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

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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.

Introduction

Rates of posttraumatic stress disorder (PTSD) in returning veterans from Iraq and Afghanistan are high, with some estimates showing that close to 20% of Army and Marine troops meet criteria for PTSD 3 to 4 months post-deployment (Hoge et al., 2006). PTSD in these veterans is associated with cognitive deficits and functional impairment in everyday life (Hoge et al., 2006, Vasterling et al., 2006). Neuropsychological studies suggest that the nature of these cognitive deficits is more closely related to inattention and interference during the encoding process than retention loss due to amnesia (Vasterling and Brailey, 2005). One such source of interference in PTSD may be attentional bias to threatening information, which disrupts ongoing cognitive activities by redirecting attentional resources away from the cognitive task at hand. For instance, combat veterans show longer response latencies while naming the color of the ink used to print trauma-related words during an emotional Stroop task (McNally et al., 1990, Kaspi et al., 1995, Constans et al., 2004). It is therefore hypothesized that delayed naming of emotional words represents a diversion of attention away from neutral stimuli toward traumatic stimuli in individuals with PTSD. Further evidence for attentional bias in PTSD comes from event-related potential (ERP) studies that show enhanced P3 amplitude responses to threat or novel distracting stimuli (Attias et al., 1996, Kimble et al., 2000, Stanford et al., 2001). These studies employed modified oddball paradigms in which infrequent salient target stimuli were interspersed with frequent standard stimuli. Alterations in P3 amplitudes and latencies for emotional versus neutral stimuli provide evidence for heightened responsivity to potentially threatening stimuli in PTSD.

While there is evidence for attentional bias for threat from behavioral and ERP studies, evidence from neuroimaging studies for threat bias is scarce. The majority of previous neuroimaging studies in PTSD have focused on investigating provocation of trauma symptoms (Rauch et al., 1996, Bremner et al., 1999, Liberzon et al., 1999, Shin et al., 1999, Lanius et al., 2001, Lanius et al., 2002, Pissiota et al., 2002, Lanius et al., 2003a, Gilboa et al., 2004, Shin et al., 2004, Yang et al., 2004, Britton et al., 2005, Sakamoto et al., 2005), while others have examined cognition in PTSD such as working memory impairment without inclusion of emotional stimuli (Clark et al., 2003). However, in order to understand the neural circuitry underlying concentration and attention difficulties in relation to PTSD symptomatology, examination of both emotion and executive processing is necessary. Few neuroimaging studies have examined both emotion and attention within the same paradigm to simulate emotional distraction that occurs during cognitive task performance in real life. Neuroimaging studies that have employed emotional Stroop tasks in patients with PTSD (Shin et al., 2001, Bremner et al., 2004) combine the focus of both emotion and attention systems on the same stimulus, rendering it difficult to separate these two processes.

The goal of the present study was to examine the neural circuitry underlying alterations in attention by emotional distraction in veterans with symptoms of PTSD. We employed a modified emotional oddball paradigm based on our previous work in healthy adults, in which we demonstrated that emotion and attention function segregate into two large-scale neural networks, with emotional content engaging fronto-limbic regions including the amygdala and inferior prefrontal cortex (IFG) and attentional targets engaging dorsolateral prefrontal cortex and posterior parietal regions (Yamasaki et al., 2002). Additionally, emotional distractors and attentional targets both engage the rostral anterior cingulate cortex (ACC) suggesting that this region is important for integrating executive and emotion processing streams (Yamasaki et al., 2002, Fichtenholtz et al., 2004). The present study tested several hypotheses. First, PTSD symptom severity should be related to greater activation in ventral-limbic regions during the emotional condition, including the ventromedial prefrontal cortex (vmPFC) and amygdala. Second, symptom severity should be related to attenuated activity in dorsal frontal and parietal regions during the attention task, such as the middle frontal gyrus (MFG) and supramarginal gyrus (SMG) reflecting the disruption of executive pathways in PTSD. Finally, based on our previous work, we hypothesized that PTSD symptomatology would be related to an altered pattern of ACC activity for emotional and target stimuli.

Section snippets

Participants

Twenty-six recently returned (mean ± S.D.; 23 ± 14 months) veterans from deployments to post-9/11 military conflicts completed the fMRI procedures. Veterans were recruited from a large recruitment database for the study of post-deployment mental health. Veterans entering the registry completed a neuropsychiatric self-assessment battery which included the Davidson Trauma Scale (DTS; Davidson et al., 1997), Beck Depression Inventory-II (BDI-II; Beck et al., 1996), Combat Exposure Scale (CES; Keane et

Behavioral performance

Behavioral analysis is based on 11 high DTS participants and 11 low DTS participants. Three participants were excluded from the behavioral analysis because they did not make a button press to distractor pictures, and one participant was excluded from the behavioral analysis for making the same button press to both targets and distractors. MANOVA for reaction time with condition (emotion, neutral, target, standard) as a within subjects factor and group (low or high DTS) as a between subjects

Discussion

Examination of emotion and attention in a group of recently returned combat veterans revealed alterations in the neural circuitry associated with posttraumatic stress symptomatology indicating an attentional bias to emotional stimuli in PTSD. Integration of the findings within the broader emotion and PTSD literature is discussed below.

Conclusions

Understanding the challenges post-9/11 soldiers face as they attempt to re-integrate into civilian life is an important public health concern, as cognitive deficits can have negative implications on work and school related productivity. In the present study, participants with high levels of PTSD symptomatology showed attenuated activity in dorsolateral prefrontal cortex and parietal regions for neutral targets but enhanced activity for emotional distractors, which coincided with lowered

Acknowledgements

This research was supported by the Department of Veterans Affairs, Mental Illness Research Education and Clinical Center Grant for Post-Deployment Mental Health and by the National Institute of Mental Health Grant K23 MH073091. We would like to thank Debra Cooper, Srishti Seth, Lihong Wang, Larry Tupler, as well as the Journal editors and reviewers for their helpful comments and contributions to the paper.

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