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Temporally Extended Dopamine Responses to Perceptually Demanding Reward-Predictive Stimuli
Open accessAbstract
Midbrain dopamine neurons respond to reward-predictive stimuli. In the natural environment reward-predictive stimuli are often perceptually complicated. Thus, to discriminate one stimulus from another, elaborate sensory processing is necessary. Given that previous studies have used simpler types of reward-predictive stimuli, it has yet to be clear whether and, if so, how dopamine neurons obtain reward information from perceptually complicated stimuli. To investigate this, we recorded the activities of monkey dopamine neurons while they were performing discrimination between two coherent motion directions in random-dot motion stimuli. These coherent directions were paired with different magnitudes of reward. We found that dopamine neurons showed reward-predictive responses to random-dot motion stimuli. Moreover, dopamine neurons showed temporally extended activity correlated with changes in reward prediction (i.e., reward prediction error) from coarse to fine scales between initial motion detection and subsequent motion discrimination phases. Noticeably, dopamine reward-predictive responses became differential in a later phase than previously reported. This response pattern was consistent with the time course of processing required for the estimation of expected reward value that parallels the motion direction discrimination processing. The results demonstrate that dopamine neurons are able to reflect the reward value of perceptually complicated stimuli, and suggest that dopamine neurons use the moment-to-moment reward prediction associated with environmental stimuli to compute a reward prediction error.
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“True to the notion that dopamine neurons are involved in temporal prediction-error coding, the initial activation is sensitive to the time of stimulus occurrence and thus codes a temporal-event prediction error33.”
From Dopamine reward prediction-error signalling: A two-component response (2016) · cites this paper as [33]
In the citing paper
“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 [33]
In the citing paper
“Dopamine neurons in medial and lateral, or dorsal and ventral, midbrain positions do show graded differences in responses to rewarding and aversive stimuli2,23,24,26,33.”
From Dopamine reward prediction-error signalling: A two-component response (2016) · cites this paper as [33]
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Metadata
- Authors
- Nomoto, K., Schultz, W., Watanabe, T., & Sakagami, M.
- Affiliations
- Tamagawa University (JP)
- Boston University (US)
- Corresponding author
- Sakagami, Masamichi
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2010-08-11
- Volume
- 30
- Issue
- 32
- Pages
- 10692-10702
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC3297489
- OpenAlex
- W2120222754
- Cited by
- 158
- References
- 41
- Citations by year
- 2026: 3 · 2025: 2 · 2024: 7 · 2023: 9 · 2022: 7 · 2021: 11 · 2020: 11 · 2019: 10 · 2018: 14 · 2017: 16 · 2016: 14 · 2015: 5 · 2014: 16 · 2013: 13 · 2012: 10
- FWCI
- 4.26
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Wellcome Trust (095495)
- National Institutes of Health
- National Eye Institute (R01EY015980, R01EY019466)
- 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, reward prediction error, reward prediction, random dot motion, motion direction discrimination, midbrain dopamine
- MeSH terms
- Acoustic Stimulation, Analysis of Variance, Animals, Behavior, Animal, Conditioning, Operant, Discrimination, Psychological, Dopamine, Functional Laterality, Macaca fascicularis, Magnetic Resonance Imaging, Male, Mesencephalon, Motion Perception, Neurons, Orientation, Photic Stimulation, Predictive Value of Tests, Reward, Saccades, Time Factors, Tyrosine 3-Monooxygenase, Feedback, Physiological
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