Neural correlates of attention bias to threat in post-traumatic stress disorder

Attentional biases have been proposed to contribute to symptom maintenance in posttraumatic stress disorder (PTSD), although the neural correlates of these processes have not been well defined; this was the goal of the present study. We administered an attention bias task, the dot probe, to a sample of 37 (19 control, 18 PTSD+) traumatized African-American adults during fMRI. Compared to controls, PTSD+ participants demonstrated increased activation in the dorsolateral prefrontal cortex (dlPFC) in response to threat cue trials. In addition, attentional avoidance of threat corresponded with increased ventrolateral prefrontal cortex (vlPFC) and dorsal anterior cingulate cortex (dACC) activation in the PTSD group, a pattern that was not observed in controls. These data provide evidence to suggest that relative increases in dlPFC, dACC and vlPFC activation represent neural markers of attentional bias for threat in individuals with PTSD, reflecting selective disruptions in attentional control and emotion processing networks in this disorder.

[1]  T. Dalgleish,et al.  Patterns of Processing Bias for Emotional Information Across Clinical Disorders: A Comparison of Attention, Memory, and Prospective Cognition in Children and Adolescents With Depression, Generalized Anxiety, and Posttraumatic Stress Disorder , 2003, Journal of clinical child and adolescent psychology : the official journal for the Society of Clinical Child and Adolescent Psychology, American Psychological Association, Division 53.

[2]  A. Beck,et al.  Beck Depression Inventory–II , 2011 .

[3]  K. Ressler,et al.  Influence of child abuse on adult depression: moderation by the corticotropin-releasing hormone receptor gene. , 2008, Archives of general psychiatry.

[4]  Eric Vermetten,et al.  Neural correlates of the classic color and emotional stroop in women with abuse-related posttraumatic stress disorder , 2004, Biological Psychiatry.

[5]  J. Tanaka,et al.  The NimStim set of facial expressions: Judgments from untrained research participants , 2009, Psychiatry Research.

[6]  G. McCarthy,et al.  Alterations in the neural circuitry for emotion and attention associated with posttraumatic stress symptomatology , 2009, Psychiatry Research: Neuroimaging.

[7]  A. David,et al.  Predictors of amygdala activation during the processing of emotional stimuli: A meta-analysis of 385 PET and fMRI studies , 2008, Brain Research Reviews.

[8]  E. Foa,et al.  Emotional Processing Theory: An Update. , 2006 .

[9]  G. McCarthy,et al.  Dissociable prefrontal brain systems for attention and emotion , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[10]  Eric Vermetten,et al.  Circuits and systems in stress. II. Applications to neurobiology and treatment in posttraumatic stress disorder , 2002, Depression and anxiety.

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

[12]  S. Rauch,et al.  The counting stroop: An interference task specialized for functional neuroimaging—validation study with functional MRI , 1998, Human brain mapping.

[13]  D. H Weissman,et al.  Conflict monitoring in the human anterior cingulate cortex during selective attention to global and local object features , 2003, NeuroImage.

[14]  Ravi S. Menon,et al.  Brain activation during script-driven imagery induced dissociative responses in PTSD: a functional magnetic resonance imaging investigation , 2002, Biological Psychiatry.

[15]  D. Pandya,et al.  Comparative cytoarchitectonic analysis of the human and the macaque ventrolateral prefrontal cortex and corticocortical connection patterns in the monkey , 2002, The European journal of neuroscience.

[16]  G. McCarthy,et al.  Neural systems for executive and emotional processing are modulated by symptoms of posttraumatic stress disorder in Iraq War veterans , 2008, Psychiatry Research: Neuroimaging.

[17]  K. Ressler,et al.  Association of FKBP5 polymorphisms and childhood abuse with risk of posttraumatic stress disorder symptoms in adults. , 2008, JAMA.

[18]  Ravi S. Menon,et al.  Neural correlates of traumatic memories in posttraumatic stress disorder: a functional MRI investigation. , 2001, The American journal of psychiatry.

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

[20]  Dick J Veltman,et al.  Increased anterior cingulate cortex and hippocampus activation in Complex PTSD during encoding of negative words. , 2013, Social cognitive and affective neuroscience.

[21]  J. Bremner Functional neuroimaging in post-traumatic stress disorder , 2007, Expert review of neurotherapeutics.

[22]  Peter Herscovitch,et al.  Regional cerebral blood flow correlated with flashback intensity in patients with posttraumatic stress disorder , 2001, Biological Psychiatry.

[23]  H. Resnick,et al.  The Modified PTSD Symptom Scale: A brief self-report measure of posttraumatic stress disorder. , 1993 .

[24]  Monique Ernst,et al.  Attention bias to threat in maltreated children: implications for vulnerability to stress-related psychopathology. , 2005, The American journal of psychiatry.

[25]  J. Gross,et al.  The cognitive control of emotion , 2005, Trends in Cognitive Sciences.

[26]  Denise C. Park,et al.  A lifespan database of adult facial stimuli , 2004, Behavior research methods, instruments, & computers : a journal of the Psychonomic Society, Inc.

[27]  Monique Ernst,et al.  Isolating neural components of threat bias in pediatric anxiety. , 2012, Journal of child psychology and psychiatry, and allied disciplines.

[28]  Toru Machida,et al.  Parahippocampal activation evoked by masked traumatic images in posttraumatic stress disorder: A functional MRI study , 2005, NeuroImage.

[29]  R. Mitchell Linear increases in BOLD response associated with increasing proportion of incongruent trials across time in a colour Stroop task , 2010, Experimental Brain Research.

[30]  Tobias Egner,et al.  The neural correlates and functional integration of cognitive control in a Stroop task , 2005, NeuroImage.

[31]  B. Bradley,et al.  Impaired fear inhibition is a biomarker of PTSD but not depression , 2010, Depression and anxiety.

[32]  Matthew J. Barton,et al.  Neural Networks of Information Processing in Posttraumatic Stress Disorder: A Functional Magnetic Resonance Imaging Study , 2005, Biological Psychiatry.

[33]  B. Bradley,et al.  Trauma exposure and stress-related disorders in inner city primary care patients. , 2009, General hospital psychiatry.

[34]  Lawrence H Staib,et al.  Neural correlates of exposure to traumatic pictures and sound in Vietnam combat veterans with and without posttraumatic stress disorder: a positron emission tomography study , 1999, Biological Psychiatry.

[35]  K. Ressler,et al.  Posttraumatic stress disorder among African Americans in an inner city mental health clinic. , 2005, Psychiatric services.

[36]  Erin B. McClure-Tone,et al.  Attention Bias in Adult Survivors of Childhood Maltreatment with and without Posttraumatic Stress Disorder , 2011, Cognitive Therapy and Research.

[37]  J L Lancaster,et al.  Automated Talairach Atlas labels for functional brain mapping , 2000, Human brain mapping.

[38]  Monique Ernst,et al.  Ventrolateral prefrontal cortex activation and attentional bias in response to angry faces in adolescents with generalized anxiety disorder. , 2006, The American journal of psychiatry.

[39]  P. Buckley Association of Fkbp5 Polymorphisms and Childhood Abuse with Risk of Posttraumatic Stress Disorder Symptoms in Adults , 2009 .

[40]  Christian Grillon,et al.  The adaptive threat bias in anxiety: Amygdala–dorsomedial prefrontal cortex coupling and aversive amplification , 2012, NeuroImage.

[41]  G. Sartory,et al.  Initial symptoms and reactions to trauma‐related stimuli and the development of posttraumatic stress disorder , 2005, Depression and anxiety.

[42]  Katharina Domschke,et al.  Imaging genetics of anxiety disorders , 2010, NeuroImage.

[43]  S. Bishop,et al.  Neural Mechanisms Underlying Selective Attention to Threat , 2008, Annals of the New York Academy of Sciences.

[44]  B. Bradley,et al.  Attention bias toward threat is associated with exaggerated fear expression and impaired extinction in PTSD , 2011, Psychological Medicine.

[45]  R. Dolan,et al.  Amygdala Automaticity in Emotional Processing , 2003, Annals of the New York Academy of Sciences.

[46]  J. Talairach,et al.  Co-Planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging , 1988 .

[47]  Avram J. Holmes,et al.  Dissociable recruitment of rostral anterior cingulate and inferior frontal cortex in emotional response inhibition , 2008, NeuroImage.

[48]  S. Rauch,et al.  An fMRI study of anterior cingulate function in posttraumatic stress disorder , 2001, Biological Psychiatry.

[49]  A. Etkin,et al.  Functional neuroimaging of anxiety: a meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. , 2007, The American journal of psychiatry.

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

[51]  K. Felmingham,et al.  Anterior cingulate activity to salient stimuli is modulated by autonomic arousal in Posttraumatic Stress Disorder , 2009, Psychiatry Research: Neuroimaging.

[52]  K. Mogg,et al.  Attentional biases for negative information in induced and naturally occurring dysphoria. , 1997, Behaviour research and therapy.

[53]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

[54]  S. Southwick,et al.  Neural correlates of memories of childhood sexual abuse in women with and without posttraumatic stress disorder. , 1999, The American journal of psychiatry.

[55]  G. Sartory,et al.  Attention, heart rate, and startle response during exposure to trauma-relevant pictures: a comparison of recent trauma victims and patients with posttraumatic stress disorder. , 2004, Journal of abnormal psychology.

[56]  T. Egner,et al.  Emotional processing in anterior cingulate and medial prefrontal cortex , 2011, Trends in Cognitive Sciences.

[57]  P. Ekman,et al.  Facial Expressions of Emotion , 1979 .

[58]  D. Weber,et al.  Information Processing Bias in Post-traumatic Stress Disorder , 2008, The open neuroimaging journal.

[59]  R A Bryant,et al.  Attentional bias in posttraumatic stress disorder. , 1997, Journal of traumatic stress.

[60]  Marie T Banich,et al.  Differential engagement of anterior cingulate cortex subdivisions for cognitive and emotional function. , 2007, Psychophysiology.

[61]  Derek G. V. Mitchell,et al.  The impact of processing load on emotion , 2007, NeuroImage.

[62]  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.

[63]  R. Lanius,et al.  Neural correlates of reexperiencing, avoidance, and dissociation in PTSD: symptom dimensions and emotion dysregulation in responses to script-driven trauma imagery. , 2007, Journal of traumatic stress.

[64]  Monique Ernst,et al.  Amygdala and ventrolateral prefrontal cortex activation to masked angry faces in children and adolescents with generalized anxiety disorder. , 2008, Archives of general psychiatry.

[65]  Joseph E. LeDoux,et al.  Emotional memory and psychopathology. , 1997, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[66]  Aysenil Belger,et al.  Emotional priming effects during Stroop task performance , 2009, NeuroImage.

[67]  M. Kozak,et al.  Emotional processing of fear: exposure to corrective information. , 1986, Psychological bulletin.

[68]  Emotional Priming Effects during Stroop Task Performance , 2009, NeuroImage.

[69]  Monique Ernst,et al.  Relationship between trait anxiety, prefrontal cortex, and attention bias to angry faces in children and adolescents , 2008, Biological Psychology.

[70]  Kristen L. Mackiewicz,et al.  Cognitive control mechanisms, emotion and memory: A neural perspective with implications for psychopathology , 2009, Neuroscience & Biobehavioral Reviews.

[71]  Xenophon Papademetris,et al.  More accurate Talairach coordinates for neuroimaging using non-linear registration , 2008, NeuroImage.