Kevin Maluenda Tan

Neuroimaging studies of mentalizing (i.e., theory of mind) consistently implicate the default mode network (DMN). Nevertheless, the social cognitive functions of individual DMN regions remain unclear, perhaps due to limited spatiotemporal resolution in neuroimaging. Here we use electrocorticography (ECoG) to directly record neuronal population activity while 16 human participants judge the psychological traits of themselves and others. Self- and other-mentalizing recruit near-identical cortical sites in a common spatiotemporal sequence. Activations begin in the visual cortex, followed by temporoparietal DMN regions, then finally in medial prefrontal regions. Moreover, regions with later activations exhibit stronger functional specificity for mentalizing, stronger associations with behavioral responses, and stronger self/other differentiation. Specifically, other-mentalizing evokes slower and longer activations than self-mentalizing across successive DMN regions, implying lengthier processing at higher levels of representation. Our results suggest a common neurocognitive pathway for self- and other-mentalizing that follows a complex spatiotemporal gradient of functional specialization across DMN and beyond.

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 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.

Background: Social impairments, specifically in mentalizing and emotion recognition, are common and debilitating symptoms of posttraumatic stress disorder (PTSD). Despite this, little is known about the neural underpinnings of these impairments, as there have been 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). The PTSD group 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 non-emotional targets.Results: Hyperactivation to emotional stimuli differentiated PTSD patients from controls, correlated with symptom severity, and predicted training outcomes. Critically, these effects were generally non-significant for non-emotional stimuli. PTSD-related effects were widely distributed throughout DMN and MNS. Effects were strongest in regions associated with the dorsal attention, ventral attention, and frontoparietal control networks. Unexpectedly, effects were non-significant in core affect regions.Conclusions: The array of social cognitive processes subserved by DMN and MNS may be inordinately selective for emotional stimuli in PTSD. This selectivity may be tightly linked with attentional processes, as effects were strongest in attention-related regions. Putatively, we propose an attentional account of social inference dysfunction in PTSD, in which affective attentional biases drive widespread affect-selectivity throughout the social brain. This account aligns with numerous findings of affect-biased attentional processing in PTSD.