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The Role of the Cerebellum in Learning to Predict Reward: Evidence from Cerebellar Ataxia

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Abstract

Recent findings in animals have challenged the traditional view of the cerebellum solely as the site of motor control, suggesting that the cerebellum may also be important for learning to predict reward from trial-and-error feedback. Yet, evidence for the role of the cerebellum in reward learning in humans is lacking. Moreover, open questions remain about which specific aspects of reward learning the cerebellum may contribute to. Here we address this gap through an investigation of multiple forms of reward learning in individuals with cerebellum dysfunction, represented by cerebellar ataxia cases. Nineteen participants with cerebellar ataxia and 57 age- and sex-matched healthy controls completed two separate tasks that required learning about reward contingencies from trial-and-error. To probe the selectivity of reward learning processes, the tasks differed in their underlying structure: while one task measured incremental reward learning ability alone, the other allowed participants to use an alternative learning strategy based on episodic memory alongside incremental reward learning. We found that individuals with cerebellar ataxia were profoundly impaired at reward learning from trial-and-error feedback on both tasks, but retained the ability to learn to predict reward based on episodic memory. These findings provide evidence from humans for a specific and necessary role for the cerebellum in incremental learning of reward associations based on reinforcement. More broadly, the findings suggest that alongside its role in motor learning, the cerebellum likely operates in concert with the basal ganglia to support reinforcement learning from reward.

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Data Availability

All code used to analyze the data in this study may be found here: https://github.com/boomsbloom/ataxia-rl. Data is available upon request from the corresponding authors.

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Funding

J.N. was supported by the NSF Graduate Research Fellowship (1644869). S.H.K. was supported by NINDS R01NS104423, NINDS R01 NS118179, NINDS R01 NS124854, and National Ataxia Foundation. D.S. was supported by an NSF CRCNS award (1822619), NIMH R01 MH121093 and the Kavli Foundation.

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Authors

Contributions

J.N., C.R.L., L.M.K., M.K.P., S.K., and D.S. designed the study. C.A., N.D., and C.R.L. collected data from cerebellar ataxia participants. J.N. collected data from healthy control participants. J.N. analyzed the data and prepared all figures. J.N. and C.A. wrote the main manuscript text. All authors reviewed the manuscript.

Corresponding authors

Correspondence to Sheng-Han Kuo or Daphna Shohamy.

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Informed consent from all participants in the study was obtained with approval from the Columbia University Institutional Review Board.

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Nicholas, J., Amlang, C., Lin, CY.R. et al. The Role of the Cerebellum in Learning to Predict Reward: Evidence from Cerebellar Ataxia. Cerebellum (2023). https://doi.org/10.1007/s12311-023-01633-2

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