Diversity and Homogeneity in Responses of Midbrain Dopamine Neurons
Open accessAbstract
Dopamine neurons of the ventral midbrain have been found to signal a reward prediction error that can mediate positive reinforcement. Despite the demonstration of modest diversity at the cellular and molecular levels, there has been little analysis of response diversity in behaving animals. Here we examine response diversity in rhesus macaques to appetitive, aversive, and neutral stimuli having relative motivational values that were measured and controlled through a choice task. First, consistent with previous studies, we observed a continuum of response variability and an apparent absence of distinct clusters in scatter plots, suggesting a lack of statistically discrete subpopulations of neurons. Second, we found that a group of “sensitive” neurons tend to be more strongly suppressed by a variety of stimuli and to be more strongly activated by juice. Third, neurons in the “ventral tier” of substantia nigra were found to have greater suppression, and a subset of these had higher baseline firing rates and late “rebound” activation after suppression. These neurons could belong to a previously identified subgroup of dopamine neurons that express high levels of H-type cation channels but lack calbindin. Fourth, neurons further rostral exhibited greater suppression. Fifth, although we observed weak activation of some neurons by aversive stimuli, this was not associated with their aversiveness. In conclusion, we find a diversity of response properties, distributed along a continuum, within what may be a single functional population of neurons signaling reward prediction error.
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Recent reports that distinguished between different stimulus components of punishers suggest that the physical impact of punishers is the major determinant for dopamine activations, and the psychophysically assessed aversive nature of the punishers did not explain the recorded dopamine activations.
“However, recent reports that distinguished between different stimulus components of punishers suggest that the physical impact of punishers is the major determinant for dopamine activations, and the psychophysically assessed aversive nature of the punishers did not explain the recorded dopamine activations25–27.”
From Dopamine reward prediction-error signalling: A two-component response (2016) · cites this paper as [26]
Dopamine neurons in medial and lateral, or dorsal and ventral, midbrain positions show graded differences in responses to rewarding and aversive stimuli.
“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 [26]
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- Authors
- Fiorillo, C. D., Yun, S. R., & Song, M. R.
- Affiliations
- Korea Advanced Institute of Science and Technology (KR)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2013-03-13
- Volume
- 33
- Issue
- 11
- Pages
- 4693-4709
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC3873403
- OpenAlex
- W2123563550
- Cited by
- 99
- References
- 30
- Citations by year
- 2026: 3 · 2025: 7 · 2024: 1 · 2023: 2 · 2022: 2 · 2021: 6 · 2020: 4 · 2019: 5 · 2018: 10 · 2017: 9 · 2016: 12 · 2015: 18 · 2014: 14 · 2013: 6
- FWCI
- 8.18
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Howard Hughes Medical Institute
- National Research Foundation
- National Research Foundation of Korea
- Ministry of Education, Science and Technology (R32-2008-000-10218-0)
- National Eye Institute (R01EY005603)
- 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, ventral midbrain, substantia nigra, response diversity, reward prediction error, rhesus monkeys, appetitive stimuli, aversive stimuli, motivational value, neuronal subpopulations, calbindin, choice task
- MeSH terms
- Action Potentials, Animals, Appetitive Behavior, Avoidance Learning, Brain Mapping, Choice Behavior, Conditioning, Operant, Female, Macaca mulatta, Male, Mesencephalon, Motivation, Neural Inhibition, Photic Stimulation, Reaction Time, Reinforcement, Psychology, Reward, Statistics as Topic, Dopaminergic Neurons
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