The DOI matches its Crossref record; 24 of the 24 references it cites were found in a registry or an index.
Adaptive Coding of Reward Value by Dopamine Neurons
Abstract
It is important for animals to estimate the value of rewards as accurately as possible. Because the number of potential reward values is very large, it is necessary that the brain's limited resources be allocated so as to discriminate better among more likely reward outcomes at the expense of less likely outcomes. We found that midbrain dopamine neurons rapidly adapted to the information provided by reward-predicting stimuli. Responses shifted relative to the expected reward value, and the gain adjusted to the variance of reward value. In this way, dopamine neurons maintained their reward sensitivity over a large range of reward values.
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In the citing paper
“Neurons in MBD nuclei are believed to encode reward prediction errors (RPEs).45”
From Two prefrontal-subcortical circuits estimate controllability and reflect its impact on learning (2026) · cites this paper as [45]
In the citing paper
“As is the case for dopamine neurons, 46 reward-related BOLD signals should maintain their sensitivity over a large range of reward values.”
From Increased neural responses to reward in adolescents and young adults with attention-deficit/hyperactivity disorder and their unaffected siblings (2015) · cites this paper as [46]
In the citing paper
“Indeed, reward-related responses adapt to the context in which a reward is presented 46, in the sense that they depend on a combination of the overall expected value and their variance rather than the absolute magnitude of reward value.”
From Increased neural responses to reward in adolescents and young adults with attention-deficit/hyperactivity disorder and their unaffected siblings (2015) · cites this paper as [46]
In the citing paper
“Yet, both reward magnitude and reward probability are coded relatively rather than absolutely. 46”
From Increased neural responses to reward in adolescents and young adults with attention-deficit/hyperactivity disorder and their unaffected siblings (2015) · cites this paper as [46]
In the citing paper
“Activity in individual neurons in both habenula and VTA reflects both the value of a stimulus in terms of the reward that it predicts58–60 as well as VoI21,22,27,61”
From Interpretable abstractions of artificial neural networks predict behavior and neural activity during human information gathering (2026) · cites this paper as [59]
In the citing paper
“For example, the gain of RPE signals produced by dopamine neurons in the ventral tegmental area is modulated by the variance of reward value.100,101”
From Serotonin neurons modulate learning rate through uncertainty (2022) · cites this paper as [101]
In the citing paper
“Consistent with a prediction error signal, spiking activity of dopamine neurons increases with both reward magnitude and probability (Fiorillo et al., 2003; Tobler et al., 2005; Roesch et al., 2007).”
From Decision Making in Recurrent Neuronal Circuits (2008) · cites this paper as Tobler et al., 2005
In the citing paper
“Research in non-human primates, confirmed in humans, indicates that differences the probability with which a cue predicts a reward produce a quantitative change in the engagement of dopaminergic systems.46,47”
From Striatal sensitivity during reward processing in attention-deficit/hyperactivity disorder (2012) · cites this paper as [46]
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“gic midbrain (Tobler et al., 2005), prefrontal cortex (Wa-”
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BackgroundBehavioral specifications of reward-associated long-term memory enhancement in humans
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“This experiment closely followed one conducted in nonhuman primates which showed that activity in dopaminergic circuitry did not signal the absolute prediction error but rather an adaptively scaled, binary version of it in terms of “better” or “worse” of two possible outcomes (Tobler et al. 2005).”
InfluentialDifferential mechanisms underlie trace and delay conditioning in Drosophila
Grover, D., Chen, J., Xie, J. L., Li, J., Changeux, J., & Greenspan, R. J. (2022) · Nature · doi:10.1038/s41586-022-04433-6 · Cited by 63
Perspectives on adaptive dynamical systems
Sawicki, J., Berner, R., Loos, S. A. M., Anvari, M., Bader, R., Barfuß, W., Botta, N., Brede, N., Franović, I., Gauthier, D. J., et al. (2023) · Chaos An Interdisciplinary Journal of Nonlinear Science · doi:10.1063/5.0147231 · Cited by 72
Theoretical and Empirical Studies of Learning
Niv, Y., & Montague, P. R. (2009) · Elsevier eBooks · doi:10.1016/b978-0-12-374176-9.00022-1 · Cited by 65
Isolating the delay component of impulsive choice in adolescent rats
McClure, J., Podos, J., & Richardson, H. N. (2014) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2014.00003 · Cited by 62
Pattern of dopamine signaling during aversive events predicts active avoidance learning
Stelly, C. E., Haug, G. C., Fonzi, K. M., Garcia, M. A., Tritley, S. C., Magnon, A. P., Ramos, M. A. P., & Wanat, M. J. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1904249116 · Cited by 63
Sohn, J.-W., & Lee, D. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.2982-07.2007 · Cited by 64
“Signals related to the im- mediacy, probability, and magnitude of reward are broadly distributed in many brain areas (Platt and Glimcher, 1999; Roesch and Olson, 2003, 2005a,b; Sugrue et al., 2004; Tobler et al., 2005; Tsujimoto and Sawaguchi, 2005).”
BackgroundNeuroeconomics: what have we found, and what should we search for
Rustichini, A. (2009) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2009.09.012 · Cited by 65
Neurobiology of placebo effects: expectations or learning?
Peciña, M., Stohler, C. S., & Zubieta, J.-K. (2013) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nst079 · Cited by 67
“Consistently with the role of DA in prediction error signal (Schultz, 1998; Fiorillo et al., 2003; Tobler et al., 2005; Fiorillo et al., 2008), we have previously shown that the introduction of a placebo during pain anticipation was associated with the activation of DA neurotransmission and D2/D3…”
Multiple timescales of normalized value coding underlie adaptive choice behavior
Zimmermann, J., Glimcher, P. W., & Louie, K. (2018) · Nature Communications · doi:10.1038/s41467-018-05507-8 · Cited by 60
A neuronal mechanism underlying decision-making deficits during hyperdopaminergic states
Verharen, J. P. H., de Jong, J. W., Roelofs, T. J. M., Huffels, C. F. M., van Zessen, R., Luijendijk, M. C. M., Hamelink, R., Willuhn, I., den Ouden, H. E. M., van der Plasse, G., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-03087-1 · Cited by 62
Kohno, M., Okita, K., Morales, A. M., Robertson, C. L., Dean, A. C., Ghahremani, D. G., Sabb, F. W., Rawson, R. A., Mandelkern, M. A., Bilder, R. M., et al. (2016) · Molecular Psychiatry · doi:10.1038/mp.2015.223 · Cited by 62
“The firing of dopaminergic neurons codes for the magnitude and probability of the incentive-value of a stimulus (58), and signaling through the mesolimbic system promotes motivated drugseeking behavior (59, 60).”
Stimulus-response and response-outcome learning mechanisms in the striatum
Horvitz, J. C. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.12.014 · Cited by 58
Leptin Regulates Dopamine Responses to Sustained Stress in Humans
Burghardt, P. R., Love, T., Stohler, C. S., Hodgkinson, C. A., Shen, P., Enoch, M., Goldman, D. A., & Zubieta, J. K. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.2521-12.2012 · Cited by 60
“There is substantial evidence implicating dopaminergic neurotransmission in the ventral basal ganglia in appetitive behavior, consistent with its role in reward processing, in addition to its role in responding to salient stressful stimuli (Horvitz, 2000; Tobler et al., 2005).”
BackgroundRajkumar, C., Veerakumar, P., Chen, S., Thirumalraj, B., & Liu, S.-B. (2017) · Nanoscale · doi:10.1039/c7nr00967d · Cited by 60
Risk-sensitivity and the mean-variance trade-off: decision making in sensorimotor control
Nagengast, A. J., Braun, D. A., & Wolpert, D. M. (2011) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2010.2518 · Cited by 59
Exposure therapy for pediatric irritability: Theory and potential mechanisms
Kircanski, K., Craske, M. G., Averbeck, B. B., Pine, D. S., Leibenluft, E., & Brotman, M. A. (2019) · Behaviour Research and Therapy · doi:10.1016/j.brat.2019.04.007 · Cited by 58
Neural substrates of appetitive and aversive prediction error
Iordanova, M. D., Yau, J. O.-Y., McDannald, M. A., & Corbit, L. H. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.10.029 · Cited by 63
“Variations in the conditions of reinforcement such as reward probability and reward magnitude modulate the DA signal (Fiorillo, Tobler, & Schultz, 2003; Tobler et al., 2005).”
BackgroundLearning with reinforcement prediction errors in a model of the Drosophila mushroom body
Bennett, J., Philippides, A. O., & Nowotny, T. (2021) · Nature Communications · doi:10.1038/s41467-021-22592-4 · Cited by 64
The neuroscience of active learning and direct instruction
Dubinsky, J. M., & Hamid, A. (2024) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2024.105737 · Cited by 121
“At outcomes, the posterior cingulate and anterior insula also signal subjective value (Bartra et al., 2013; Tobler et al., 2005).”
BackgroundAging and the neuroeconomics of decision making: A review
Brown, S. B. R. E., & Ridderinkhof, K. R. (2009) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/cabn.9.4.365 · Cited by 62
Anatomical Inputs From the Sensory and Value Structures to the Tail of the Rat Striatum
Jiang, H., & Kim, H. F. (2018) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2018.00030 · Cited by 57
“We found that the TS received inputs from the SN and DRN, two brain stem regions known to encode reward information (Tobler et al., 2005; Nakamura et al., 2008; Kim et al., 2015; Li et al., 2016).”
MethodIke, K. G. O., de Boer, S. F., Buwalda, B., & Kas, M. J. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.06.030 · Cited by 64
“When an animal is exposed to a reward, the dopaminergic reaction to this reward adapts based on the predicted value of the reward (Tobler et al., 2005).”
BackgroundContext-Dependent Multiplexing by Individual VTA Dopamine Neurons
Kremer, Y., Flakowski, J., Rohner, C., & Lüscher, C. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.0502-20.2020 · Cited by 57
Kufahl, P. R., Li, Z., Risinger, R. C., Rainey, C. J., Piacentine, L. B., Wu, G., Bloom, A. S., Zheng, Y., & Li, S. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2007.03.021 · Cited by 57
Wang, Y., Toyoshima, O., Kunimatsu, J., Yamada, H., & Matsumoto, M. (2021) · eLife · doi:10.7554/elife.63166 · Cited by 59
“Midbrain dopamine neurons respond to reward-predicting cues with phasic activity, and this phasic activity has been shown to represent the value of cued rewards (Matsumoto and Hikosaka, 2009; Roesch et al., 2007; Tobler et al., 2005).”
BackgroundInfluentialArnsten, A. F. T., Joyce, M. K. P., & Roberts, A. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.105000 · Cited by 64
“Most research on DA has focused on its role in reward, where DA “Value” cells projecting to the striatum increase their firing to unexpected rewards, or to stimuli that predict rewards, but decrease their firing to the loss of an expected reward (Tobler et al., 2005).”
BackgroundKrigolson, O. E., Hassall, C. D., & Handy, T. C. (2013) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_00509 · Cited by 64
Amphetamine Reverses Escalated Cocaine Intake via Restoration of Dopamine Transporter Conformation
Siciliano, C. A., Saha, K., Calipari, E. S., Fordahl, S. C., Chen, R., Khoshbouei, H., & Jones, S. R. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.2604-17.2017 · Cited by 56
Sanfey, A. G. (2007) · Current Directions in Psychological Science · doi:10.1111/j.1467-8721.2007.00494.x · Cited by 61
Supplementary Eye Field Encodes Reward Prediction Error
So, N., & Stuphorn, V. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.4419-11.2012 · Cited by 59
“Similar relative reward encoding was also found in other reward-related brain areas, such as midbrain dopamine nuclei (Tobler et al., 2005), habenula (Matsumoto and Hikosaka, 2009a), orbitofrontal (Tremblay and Schultz, 1999), and medial frontal cortex (Seo and Lee, 2009).”
ResultEpistasis effects of dopamine genes on interval timing and reward magnitude in humans
Balcı, F., Wiener, M., Çavdaroğlu, B., & Coslett, H. B. (2012) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2012.08.002 · Cited by 58
Metadata
- Authors
- Tobler, P. N., Fiorillo, C. D., & Schultz, W.
- Affiliations
- University of Fribourg (CH)
- Corresponding author
- Fiorillo, Christopher D.
- Schultz, Wolfram
- Venue
- Science
- Published
- 2005-03-11
- Volume
- 307
- Issue
- 5715
- Pages
- 1642-1645
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- OpenAlex
- W2098534820
- Cited by
- 1,276
- References
- 24
- Citations by year
- 2026: 36 · 2025: 32 · 2024: 47 · 2023: 56 · 2022: 53 · 2021: 72 · 2020: 57 · 2019: 69 · 2018: 63 · 2017: 65 · 2016: 74 · 2015: 58 · 2014: 72 · 2013: 76 · 2012: 72
- FWCI
- 22.78
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- Zurich Open Repository and Archive (University of Zurich) (acceptedVersion)
- reroDoc Digital Library (submittedVersion)
- Zurich Open Repository and Archive (University of Zurich) (submittedVersion)
- Funders
- Wellcome Trust (095495)
- 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, adaptive coding, midbrain, reward prediction, gain modulation, variance, reward sensitivity, neural adaptation
- MeSH terms
- Adaptation, Physiological, Animals, Discrimination, Psychological, Dopamine, Electrophysiology, Female, Learning, Macaca fascicularis, Mesencephalon, Neurons, Photic Stimulation, Probability, Reward
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