Probing Visual Correlates of Excitatory/Inhibitory Imbalance Using EEG: A Transdiagnostic Study in ASD and Schizophrenia

Background: Excitatory/inhibitory imbalance is a mechanistic theory posited to explain dysfunction in both autism spectrum disorder (ASD) and schizophrenia (SCZ). In visual cortex, excitatory/inhibitory balance underlies surround suppression effects, in which neural response to a central stimulus is suppressed when it is surrounded by parallel stimuli but facilitated when it is surrounded by perpendicular stimuli. By assessing suppression of neural response in the context of parallel vs. perpendicular surround, this study provides a direct probe of the excitatory/inhibitory imbalance hypothesis across disorders.

Objectives: This study aimed to (i) evaluate an event related potentials (ERP) index of surround suppression in adults with ASD and schizophrenia and (ii) examine transdiagnostic associations between neural response and social and perceptual difficulties.

Methods: Participants included 14 adults with ASD and 12 with SCZ. EEG data was recorded using a 128-channel sensor net. Participants observed vertical sinusoidal gratings filling a central annulus, either alone, surrounded by gratings that were perpendicular, or surrounded by parallel gratings (Fig.1). With intact surround suppression, attenuated ERP amplitudes are expected to parallel vs. perpendicular surround. To maintain attention, participants pressed a button when a central fixation turned green; these trials were discarded from analysis. EEG data was preprocessed off-line, and the P50 and N1 components were extracted over occipital scalp (Oz). Participants completed the Social Responsiveness Scale (SRS), Schizotypal Personality Questionnaire (SPQ), and Sensory Gating Inventory (SGI). Between-group differences were examined with repeated measures ANOVAs (DVs: P50 and N1 mean amplitude, 40-60ms and 75-125ms after stimulus onset, respectively). Transdiagnostic associations between neural response to perpendicular versus parallel surround and self-report of social and perceptual difficulties were explored with bivariate correlations.

Results: For the P50, there was a significant main effect of Group (F=4.41, p=.046) such that P50 amplitude was attenuated in ASD vs. SCZ across conditions. There was no main effect of Condition and no Condition by Group interaction (ps>.26), indicating that neither group showed significant suppression of the P50 response with parallel surround (Fig.2). For the N1, there was a marginally significant main effect of Condition (F=4.04, p=.056), wherein N1 amplitude was attenuated to parallel vs. perpendicular surround across groups; however, there was no significant interaction or main effect of Group (ps>.26). Across ASD and SCZ, suppression of N1 response was not associated with self-report of ASD symptoms on the SRS. However, reduced N1 suppression was associated with greater levels of symptoms on the SPQ ideas of reference scale (r=-.688, p=.04). Stronger N1 suppression was associated with greater fatigue and stress vulnerability with sensory input on the SGI (r=.578, p=.039).

Conclusions: Here, we show evidence for surround suppression in both ASD and SCZ in the N1 response to parallel versus perpendicular surround that does not differ by diagnostic category. Instead, strength of suppression mechanisms related to perceptual delusional beliefs and behavioral experience with sensory stimuli, transdiagnostically. These findings support a dimensional (RDoC) approach to understanding the extent and impact of excitatory/inhibitory imbalance in ASD and related disorders.