The Cost of Social Integration: Distinct Neural Inefficiency in Autistic Children Underlies Symptom Severity

Autism Spectrum Disorder (ASD) is characterized by difficulties in social interaction, as individuals with ASD process social cues like gestures and facial expressions in a unique way. Despite this knowledge, the exact neurophysiological mechanisms driving these differences and their direct impact on clinical symptoms remain unclear. This study delves deeper into understanding the neurophysiological mechanisms involved in social cue integration, moving beyond mere behavioral observations. Specifically, we investigated how autistic children and typically developing (TD) peers process congruent and incongruent social signals in everyday situations. We compared 34 male autistic (2.5-6 years) versus 34 TD children via eye-tracking and functional near-infrared spectroscopy to measure gaze, pupil dilation, and frontal activation during gesture-face integration. TD children exhibited heightened attention to happy faces while maintaining equal attention to neutral faces and gestures when reward gestures were paired. The ASD group did not demonstrate an effective processing strategy. ASD children exhibited heightened pupil dilation and anterior prefrontal cortex (aPFC) activation in all conditions. Crucially, their gaze patterns and aPFC activation significantly correlated with poorer adaptive functioning and positively predicted autism severity. Autistic children go through a distinct, neurologically demanding, and inefficient process to integrate multimodal social cues. This inefficient compensatory attempt results in a metabolically costly physiological state, which is directly connected to the core challenges of ASD. The identified features provide a preliminary proof-of-concept for objective biomarkers, offering quantifiable, physiological indices of severity, thus enabling the development of targeted neurocognitive interventions.