Schizophrenia is associated with marked impairments in social cognition. However, the neural correlates of these deficits remain unclear. Here we use naturalistic stimuli to examine the role of the right temporoparietal junction/posterior superior temporal sulcus (TPJ-pSTS)—an integrative hub for the cortical networks pertinent to the understanding complex social situations—in social inference, a key component of social cognition, in schizophrenia. 27 schizophrenia participants (SzP) and 21 healthy controls watched a clip of the movie “The Good, the Bad, and the Ugly” while high resolution multiband fMRI images were collected. We used inter-subject correlation (ISC) to measure the evoked activity, which we then compared to social cognition as measured by The Awareness of Social Inference Test (TASIT). We also compared between groups the TPJ-pSTS BOLD activity 1) relationship with the motion content in the movie, 2) synchronization with other cortical areas involved in the viewing of the movie, and 3) relationship with the frequency of saccades made during the movie. Activation deficits were greatest in middle TPJ (TPJm) and correlated significantly with impaired TASIT performance across groups. Follow-up analyses of the TPJ-pSTS revealed decreased synchronization with other cortical areas, decreased correlation with the motion content of the movie, and decreased correlation with the saccades made during the movie. The functional impairment of the TPJm, a hub area in the middle of the TPJ-pSTS, predicts deficits in social inference in SzP by disrupting the integration of visual motion processing into the TPJ. This disrupted integration then affects the use of the TPJ to guide saccades during the visual scanning of the movie clip. These findings suggest that the TPJ may be a treatment target for improving deficits in a key component of social cognition in SzP.

Background Impairments in social cognition contribute significantly to disability in schizophrenia patients (SzP). Perception of facial expressions is critical for social cognition. Intact perception requires an individual to visually scan a complex dynamic social scene for transiently moving facial expressions that may be relevant for understanding the scene. The relationship of visual scanning for these facial expressions and social cognition remains unknown. Methods In 39 SzP and 27 healthy controls (HC), we used eye-tracking to examine the relationship between performance on The Awareness of Social Inference Test (TASIT), which tests social cognition using naturalistic video clips of social situations, and visual scanning, measuring each individual's relative to the mean of HC. We then examined the relationship of visual scanning to the specific visual features (motion, contrast, luminance, faces) within the video clips. Results TASIT performance was significantly impaired in SzP for trials involving sarcasm (p < 10−5). Visual scanning was significantly more variable in SzP than HC (p < 10−6), and predicted TASIT performance in HC (p = 0.02) but not SzP (p = 0.91), differing significantly between groups (p = 0.04). During the visual scanning, SzP were less likely to be viewing faces (p = 0.0001) and less likely to saccade to facial motion in peripheral vision (p = 0.008). Conclusions SzP show highly significant deficits in the use of visual scanning of naturalistic social scenes to inform social cognition. Alterations in visual scanning patterns may originate from impaired processing of facial motion within peripheral vision. Overall, these results highlight the utility of naturalistic stimuli in the study of social cognition deficits in schizophrenia.

Highlights Examined attention systems in SzP with resting-state connectivity and task fMRI. SzP have functional connectivity deficits in late visual cortex and prefrontal areas. Task performance correlated with ventral attention network deactivation in SzP only. This relationship is mediated by connectivity of key attentional control components. Results reveal deficits and potential compensation in SzP visual processing/attention.

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