Trait anxiety modulates anterior cingulate activation to threat interference

Background: Individuals vary in the degree to which salient threatening stimuli disrupt or distract from goal‐directed cognitive processes. Excessive attention to threat or difficulty resolving the interference created by threat cues could contribute to anxious psychopathology; disruptions in frontal brain regions implicated in attentional control or resolution of emotional interference (e.g. anterior cingulate cortex, “ACC”) might play a role. In this study, we explored the hypothesis that trait anxiety would be associated with ACC activity in an attentional control task with varying levels of threat interference. Methods: During functional magnetic resonance imaging, 20 healthy individuals who varied in trait anxiety levels viewed angry, fearful, and neutral faces superimposed on an indoor or outdoor scene. In a high‐threat interference condition, subjects identified the gender of the face (Attend Face). In a low‐threat interference condition, they identified the scene type (Attend Scene). Whole‐brain analysis was used to compare Attend Face with Attend Scene for angry and fearful (versus neutral) faces. Contrasts were correlated with trait anxiety level. Results: Behavioral data confirmed that Attend Face produced greater threat interference than Attend Scene. Brain imaging results showed that trait anxiety was inversely associated with bilateral rostral ACC activity for Attend Face relative to Attend Scene for angry faces. A similar relationship was not seen for fearful faces. Conclusions: The rostral ACC is implicated in assessing the salience of emotional information and controlling attention to resolve emotional interference. The link between higher trait anxiety and decreased ACC activation for angry faces suggests reduced attentional control for signals of interpersonal threat in healthy anxiety‐prone individuals. Depression and Anxiety 28:194–201, 2011. © 2011 Wiley‐Liss, Inc.

[1]  A. Anderson,et al.  Neural Correlates of the Automatic Processing of Threat Facial Signals , 2022 .

[2]  S. Kotz,et al.  Emotion speeds up conflict resolution: a new role for the ventral anterior cingulate cortex? , 2011, Cerebral cortex.

[3]  Michael W. Otto,et al.  Anxiety and Its Disorders: The Nature and Treatment of Anxiety and Panic , 1989 .

[4]  F. McKenna,et al.  Effects of unattended emotional stimuli on color-naming performance , 1986 .

[5]  P. Ekman,et al.  Matsumoto and Ekman's Japanese and Caucasian Facial Expressions of Emotion (JACFEE): Reliability Data and Cross-National Differences , 1997 .

[6]  J. Duncan,et al.  Prefrontal cortical function and anxiety: controlling attention to threat-related stimuli , 2004, Nature Neuroscience.

[7]  Cameron S Carter,et al.  Adding fear to conflict: A general purpose cognitive control network is modulated by trait anxiety , 2010, Cognitive, affective & behavioral neuroscience.

[8]  M. Lader Current Controversies in the Anxiety Disorders , 1996 .

[9]  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.

[10]  T. Egner,et al.  Dissociable neural systems resolve conflict from emotional versus nonemotional distracters. , 2008, Cerebral cortex.

[11]  M. Eysenck,et al.  Anxiety and Performance: The Processing Efficiency Theory , 1992 .

[12]  Y. Bar-Haim,et al.  Threat-related attentional bias in anxious and nonanxious individuals: a meta-analytic study. , 2007, Psychological bulletin.

[13]  A. Ohman,et al.  The face in the crowd revisited: a threat advantage with schematic stimuli. , 2001, Journal of personality and social psychology.

[14]  Leslie G. Ungerleider,et al.  Attentional control of the processing of neural and emotional stimuli. , 2002, Brain research. Cognitive brain research.

[15]  K. Mogg,et al.  Some methodological issues in assessing attentional biases for threatening faces in anxiety: a replication study using a modified version of the probe detection task. , 1999, Behaviour research and therapy.

[16]  M. Posner,et al.  Cognitive and emotional influences in anterior cingulate cortex , 2000, Trends in Cognitive Sciences.

[17]  C. MacLeod,et al.  Attentional bias in emotional disorders. , 1986, Journal of abnormal psychology.

[18]  George Bush,et al.  The emotional counting Stroop: a task for assessing emotional interference during brain imaging , 2006, Nature Protocols.

[19]  P. Ekman,et al.  Strong evidence for universals in facial expressions: a reply to Russell's mistaken critique. , 1994, Psychological bulletin.

[20]  R. Desimone,et al.  Neural mechanisms of selective visual attention. , 1995, Annual review of neuroscience.

[21]  D. Derryberry,et al.  Anxiety-related attentional biases and their regulation by attentional control. , 2002, Journal of abnormal psychology.

[22]  Luca Passamonti,et al.  Anxiety predicts a differential neural response to attended and unattended facial signals of anger and fear , 2009, NeuroImage.

[23]  Rob Jenkins,et al.  Neural processing of fearful faces: effects of anxiety are gated by perceptual capacity limitations. , 2007, Cerebral cortex.

[24]  P. Vuilleumier,et al.  How brains beware: neural mechanisms of emotional attention , 2005, Trends in Cognitive Sciences.

[25]  George Bush,et al.  The emotional counting stroop paradigm: a functional magnetic resonance imaging probe of the anterior cingulate affective division , 1998, Biological Psychiatry.

[26]  K. Mogg,et al.  Attentional Bias for Threatening Facial Expressions in Anxiety: Manipulation of Stimulus Duration , 1998 .

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

[28]  Justin S. Feinstein,et al.  Increased amygdala and insula activation during emotion processing in anxiety-prone subjects. , 2007, The American journal of psychiatry.

[29]  David C. Alsop,et al.  Brain Activation during Facial Emotion Processing , 2002, NeuroImage.

[30]  Colin M. Macleod Half a century of research on the Stroop effect: an integrative review. , 1991, Psychological bulletin.

[31]  E. Kandel,et al.  Resolving Emotional Conflict: A Role for the Rostral Anterior Cingulate Cortex in Modulating Activity in the Amygdala , 2006, Neuron.

[32]  R. McNally Anxiety and Its Disorders: The Nature and Treatment of Anxiety and Panic, 2nd ed. , 2002 .

[33]  A. Calder,et al.  Anxiety and sensitivity to gaze direction in emotionally expressive faces. , 2007, Emotion.

[34]  P. Vuilleumier,et al.  Facial expression and selective attention , 2002 .