Alterations in the neural circuitry for emotion and attention associated with posttraumatic stress symptomatology

Abstract

Information processing models of posttraumatic stress disorder (PTSD) suggest that PTSD is characterized by preferential allocation of attentional resources to potentially threatening stimuli. However, few studies have examined the neural pattern underlying attention and emotion in association with PTSD symptomatology. In the present study, combat veterans with PTSD symptomatology engaged in an emotional oddball task while undergoing functional magnetic resonance imaging (fMRI). Veterans were classified into a high or low symptomatology group based on their scores on the Davidson Trauma Scale (DTS). Participants discriminated infrequent target stimuli (circles) from frequent standards (squares) while emotional and neutral distractors were presented infrequently and irregularly. Results revealed that participants with greater PTSD symptomatology showed enhanced neural activity in ventral-limbic and dorsal regions for emotional stimuli and attenuated activity in dorsolateral prefrontal and parietal regions for attention targets. In the anterior cingulate gyrus, participants with fewer PTSD symptoms showed equivalent responses to attentional and emotional stimuli while the high symptom group showed greater activation for negative emotional stimuli. Taken together, the results suggest that hyperresponsive ventral-limbic activity coupled with altered dorsal-attention and anterior cingulate function may be a neural marker of attention bias in PTSD.

Figure 1

Dissociable systems for ventral and dorsal regions in all 26 subjects. (a) Emotional distracters elicited activation in ventral regions including inferior frontal gyrus (IFG) and amygdala (AMY) (b) Target circles elicited activation in dorsal attention regions including middle frontal gyrus (MFG), and supramarginal gyrus (SMG).

Figure 2

Comparison of mean percent signal change in ventral emotional regions corresponding to emotional, neutral, and target stimuli in the low and high PTSD symptom groups. (a) Activation in the ventromedial prefrontal cortex (vmPFC) was greater for emotional distracters in the high symptom group but not in the low symptom group. (b) Activation in the inferior frontal gyrus (IFG) was greater for emotional distracters in the low symptom group but not the high symptom group.

Figure 3

Comparison of mean percent signal change in dorsal executive-attention regions corresponding to emotional, neutral, and target stimuli in the low and high PTSD symptom groups. (a) Activation in the middle frontal gyrus (MFG) prefrontal cortex was greater for circle targets in the low symptom group than the high symptom group. (b) Activation in the supramarginal gyrus (SMG) was also greater for circle targets in the low symptom group than the high symptom group.

Figure 4

Regions of overlap where both emotion and target stimuli evoked greater activation than neutral stimuli in the entire group of subjects. (a) In region 1, the low symptom group showed equivalent activity for emotion and target whereas the high symptom group showed the greatest activation for emotion. (b) In region 2, the low symptom group did not differentiate between target, emotion, and neutral stimuli. The high symptom group had greater activity to emotional stimuli than the low symptom group. (c) In region 3, the low symptom group again showed equivalent activity for emotion and target stimuli. In the high symptom group, there was a trend for greater activity for emotion than target stimuli.