Beyond single-person paradigms: N400 alterations in a social context in schizophrenia

Impairments in social cognition and context-dependent information processing constitute prominent features of schizophrenia. Among event-related potentials (ERPs), the N400 is known to be sensitive to semantic and social contextual information. However, its role in social contexts has received limited attention in schizophrenia research, as previous studies have largely examined the N400 in isolated, single-person paradigms or have focused on the P300 component.

In this study, we examined the N400 ERP component in a real-world social context using EEG hyperscanning. Patients with schizophrenia (SZ; N = 34) and healthy controls (HC; N = 48) performed an actor-observer Go/NoGo task in pairs using the International Affective Picture System (IAPS) with emotionally valenced and neutral images. The task was repeated, with participants switching roles, and analyses were restricted to the actor condition at fronto-central electrodes. Clinical symptoms were assessed using the Positive and Negative Syndrome Scale (PANSS). Although our analysis focused on the N400, we also examined the P300 amplitude, given the functional relationship between these components during information processing.

Primary analysis revealed significantly reduced N400 amplitudes in patients with schizophrenia compared with healthy controls, both across all stimuli and specifically in response to negative and positive stimuli. With second stimulus exposure, N400 amplitudes remained stable in healthy controls but showed a significant decline in the schizophrenia group. During the second exposure, higher PANSS total scores and higher scores on the negative and general psychopathology subscales were significantly associated with attenuated N400 amplitudes, whereas lower levels of psychopathology were associated with a polarity reversal. Secondary analyses revealed significantly reduced P300 amplitudes in patients with schizophrenia for positive stimuli and for all stimulus-valences combined. With second exposure, P300 amplitudes increased in the schizophrenia group, whereas they decreased in healthy controls.

The observed alterations in N400 responses indicate that impairments in context-dependent affective information processing in schizophrenia extend to social context. Alterations in the P300 component may further reflect deficits in cognitive control and response inhibition. Collectively, these findings suggest a dysfunction in neural processes responsible for monitoring and resolving mismatches between internal predictions and social contexts.