The cerebellum contributes to prediction error coding in reinforcement learning in humans

Recent rodent data suggest that the cerebellum – a region typically associated with processing sensory prediction errors (PEs) – also processes PEs in reinforcement learning (RL-PEs; i.e., learning from action outcomes). We tested whether cerebellar output is necessary for RL-PE processing in regions more traditionally associated with action-outcome processing, such as striatum and anterior cingulate cortex. The feedback-related negativity (FRN) was measured as a proxy of cerebral RL-PE processing in a probabilistic feedback learning task using electroencephalography. Two complementary experiments were performed in humans. First, patients with chronic cerebellar stroke (20 male, 6 female) and matched healthy controls (19 male, 7 female) were tested. Second, single-pulse cerebellar transcranial magnetic stimulation (TMS) was applied in healthy participants (7 male, 17 female), thus implementing a virtual lesion approach. Consistent with previous studies, learning of action-outcome associations was intact with only minor changes in behavioural flexibility. Importantly, no significant RL-PE processing was observed in the FRN in patients with cerebellar stroke, and in participants receiving cerebellar TMS. Findings in both experiments show that RL-PE processing in the forebrain depends on cerebellar output in humans, complementing and extending previous findings in rodents. Significance statement While processing of prediction errors in reinforcement learning (RL-PEs) is usually attributed to midbrain and forebrain, recent rodent studies have recorded RL-PE signals in the cerebellum. It is not yet clear whether these cerebellar RL-PE signals contribute to RL-PE processing in the forebrain/midbrain. In the current study, we could show that forebrain RL-PE coding is blunted when the cerebellum is affected across two complementary lesion models (patients with cerebellar stroke, cerebellar TMS). Our results support direct involvement of the cerebellum in RL-PE processing. We can further show that the cerebellum is necessary for RL-PE coding in the forebrain.