Opposite sides of different coins: near-diametrical opposition of physiological indices of reduced accuracy of face emotion recognition in schizophrenia and autism spectrum disorders

Background: Schizophrenia (Sz) and autism spectrum disorder (ASD) are associated with reduced accuracy offace emotion recognition (FER). Nevertheless, the underlying pathophysiological mechanisms may diverge, potentially related to differential processing patterns within the early visual system. Here, we investigated physiological-level responses to emotional faces. We hypothesized that Sz and ASD would be associated with convergent behavioral performance, but divergent pathophysiological mechanisms. Study design: Simultaneous eye-tracking and continuous EEG data were obtained from 23 adults diagnosed with schizophrenia (Sz), 21 autistic adults, and 24 neurotypical controls (NC) in response to intact and chimeric emotion faces. Event-related potentials (ERP) were calculated from the ongoing EEG data using time- and time-frequency (TF) domain approaches. Symptoms were rated using the Positive and Negative Symptom Scale (PANSS) and the Autism Diagnostic Observation Schedule, Second Edition (ADOS-2) in Sz and ASD, respectively. Study results: As predicted, Sz and ASD were associated with similar levels of reduced FER accuracy relative to NC, but differential patterns of eye tracking and EEG-related activity. Rates of eye- vs. mouth-fixations were reduced across groups but did not correlate with FER. Nevertheless, the ability to utilize eye-information diverged across groups. Thus, when viewing chimeric faces, Sz was associated with reduced tendency to utilize eye information and increased tendency to utilize mouth information even when fixation location was considered. In TF analyses, reduced FER accuracy was associated with reduced initial sensory responses in Sz, as reflected in the theta-band time-frequency response. In contrast, in ASD, reduced FER accuracy was associated with increased alpha-frequency event-related desynchronization (alpha-ERD) consistent with hyper-engagement of secondary visual regions (V2). A combination of physiological and eye-tracking measures differentiated schizophrenia and ASD with >90% accuracy. V2 hyper-engagement in ASD correlated with both reduced FER accuracy and ADOS Social Interaction domain scores. Conclusion: Schizophrenia and ASD are associated with divergent physiological-level alterations within the early visual system during emotional face processing, supporting models of magnocellular visual hypoactivity in schizophrenia but retinotectal visual hyperactivity leading to hyper-engagement of non-face regions (V2) by face stimuli in ASD. These alterations, in turn, may serve as targets for future intervention studies related to social cognition.