Abstract
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.
Highlights
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
Recent evidence suggest that cerebellar activity is correlated with aspects of behavior that do not involve correcting the kinematics of movement: for example classical conditioning[11], stimulus prediction[12,13], and the magnitude of predicted reward[14,15]
After a fixed duration (800 ms), one of the two symbols briefly appeared on the screen and they released the hand associated with that symbol, as soon as possible, with a welllearned stereotypic hand movement to earn a liquid reward (Fig. 1a)
Summary
Two non-human primates performed a two-alternative forcedchoice discrimination task where, in each session, they associated one of two visual symbols with a left-hand movement and the other visual symbol with a right-hand movement[17]. They grabbed the two bars, each with one hand to initiate the trial. We presented them with two novel symbols that they learned to associate with specific choices (hand releases), through trial and error They typically achieved criterion for learning (see Methods) in ~50–70 trials on an average through an adaptive learning mechanism (Fig. 1b). The mid-lateral cerebellar P-cell SS encode a reinforcement error signal when animals learn a new visuomotor association, by reporting the outcome of the most recent decision in short epochs called “delta epochs” in a manner entirely a fixed interval fixed interval
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