The cost of obtaining rewards enhances the reward prediction error signal of midbrain dopamine neurons
Midbrain dopamine neurons are known to encode reward prediction errors (RPE) used to update value predictions. Here, we examine whether RPE signals coded by midbrain dopamine neurons are modulated by the cost paid to obtain rewards, by recording from dopamine neurons in awake behaving monkeys during performance of an effortful saccade task. Dopamine neuron responses to cues predicting reward and to the delivery of rewards were increased after the performance of a costly action compared to a less costly action, suggesting that RPEs are enhanced following the performance of a costly action. At the behavioral level, stimulus-reward associations are learned faster after performing a costly action compared to a less costly action. Thus, information about action cost is processed in the dopamine reward system in a manner that amplifies the following dopamine RPE signal, which in turn promotes more rapid learning under situations of high cost.
Additional Information© 2019 The Author(s). This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/. Received 22 November 2018; Accepted 09 July 2019; Published 15 August 2019. This work was supported by MEXT/JSPS Grants-in-Aid for Scientific Research (Kakenhi) Grant numbers JP16H06571 and JP18H03662 to M.S. This research was partially supported by the Strategic Research Program for Brain Sciences supported by Japan Agency for Medical Research and Development (AMED) and the Japan-U.S. Brain Research Cooperation Program. This research was supported by the National Bio-Resource Project at National Institute of Physiological Science (NBRP at NIPS) from Japan Agency for Medical Research and Development, AMED. We thank Bernard W. Balleine and Andrew R. Delamater for their help on writing the paper. Author Contributions: S.T., J.P.O. and M.S. designed the experiments. S.T. performed the experiments, and analyzed the data. J.P.O. and M.S. refined the experiments and the data analyses. S.T., J.P.O. and M.S. wrote the manuscript. The authors declare no competing interests.
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