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Coincident but Distinct Messages of Midbrain Dopamine and Striatal Tonically Active Neurons
Open accessAbstract
Midbrain dopamine and striatal tonically active neurons (TANs, presumed acetylcholine interneurons) signal behavioral significance of environmental events. Since striatal dopamine and acetylcholine affect plasticity of cortico-striatal transmission and are both crucial to learning, they may serve as teachers in the basal ganglia circuits. We recorded from both neuronal populations in monkeys performing a probabilistic instrumental conditioning task. Both neuronal types respond robustly to reward-related events. Although different events yielded responses with different latencies, the responses of the two populations coincided, indicating integration at the target level. Yet, while the dopamine neurons' response reflects mismatch between expectation and outcome in the positive domain, the TANs are invariant to reward predictability. Finally, TAN pairs are synchronized, compared to a minority of dopamine neuron pairs. We conclude that the striatal cholinergic and dopaminergic systems carry distinct messages by different means, which can be integrated differently to shape the basal ganglia responses to reward-related events.
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“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 [59]
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Cites
Reinforcement Learning: An Introduction
Sutton, R. S., & Barto, A. G. (1998) · IEEE Transactions on Neural Networks · doi:10.1109/tnn.1998.712192 · Cited by 27,225
Reinforcement Learning: An Introduction
Sutton, R. S., & Barto, A. (2005) · IEEE Transactions on Neural Networks · doi:10.1109/tnn.2004.842673 · Cited by 25,268
A neural substrate of prediction and reward
Schultz, W., Dayan, P., & Montague, P. R. (1997) · Science · doi:10.1126/science.275.5306.1593 · Cited by 9,388
Herrnstein, R. J. (1970) · Journal of the Experimental Analysis of Behavior · doi:10.1901/jeab.1970.13-243 · Cited by 2,611
Discrete coding of reward probability and uncertainty by dopamine neurons
Fiorillo, C. D., Tobler, P. N., & Schultz, W. (2003) · Science · doi:10.1126/science.1077349 · Cited by 2,085
A neostriatal habit learning system in humans
Knowlton, B. J., Mangels, J. A., & Squire, L. R. (1996) · Science · doi:10.1126/science.273.5280.1399 · Cited by 1,777
Roitman, J. D., & Shadlen, M. N. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-21-09475.2002 · Cited by 1,589 · cited 2×
“In such cases it has been shown both theoretically and experimentally (Reddi and Carpenter, 2000; Carpenter and Williams, 1995; Roitman and Shadlen, 2002; Goodie and Crooks, 2004) that performance is suboptimal, similar to the speed/accuracy tradeoff effect in motor performance.”
BackgroundNeuronal Spike Trains and Stochastic Point Processes
Perkel, D. H., Gerstein, G. L., & Moore, G. (1967) · Biophysical Journal · doi:10.1016/s0006-3495(67)86596-2 · Cited by 1,482
The Basal Ganglia and Adaptive Motor Control
Graybiel, A. M., Aosaki, T., Flaherty, A. W., & Kimura, M. (1994) · Science · doi:10.1126/science.8091209 · Cited by 1,324
Neuronal Spike Trains and Stochastic Point Processes
Perkel, D. H., Gerstein, G. L., & Moore, G. P. (1967) · Biophysical Journal · doi:10.1016/s0006-3495(67)86597-4 · Cited by 1,310
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Research works printed but not linked: 2
- Barbeau, 1962, The pathogensis of Parkinson's disease, Can. Med. Assoc. J., 87, 802
- DeBoer, 1996, Physiological release of striatal acetylcholine in vivo, J. Pharmacol. Exp. Ther., 277, 775
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Self-citation
Metadata
- Authors
- Morris, G., Arkadir, D., Nevet, A., Vaadia, E., & Bergman, H.
- Affiliations
- Hebrew University of Jerusalem (IL)
- Corresponding author
- Morris, Genela
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2004-07
- Volume
- 43
- Issue
- 1
- Pages
- 133-143
- ISSN
- 0896-6273 (ISSN-L)
- OpenAlex
- W2154145851
- Semantic Scholar
- fd94217912e9b183da7428af2af0960f198fcd3c
- Cited by
- 574
- References
- 75
- Citations by year
- 2026: 13 · 2025: 15 · 2024: 11 · 2023: 14 · 2022: 24 · 2021: 21 · 2020: 49 · 2019: 32 · 2018: 24 · 2017: 22 · 2016: 32 · 2015: 31 · 2014: 29 · 2013: 18 · 2012: 20
- FWCI
- 9.83
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- 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 › Memory and Neural Mechanisms
- Keywords
- midbrain dopamine, basal ganglia, reward prediction, neuronal synchronization, signal integration
- MeSH terms
- Acetylcholine, Action Potentials, Animals, Behavior, Animal, Dopamine, Female, Interneurons, Learning, Macaca mulatta, Male, Mesencephalon, Neural Pathways, Synaptic Transmission, Neuronal Plasticity, Reaction Time, Reward, Substantia Nigra, Neostriatum
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