Adaptive Prediction for Social Contexts: The Cerebellar Contribution to Typical and Atypical Social Behaviors

Abstract

Social interactions involve processes ranging from face recognition to understanding others' intentions. To guide appropriate behavior in a given context, social interactions rely on accurately predicting the outcomes of one's actions and the thoughts of others. Because social interactions are inherently dynamic, these predictions must be continuously adapted. The neural correlates of social processing have largely focused on emotion, mentalizing, and reward networks, without integration of systems involved in prediction. The cerebellum forms predictive models to calibrate movements and adapt them to changing situations, and cerebellar predictive modeling is thought to extend to nonmotor behaviors. Primary cerebellar dysfunction can produce social deficits, and atypical cerebellar structure and function are reported in autism, which is characterized by social communication challenges and atypical predictive processing. We examine the evidence that cerebellar-mediated predictions and adaptation play important roles in social processes and argue that disruptions in these processes contribute to autism.

Keywords: adaptation; autism; cerebellum; implicit; prediction; social.

Figure 1

Cerebellar predictive modeling of social information. Supratentorial networks involved in mirroring, mentalizing, and emotion (based on Kennedy & Adolphs 2012) send context and goal-related information to the cerebellum via mossy fiber inputs. This information routes through the cerebellar circuit to produce internal models of the behavior, which, once trained, provide predictions to the cerebral cortex. These models can be adapted based on reinforcement (blue check mark) or error (blue x) information via plasticity driven by climbing fiber inputs from the inferior olive. These inputs modify the firing of Purkinje cells, altering the signal projecting back to supratentorial regions via the CN. These predictions and adaptations are critical for proper social behaviors, and breakdown of these adaptive prediction models contributes to the core symptoms of autism. Abbreviations: ACC: anterior cingulate cortex; CN, cerebellar nuclei; IFG, inferior frontal gyrus; IPL, inferior parietal lobule; mPFC, medial prefrontal cortex; PCC, posterior cingulate cortex; PreC, precuneus; STS, superior temporal sulcus; ToM, theory of mind; TP, temporal pole; TPJ, temporoparietal junction; vmPFC, ventromedial prefrontal cortex.