Correlated Coding of Motivation and Outcome of Decision by Dopamine Neurons
Open accessAbstract
We recorded the activity of midbrain dopamine neurons in an instrumental conditioning task in which monkeys made a series of behavioral decisions on the basis of distinct reward expectations. Dopamine neurons responded to the first visual cue that appeared in each trial [conditioned stimulus (CS)] through which monkeys initiated trial for decision while expecting trial-specific reward probability and volume. The magnitude of neuronal responses to the CS was approximately proportional to reward expectations but with considerable discrepancy. In contrast, CS responses appear to represent motivational properties, because their magnitude at trials with identical reward expectation had significant negative correlation with reaction times of the animal after the CS. Dopamine neurons also responded to reinforcers that occurred after behavioral decisions, and the responses precisely encoded positive and negative reward expectation errors (REEs). The gain of coding REEs by spike frequency increased during learning act-outcome contingencies through a few months of task training, whereas coding of motivational properties remained consistent during the learning. We found that the magnitude of CS responses was positively correlated with that of reinforcers, suggesting a modulation of the effectiveness of REEs as a teaching signal by motivation. For instance, rate of learning could be faster when animals are motivated, whereas it could be slower when less motivated, even at identical REEs. Therefore, the dual correlated coding of motivation and REEs suggested the involvement of the dopamine system, both in reinforcement in more elaborate ways than currently proposed and in motivational function in reward-based decision-making and learning.
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These slow changes fail to occur with more-controlled arm, mouth and eye movements in a considerable range of studies.
“these changes fail to occur with more-controlled arm, mouth and eye movements in a considerable range of studies2,5,9,13,151,152,154”
From Dopamine reward prediction-error signalling: A two-component response (2016) · cites this paper as [151]
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.”
From Dopamine reward prediction-error signalling: A two-component response (2016) · cites this paper as [151]
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Self-citation
- Authors
- Satoh, T., Nakai, S., Sato, T., & Kimura, M.
- Affiliations
- Kyoto Prefectural University of Medicine (JP)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2003-10-29
- Volume
- 23
- Issue
- 30
- Pages
- 9913-9923
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6740875
- OpenAlex
- W1515543691
- Cited by
- 298
- References
- 50
- Citations by year
- 2026: 1 · 2025: 4 · 2024: 4 · 2023: 8 · 2022: 6 · 2021: 6 · 2020: 7 · 2019: 7 · 2018: 11 · 2017: 10 · 2016: 13 · 2015: 21 · 2014: 15 · 2013: 13 · 2012: 23
- FWCI
- 5.31
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- dopaminergic neurons, midbrain dopamine system, reward-based decision-making, operant conditioning, reaction time, learning rate, teaching signal
- MeSH terms
- Action Potentials, Animals, Behavior, Animal, Choice Behavior, Conditioning, Operant, Cues, Decision Making, Dopamine, Macaca, Male, Mesencephalon, Motivation, Neurons, Photic Stimulation, Reward
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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