Cited by 83Neurotransmitter Receptor Influence on BehaviorNeural and Behavioral Psychology StudiesReinforcement Learning in Robotics

Dopamine neurons learn to encode the long-term value of multiple future rewards

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Enomoto, Kazuki, Matsumoto, Naoyuki, Nakai, Sadamu, Satoh, Takemasa, Sato, Tatsuo K., Ueda, Yasumasa, Inokawa, Hitoshi, Haruno, Masahiko +1 more·2011·Proceedings of the National Academy of Sciences

Abstract

Midbrain dopamine neurons signal reward value, their prediction error, and the salience of events. If they play a critical role in achieving specific distant goals, long-term future rewards should also be encoded as suggested in reinforcement learning theories. Here, we address this experimentally untested issue. We recorded 185 dopamine neurons in three monkeys that performed a multistep choice task in which they explored a reward target among alternatives and then exploited that knowledge to receive one or two additional rewards by choosing the same target in a set of subsequent trials. An analysis of anticipatory licking for reward water indicated that the monkeys did not anticipate an immediately expected reward in individual trials; rather, they anticipated the sum of immediate and multiple future rewards. In accordance with this behavioral observation, the dopamine responses to the start cues and reinforcer beeps reflected the expected values of the multiple future rewards and their errors, respectively. More specifically, when monkeys learned the multistep choice task over the course of several weeks, the responses of dopamine neurons encoded the sum of the immediate and expected multiple future rewards. The dopamine responses were quantitatively predicted by theoretical descriptions of the value function with time discounting in reinforcement learning. These findings demonstrate that dopamine neurons learn to encode the long-term value of multiple future rewards with distant rewards discounted.

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  • Dopamine responses in elaborate tasks constitute standard reward prediction-error signals.

    “However, on closer inspection, dopamine responses in such elaborate tasks constitute standard reward prediction-error signals2,33,59,66,69,75,151–153.”

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Authors
Enomoto, K., Matsumoto, N., Nakai, S., Satoh, T., Sato, T. K., Ueda, Y., Inokawa, H., Haruno, M., & Kimura, M.
Affiliations
  • Tamagawa University (JP)
  • Prefectural University of Kumamoto (JP)
  • Tokyo University of Science (JP)
  • Kyoto Prefectural University of Medicine (JP)
Venue
Proceedings of the National Academy of Sciences
Published
2011-08-30
Volume
108
Issue
37
Pages
15462-15467
ISSN
  • 0027-8424 (ISSN-L)
  • 1091-6490
OpenAlex
W2003565109
Cited by
83
References
39
Citations by year
2026: 2 · 2025: 6 · 2024: 2 · 2023: 1 · 2022: 1 · 2021: 2 · 2020: 9 · 2019: 4 · 2018: 6 · 2017: 10 · 2016: 10 · 2015: 8 · 2014: 8 · 2013: 7 · 2012: 5
FWCI
2.78
Type
journal article
Language
en
Open access
Locations
  • Proceedings of the National Academy of Sciences (publishedVersion)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • UCL Discovery (University College London) (submittedVersion)
Funders
Japan Society for the Promotion of Science (23700503)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
  • Physical Sciences › Computer Science › Artificial Intelligence › Reinforcement Learning in Robotics
Keywords
dopaminergic neurons, delay discounting, reinforcement learning, prediction error, value function, reward anticipation, midbrain dopamine
MeSH terms
Animals, Haplorhini, Behavior, Animal, Dopamine, Learning, Neurons, Reward, Time Factors, Anticipation, Psychological

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