Dopamine error signal to actively cope with lack of expected reward

Author:

Ishino Seiya123ORCID,Kamada Taisuke1ORCID,Sarpong Gideon A.1ORCID,Kitano Julia1,Tsukasa Reo1,Mukohira Hisa1ORCID,Sun Fangmiao456,Li Yulong456ORCID,Kobayashi Kenta78ORCID,Naoki Honda9101112ORCID,Oishi Naoya1ORCID,Ogawa Masaaki123ORCID

Affiliation:

1. Medical Innovation Center/SK Project, Graduate School of Medicine, Kyoto University, Kyoto 606-8507, Japan.

2. Department of Neuroscience, Graduate School of Medicine, Kyoto University, Kyoto 606-8501, Japan.

3. Department of Developmental Physiology, National Institute for Physiological Sciences, Okazaki, Aichi 444-8585, Japan.

4. State Key Laboratory of Membrane Biology, Peking University School of Life Sciences, Beijing 100871, China.

5. Peking-Tsinghua Center for Life Sciences, Beijing 100871, China.

6. PKU-IDG/McGovern Institute for Brain Research, Beijing 100871, China.

7. Section of Viral Vector Development, National Institute for Physiological Sciences, Okazaki, Aichi 444-8585, Japan.

8. SOKENDAI (The Graduate University for Advanced Studies), Okazaki, Aichi 444-8585, Japan.

9. Laboratory of Data-driven Biology, Graduate School of Integrated Sciences for Life, Hiroshima University, Higashi-Hiroshima, Hiroshima 739-8526, Japan.

10. Theoretical Biology Research Group, Exploratory Research Center on Life and Living Systems (ExCELLS), National Institutes of Natural Sciences, Okazaki, Aichi 444-8787, Japan.

11. Laboratory of Theoretical Biology, Graduate School of Biostudies, Kyoto University, Kyoto 606-8315, Japan.

12. Kansei-Brain Informatics Group, Center for Brain, Mind and Kansei Sciences Research (BMK Center), Hiroshima University, Kasumi, Minami-ku, Hiroshima 734-8551, Japan.

Abstract

To obtain more of a particular uncertain reward, animals must learn to actively overcome the lack of reward and adjust behavior to obtain it again. The neural mechanisms underlying such coping with reward omission remain unclear. Here, we developed a task in rats to monitor active behavioral switch toward the next reward after no reward. We found that some dopamine neurons in the ventral tegmental area exhibited increased responses to unexpected reward omission and decreased responses to unexpected reward, following the opposite responses of the well-known dopamine neurons that signal reward prediction error (RPE). The dopamine increase reflected in the nucleus accumbens correlated with behavioral adjustment to actively overcome unexpected no reward. We propose that these responses signal error to actively cope with lack of expected reward. The dopamine error signal thus cooperates with the RPE signal, enabling adaptive and robust pursuit of uncertain reward to ultimately obtain more reward.

Publisher

American Association for the Advancement of Science (AAAS)

Subject

Multidisciplinary

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