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.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
Inhomogeneous neuronal release of acetylcholine, glutamate and substance P affects dopamine release, which, together with the heterogeneous striosome-matrix compartments, would result in diverse dopamine release.
“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]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
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 · see citing works
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 · see citing works
Kelly, P. H., Seviour, P. W., & Iversen, S. D. (1975) · Brain Research · doi:10.1016/0006-8993(75)90233-4 · Cited by 1,740 · see citing works
Ikemoto, S. (2007) · Brain Research Reviews · doi:10.1016/j.brainresrev.2007.05.004 · Cited by 1,477 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Updating dopamine reward signals
Schultz, W. (2013) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2012.11.012 · Cited by 651 · see citing works
Atasoy, D., Aponte, Y., Su, H. H., & Sternson, S. M. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.1954-08.2008 · Cited by 614 · see citing works
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 611 · see citing works
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 · see citing works
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 · see citing works
Physiology and pharmacology of striatal neurons
Kreitzer, A. C. (2009) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.051508.135422 · Cited by 530 · see citing works
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 · see citing works
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 · see citing works
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 519 · see citing works
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 · see citing works
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 462 · see citing works
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 · see citing works
Self-citationDissecting the diversity of midbrain dopamine neurons
Roeper, J. (2013) · Trends in Neurosciences · doi:10.1016/j.tins.2013.03.003 · Cited by 372 · see citing works
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 368 · see citing works
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 · see citing works
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 328 · see citing works
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 · see citing works
X-ray structure of the mammalian GIRK2–βγ G-protein complex
Whorton, M. R., & MacKinnon, R. (2013) · Nature · doi:10.1038/nature12241 · Cited by 298 · see citing works
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 273 · see citing works
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 · see citing works
Self-citationYan, Z., & Surmeier, D. J. (1997) · Neuron · doi:10.1016/s0896-6273(00)80402-x · Cited by 195 · see citing works
Giessel, A. J., & Sabatini, B. L. (2010) · Neuron · doi:10.1016/j.neuron.2010.09.004 · Cited by 156 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 99 · see citing works
Dimova, R. N., Vuillet, J., Nieoullon, A., & Goff, L. K. (1993) · Neuroscience · doi:10.1016/0306-4522(93)90489-3 · Cited by 98 · see citing works
Momiyama, T., & Koga, E. (2001) · The Journal of Physiology · doi:10.1111/j.1469-7793.2001.0479a.x · Cited by 97 · see citing works
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 89 · see citing works
Wilson, C. J., & Goldberg, J. A. (2005) · Journal of Neurophysiology · doi:10.1152/jn.00630.2005 · Cited by 89 · see citing works
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 · see citing works
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 75 · see citing works
Effects of acetylcholine in the striatum
Benarroch, E. E. (2012) · Neurology · doi:10.1212/wnl.0b013e31825fe154 · Cited by 67 · see citing works
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 · see citing works
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 · see citing works
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 39 · see citing works
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 · see citing works
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 · see citing works
Whorton, M. R., & MacKinnon, R. (2013) · Worldwide Protein Data Bank · doi:10.2210/pdb4kfm/pdb · Cited by 36 · see citing works
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 19 · see citing works
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 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Ventral tegmental area: cellular heterogeneity, connectivity and behaviour
Morales, M., & Margolis, E. B. (2017) · Nature reviews. Neuroscience · doi:10.1038/nrn.2016.165 · Cited by 1,108 · see citing works
Dopamine reward prediction-error signalling: A two-component response
Schultz, W. (2016) · Nature Reviews Neuroscience · doi:10.1038/nrn.2015.26 · Cited by 1,036 · see citing works
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 · see citing works
Pathway-specific dopamine abnormalities in schizophrenia
Weinstein, J., Chohan, M. O., Slifstein, M., Kegeles, L., Moore, H., & Abi-Dargham, A. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2016.03.2104 · Cited by 275 · see citing works
Self-citationCastro, D. C., & Bruchas, M. R. (2019) · Neuron · doi:10.1016/j.neuron.2019.03.003 · Cited by 287 · see citing works
Striatal cholinergic interneuron regulation and circuit effects
Lim, S. A. O., Kang, U. J., & McGehee, D. S. (2014) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2014.00022 · Cited by 236 · see citing works
Dual-transmitter neurons: functional implications of co-release and co-transmission
Vaaga, C. E., Borisovska, M., & Westbrook, G. L. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.04.010 · Cited by 221 · see citing works
Glutamate neurons within the midbrain dopamine regions
Morales, M., & Root, D. H. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.05.032 · Cited by 218 · see citing works
Ventral tegmental area glutamate neurons co-release GABA and promote positive reinforcement
Yoo, J. H., Zell, V., Gutierrez-Reed, N. A., Wu, J., Ressler, R. L., Shenasa, M. A., Johnson, A. B., Fife, K. H., Faget, L. C., & Hnasko, T. S. (2016) · Nature Communications · doi:10.1038/ncomms13697 · Cited by 210 · see citing works
VTA glutamatergic inputs to nucleus accumbens drive aversion by acting on GABAergic interneurons
Qi, J., Zhang, S., Wang, H., Barker, D. J., Miranda-Barrientos, J. A., & Morales, M. (2016) · Nature Neuroscience · doi:10.1038/nn.4281 · Cited by 203 · see citing works
Local control of striatal dopamine release
Cachope, R., & Cheer, J. F. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00188 · Cited by 183 · see citing works
Parallel basal ganglia circuits for voluntary and automatic behaviour to reach rewards
Kim, H. F., & Hikosaka, O. (2015) · Brain · doi:10.1093/brain/awv134 · Cited by 181 · see citing works
Afferent Inputs to Neurotransmitter-Defined Cell Types in the Ventral Tegmental Area
Faget, L. C., Osakada, F., Duan, J., Ressler, R. L., Johnson, A. B., Proudfoot, J., Yoo, J. H., Callaway, E. M., & Hnasko, T. S. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.05.057 · Cited by 180 · see citing works
Dopamine: A Modulator of Circadian Rhythms in the Central Nervous System
Korshunov, K. S., Blakemore, L. J., & Trombley, P. Q. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00091 · Cited by 173 · see citing works
Nucleus Accumbens Modulation in Reward and Aversion
Klawonn, A. M., & Malenka, R. C. (2018) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.2018.83.037457 · Cited by 163 · see citing works
Communication in Neural Circuits: Tools, Opportunities, and Challenges
Lerner, T. N., Ye, L., & Deisseroth, K. (2016) · Cell · doi:10.1016/j.cell.2016.02.027 · Cited by 159 · see citing works
Dopamine and glutamate regulate striatal acetylcholine in decision-making
Chantranupong, L., Beron, C. C., Zimmer, J. A., Wen, M. J., Wang, W., & Sabatini, B. L. (2023) · Nature · doi:10.1038/s41586-023-06492-9 · Cited by 153 · see citing works
The multilingual nature of dopamine neurons
Trudeau, L., Hnasko, T. S., Wallén‐Mackenzie, Å., Morales, M., Rayport, S., & Sulzer, D. L. (2014) · Progress in brain research · doi:10.1016/b978-0-444-63425-2.00006-4 · Cited by 138 · see citing works
Self-citationGlutamatergic and dopaminergic neurons in the mouse ventral tegmental area
Yamaguchi, T., Qi, J., Wang, H., Zhang, S. S., & Morales, M. (2015) · European Journal of Neuroscience · doi:10.1111/ejn.12818 · Cited by 139 · see citing works
Intrinsic dopamine and acetylcholine dynamics in the striatum of mice
Krok, A. C., Maltese, M., Mistry, P. N., Miao, X., Li, Y., & Tritsch, N. X. (2023) · Nature · doi:10.1038/s41586-023-05995-9 · Cited by 144 · see citing works
Local and afferent synaptic pathways in the striatal microcircuitry
Silberberg, G., & Bolam, J. P. (2015) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2015.05.002 · Cited by 135 · see citing works
Multiphasic modulation of cholinergic interneurons by nigrostriatal afferents
Straub, C., Tritsch, N. X., Hagan, N. A., Gu, C., & Sabatini, B. L. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.0589-14.2014 · Cited by 130 · see citing works
Cholinergic modulation of striatal microcircuits
Abudukeyoumu, N., Hernández-Flores, T., Garcia-Munoz, M., & Arbuthnott, G. W. (2018) · European Journal of Neuroscience · doi:10.1111/ejn.13949 · Cited by 128 · see citing works
Gjorgjieva, J., Drion, G., & Marder, E. (2016) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2015.12.008 · Cited by 127 · see citing works
VTA Glutamate Neuron Activity Drives Positive Reinforcement Absent Dopamine Co-release
Zell, V., Steinkellner, T., Hollon, N. G., Warlow, S. M., Souter, E. A., Faget, L. C., Hunker, A. C., Jin, X., Zweifel, L. S., & Hnasko, T. S. (2020) · Neuron · doi:10.1016/j.neuron.2020.06.011 · Cited by 127 · see citing works
The Evolving Understanding of Dopamine Neurons in the Substantia Nigra and Ventral Tegmental Area
Gantz, S. C., Ford, C., Morikawa, H., & Williams, J. T. (2017) · Annual Review of Physiology · doi:10.1146/annurev-physiol-021317-121615 · Cited by 122 · see citing works
Somatodendritic dopamine release: recent mechanistic insights
Rice, M. E., & Patel, J. C. (2015) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2014.0185 · Cited by 121 · see citing works
Checks and balances on cholinergic signaling in brain and body function
Soreq, H. (2015) · Trends in Neurosciences · doi:10.1016/j.tins.2015.05.007 · Cited by 117 · see citing works
Kharkwal, G., Brami‐Cherrier, K., Lizardi-Ortiz, J. E., Nelson, A., Ramos, M., Barrio, D. D., Sulzer, D. L., Kreitzer, A. C., & Borrelli, E. (2016) · Neuron · doi:10.1016/j.neuron.2016.06.014 · Cited by 113 · see citing works
Tozzi, A., de Iure, A., Bagetta, V., Tantucci, M., Durante, V., Quiroga‐Varela, A., Costa, C., Filippo, M. D., Ghiglieri, V., Latagliata, E. C., et al. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.08.013 · Cited by 112 · see citing works
Al‐Hasani, R., Gowrishankar, R., Schmitz, G. P., Pedersen, C. E., Marcus, D. J., Shirley, S. E., Hobbs, T. G., Elerding, A. J., Renaud, S. J., Jing, M., et al. (2021) · Nature Neuroscience · doi:10.1038/s41593-021-00898-2 · Cited by 110 · see citing works
Dopamine and Acetylcholine, a Circuit Point of View in Parkinson’s Disease
Rizzi, G., & Tan, K. R. (2017) · Frontiers in Neural Circuits · doi:10.3389/fncir.2017.00110 · Cited by 101 · see citing works
Glutamate neurons are intermixed with midbrain dopamine neurons in nonhuman primates and humans
Root, D. H., Wang, H., Liu, B., Barker, D. J., Mód, L., Szocsics, P., Silva, A. C., Maglóczky, Z., & Morales, M. (2016) · Scientific Reports · doi:10.1038/srep30615 · Cited by 98 · see citing works
Dopamine promotes aggression in mice via ventral tegmental area to lateral septum projections
Mahadevia, D., Saha, R., Manganaro, A., Chuhma, N., Ziolkowski-Blake, A., Morgan, A. A., Dumitriu, D., Rayport, S., & Ansorge, M. S. (2021) · Nature Communications · doi:10.1038/s41467-021-27092-z · Cited by 97 · see citing works
Self-citationFunctional Connectome Analysis of Dopamine Neuron Glutamatergic Connections in Forebrain Regions
Mingote, S., Chuhma, N., Kusnoor, S. V., Field, B. C., Deutch, A. Y., & Rayport, S. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.1674-15.2015 · Cited by 93 · see citing works
Self-citationHeterogeneity in striatal dopamine circuits: Form and function in dynamic reward seeking
Collins, A. L., & Saunders, B. T. (2020) · Journal of Neuroscience Research · doi:10.1002/jnr.24587 · Cited by 87 · see citing works
Striatal cholinergic interneurons and Parkinson's disease
Tanimura, A., Pancani, T., Lim, S. A. O., Tubert, C., Melendez-Zaidi, A. E., Shen, W., & Surmeier, D. J. (2017) · European Journal of Neuroscience · doi:10.1111/ejn.13638 · Cited by 92 · see citing works
Detection of phasic dopamine by D1 and D2 striatal medium spiny neurons
Yapo, C., Nair, A. G., Clement, L., Castro, L. R., Kotaleski, J. H., & Vincent, P. (2017) · The Journal of Physiology · doi:10.1113/jp274475 · Cited by 88 · see citing works
Oculogyric crises: Etiology, pathophysiology and therapeutic approaches
Barow, E., Schneider, S. A., Bhatia, K. P., & Ganos, C. (2016) · Parkinsonism & Related Disorders · doi:10.1016/j.parkreldis.2016.11.012 · Cited by 89 · see citing works
Relevance of interactions between dopamine and glutamate neurotransmission in schizophrenia
Buck, S. A., Erickson-Oberg, M. Q., Logan, R. W., & Freyberg, Z. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01649-w · Cited by 92 · see citing works
Cai, Y., & Ford, C. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.11.053 · Cited by 86 · see citing works
Chuhma, N., Mingote, S., Kalmbach, A., Yetnikoff, L., & Rayport, S. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2016.07.002 · Cited by 82 · see citing works
Self-citationCholinergic Interneurons Underlie Spontaneous Dopamine Release in Nucleus Accumbens
Yorgason, J. T., Zeppenfeld, D. M., & Williams, J. T. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.3064-16.2017 · Cited by 80 · see citing works
Trudeau, L., & Mestikawy, S. E. (2018) · Frontiers in Neural Circuits · doi:10.3389/fncir.2018.00113 · Cited by 79 · see citing works
Dopamine-glutamate neuron projections to the nucleus accumbens medial shell and behavioral switching
Mingote, S., Amsellem, A., Kempf, A., Rayport, S., & Chuhma, N. (2019) · Neurochemistry International · doi:10.1016/j.neuint.2019.104482 · Cited by 71 · see citing works
Self-citationVisual Cue-Discriminative Dopaminergic Control of Visuomotor Transformation and Behavior Selection
Yao, Y., Li, X., Zhang, B., Chen, Y., Liu, Y., Chen, W., Zeng, S., & Du, J. (2016) · Neuron · doi:10.1016/j.neuron.2015.12.036 · Cited by 78 · see citing works
The nucleus accumbens in reward and aversion processing: insights and implications
Xu, Y., Lin, Y., Yu, M., & Zhou, K. (2024) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2024.1420028 · Cited by 77 · see citing works
Dorst, M. C., Tokarska, A., Zhou, M., Lee, K., Stagkourakis, S., Broberger, C., Masmanidis, S. C., & Silberberg, G. (2020) · Nature Communications · doi:10.1038/s41467-020-18882-y · Cited by 70 · see citing works
Unraveling the dynamics of dopamine release and its actions on target cells
Sippy, T., & Tritsch, N. X. (2023) · Trends in Neurosciences · doi:10.1016/j.tins.2022.12.005 · Cited by 73 · see citing works
Upmanyu, N., Jin, J., Emde, H. V. D., Ganzella, M., Bösche, L., Malviya, V. N., Zhuleku, E., Politi, A. Z., Ninov, M., Silbern, I., et al. (2022) · Neuron · doi:10.1016/j.neuron.2022.02.008 · Cited by 69 · see citing works
Nair, A. G., Gutierrez‐Arenas, O., Eriksson, O., Vincent, P., & Kotaleski, J. H. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.0730-15.2015 · Cited by 69 · see citing works
Chuhma, N., Mingote, S., Yetnikoff, L., Kalmbach, A., Ma, T. C., Ztaou, S., Siena, A.-C., Tepler, S., Poulin, J.-F., Ansorge, M. S., et al. (2018) · eLife · doi:10.7554/elife.39786 · Cited by 66 · see citing works
Self-citationWeisenhorn, D. M. V., Giesert, F., & Wurst, W. (2016) · Journal of Neurochemistry · doi:10.1111/jnc.13670 · Cited by 67 · see citing works
Spontaneous Synaptic Activation of Muscarinic Receptors by Striatal Cholinergic Neuron Firing
Mamaligas, A. A., & Ford, C. (2016) · Neuron · doi:10.1016/j.neuron.2016.06.021 · Cited by 67 · see citing works
Shin, J. H., Adrover, M. F., & Alvarez, V. A. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.0596-17.2017 · Cited by 68 · see citing works
Tien, N.-W., Kim, T., & Kerschensteiner, D. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.04.025 · Cited by 67 · see citing works
Functional and molecular heterogeneity of D2R neurons along dorsal ventral axis in the striatum
Puighermanal, E., Castell, L., Esteve‐Codina, A., Melser, S., Kaganovsky, K., Zussy, C., Boubaker-Vitre, J., Gut, M., Rialle, S., Kellendonk, C., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-15716-9 · Cited by 59 · see citing works
Components and characteristics of the dopamine reward utility signal
Stauffer, W. R., Lak, A., Kobayashi, S., & Schultz, W. (2015) · The Journal of Comparative Neurology · doi:10.1002/cne.23880 · Cited by 62 · see citing works
Crofton, E. J., Nenov, M. N., Zhang, Y., Scala, F., Page, S. A., McCue, D. L., Li, D., Hommel, J. D., Laezza, F., & Green, T. A. (2017) · Neuropharmacology · doi:10.1016/j.neuropharm.2017.01.020 · Cited by 64 · see citing works
Acetylcholine waves and dopamine release in the striatum
Matityahu, L., Gilin, N., Sarpong, G. A., Atamna, Y., Tiroshi, L., Tritsch, N. X., Wickens, J. R., & Goldberg, J. A. (2023) · Nature Communications · doi:10.1038/s41467-023-42311-5 · Cited by 65 · see citing works
In vivo multiplex imaging of dynamic neurochemical networks with designed far-red dopamine sensors
Zheng, Y. R., Cai, R., Wang, K., Zhang, J., Zhuo, Y., Dong, H., Zhang, Y., Wang, Y., Deng, F., Ji, E., et al. (2025) · Science · doi:10.1126/science.adt7705 · Cited by 62 · see citing works
Ventral Tegmental Area Afferents and Drug-Dependent Behaviors
Oliva, I., & Wanat, M. J. (2016) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2016.00030 · Cited by 62 · see citing works
Dendritic Release of Neurotransmitters
Ludwig, M., Apps, D. K., Menzies, J. R. W., Patel, J. C., & Rice, M. E. (2016) · Comprehensive physiology · doi:10.1002/cphy.c160007 · Cited by 62 · see citing works
Pauses in Striatal Cholinergic Interneurons: What is Revealed by Their Common Themes and Variations?
Zhang, Y.-F., & Cragg, S. J. (2017) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2017.00080 · Cited by 61 · see citing works
Dopaminergic Regulation of Striatal Interneurons in Reward and Addiction: Focus on Alcohol
Clarke, R. B. C., & Adermark, L. (2015) · Neural Plasticity · doi:10.1155/2015/814567 · Cited by 64 · see citing works
Synaptic and circuit functions of multitransmitter neurons in the mammalian brain
Wallace, M. L., & Sabatini, B. L. (2023) · Neuron · doi:10.1016/j.neuron.2023.06.003 · Cited by 59 · see citing works
Warlow, S. M., Singhal, S. M., Hollon, N. G., Faget, L. C., Dowlat, D. S., Zell, V., Hunker, A. C., Zweifel, L. S., & Hnasko, T. S. (2023) · Neuron · doi:10.1016/j.neuron.2023.11.002 · Cited by 59 · see citing works
Wieland, S., Du, D., Oswald, M. J., Parlato, R., Köhr, G., & Kelsch, W. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.1175-14.2014 · Cited by 59 · see citing works
Nicotinic and opioid receptor regulation of striatal dopamine D2-receptor mediated transmission
Mamaligas, A. A., Cai, Y., & Ford, C. (2016) · Scientific Reports · doi:10.1038/srep37834 · Cited by 56 · see citing works
Ztaou, S., Oh, S. J., Tepler, S., Fleury, S., Matamales, M., Bertran‐Gonzalez, J., Chuhma, N., & Rayport, S. (2021) · eNeuro · doi:10.1523/eneuro.0196-21.2021 · Cited by 52 · see citing works
Self-citationSaddoris, M. P., Wang, X., Sugam, J. A., & Carelli, R. M. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.3468-15.2016 · Cited by 54 · see citing works
How changes in dopamine D2 receptor levels alter striatal circuit function and motivation
Simpson, E. H., Gallo, E. F., Balsam, P. D., Javitch, J. A., & Kellendonk, C. (2021) · Molecular Psychiatry · doi:10.1038/s41380-021-01253-4 · Cited by 52 · see citing works
Targeting the cholinergic system in Parkinson’s disease
Liu, C. (2020) · Acta Pharmacologica Sinica · doi:10.1038/s41401-020-0380-z · Cited by 53 · see citing works
Loss of nigral excitation of cholinergic interneurons contributes to parkinsonian motor impairments
Cai, Y., Nielsen, B. E., Boxer, E. E., Aoto, J. N., & Ford, C. (2021) · Neuron · doi:10.1016/j.neuron.2021.01.028 · Cited by 54 · see citing works
Buck, S. A., Torregrossa, M. M., Logan, R. W., & Freyberg, Z. (2020) · FEBS Journal · doi:10.1111/febs.15496 · Cited by 50 · see citing works
Divergent properties and independent regulation of striatal dopamine and GABA co-transmission
Zych, S. M., & Ford, C. P. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.110823 · Cited by 46 · see citing works
Dopamine neuron dependent behaviors mediated by glutamate cotransmission
Mingote, S., Chuhma, N., Kalmbach, A., Thomsen, G. M., Wang, Y., Mihali, A., Sferrazza, C. E., Zucker-Scharff, I., Siena, A.-C., Welch, M. G., et al. (2017) · eLife · doi:10.7554/elife.27566 · Cited by 46 · see citing works
Self-citationLindroos, R., Dorst, M. C., Du, K., Filipović, M., Keller, D. X., Ketzef, M., Kozlov, A., Kumar, A., Lindahl, M., Nair, A. G., et al. (2018) · Frontiers in Neural Circuits · doi:10.3389/fncir.2018.00003 · Cited by 44 · see citing works
Poppi, L. A., Ho-Nguyen, K.-T., Shi, A., Daut, C. T., & Tischfield, M. A. (2021) · Cells · doi:10.3390/cells10040907 · Cited by 46 · see citing works
McGovern, D. J., Polter, A. M., Prévost, E. D., Ly, A., McNulty, C. J., Rubinstein, B., & Root, D. H. (2023) · Neuropsychopharmacology · doi:10.1038/s41386-023-01637-w · Cited by 49 · see citing works
Adrover, M. F., Shin, J. H., Quiroz, C., Ferré, S., Lemos, J. C., & Alvarez, V. A. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.1327-20.2020 · Cited by 47 · see citing works
Paradoxical network excitation by glutamate release from VGluT3+ GABAergic interneurons
Pelkey, K. A., Calvigioni, D., Fang, C., Vargish, G., Ekins, T., Auville, K., Wester, J. C., Lai, M., Mackenzie-Gray Scott, C., Yuan, X., et al. (2020) · eLife · doi:10.7554/elife.51996 · Cited by 46 · see citing works
Dopamine Neurons That Cotransmit Glutamate, From Synapses to Circuits to Behavior
Eskenazi, D., Malave, L. B., Mingote, S., Yetnikoff, L., Ztaou, S., Velicu, V., Rayport, S., & Chuhma, N. (2021) · Frontiers in Neural Circuits · doi:10.3389/fncir.2021.665386 · Cited by 44 · see citing works
Self-citationLee, J. H., Ribeiro, E., Kim, J., Ko, B., Kronman, H. G., Jeong, Y. H., Kim, J. K., Janak, P. H., Nestler, E. J., Koo, J. W., et al. (2020) · Biological Psychiatry · doi:10.1016/j.biopsych.2020.05.003 · Cited by 45 · see citing works
Dopamine D2 receptors modulate the cholinergic pause and inhibitory learning
Gallo, E. F., Greenwald, J. E., Yeisley, J., Teboul, E., Martyniuk, K. M., Villarin, J. M., Li, Y., Javitch, J. A., Balsam, P. D., & Kellendonk, C. (2021) · Molecular Psychiatry · doi:10.1038/s41380-021-01364-y · Cited by 45 · see citing works
Zhai, S., Cui, Q., Simmons, D. V., & Surmeier, D. J. (2023) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2023.102798 · Cited by 44 · see citing works
Wang, D. V., Viereckel, T., Zell, V., Konradsson‐Geuken, Å., Broker, C. J., Talishinsky, A., Yoo, J. H., Galinato, M. H., Arvidsson, E., Kesner, A. J., et al. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.02.062 · Cited by 40 · see citing works
Drive and Reinforcement Circuitry in the Brain: Origins, Neurotransmitters, and Projection Fields
Wise, R. A., & McDevitt, R. A. (2017) · Neuropsychopharmacology · doi:10.1038/npp.2017.228 · Cited by 40 · see citing works
Marche, K., Martel, A., & Apicella, P. (2017) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2017.00052 · Cited by 39 · see citing works
The nucleus accumbens shell: a neural hub at the interface of homeostatic and hedonic feeding
Marinescu, A., & Labouesse, M. A. (2024) · Frontiers in Neuroscience · doi:10.3389/fnins.2024.1437210 · Cited by 40 · see citing works
Dobbs, L. K., Lemos, J. C., & Alvarez, V. A. (2016) · Genes Brain & Behavior · doi:10.1111/gbb.12361 · Cited by 38 · see citing works
Grasing, K. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.06.022 · Cited by 38 · see citing works
The dopamine neuron synaptic map in the striatum
Chuhma, N., Oh, S. J., & Rayport, S. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112204 · Cited by 37 · see citing works
Self-citationNair, A. G., Bhalla, U. S., & Kotaleski, J. H. (2016) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1005080 · Cited by 35 · see citing works
Ribeiro, F. M., Pires, R. G. W., Ferreira, T. A. A., Presti‐Silva, S. M., & Simões, A. T. (2022) · Neural Regeneration Research · doi:10.4103/1673-5374.360264 · Cited by 37 · see citing works
Co-existence of Functionally Different Vesicular Neurotransmitter Transporters
Münster‐Wandowski, A., Zander, J.-F., Richter, K., & Ahnert‐Hilger, G. (2016) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2016.00004 · Cited by 33 · see citing works
Disentangling the diverse roles of dopamine D2 receptors in striatal function and behavior
Gallo, E. F. (2019) · Neurochemistry International · doi:10.1016/j.neuint.2019.01.022 · Cited by 34 · see citing works
A mismatch between striatal cholinergic pauses and dopaminergic reward prediction errors
Duhne, M., Mohebi, A., Kim, K., Pelattini, L., & Berke, J. D. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2410828121 · Cited by 33 · see citing works
Role of the atypical vesicular glutamate transporter VGLUT3 in l-DOPA-induced dyskinesia
Gangarossa, G., Guzmán, M. S., Prado, V. F., Prado, M. A. M., Daumas, S., Mestikawy, S. E., & Valjent, E. (2015) · Neurobiology of Disease · doi:10.1016/j.nbd.2015.12.010 · Cited by 32 · see citing works
Conrad, W. S., Oriol, L., Kollman, G. J., Faget, L. C., & Hnasko, T. S. (2024) · Addiction Neuroscience · doi:10.1016/j.addicn.2024.100183 · Cited by 33 · see citing works
- 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 › Neurology › Neurological disorders and treatments
- 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
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