The DOI matches its Crossref record; 75 of the 75 references it cites were found in a registry or an index.
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.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
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 [59]
Citations
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
Correlated neuronal discharge rate and its implications for psychophysical performance
Zohary, E., Shadlen, M. N., & Newsome, W. T. (1994) · Nature · doi:10.1038/370140a0 · Cited by 1,237
Dopamine neurons report an error in the temporal prediction of reward during learning
Hollerman, J. R., & Schultz, W. (1998) · Nature Neuroscience · doi:10.1038/1124 · Cited by 1,161
Dopamine responses comply with basic assumptions of formal learning theory
Waelti, P., Dickinson, A., & Schultz, W. (2001) · Nature · doi:10.1038/35083500 · Cited by 1,018
Mesolimbocortical and nigrostriatal dopamine responses to salient non-reward events
Horvitz, J. C. (2000) · Neuroscience · doi:10.1016/s0306-4522(00)00019-1 · Cited by 967
A cellular mechanism of reward-related learning
Reynolds, J. N. J., Hyland, B. I., & Wickens, J. R. (2001) · Nature · doi:10.1038/35092560 · Cited by 879
Neural computation of log likelihood in control of saccadic eye movements
Carpenter, R. H. S., & Williams, M. L. L. (1995) · Nature · doi:10.1038/377059a0 · Cited by 823
Dopamine operates as a subsecond modulator of food seeking
Roitman, M. F., Stuber, G. D., Phillips, P. E. M., Wightman, R. M., & Carelli, R. M. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.3823-03.2004 · Cited by 718
MATCHING, UNDERMATCHING, AND OVERMATCHING IN STUDIES OF CHOICE
William, B. M. (1979) · Journal of the Experimental Analysis of Behavior · doi:10.1901/jeab.1979.32-269 · Cited by 702
Aosaki, T., Tsubokawa, H., Ishida, A., Watanabe, K., Graybiel, A. M., & Kimura, M. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-06-03969.1994 · Cited by 600
Wilson, C. J., Chang, H., & Kitai, S. (1990) · Journal of Neuroscience · doi:10.1523/jneurosci.10-02-00508.1990 · Cited by 520
Is the short-latency dopamine response too short to signal reward error?
Redgrave, P., Prescott, T. J., & Gurney, K. (1999) · Trends in Neurosciences · doi:10.1016/s0166-2236(98)01373-3 · Cited by 506
Acetylcholine-mediated modulation of striatal function
Calabresi, P., Centonze, D., Gubellini, P., Pisani, A., & Bernardi, G. (2000) · Trends in Neurosciences · doi:10.1016/s0166-2236(99)01501-5 · Cited by 452
A stereotaxic atlas of the brain of the cynomolgus monkey (Macaca fascicularis)
Szabo, J., & Cowan, W. M. (1984) · The Journal of Comparative Neurology · doi:10.1002/cne.902220208 · Cited by 415
An Economist’s Perspective on Probability Matching
Vulkan, N. (2000) · Journal of Economic Surveys · doi:10.1111/1467-6419.00106 · Cited by 413
The influence of urgency on decision time
Reddi, B. A. J., & Carpenter, R. H. S. (2000) · Nature Neuroscience · doi:10.1038/77739 · Cited by 411
Kerr, J. N. D., & Wickens, J. R. (2001) · Journal of Neurophysiology · doi:10.1152/jn.2001.85.1.117 · Cited by 395
Temporal and spatial characteristics of tonically active neurons of the primate's striatum
Aosaki, T., Kimura, M., & Graybiel, A. M. (1995) · Journal of Neurophysiology · doi:10.1152/jn.1995.73.3.1234 · Cited by 385
The pathogenesis of Parkinson's disease: a new hypothesis.
Barbeau, A. (1962) · PubMed · Cited by 340
Alexander, G. E., & DeLong, M. R. (1985) · Journal of Neurophysiology · doi:10.1152/jn.1985.53.6.1417 · Cited by 336
Spontaneous Activity of Neostriatal Cholinergic InterneuronsIn Vitro
Bennett, B. D., & Wilson, C. J. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-13-05586.1999 · Cited by 319
Coding of Predicted Reward Omission by Dopamine Neurons in a Conditioned Inhibition Paradigm
Tobler, P. N., Dickinson, A., & Schultz, W. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-32-10402.2003 · Cited by 300
Correlated Coding of Motivation and Outcome of Decision by Dopamine Neurons
Satoh, T., Nakai, S., Sato, T., & Kimura, M. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-30-09913.2003 · Cited by 298
Neurochemical architecture of the human striatum
Holt, D. J., Graybiel, A. M., & Saper, C. B. (1997) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19970721)384:1 · Cited by 297
Single cell studies of the primate putamen
Crutcher, M. D., & DeLong, M. R. (1984) · Experimental Brain Research · doi:10.1007/bf00238154 · Cited by 283
Venton, B. J., Zhang, H., Garris, P. A., Phillips, P. E. M., Sulzer, D., & Wightman, R. M. (2003) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2003.02109.x · Cited by 281
Raz, A., Feingold, A., Zelanskaya, V., Vaadia, E., & Bergman, H. (1996) · Journal of Neurophysiology · doi:10.1152/jn.1996.76.3.2083 · Cited by 258
Self-citationUnilateral Dopamine Denervation Blocks Corticostriatal LTP
Centonze, D., Gubellini, P., Picconi, B., Calabresi, P., Giacomini, P., & Bernardi, G. (1999) · Journal of Neurophysiology · doi:10.1152/jn.1999.82.6.3575 · Cited by 219
Treatment of Parkinson's disease.
Hardie, R. J. (1985) · PubMed · Cited by 218
The Left Hemisphere's Role in Hypothesis Formation
Wolford, G., Miller, M. B., & Gazzaniga, M. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-06-j0003.2000 · Cited by 216
Grace, A. A., & Bunney, B. S. (1983) · Neuroscience · doi:10.1016/0306-4522(83)90137-9 · Cited by 205
Lavoie, B. A., Smith, Y., & Parent, A. (1989) · The Journal of Comparative Neurology · doi:10.1002/cne.902890104 · Cited by 203
Nigrostriatal Dopamine System in Learning to Perform Sequential Motor Tasks in a Predictive Manner
Matsumoto, N., Hanakawa, T., Maki, S., Graybiel, A. M., & Kimura, M. (1999) · Journal of Neurophysiology · doi:10.1152/jn.1999.82.2.978 · Cited by 181
Pisani, A., Bonsi, P., Centonze, D., Calabresi, P., & Bernardi, G. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-07-j0003.2000 · Cited by 168
Jones, I. W., Bolam, J. P., & Wonnacott, S. (2001) · The Journal of Comparative Neurology · doi:10.1002/cne.1345 · Cited by 168
Temporal Difference Model Reproduces Anticipatory Neural Activity
Suri, R. E., & Schultz, W. (2001) · Neural Computation · doi:10.1162/089976601300014376 · Cited by 166
DeBoer, P., & Abercrombie, E. D. (1996) · The Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)12934-0 · Cited by 163
Apicella, P., Legallet, E., & Trouche, E. (1997) · Experimental Brain Research · doi:10.1007/pl00005773 · Cited by 162
Primate brain maps : structure of the macaque brain
Martin, R., Bowden, D. M., Wu, J. C.-C., Dubach, M. F., & Robertson, J. E. (2000) · Elsevier eBooks · Cited by 160
Muscarinic modulation of a transient K+ conductance in rat neostriatal neurons
Akins, P. T., Surmeier, D. J., & Kitai, S. T. (1990) · Nature · doi:10.1038/344240a0 · Cited by 154
Flores‐Hernández, J., Hernandez, S., Snyder, G. L., Yan, Z., Fienberg, A. A., Moss, S. J., Greengard, P., & Surmeier, D. J. (2000) · Journal of Neurophysiology · doi:10.1152/jn.2000.83.5.2996 · Cited by 150
Centonze, D., Gubellini, P., Pisani, A., Bernardi, G., & Calabresi, P. (2003) · Reviews in the Neurosciences · doi:10.1515/revneuro.2003.14.3.207 · Cited by 148
Muscarinic and Nicotinic Cholinergic Mechanisms in the Mesostriatal Dopamine Systems
Zhou, F.-M., Wilson, C. J., & Dani, J. A. (2003) · The Neuroscientist · doi:10.1177/1073858402239588 · Cited by 146
Activation of M1-like muscarinic receptors is required for the induction of corticostriatal LTP
Calabresi, P., Centonze, D., Gubellini, P., & Bernardi, G. (1999) · Neuropharmacology · doi:10.1016/s0028-3908(98)00199-3 · Cited by 126
Dopamine Release and Uptake Dynamics within Nonhuman Primate StriatumIn Vitro
Cragg, S. J., Hille, C. J., & Greenfield, S. A. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-21-08209.2000 · Cited by 120
Ravel, S., Legallet, E., & Apicella, P. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-24-08489.2003 · Cited by 118
Impairment of reward-related learning by cholinergic cell ablation in the striatum
Kitabatake, Y., Hikida, T., Watanabe, D., Pastan, I. H., & Nakanishi, S. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1032899100 · Cited by 115
A Network Representation of Response Probability in the Striatum
Blázquez, P. M., Fujii, N., Kojima, J., & Graybiel, A. M. (2002) · Neuron · doi:10.1016/s0896-6273(02)00627-x · Cited by 114
Blockade of M2-like muscarinic receptors enhances long-term potentiation at corticostriatal synapses
Calabresi, P., Centonze, D., Gubellini, P., Pisani, A., & Bernardi, G. (1998) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1998.00348.x · Cited by 108
Ravel, S., Sardo, P., Legallet, E., & Apicella, P. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-15-05730.2001 · Cited by 107
Cholinergic and dopaminergic modulation of potassium conductances in neostriatal neurons.
Kitai, S. T., & Surmeier, D. J. (1993) · PubMed · Cited by 102
Putaminal Activity for Simple Reactions or Self-Timed Movements
Lee, I. H., & Assad, J. A. (2003) · Journal of Neurophysiology · doi:10.1152/jn.01055.2002 · Cited by 101
Role of Tonically Active Neurons in Primate Caudate in Reward-Oriented Saccadic Eye Movement
Shimo, Y., & Hikosaka, O. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-19-07804.2001 · Cited by 97
Molecular and cellular mechanisms of neostriatal function
Ariano, M. A., & Surmeier, D. J. (1995) · Cited by 96
Pisani, A. (2003) · Neuropharmacology · doi:10.1016/s0028-3908(03)00137-0 · Cited by 94
Tonically active neurons in the monkey striatum do not preferentially respond to appetitive stimuli
Ravel, S., Legallet, E., & Apicella, P. (1999) · Experimental Brain Research · doi:10.1007/s002210050876 · Cited by 93
Permissive role of interneurons in corticostriatal synaptic plasticity
Centonze, D., Gubellini, P., Bernardi, G., & Calabresi, P. (1999) · Brain Research Reviews · doi:10.1016/s0165-0173(99)00018-1 · Cited by 89
Drukarch, B., Schepens, E., Schoffelmeer, A. N. M., & Stoof, J. C. (1989) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1989.tb07244.x · Cited by 63
Influence of Predictive Information on Responses of Tonically Active Neurons in the Monkey Striatum
Apicella, P., Ravel, S., Sardo, P., & Legallet, E. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.80.6.3341 · Cited by 63
Influence of Spatial Information on Responses of Tonically Active Neurons in the Monkey Striatum
Ravel, S., Sardo, P., Legallet, E., & Apicella, P. (2006) · Journal of Neurophysiology · doi:10.1152/jn.01113.2005 · Cited by 62
Time-Pressure Effects on Performance in a Base-Rate Task
Goodie, A. S., & Crooks, C. L. (2004) · The Journal of General Psychology · doi:10.3200/genp.131.1.18-28 · Cited by 42
Goal-directed, serial and synchronous activation of neurons in the primate striatum
Kimura, M., Matsumoto, N., Okahashi, K., Ueda, Y., Satoh, T., Minamimoto, T., Sakamoto, M., & Yamada, H. (2003) · Neuroreport · doi:10.1097/00001756-200305060-00004 · Cited by 41
Anticholinergic therapies in the treatment of Parkinson's disease
(2002) · Movement Disorders · doi:10.1002/mds.5556 · Cited by 31
Kudernatsch, M., & Sutor, B. (1994) · Neuroscience Letters · doi:10.1016/0304-3940(94)90571-1 · Cited by 26
Martin, R. F., & Bowden, D. M. (2000) · Cited by 16
Role of tonically active neurons in primate caudate in reward-oriented saccadic eye movement
下, 泰. (2002) · Medical Entomology and Zoology · Cited by 8
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
Cited by
Sorted by citations
Dopamine in motivational control: rewarding, aversive, and alerting
Bromberg-Martin, E. S., Matsumoto, M., & Hikosaka, O. (2010) · Neuron · doi:10.1016/j.neuron.2010.11.022 · Cited by 2,396
Habits, Rituals, and the Evaluative Brain
Graybiel, A. M. (2008) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.29.051605.112851 · Cited by 1,697
Behavioral Theories and the Neurophysiology of Reward
Schultz, W. (2006) · Annual Review of Psychology · doi:10.1146/annurev.psych.56.091103.070229 · Cited by 1,637
Multiple dopamine functions at different time courses
Schultz, W. (2007) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.28.061604.135722 · Cited by 1,415
Two types of dopamine neuron distinctly convey positive and negative motivational signals
Matsumoto, M., & Hikosaka, O. (2009) · Nature · doi:10.1038/nature08028 · Cited by 1,378
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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review