Posttraumatic Stress Disorder and the Social Brain: Affect-Related Disruption of the Default and Mirror Networks

Hundreds of neuroimaging studies show that mentalizing (i.e., theory of mind) recruits default mode network (DMN) regions with remarkable consistency. Nevertheless, the social-cognitive functions of individual DMN regions remain unclear, perhaps due to the limited spatiotemporal resolution of neuroimaging. We used electrocorticography (ECoG) to record neuronal population activity while 16 human subjects judged the psychological traits of themselves and others. Self- and other-mentalizing recruited near-identical neuronal populations in a common spatiotemporal sequence: activations were earliest in visual cortex, followed by temporoparietal DMN regions, and finally medial prefrontal cortex. Critically, regions with later activations showed greater functional specificity for mentalizing, greater self/other differentiation, and stronger associations with behavioral response times. Moreover, other-mentalizing evoked slower and lengthier activations than self-mentalizing across successive DMN regions, suggesting temporally extended demands on higher-level processes. Our results reveal a common neurocognitive pathway for self- and other-mentalizing that follows a hierarchy of functional specialization across DMN regions.

Background: Poor social connection is a central feature of posttraumatic stress disorder (PTSD), but little is known about the neurocognitive processes associated with social difficulties in this population. We examined recruitment of the default network and behavioral responses during social working memory (SWM; i.e., maintaining and manipulating social information on a moment-to-moment basis) in relation to PTSD and social connection. Methods: Participants with PTSD (n = 31) and a trauma-exposed control group (n = 21) underwent functional magnetic resonance imaging while completing a task in which they reasoned about two or four people's relationships in working memory (social condition) and alphabetized two or four people's names in working memory (nonsocial condition). Participants also completed measures of social connection (e.g., loneliness, social network size).Results: Compared to trauma-exposed controls, individuals with PTSD reported smaller social networks (p = .032) and greater loneliness (p = .038). Individuals with PTSD showed a selective deficit in SWM accuracy (p = .029) and hyperactivation in the default network, particularly in the dorsomedial subsystem, on trials with four relationships to consider. Moreover, default network hyperactivation in the PTSD group (vs. trauma-exposed group) differentially related to social network size and loneliness (p's < .05). Participants with PTSD also showed less resting state functional connectivity within the dorsomedial subsystem than controls (p = .002), suggesting differences in the functional integrity of a subsystem key to SWM.Conclusions: SWM abnormalities in the default network may be a basic mechanism underlying poorer social connection in PTSD.

Background: Social cognitive impairments, specifically in mentalizing and emotion recognition, are common and debilitating symptoms of posttraumatic stress disorder (PTSD). Despite this, little is known about the neurobiology of these impairments, as there are currently no published neuroimaging investigations of social inference in PTSD.Methods: Trauma-exposed veterans with and without PTSD (n = 20 each) performed the Why/How social inference task during functional magnetic resonance imaging (fMRI). Patients with PTSD had two fMRI sessions, between which they underwent affect labeling training. We probed the primary networks of the "social brain"-the default mode network (DMN) and mirror neuron system (MNS)-by examining neural activity evoked by mentalizing and action identification prompts, which were paired with emotional and nonemotional targets.Results: Hyperactivation to emotional stimuli differentiated PTSD patients from controls, correlated with symptom severity, and predicted training outcomes.Critically, these effects were nonsignificant or marginal for nonemotional stimuli.Results were generally consistent throughout DMN and MNS. Unexpectedly, effects were nonsignificant in core affect regions, but robust in regions that overlap with the dorsal attention, ventral attention, and frontoparietal control networks. Conclusions:The array of social cognitive processes subserved by DMN and MNS appear to be inordinately selective for emotional stimuli in PTSD. However, core affective processes do not appear to be the primary instigators of such selectivity. Instead, we propose that affective attentional biases may instigate widespread affect-selectivity throughout the social brain. Affect labeling training may inhibit such biases. These accounts align with numerous reports of affect-biased attentional processes in PTSD.