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Dopamine Neurons Control Striatal Cholinergic Neurons via Regionally Heterogeneous Dopamine and Glutamate Signaling
Open accessAbstract
Midbrain dopamine neurons fire in bursts conveying salient information. Bursts are associated with pauses in tonic firing of striatal cholinergic interneurons. Although the reciprocal balance of dopamine and acetylcholine in the striatum is well known, how dopamine neurons control cholinergic neurons has not been elucidated. Here, we show that dopamine neurons make direct fast dopaminergic and glutamatergic connections with cholinergic interneurons, with regional heterogeneity. Dopamine neurons drive a burst-pause firing sequence in cholinergic interneurons in the medial shell of the nucleus accumbens, mixed actions in the accumbens core, and a pause in the dorsal striatum. This heterogeneity is due mainly to regional variation in dopamine-neuron glutamate cotransmission. A single dose of amphetamine attenuates dopamine neuron connections to cholinergic interneurons with dose-dependent regional specificity. Overall, the present data indicate that dopamine neurons control striatal circuit function via discrete, plastic connections with cholinergic interneurons.
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“Further, inhomogeneous neuronal release of acetylcholine, glutamate and substance P affects dopamine release159–161, which, together with the heterogeneous striosome-matrix compartments, would result in diverse dopamine release.”
From Dopamine reward prediction-error signalling: A two-component response (2016) · cites this paper as [160]
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Cites
Di Chiara, G., & Imperato, A. (1988) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.85.14.5274 · Cited by 4,733
Optogenetics in neural systems
Yizhar, O., Fenno, L. E., Davidson, T. J., Mogri, M., & Deisseroth, K. (2011) · Neuron · doi:10.1016/j.neuron.2011.06.004 · Cited by 1,881
Kelly, P. H., Seviour, P. W., & Iversen, S. D. (1975) · Brain Research · doi:10.1016/0006-8993(75)90233-4 · Cited by 1,740
Ikemoto, S. (2007) · Brain Research Reviews · doi:10.1016/j.brainresrev.2007.05.004 · Cited by 1,477
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
Phasic Firing in Dopaminergic Neurons Is Sufficient for Behavioral Conditioning
Tsai, H.-C., Zhang, F., Adamantidis, A., Stuber, G. D., Bonci, A., de Lecea, L., & Deisseroth, K. (2009) · Science · doi:10.1126/science.1168878 · Cited by 1,266
Drug-evoked synaptic plasticity in addiction: from molecular changes to circuit remodeling
Lüscher, C., & Malenka, R. C. (2011) · Neuron · doi:10.1016/j.neuron.2011.01.017 · Cited by 1,105
Nucleus accumbens shell and core dopamine: differential role in behavior and addiction
Di Chiara, G. (2002) · Behavioural Brain Research · doi:10.1016/s0166-4328(02)00286-3 · Cited by 996
Striatal Dopamine Release Is Triggered by Synchronized Activity in Cholinergic Interneurons
Threlfell, S., Lalic, T., Platt, N. J., Jennings, K. A., Deisseroth, K., & Cragg, S. J. (2012) · Neuron · doi:10.1016/j.neuron.2012.04.038 · Cited by 845
Updating dopamine reward signals
Schultz, W. (2013) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2012.11.012 · Cited by 651
Atasoy, D., Aponte, Y., Su, H. H., & Sternson, S. M. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.1954-08.2008 · Cited by 635
Ventral Tegmental Area Neurons in Learned Appetitive Behavior and Positive Reinforcement
Fields, H. L., Hjelmstad, G. O., Margolis, E. B., & Nicola, S. M. (2007) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.30.051606.094341 · Cited by 632
The dopamine transporter: immunochemical characterization and localization in brain
Ciliax, B. J., Heilman, C. J., Demchyshyn, L. L., Pristupa, Z. B., Ince, E., Hersch, S. M., Niznik, H. B., & Levey, A. I. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-03-01714.1995 · Cited by 589
Dopaminergic neurons inhibit striatal output through non-canonical release of GABA
Tritsch, N. X., Ding, J. B., & Sabatini, B. L. (2012) · Nature · doi:10.1038/nature11466 · Cited by 576
Physiology and pharmacology of striatal neurons
Kreitzer, A. C. (2009) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.051508.135422 · Cited by 530
Cachope, R., Mateo, Y., Mathur, B. N., Irving, J. M., Wang, H., Morales, M., Lovinger, D. M., & Cheer, J. F. (2012) · Cell Reports · doi:10.1016/j.celrep.2012.05.011 · Cited by 529
Dopaminergic terminals in the nucleus accumbens but not the dorsal striatum corelease glutamate
Stuber, G. D., Hnasko, T. S., Britt, J. P., Edwards, R. H., & Bonci, A. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.1754-10.2010 · Cited by 529
Belin, D., Jonkman, S., Dickinson, A., Robbins, T. W., & Everitt, B. J. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.09.027 · Cited by 520
Thalamic Gating of Corticostriatal Signaling by Cholinergic Interneurons
Ding, J., Guzmán, J. N., Peterson, J. D., Goldberg, J. A., & Surmeier, D. J. (2010) · Neuron · doi:10.1016/j.neuron.2010.06.017 · Cited by 478
Bäckman, C. M., Malik, N., Zhang, Y., Shan, L., Grinberg, A., Hoffer, B. J., Westphal, H., & Tomac, A. C. (2006) · genesis · doi:10.1002/dvg.20228 · Cited by 463
Vesicular glutamate transport promotes dopamine storage and glutamate corelease in vivo
Hnasko, T. S., Chuhma, N., Zhang, H., Goh, G. Y., Sulzer, D., Palmiter, R. D., Rayport, S., & Edwards, R. H. (2010) · Neuron · doi:10.1016/j.neuron.2010.02.012 · Cited by 405
Self-citationDissecting the diversity of midbrain dopamine neurons
Roeper, J. (2013) · Trends in Neurosciences · doi:10.1016/j.tins.2013.03.003 · Cited by 395
Brown, M. T. C., Tan, K. R., O’Connor, E. C., Nikonenko, I., Müller, D., & Lüscher, C. (2012) · Nature · doi:10.1038/nature11657 · Cited by 393
Vesicular Dopamine Release Elicits an Inhibitory Postsynaptic Current in Midbrain Dopamine Neurons
Beckstead, M. J., Grandy, D. K., Wickman, K. D., & Williams, J. T. (2004) · Neuron · doi:10.1016/j.neuron.2004.05.019 · Cited by 368
Two-photon optogenetic toolbox for fast inhibition, excitation and bistable modulation
Prakash, R., Yizhar, O., Grewe, B. F., Ramakrishnan, C., Wang, N. N., Goshen, I., Packer, A. M., Peterka, D. S., Yuste, R., Schnitzer, M. J., et al. (2012) · Nature Methods · doi:10.1038/nmeth.2215 · Cited by 344
X-ray structure of the mammalian GIRK2–βγ G-protein complex
Whorton, M. R., & MacKinnon, R. (2013) · Nature · doi:10.1038/nature12241 · Cited by 312
Glutamatergic signaling by mesolimbic dopamine neurons in the nucleus accumbens
Tecuapetla, F., Patel, J. C., Xenias, H., English, D., Tadros, I., Shah, F., Berlin, J., Deisseroth, K., Rice, M. E., Tepper, J. M., et al. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.0265-10.2010 · Cited by 310
Functional Connectome of the Striatal Medium Spiny Neuron
Chuhma, N., Tanaka, K. F., Hen, R., & Rayport, S. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.3833-10.2011 · Cited by 287
Self-citationDopamine Neurons Mediate a Fast Excitatory Signal via Their Glutamatergic Synapses
Chuhma, N., Zhang, H., Masson, J., Zhuang, X., Sulzer, D. L., Hen, R., & Rayport, S. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.4317-03.2004 · Cited by 228
Self-citationYan, Z., & Surmeier, D. J. (1997) · Neuron · doi:10.1016/s0896-6273(00)80402-x · Cited by 195
Giessel, A. J., & Sabatini, B. L. (2010) · Neuron · doi:10.1016/j.neuron.2010.09.004 · Cited by 156
Molecular phenotype of rat striatal neurons expressing the dopamine D5 receptor subtype
Rivera, A., Alberti, I., Martín, A. B., Narváez, J. Á., de la Calle, A., & Moratalla, R. (2002) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2002.02280.x · Cited by 131
Li, X., Qi, J., Yamaguchi, T., Wang, H., & Morales, M. (2012) · Brain Structure and Function · doi:10.1007/s00429-012-0452-z · Cited by 129
VGLUT2 in dopamine neurons is required for psychostimulant-induced behavioral activation
Birgner, C., Nordenankar, K., Lundblad, M., Méndez, J. A. T., Smith, C., Grevès, M. L., Galter, D., Olson, L., Fredriksson, A., Trudeau, L., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0910986107 · Cited by 119
Two-Photon Optical Interrogation of Individual Dendritic Spines with Caged Dopamine
Araya, R., Andino-Pavlovsky, V., Yuste, R., & Etchenique, R. (2013) · ACS Chemical Neuroscience · doi:10.1021/cn4000692 · Cited by 103
Dimova, R. N., Vuillet, J., Nieoullon, A., & Goff, L. K. (1993) · Neuroscience · doi:10.1016/0306-4522(93)90489-3 · Cited by 98
Momiyama, T., & Koga, E. (2001) · The Journal of Physiology · doi:10.1111/j.1469-7793.2001.0479a.x · Cited by 97
Pause and rebound: sensory control of cholinergic signaling in the striatum
Schulz, J. M., & Reynolds, J. N. J. (2012) · Trends in Neurosciences · doi:10.1016/j.tins.2012.09.006 · Cited by 95
Wilson, C. J., & Goldberg, J. A. (2005) · Journal of Neurophysiology · doi:10.1152/jn.00630.2005 · Cited by 90
Spontaneous Inhibitory Synaptic Currents Mediated by a G Protein-Coupled Receptor
Gantz, S. C., Bunzow, J. R., & Williams, J. T. (2013) · Neuron · doi:10.1016/j.neuron.2013.04.013 · Cited by 88
Functional roles of neurotransmitters and neuromodulators in the dorsal striatumPreprint
Do, J., Kim, J., Bakes, J., Lee, K., & Kaang, B. (2012) · Learning & Memory · doi:10.1101/lm.025015.111 · Cited by 82
Effects of acetylcholine in the striatum
Benarroch, E. E. (2012) · Neurology · doi:10.1212/wnl.0b013e31825fe154 · Cited by 67
Bimodal effect of amphetamine on motor behaviors in C57BL/6 mice
Yates, J. W., Meij, J. T. A., Sullivan, J. R., Richtand, N. M., & Yu, L. (2007) · Neuroscience Letters · doi:10.1016/j.neulet.2007.09.011 · Cited by 64
Oswald, M. J., Oorschot, D. E., Schulz, J. M., Lipski, J., & Reynolds, J. N. J. (2009) · The Journal of Physiology · doi:10.1113/jphysiol.2009.177600 · Cited by 52
Acute in vivo nicotine administration enhances synchrony among dopamine neurons
Li, W., Doyon, W. M., & Dani, J. A. (2011) · Biochemical Pharmacology · doi:10.1016/j.bcp.2011.06.006 · Cited by 42
Lohse, M. J., Hoffmann, C., Nikolaev, V. O., Vilardaga, J., & Bünemann, M. (2007) · Advances in protein chemistry · doi:10.1016/s0065-3233(07)74005-6 · Cited by 38
Bérubé‐Carrière, N., Guay, G., Fortin, G. M., Kullander, K., Olson, L., Wallén‐Mackenzie, Å., Trudeau, L., & Descarries, L. (2012) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2012.07992.x · Cited by 37
Whorton, M. R., & MacKinnon, R. (2013) · Worldwide Protein Data Bank · doi:10.2210/pdb4kfm/pdb · Cited by 36
The Cholinergic Interneurons of the Striatum
Goldberg, J. A., & Wilson, C. J. (2010) · Handbook of behavioral neuroscience · doi:10.1016/b978-0-12-374767-9.00007-x · Cited by 20
Ishikawa, M., Otaka, M., Neumann, P. A., Wang, Z., Cook, J. M., Schlüter, O. M., Dong, Y., & Huang, Y. H. (2013) · The Journal of Physiology · doi:10.1113/jphysiol.2013.262915 · Cited by 18
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Schultz, W. (2016) · Nature Reviews Neuroscience · doi:10.1038/nrn.2015.26 · Cited by 1,036
Schizophrenia, dopamine and the striatum: From biology to symptoms
McCutcheon, R. A., Abi-Dargham, A., & Howes, O. D. (2019) · Trends in Neurosciences · doi:10.1016/j.tins.2018.12.004 · Cited by 763
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Weinstein, J. J., Chohan, M. O., Slifstein, M., Kegeles, L. S., Moore, H. M., & Abi‐Dargham, A. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2016.03.2104 · Cited by 308
Self-citationCastro, D. C., & Bruchas, M. R. (2019) · Neuron · doi:10.1016/j.neuron.2019.03.003 · Cited by 306
Metadata
- Authors
- Chuhma, N., Mingote, S., Moore, H., & Rayport, S.
- Affiliations
- Columbia University Irving Medical Center (US)
- New York State Psychiatric Institute (US)
- Columbia University (US)
- Corresponding author
- Chuhma, Nao
- Rayport, Stephen
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2014-02
- Volume
- 81
- Issue
- 4
- Pages
- 901-912
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC3933825
- OpenAlex
- W2016558598
- Cited by
- 233
- References
- 50
- Citations by year
- 2026: 10 · 2025: 21 · 2024: 19 · 2023: 17 · 2022: 18 · 2021: 27 · 2020: 24 · 2019: 10 · 2018: 12 · 2017: 22 · 2016: 28 · 2015: 17 · 2014: 8
- FWCI
- 11.42
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Columbia Academic Commons (Columbia University)
- Funders
- National Alliance for Research on Schizophrenia and Depression
- National Institutes of Health (5p50mh066171-05)
- National Institute of Mental Health (P50MH086404, P50-MH066171, MH086404, NIMH P50)
- National Institute on Drug Abuse (DA017978, R01DA017978)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Health Sciences › Medicine › Clinical Neurology › Deep Brain Stimulation and Movement Disorders
- Keywords
- dopaminergic neurons, striatal cholinergic interneurons, burst firing, nucleus accumbens shell, nucleus accumbens core, dorsal striatum, amphetamine, synaptic plasticity
- MeSH terms
- Acetylcholine, Animals, Dopamine, Interneurons, Mice, Inbred C57BL, Nucleus Accumbens, Receptors, Nicotinic, Signal Transduction, Glutamic Acid, Mice, Dopaminergic Neurons, Cholinergic Neurons
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