Dopamine error signal to actively cope with lack of expected reward

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  • Ishino, Seiya
    Medical Innovation Center/SK Project, Graduate School of Medicine, Kyoto University; Department of Neuroscience, Graduate School of Medicine, Kyoto University; Department of Developmental Physiology, National Institute for Physiological Sciences
  • Kamada, Taisuke
    Medical Innovation Center/SK Project, Graduate School of Medicine, Kyoto University
  • Sarpong, Gideon A.
    Medical Innovation Center/SK Project, Graduate School of Medicine, Kyoto University
  • Kitano, Julia
    Medical Innovation Center/SK Project, Graduate School of Medicine, Kyoto University
  • Tsukasa, Reo
    Medical Innovation Center/SK Project, Graduate School of Medicine, Kyoto University
  • Mukohira, Hisa
    Medical Innovation Center/SK Project, Graduate School of Medicine, Kyoto University
  • Sun, Fangmiao
    State Key Laboratory of Membrane Biology, Peking University School of Life Sciences; Peking-Tsinghua Center for Life Sciences; PKU-IDG/McGovern Institute for Brain Research
  • Li, Yulong
    State Key Laboratory of Membrane Biology, Peking University School of Life Sciences; Peking-Tsinghua Center for Life Sciences; PKU-IDG/McGovern Institute for Brain Research
  • Kobayashi, Kenta
    Section of Viral Vector Development, National Institute for Physiological Sciences; SOKENDAI (The Graduate University for Advanced Studies)
  • Naoki, Honda
    Laboratory of Data-driven Biology, Graduate School of Integrated Sciences for Life, Hiroshima University; Theoretical Biology Research Group, Exploratory Research Center on Life and Living Systems (ExCELLS), National Institutes of Natural Sciences; Laboratory of Theoretical Biology, Graduate School of Biostudies, Kyoto University; Kansei-Brain Informatics Group, Center for Brain, Mind and Kansei Sciences Research (BMK Center), Hiroshima University
  • Oishi, Naoya
    Medical Innovation Center/SK Project, Graduate School of Medicine, Kyoto University
  • Ogawa, Masaaki
    Medical Innovation Center/SK Project, Graduate School of Medicine, Kyoto University; Department of Neuroscience, Graduate School of Medicine, Kyoto University; Department of Developmental Physiology, National Institute for Physiological Sciences

Description

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.

Journal

  • Science Advances

    Science Advances 9 (10), 2023-03

    American Association for the Advancement of Science (AAAS)

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