Cited by 597Neurotransmitter Receptor Influence on BehaviorNeural and Behavioral Psychology StudiesNeural dynamics and brain function

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Dopamine reward prediction error coding

Open access
Schultz, Wolfram·2016·Dialogues in Clinical Neuroscience

Abstract

Reward prediction errors consist of the differences between received and predicted rewards. They are crucial for basic forms of learning about rewards and make us strive for more rewards-an evolutionary beneficial trait. Most dopamine neurons in the midbrain of humans, monkeys, and rodents signal a reward prediction error; they are activated by more reward than predicted (positive prediction error), remain at baseline activity for fully predicted rewards, and show depressed activity with less reward than predicted (negative prediction error). The dopamine signal increases nonlinearly with reward value and codes formal economic utility. Drugs of addiction generate, hijack, and amplify the dopamine reward signal and induce exaggerated, uncontrolled dopamine effects on neuronal plasticity. The striatum, amygdala, and frontal cortex also show reward prediction error coding, but only in subpopulations of neurons. Thus, the important concept of reward prediction errors is implemented in neuronal hardware.

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Crossref · 10.31887/dcns.2016.18.1/wschultz

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Figures

Figure 1. Scheme of learning by prediction error. Red: a prediction error exists when the reward differs from its prediction. Blue: no error exists when the outcome matches the prediction, and the behavior remains unchanged.
Figure 1. Scheme of learning by prediction error. Red: a prediction error exists when the reward differs from its prediction. Blue: no error exists when the outcome matches the prediction, and the behavior remains unchanged.CC BY-NC-ND · PubMed Central
Figure 2. Reward prediction error responses at the time of reward (right) and reward-predicting visual stimuli (left in bottom two graphs). The dopamine neuron is activated by the unpredicted reward eliciting a positive reward prediction error (blue, + error, top), shows no response to the fully predicted reward eliciting no prediction error (0 error, middle), and is depressed by the omission of predicted reward eliciting a negative prediction error (- error, bottom). Reproduced from ref 8: Schultz W, Dayan P, Montague RR. A neural substrate of prediction and reward. Science 1997;275:1593-1599. Copyright © American Association for the Advancement of Science 1997
Figure 2. Reward prediction error responses at the time of reward (right) and reward-predicting visual stimuli (left in bottom two graphs). The dopamine neuron is activated by the unpredicted reward eliciting a positive reward prediction error (blue, + error, top), shows no response to the fully predicted reward eliciting no prediction error (0 error, middle), and is depressed by the omission of predicted reward eliciting a negative prediction error (- error, bottom). Reproduced from ref 8: Schultz W, Dayan P, Montague RR. A neural substrate of prediction and reward. Science 1997;275:1593-1599. Copyright © American Association for the Advancement of Science 1997CC BY-NC-ND · PubMed Central
Figure 3. (A) Stepwise transfer of dopamine response from reward to first reward-predicting stimulus. CS2: earliest reward-predicting stimulus, CS1: subsequent reward-predicting stimulus. From Schultz 12. (B) Reward prediction error responses in sequential stimulus-reward task (gray bars) closely parallel prediction errors of formal temporal difference (TD) reinforcement model (black lines). Averaged population responses of 26 dopamine neurons follow the reward probabilities at each sequence step (numbers indicate reward probabilities in %) and match the time course of TD prediction errors. Reproduced from ref 16: Enomoto K, Matsumoto N, Nakai S, et al. Dopamine neurons learn to encode the long-term value of multiple future rewards. Proc Natl Acad Sci USA. 2011;108:15462-15467. Copyright © National Academy of Sciences 2011
Figure 3. (A) Stepwise transfer of dopamine response from reward to first reward-predicting stimulus. CS2: earliest reward-predicting stimulus, CS1: subsequent reward-predicting stimulus. From Schultz 12. (B) Reward prediction error responses in sequential stimulus-reward task (gray bars) closely parallel prediction errors of formal temporal difference (TD) reinforcement model (black lines). Averaged population responses of 26 dopamine neurons follow the reward probabilities at each sequence step (numbers indicate reward probabilities in %) and match the time course of TD prediction errors. Reproduced from ref 16: Enomoto K, Matsumoto N, Nakai S, et al. Dopamine neurons learn to encode the long-term value of multiple future rewards. Proc Natl Acad Sci USA. 2011;108:15462-15467. Copyright © National Academy of Sciences 2011CC BY-NC-ND · PubMed Central
Figure 4. Schematic of the two phasic dopamine response components. The initial component (blue) detects the event before having identified its value. It increases with sensory impact (physical salience), generalization to rewarded stimuli, reward context and novelty (novelty/surprise salience). The second component (red) codes reward value (as reward utility prediction error). The two components become more distinct with more demanding stimuli. Adapted from data graph in ref 17: Fiorillo CD, Song MR, Yun SR. Multiphasic temporal dynamics in responses of midbrain dopamine neurons to a ppetitive and aversive stimuli. J Neurosci. 2013;33:4710-4725. Copyright © Society for Neuroscience 2013
Figure 4. Schematic of the two phasic dopamine response components. The initial component (blue) detects the event before having identified its value. It increases with sensory impact (physical salience), generalization to rewarded stimuli, reward context and novelty (novelty/surprise salience). The second component (red) codes reward value (as reward utility prediction error). The two components become more distinct with more demanding stimuli. Adapted from data graph in ref 17: Fiorillo CD, Song MR, Yun SR. Multiphasic temporal dynamics in responses of midbrain dopamine neurons to a ppetitive and aversive stimuli. J Neurosci. 2013;33:4710-4725. Copyright © Society for Neuroscience 2013CC BY-NC-ND · PubMed Central
Figure 5. (A) Top: testing risky rewards: an animal chooses between a safe reward whose amount is adjusted by the experimenter (left) and a fixed, binary, equiprobable gamble (right). Height of each bar indicates juice volume; two bars indicate occurrence of each indicated amount with P=0.5 (risky reward). Bottom: Two psychophysical assessments of risk attitude in a monkey. CE indicates amount of safe reward at choice indifference against gamble (certainty equivalent). EV = expected value of gamble. A CE > EV suggests risk seeking (subjective gamble value CE exceeds objective gamble value EV, left), CE < EV indicates risk avoidance (right). (B) Positive utility prediction error responses to unpredicted juice rewards. Red: utility function derived from binary, equiprobable gambles. Black: corresponding, nonlinear increase of population response (n=14 dopamine neurons) in the same animal. A and B reproduced from ref 25: Stauffer WR, Lak A, Schultz W. Dopamine reward prediction error responses reflect marginal utility. Curr Biol. 2014;24:2491-2500. Copyright © Cell Press 2014
Figure 5. (A) Top: testing risky rewards: an animal chooses between a safe reward whose amount is adjusted by the experimenter (left) and a fixed, binary, equiprobable gamble (right). Height of each bar indicates juice volume; two bars indicate occurrence of each indicated amount with P=0.5 (risky reward). Bottom: Two psychophysical assessments of risk attitude in a monkey. CE indicates amount of safe reward at choice indifference against gamble (certainty equivalent). EV = expected value of gamble. A CE > EV suggests risk seeking (subjective gamble value CE exceeds objective gamble value EV, left), CE < EV indicates risk avoidance (right). (B) Positive utility prediction error responses to unpredicted juice rewards. Red: utility function derived from binary, equiprobable gambles. Black: corresponding, nonlinear increase of population response (n=14 dopamine neurons) in the same animal. A and B reproduced from ref 25: Stauffer WR, Lak A, Schultz W. Dopamine reward prediction error responses reflect marginal utility. Curr Biol. 2014;24:2491-2500. Copyright © Cell Press 2014CC BY-NC-ND · PubMed Central

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Citations

Cites

Research works printed but not linked: 3

  1. Pavlov PI., 1927, Conditioned Reflexes. London, UK: Oxford University Press:
  2. Rescorla RA., 1972, Classical Conditioning II: Current Research and Theory. New York, NY: Appleton Century Crofts:, 64
  3. von Neumann J., 1944, The Theory of Games and Economic Behavior. Princeton, NJ: Princeton University Press:

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Metadata

Authors
Schultz, W.
Affiliations
University of Cambridge (GB)
Corresponding author
Schultz, Wolfram
Venue
Dialogues in Clinical Neuroscience
Published
2016-03-31
Volume
18
Issue
1
Pages
23-32
ISSN
  • 1294-8322 (ISSN-L)
  • 1958-5969
OpenAlex
W2419438565
Cited by
597
References
37
Citations by year
2026: 84 · 2025: 83 · 2024: 77 · 2023: 68 · 2022: 64 · 2021: 53 · 2020: 36 · 2019: 62 · 2018: 45 · 2017: 20 · 2016: 4
FWCI
24.37
Type
journal article
Language
en
Open access
Locations
  • Dialogues in Clinical Neuroscience (publishedVersion, cc-by-nc-nd)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
Funders
Wellcome Trust (093875)
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
dopamine, reward prediction error, midbrain dopaminergic neurons, reward learning, drug addiction, neuroplasticity, striatum, amygdala, frontal cortex
MeSH terms
Animals, Brain, Dopamine, Forecasting, Humans, Learning, Nerve Net, Neuronal Plasticity, Reward

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