Cortico-Cerebellar neurodynamics during social interaction in Autism Spectrum Disorders

Background: Exploring neural network dynamics during social interaction could help to identify biomarkers of Autism Spectrum Disorders (ASD). A cerebellar involvement in autism has long been suspected and recent methodological advances now enable studying cerebellar functioning in a naturalistic setting. Here, we investigated the electrophysiological activity of the cerebro-cerebellar network during real-time social interaction in ASD. We focused our analysis on theta oscillations (3–8 Hz), which have been associated with large-scale coordination of distant brain areas and might contribute to interoception, motor control, and social event anticipation, all skills known to be altered in ASD. Methods: We combined the Human Dynamic Clamp, a paradigm for studying realistic social interactions using a virtual avatar, with high-density electroencephalography (HD-EEG). Using source reconstruction, we investigated power in the cortex and the cerebellum, along with coherence between the cerebellum and three cerebral-cortical areas, and compared our findings in a sample of participants with ASD (n = 107) and with typical development (TD) (n = 33). We developed an open-source pipeline to analyse neural dynamics at the source level from HD-EEG data. Results: Individuals with ASD showed a significant increase in theta band power over the cerebellum and the frontal and temporal cortices during social interaction compared to resting state, along with significant coherence increases between the cerebellum and the sensorimotor, frontal and parietal cortices. However, a phase-based connectivity measure did not support a strict activity increase in the cortico-cerebellar functional network. We did not find any significant differences between the ASD and the TD group. Conclusions: This exploratory study uncovered increases in the theta band activity of participants with ASD during social interaction, pointing at the presence of neural interactions between the cerebellum and cerebral networks associated with social cognition. It also emphasizes the need for complementary functional connectivity measures to capture network-level alterations. Future work will focus on optimizing artifact correction to include more participants with TD and increase the statistical power of group-level contrasts.