a lifetime occurrence of anxiety disorders. , 2009, Journal of the American Academy of Child and Adolescent Psychiatry.

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

[31]  Kagan,et al.  The physiology and psychology of behavioral inhibition in children. , 1987, Child development.

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

[33]  Karl J. Friston,et al.  The choice of basis functions in event-related fMRI , 2001, NeuroImage.

[34]  R. Plomin,et al.  The Study of temperament : changes, continuities, and challenges , 1986 .

[35]  L. Schmidt,et al.  Different neural responses to stranger and personally familiar faces in shy and bold adults. , 2008, Behavioral neuroscience.

[36]  C. Grillon,et al.  The strong situation: A potential impediment to studying the psychobiology and pharmacology of anxiety disorders , 2006, Biological Psychology.

[37]  P. Muris,et al.  Relations among behavioral inhibition, Big Five personality factors, and anxiety disorder symptoms in non-clinical children , 2009 .

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