A neuronal marker of eye contact spontaneously activated in neurotypical subjects but not in autistic spectrum disorders

Abstract

Attention to faces and eye contact are key behaviors for establishing social bonds in humans. In Autism Spectrum Disorders (ASD), a disturbance in neurodevelopment, impaired face processing and gaze avoidance are key clinical features for ASD diagnosis. The biological alterations underlying these impairments are not yet clearly established. Using high-density electroencephalography coupled with multi-variate pattern classification and group blind source separation methods we searched for face- and-face components-related neural signals that could best discriminate visual processing of neurotypical subjects (N = 38) from ASD participants (N = 27). We isolated a face-specific neural signal in the superior temporal sulcus peaking at 240 msec after face-stimulus onset. A machine learning algorithm applied on the extracted neural component reached 74% decoding accuracy at the same latencies, discriminating the neurotypical population from ASD subjects in whom this signal was weak. By manipulating attention on different parts of the face, we also found that the power of the evoked signal in neurotypical subjects varied depending on the region observed: it was strong when the eye region fell on the fovea to decrease on regions further away and outside the stimulus face. Such face and face-components selective neural modulations were not found in ASD, although they did show typical early face-related P100 and N170 signals. These results show that specialized cortical mechanisms for face perception show higher responses for eyes when attention is focused on gaze and that these mechanisms may be particularly affected in autism spectrum disorders.