THE CEREBELLAR CONTRIBUTION TO SOCIAL PREDICTION AND LEARNING IN AUTISM

Atypical social communication is a core feature of Autism Spectrum Disorder, yet its neural bases remain unclear. The cerebellum is one candidate region: structural and functional differences are well-characterized in autism, mentalizing tasks engage right cerebellar lobule VII, and grey matter reductions within this region in autism correlate with core symptoms. We hypothesized that atypical cerebellar function in autism may impact the acquisition of social information and formation of internal predictive models, and that cerebellar neuromodulation may alter performance and neural activation patterns on a social learning task. We used cerebellar transcranial direct current stimulation (tDCS) with and without concurrent neuroimaging (functional MRI [fMRI]) to investigate the impact of cerebellar neuromodulation on behavioral performance and neural activation patterns during a social ball toss game (Cyberball), whereby participants implicitly learned patterns of social reciprocity to improve performance. Neurotypical adults (NT; Study 1, n=25; Study 2, n=16) and age-matched adults with autism (AG; Study 3, n=10) played Cyberball after 20min of excitatory (anodal), inhibitory (cathodal), or sham tDCS targeting right lobule VII. Participants completed three sessions (tDCS order counterbalanced), separated by one week. Task and resting state fMRI data were acquired and analyzed in Studies 1 and 2. Learning scores were computed as the proportion of tosses to the good versus bad reciprocal player. The effects of tDCS condition, session, task stage, and group on learning scores and median response times were assessed using linear mixed effects models. NT and AG groups showed significant learning during Cyberball, though higher autism symptom scores were associated with less learning. Better learning was associated with higher cerebellar engagement in the NT group, but the AG showed reduced cerebellar activation during the task. In NT participants, active cerebellar tDCS disrupted social learning. Social learning improved and cerebellar activation increased in the AG following cathodal tDCS. Functional connectivity patterns were disrupted in AG following anodal tDCS and normalized in AG following cathodal tDCS. These results suggest that the cerebellum is involved in social learning and that cerebellar neuromodulation may impact social behaviors in autism through increasing activation in cerebellar regions that promote successful task performance.