What you see is what you get: visual scanning failures of naturalistic social scenes in schizophrenia

Abstract

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.

The road not taken: disconnection of a human-unique cortical pathway in schizophrenia and its effects on naturalistic social cognition

“…Demographically, SzP were matched to HC, with a small increase in mean(sd) age (39.8(10.8) vs. 34.9(9.6), p=.03) in SzP (see Table 1 ). As shown previously in a sub-sample of these participants (11), SzP were more impaired in TASIT Sarcasm versus TASIT Lie performance and on the Processing Speed Index. Other demographics and SzP characteristics are in Table 1 .…”

“…These results complement those reported in previous studies from our group (8,11) from overlapping samples and demonstrate several previously unreported organizational principles and relationships; therefore, the results will need to be replicated in an independent sample. Larger samples will also allow for the study of how intervening levels of analysis (task activation, low-level behaviors) mediate the relationship between resting-state functional connectivity and high-level behaviors linked to symptoms.…”

“…These observations suggest that in SzP the more visual information enters the theory-of-mind network through prefrontal cortex, the more “normal” the activity is in the theory-of-mind areas such as TPJp. However, the visual strategy enacted by use of the PFC pathway could also result in differences in the relationship between visual scanning and theory-of-mind operations, as we observed recently (11).…”

“…First, in Patel et al 2021 (8), we observed that in SzP the TPJ was less synchronized with visual and dorsal attention areas but more synchronized with prefrontal theory-of-mind and cognitive control areas than in HC, suggesting that the disconnection from visual processing areas had resulted in increased communication with prefrontal areas. Second, we observed that in SzP (but not HC) only the Processing Speed Index (PSI) from the WAIS-III IQ test strongly predicted TASIT performance (11). The tasks that compose the PSI all involve some degree of top-down driven visual search which is guided by dorsolateral prefrontal cortex, the same areas that correlate with TPJp performance in this manuscript.…”

“…In a subsequent study (8), we used a naturalistic visual stimulus—a 15-minute clip from the movie “The Good, the Bad, and the Ugly” with the soundtrack removed—to show that in schizophrenia the TPJ-pSTS pathway appeared to be functionally “disconnected”, in that it did not appropriately respond to visual motion inputs, communicate with other visual processing and attention areas, and was not appropriately involved in a key output behavior, saccades. Activation of the TPJ-pSTS was also correlated with performance on a naturalistic test of social cognition, The Awareness of Social Inference Test (TASIT) (10), which we had previously linked to the ability to orient attention/gaze to moving facial expressions in peripheral vision (11).…”