Mid-lateral cerebellar complex spikes encode multiple independent reward-related signals during reinforcement learning

The role of complex spikes in reinforcement learning is still unclear. Here, the authors show that complex spikes carry multiple context based, cell type specific and learning dependent signals that are independent of changes in any motor kinematics and unlikely to instruct the concurrent simple spike activity during reinforcement learning. Although the cerebellum has been implicated in simple reward-based learning recently, the role of complex spikes (CS) and simple spikes (SS), their interaction and their relationship to complex reinforcement learning and decision making is still unclear. Here we show that in a context where a non-human primate learned to make novel visuomotor associations, classifying CS responses based on their SS properties revealed distinct cell-type specific encoding of the probability of failure after the stimulus onset and the non-human primate's decision. In a different context, CS from the same cerebellar area also responded in a cell-type and learning independent manner to the stimulus that signaled the beginning of the trial. Both types of CS signals were independent of changes in any motor kinematics and were unlikely to instruct the concurrent SS activity through an error based mechanism, suggesting the presence of context dependent, flexible, multiple independent channels of neural encoding by CS and SS. This diversity in neural information encoding in the mid-lateral cerebellum, depending on the context and learning state, is well suited to promote exploration and acquisition of wide range of cognitive behaviors that entail flexible stimulus-action-reward relationships but not necessarily motor learning.

Automated summary

The role of complex spikes in reinforcement learning and their interaction with simple spikes remain unclear. This study reveals that complex spikes carry multiple context-based signals independent of motor kinematics and unlikely to guide concurrent simple spike activity through an error-based mechanism. The diverse neural encoding in the cerebellum supports flexible stimulus-action-reward relationships in different contexts and learning states.