The Cerebellum Contributes to Prediction Error Coding in Reinforcement Learning in Humans

Abstract

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 the 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 behavioral 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.