The role of trauma-related distractors on neural systems for working memory and emotion processing in posttraumatic stress disorder

Abstract

The relevance of emotional stimuli to threat and survival confers a privileged role in their processing. In PTSD, the ability of trauma-related information to divert attention is especially pronounced. Information unrelated to the trauma may also be highly distracting when it shares perceptual features with trauma material. Our goal was to study how trauma-related environmental cues modulate working memory networks in PTSD. We examined neural activity in participants performing a visual working memory task while distracted by task-irrelevant trauma and non-trauma material. Recent post-9/11 veterans were divided into a PTSD group (n=22) and a trauma-exposed control group (n=20) based on the Davidson trauma scale. Using fMRI, we measured hemodynamic change in response to emotional (trauma-related) and neutral distraction presented during the active maintenance period of a delayed-response working memory task. The goal was to examine differences in functional networks associated with working memory (dorsolateral prefrontal cortex and lateral parietal cortex) and emotion processing (amygdala, ventrolateral prefrontal cortex, and fusiform gyrus). The PTSD group showed markedly different neural activity compared to the trauma-exposed control group in response to task-irrelevant visual distractors. Enhanced activity in ventral emotion processing regions was associated with trauma distractors in the PTSD group, whereas activity in brain regions associated with working memory and attention regions was disrupted by distractor stimuli independent of trauma content. Neural evidence for the impact of distraction on working memory is consistent with PTSD symptoms of hypervigilance and general distractibility during goal-directed cognitive processing.

Fig. 1

Diagram of the working memory task showing the event order and trial types. Subjects were instructed to encode the memoranda (3 faces) and had to actively maintain them in working memory during a delay period while looking at distractors. During the retrieve period subjects were required to press a response button to indicate whether the probe (single-face) was part of the memoranda. Three categories of trials were presented during the working memory delay period, defined by the type of distractors (i) combat-related scenes from Iraq or Afghanistan, (ii) non-combat scenes, or (iii) digitally scrambled images. Each trial contained two distractors from the same category that were presented, consecutively, for 3 s each.

Fig. 2

Dissociable dorsal–ventral patterns of activity from subjects (n = 42) observed in the presence of combat-related distracters. Combat distracters produced the most disrupting effect on activity during the delay period in a set of dorsal brain regions associated with working memory (blue blobs) while producing the most enhancing effect on activity on ventral brain regions associated with emotion processing (red blobs). The activation maps show direct contrasts between the most versus least distracting conditions, combat > scrambled (red) and scrambled > combat (blue), superimposed on a high-resolution brain image. The colored horizontal bars at the bottom of the brain image indicate the gradients of the t values for the activation maps displayed.

Fig. 3

Working memory performance measured by d-prime scores for control and PTSD groups for combat, non-combat, and scrambled distractor types.

Fig. 4

Comparison of mean percent signal change in ventral emotional regions corresponding to combat, non-combat, and scrambled distractors displayed during the active maintenance period of working memory in the PTSD (n = 22) and control (n = 20) groups. Activation in the was greater for combat than non-combat distractors in the PTSD group but not in the control group in the (a) amygdala (AMG) (b) ventrolateral prefrontal cortex (vlPFC), and (c) the fusiform gyrus (FFG). (d) Mean percent signal change for the entire trial epoch by condition in the vlPFC for the control group and the PTSD group.

Fig. 5

Comparison of mean percent signal change in dorsal executive regions corresponding to combat, non-combat, and scrambled distractors displayed during the active maintenance period of working memory in the PTSD (n = 22) and control (n = 20) groups. (a) Combat related distractors showed differential dlPFC deactivation in the control group but not in the PTSD group. (b) There was a trend level group by distractor type interaction effect in the lateral parietal cortex (LPC). (c) Mean percent signal change for the entire trial epoch by condition in the dlPFC for the control Group and the PTSD group.