PTSD symptom severity is associated with increased recruitment of top-down attentional control in a trauma-exposed sample

Stuart F White, Michelle E Costanzo, James R Blair, Michael J Roy, Stuart F White, Michelle E Costanzo, James R Blair, Michael J Roy

Abstract

Background: Recent neuroimaging work suggests that increased amygdala responses to emotional stimuli and dysfunction within regions mediating top down attentional control (dorsomedial frontal, lateral frontal and parietal cortices) may be associated with the emergence of anxiety disorders, including posttraumatic stress disorder (PTSD). This report examines amygdala responsiveness to emotional stimuli and the recruitment of top down attention systems as a function of task demands in a population of U.S. military service members who had recently returned from combat deployment in Afghanistan/Iraq. Given current interest in dimensional aspects of pathophysiology, it is worthwhile examining patients who, while not meeting full PTSD criteria, show clinically significant functional impairment.

Methods: Fifty-seven participants with sub-threshold levels of PTSD symptoms completed the affective Stroop task while undergoing fMRI. Participants with PTSD or depression at baseline were excluded.

Results: Greater PTSD symptom severity scores were associated with increased amygdala activation to emotional, particularly positive, stimuli relative to neutral stimuli. Furthermore, greater PTSD symptom severity was associated with increased superior/middle frontal cortex response during task conditions relative to passive viewing conditions. In addition, greater PTSD symptom severity scores were associated with: (i) increased activation in the dorsolateral prefrontal, lateral frontal, inferior parietal cortices and dorsomedial frontal cortex/dorsal anterior cingulate cortex (dmFC/dACC) in response to emotional relative to neutral stimuli; and (ii) increased functional connectivity during emotional trials, particularly positive trials, relative to neutral trials between the right amygdala and dmFC/dACC, left caudate/anterior insula cortex, right lentiform nucleus/caudate, bilateral inferior parietal cortex and left middle temporal cortex.

Conclusions: We suggest that these data may reflect two phenomena associated with increased PTSD symptomatology in combat-exposed, but PTSD negative, armed services members. First, these data indicate increased emotional responsiveness by: (i) the positive relationship between PTSD symptom severity and amygdala responsiveness to emotional relative to neutral stimuli; (ii) greater BOLD response as a function of PTSD symptom severity in regions implicated in emotion (striatum) and representation (occipital and temporal cortices) during emotional relative to neutral conditions; and (iii) increased connectivity between the amygdala and regions implicated in emotion (insula/caudate) and representation (middle temporal cortex) as a function of PTSD symptom severity during emotional relative to neutral trials. Second, these data indicate a greater need for the recruitment of regions implicated in top down attention as indicated by (i) greater BOLD response in superior/middle frontal gyrus as a function of PTSD symptom severity in task relative to view conditions; (ii) greater BOLD response in dmFC/dACC, lateral frontal and inferior parietal cortices as a function of PTSD symptom severity in emotional relative to neutral conditions and (iii) greater functional connectivity between the amygdala and inferior parietal cortex as a function of PTSD symptom severity during emotional relative to neutral conditions.

Trial registration: ClinicalTrials.gov NCT01296126.

Keywords: Amygdala; Emotion attention; Post-traumatic stress disorder; Top down attention.

Figures

Fig. 1
Fig. 1
The affective Stroop task. Participants were exposed to neutral, positive or negative images followed either by a fixation cross (a), a screen showing digits congruent in their value and quantity (e.g. two 2 s; b) or a screening digits incongruent in their value and quantity (e.g. three 4 s; c). The fixation/numeric images were followed by a second exposure to the neutral positive or negative image. A negative image is depicted here.
Fig. 2
Fig. 2
Task condition-by-PTSD checklist score interaction in the right superior/middle frontal cortex in 57 trauma-exposed combat veterans. Participants showed greater levels of increased activation in the right superior/middle frontal gyrus as a function of increased PTSD symptom severity during both congruent and incongruent trials relative to passive viewing trials.
Fig. 3
Fig. 3
Emotion-by-PTSD checklist score interaction in the right lateral frontal cortex and right dorsolateral prefrontal cortex in 57 trauma-exposed combat veterans. Participants showed greater levels of increased activation in the right lateral frontal cortex and dorsolateral prefrontal cortex as a function of increased PTSD symptom severity to both positive and negative stimuli relative to neutral stimuli.
Fig. 4
Fig. 4
Emotion-by-PTSD checklist score interaction examining differential functional connectivity between amygdala and left middle temporal cortex and right inferior parietal cortex in 57 trauma-exposed combat veterans. Participants showed greater levels of increased functional connectivity in the left middle temporal cortex and right inferior parietal cortex as a function of increased PTSD symptom severity to both positive and negative stimuli relative to neutral stimuli.

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