Skip to main content
×
Home
    • Aa
    • Aa

Attention bias toward threat is associated with exaggerated fear expression and impaired extinction in PTSD

  • N. Fani (a1) (a2) (a3), E. B. Tone (a1), J. Phifer (a2), S. D. Norrholm (a2) (a3), B. Bradley (a2) (a3), K. J. Ressler (a2) (a4), A. Kamkwalala (a2) and T. Jovanovic (a2)...
Abstract
Background

Post-traumatic stress disorder (PTSD) develops in a minority of traumatized individuals. Attention biases to threat and abnormalities in fear learning and extinction are processes likely to play a critical role in the creation and/or maintenance of PTSD symptomatology. However, the relationship between these processes has not been established, particularly in highly traumatized populations; understanding their interaction can help inform neural network models and treatments for PTSD.

Method

Attention biases were measured using a dot probe task modified for use with our population; task stimuli included photographs of angry facial expressions, which are emotionally salient threat signals. A fear-potentiated startle paradigm was employed to measure atypical physiological response during acquisition and extinction phases of fear learning. These measures were administered to a sample of 64 minority (largely African American), highly traumatized individuals with and without PTSD.

Results

Participants with PTSD demonstrated attention biases toward threat; this attentional style was associated with exaggerated startle response during fear learning and early and middle phases of extinction, even after accounting for the effects of trauma exposure.

Conclusions

Our findings indicate that an attentional bias toward threat is associated with abnormalities in ‘fear load’ in PTSD, providing seminal evidence for an interaction between these two processes. Future research combining these behavioral and psychophysiological techniques with neuroimaging will be useful toward addressing how one process may modulate the other and understanding whether these phenomena are manifestations of dysfunction within a shared neural network. Ultimately, this may serve to inform PTSD treatments specifically designed to correct these atypical processes.

Copyright
Corresponding author
*Address for correspondence: N. Fani, Ph.D., Department of Psychiatry and Behavioral Sciences, Emory University, School of Medicine, 49 Jesse Hill Jr. Ave, Atlanta, GA 30303, USA. (Email: nfani@emory.edu)
Linked references
Hide All

This list contains references from the content that can be linked to their source. For a full set of references and notes please see the PDF or HTML where available.

DP Bernstein , JA Stein , MD Newcomb , E Walker , D Pogge , T Ahluvalia , J Stokes , L Handelsman , M Medrano , D Desmond , W Zule (2003). Development and validation of a brief screening version of the Childhood Trauma Questionnaire. Child Abuse and Neglect 27, 169190.

SJ Bishop (2007). Neurocognitive mechanisms of anxiety: an integrative account. Trends in Cognitive Sciences 11, 307316.

BP Bradley , K Mogg , SC Lee (1997). Attentional biases for negative information in induced and naturally occurring dysphoria. Behaviour Research and Therapy 35, 911927.

RG Bradley , EB Binder , MP Epstein , Y Tang , HP Nair , W Liu , CF Gillespie , T Berg , M Evces , DJ Newport , ZN Stowe , CM Heim , CB Nemeroff , A Schwartz , JF Cubells , KJ Ressler (2008). Influence of child abuse on adult depression: moderation by the corticotropin-releasing hormone receptor gene. Archives of General Psychiatry 65, 190200.

RA Bryant , AG Harvey (1995). Processing of threatening information in posttraumatic stress disorder. Journal of Abnormal Psychology 104, 537541.

KL Cassiday , RJ McNally , SB Zeitlin (1992). Cognitive processing of trauma cues in rape victims with post-traumatic stress disorder. Cognitive Therapy and Research 16, 283295.

HM Claypool , K Hugenberg , MK Housley , DM Mackie (2007). Familiar eyes are smiling: on the role of familiarity in the perception of facial affect. European Journal of Social Psychology 37, 856866.

T Dalgleish , R Taghavi , N Hamid , A Moradi , R Canterbury , W Yule (2003). 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. Journal of Clinical Child and Adolescent Psychology 32, 1021.

M Davis (1992). The role of the amygdala in fear-potentiated startle: implications for animal models of anxiety. Trends in Pharmacological Sciences 13, 3541.

K Elsesser , G Sartory , A Tackenberg (2004). Attention, heart rate, and startle response during exposure to trauma-relevant pictures: a comparison of recent trauma victims and patients with posttraumatic stress disorder. Journal of Abnormal Psychology 113, 289301.

K Elsesser , G Sartory , A Tackenberg (2005). Initial symptoms and reactions to trauma-related stimuli and the development of posttraumatic stress disorder. Depression and Anxiety 21, 6170.

N Fani , RG Bradley , KJ Ressler , EB McClure-Tone (2010). Attention bias in adult survivors of childhood maltreatment with and without posttraumatic stress disorder. Cognitive Therapy and Research 35, 5767.

DL Filion , ME Dawson , AM Schell (1998). The psychological significance of human startle eyeblink modification: a review. Biological Psychology 47, 143.

EB Foa , U Feske , TB Murdock , MJ Kozac , PR McCarthy (1991). Processing of threat-related material in rape victims. Journal of Abnormal Psychology 100, 156162.

CF Gillespie , B Bradley , K Mercer , AK Smith , K Conneely , M Gapen , T Weiss , AC Schwartz , JF Cubells , KJ Ressler (2009). Trauma exposure and stress-related disorders in inner city primary care patients. General Hospital Psychiatry 31, 505514.

C Grillon , CA Morgan 3rd (1999). Fear-potentiated startle conditioning to explicit and contextual cues in Gulf War veterans with posttraumatic stress disorder. Journal of Abnormal Psychology 108, 134142.

T Jovanovic , NQ Blanding , SD Norrholm , E Duncan , B Bradley , KJ Ressler (2009 a). Childhood abuse is associated with increased startle reactivity in adulthood. Depression and Anxiety 26, 10181026.

T Jovanovic , M Keyes , A Fiallos , KM Myers , M Davis , EJ Duncan (2005). Fear potentiation and fear inhibition in a human fear-potentiated startle paradigm. Biological Psychiatry 57, 15591564.

T Jovanovic , SD Norrholm , NQ Blanding , M Davis , E Duncan , B Bradley , KJ Ressler (2010). Impaired fear inhibition is a biomarker of PTSD but not depression. Depression and Anxiety 27, 244251.

T Jovanovic , SD Norrholm , JE Fennell , M Keyes , AM Fiallos , KM Myers , M Davis , EJ Duncan (2009 b). Posttraumatic stress disorder may be associated with impaired fear inhibition: relation to symptom severity. Psychiatry Research 167, 151160.

T Jovanovic , SD Norrholm , M Keyes , A Fiallos , S Jovanovic , KM Myers , M Davis , EJ Duncan (2006). Contingency awareness and fear inhibition in a human fear-potentiated startle paradigm. Behavioral Neuroscience 120, 995–1004.

T Jovanovic , SD Norrholm , AJ Sakoman , S Esterajher , D Kozaric-Kovacic (2009 c). Altered resting psychophysiology and startle response in Croatian combat veterans with PTSD. International Journal of Psychophysiology 71, 264268.

SP Kaspi , RJ McNally , N Amir (1995). Cognitive processing of emotional information in posttraumatic stress disorder. Cognitive Therapy and Research 19, 433444.

MM Kelly , JP Forsyth (2007). Observational fear conditioning in the acquisition and extinction of attentional bias for threat: an experimental evaluation. Emotion 7, 324335.

RC Kessler , A Sonnega , E Bromet , M Hughes , CB Nelson (1995). Posttraumatic stress disorder in the National Comorbidity Survey. Archives of General Psychiatry 52, 10481060.

DC Knight , HT Nguyen , PA Bandettini (2005). The role of the human amygdala in the production of conditioned fear responses. Neuroimage 26, 11931200.

KS LaBar , JC Gatenby , JC Gore , JE LeDoux , EA Phelps (1998). Human amygdala activation during conditioned fear acquisition and extinction: a mixed-trial fMRI study. Neuron 20, 937945.

J Liebschutz , R Saltz , V Brower , TM Keane , C Lloyd-Travaglini , T Averbuch , JH Samet (2007). PTSD in urban primary care: high prevalence and low physician recognition. Journal of General Internal Medicine 22, 719726.

S Lissek , AS Powers , EB McClure , EA Phelps , G Woldehawariat , C Grillon , DS Pine (2005). Classical fear conditioning in the anxiety disorders: a meta-analysis. Behaviour Research & Therapy 43, 13911424.

RJ McNally , GE English , HJ Lipke (1993). Assessment of intrusive cognition in PTSD: use of the modified Stroop paradigm. Journal of Traumatic Stress 6, 3341.

RJ McNally , SP Kaspi , BC Reimann , SB Zeitlin (1990). Selective processing of threat cues in post-traumatic stress disorder. Journal of Abnormal Psychology 99, 398402.

LM McTeague , PJ Lang , MC Laplante , BN Cuthbert , JR Shumen , MM Bradley (2010). Aversive imagery in posttraumatic stress disorder: trauma recurrence, comorbidity, and physiological reactivity. Biological Psychiatry 67, 346356.

MR Milad , RK Pitman , CB Ellis , AL Gold , LM Shin , NB Lasko , MA Zeidan , K Handwerger , SP Orr , SL Rauch (2009). Neurobiological basis of failure to recall extinction memory in posttraumatic stress disorder. Biological Psychiatry 66, 10751082.

MR Milad , GJ Quirk , RK Pitman , SP Orr , B Fischl , SL Rauch (2007). A role for the human dorsal anterior cingulate cortex in fear expression. Biological Psychiatry 62, 11911194.

M Minear , DC Park (2004). A lifespan database of adult facial stimuli. Behavior Research Methods, Instruments, & Computers 36, 630633.

CS Monk , EE Nelson , EB McClure , K Mogg , BP Bradley , E Leibenluft , RJ Blair , G Chen , DS Charney , M Ernst , DS Pine (2006). Ventrolateral prefrontal cortex activation and attentional bias in response to angry faces in adolescents with generalized anxiety disorder. American Journal of Psychiatry 163, 10911097.

SD Norrholm , T Jovanovic , IW Olin , LA Sands , I Karapanou , B Bradley , KJ Ressler (2011). Fear extinction in traumatized civilians with posttraumatic stress disorder: relation to symptom severity. Biological Psychiatry 69, 553563.

SD Norrholm , T Jovanovic , B Vervliet , KM Myers , M Davis , BO Rothbaum , EJ Duncan (2006). Conditioned fear extinction and reinstatement in a human fear-potentiated startle paradigm. Learning & Memory 13, 681685.

EA Phelps , MR Delgado , KI Nearing , JE LeDoux (2004). Extinction learning in humans: role of the amygdala and vmPFC. Neuron 43, 897905.

EA Phelps , JE LeDoux (2005). Contributions of the amygdala to emotion processing: from animal models to human behavior. Neuron 48, 175187.

DS Pine , K Mogg , BP Bradley , L Montgomery , CS Monk , EB McClure , AE Guyer , M Ernst , DS Charney , J Kaufman (2005). Attention bias to threat in maltreated children: implications for vulnerability to stress-related psychopathology. American Journal of Psychiatry 162, 291296.

SL Pineles , JC Shipherd , LP Welch , I Yovel (2007). The role of attentional biases in PTSD: is it interference or facilitation? Behaviour Research and Therapy 45, 19031913.

N Pole , TC Neylan , C Otte , TJ Metzler , SR Best , C Henn-Haase , CR Marmar (2007). Associations between childhood trauma and emotion-modulated psychophysiological responses to startling sounds: a study of police cadets. Journal of Abnormal Psychology 116, 352361.

N Tottenham , JW Tanaka , AC Leon , T McCarry , M Nurse , TA Hare , DJ Marcus , A Westerlund , BJ Casey , C Nelson (2009). The NimStim set of facial expressions: judgments from untrained research participants. Psychiatry Research 168, 241249.

AC Schwartz , RL Bradley , M Sexton , A Sherry , KJ Ressler (2005). Posttraumatic stress disorder among African Americans in an inner city mental health clinic. Psychiatric Services 56, 212215.

SR Vrana , A Roodman , JC Beckham (1995). Selective processing of trauma-relevant words in posttraumatic stress disorder. Journal of Anxiety Disorders 9, 515530.

Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Psychological Medicine
  • ISSN: 0033-2917
  • EISSN: 1469-8978
  • URL: /core/journals/psychological-medicine
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords:

Metrics

Altmetric attention score