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Midbrain Dopamine Neurons Signal Belief in Choice Accuracy during a Perceptual Decision
Open accessAbstract
Central to the organization of behavior is the ability to predict the values of outcomes to guide choices. The accuracy of such predictions is honed by a teaching signal that indicates how incorrect a prediction was ("reward prediction error," RPE). In several reinforcement learning contexts, such as Pavlovian conditioning and decisions guided by reward history, this RPE signal is provided by midbrain dopamine neurons. In many situations, however, the stimuli predictive of outcomes are perceptually ambiguous. Perceptual uncertainty is known to influence choices, but it has been unclear whether or how dopamine neurons factor it into their teaching signal. To cope with uncertainty, we extended a reinforcement learning model with a belief state about the perceptually ambiguous stimulus; this model generates an estimate of the probability of choice correctness, termed decision confidence. We show that dopamine responses in monkeys performing a perceptually ambiguous decision task comply with the model's predictions. Consequently, dopamine responses did not simply reflect a stimulus' average expected reward value but were predictive of the trial-to-trial fluctuations in perceptual accuracy. These confidence-dependent dopamine responses emerged prior to monkeys' choice initiation, raising the possibility that dopamine impacts impending decisions, in addition to encoding a post-decision teaching signal. Finally, by manipulating reward size, we found that dopamine neurons reflect both the upcoming reward size and the confidence in achieving it. Together, our results show that dopamine responses convey teaching signals that are also appropriate for perceptual decisions.
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“Previous experimental work has shown that the phasic activity of midbrain dopamine neurons resembles the RPEs of TD learning in partially observable environments, where TD learning is performed on belief states rather than observations [6][7][8][9][10][11].”
From Emergence of belief-like representations through reinforcement learning (2023) · cites this paper as [8]
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Lak, A., Okun, M., Moss, M. M., Gurnani, H., Farrell, K., Wells, M. J., Reddy, C. B., Kepecs, Á., Harris, K. D., & Carandini, M. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/411413 · Cited by 9
Self-citationStriatal Dopamine Represents Valence on Dynamic Regional Scales
Bornhoft, K. N., Prohofsky, J., O’Neal, T. J., Wolff, A. R., & Saunders, B. T. (2025) · Journal of Neuroscience · doi:10.1523/jneurosci.1551-24.2025 · Cited by 11
Dopamine neurons encode trial-by-trial subjective reward value in an auction-like task
Hill, D. F., Hickman, R. W., Al-Mohammad, A., Stasiak, A., & Schultz, W. (2024) · Nature Communications · doi:10.1038/s41467-024-52311-8 · Cited by 9
Single-Neuron Correlates of Decision Confidence in the Human Medial Temporal Lobe
Unruh-Pinheiro, A., Hill, M. R., Weber, B., Boström, J. P., Elger, C. E., & Mormann, F. (2020) · Current Biology · doi:10.1016/j.cub.2020.09.021 · Cited by 8
Lee, H.-J., Lee, H., Lim, C. Y., Rhim, I., & Lee, S. (2023) · PLoS Biology · doi:10.1371/journal.pbio.3002373 · Cited by 8
de Gee, J. W., Corrêa, C. M. C., Weaver, M., Donner, T. H., & van Gaal, S. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.06.25.164962 · Cited by 7
Metadata
- Authors
- Lak, A., Nomoto, K., Keramati, M., Sakagami, M., & Kepecs, A.
- Affiliations
- Cold Spring Harbor Laboratory (US)
- Tamagawa University (JP)
- Gatsby Computational Neuroscience Unit (GB)
- Venue
- Current Biology
- Publisher
- Elsevier BV
- Published
- 2017-03
- Volume
- 27
- Issue
- 6
- Pages
- 821-832
- ISSN
- 0960-9822 (ISSN-L)
- PMC
- PMC5819757
- OpenAlex
- W2592093412
- Cited by
- 170
- References
- 52
- Citations by year
- 2026: 14 · 2025: 16 · 2024: 22 · 2023: 19 · 2022: 9 · 2021: 16 · 2020: 24 · 2019: 22 · 2018: 20 · 2017: 8
- FWCI
- 9.90
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Current Biology (publishedVersion)
- PubMed (publishedVersion)
- City Research Online (City University London) (acceptedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Cold Spring Harbor Laboratory Institutional Repository (Cold Spring Harbor Laboratory) (acceptedVersion)
- UCL Discovery (University College London) (submittedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- Funders
- Sir Henry Wellcome Trust Postdoctoral Fellowship (106101/Z/14/Z)
- Swartz Foundation
- National Institute of Mental Health (NIH) (R01MH097061)
- 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
- midbrain dopaminergic neurons, reward prediction error, perceptual decision making, perceptual uncertainty, decision confidence, belief states, reinforcement learning models, perceptual ambiguity, reward magnitude, teaching signal, choice accuracy
- MeSH terms
- Animals, Choice Behavior, Decision Making, Dopamine, Macaca, Male, Mesencephalon, Perception, Reinforcement, Psychology, Reward, Models, Animal, Dopaminergic Neurons
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