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An action potential initiation mechanism in distal axons for the control of dopamine release
Open accessAbstract
Information flow in neurons proceeds by integrating inputs in dendrites, generating action potentials near the soma, and releasing neurotransmitters from nerve terminals in the axon. We found that in the striatum, acetylcholine-releasing neurons induce action potential firing in distal dopamine axons. Spontaneous activity of cholinergic neurons produced dopamine release that extended beyond acetylcholine-signaling domains, and traveling action potentials were readily recorded from dopamine axons in response to cholinergic activation. In freely moving mice, dopamine and acetylcholine covaried with movement direction. Local inhibition of nicotinic acetylcholine receptors impaired dopamine dynamics and affected movement. Our findings uncover an endogenous mechanism for action potential initiation independent of somatodendritic integration and establish that this mechanism segregates the control of dopamine signaling between axons and somata.
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“These axonally induced APs are capable of driving DA release in vitro 61 and have been hypothesized to act as a mechanism for local control of DA release within the striatum.[64][65][66][67][68]”
From Synaptic and circuit functions of multitransmitter neurons in the mammalian brain (2023) · cites this paper as [61]
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DeepLabCut: markerless pose estimation of user-defined body parts with deep learning
Mathis, A., Mamidanna, P., Cury, K. M., Abe, T., Murthy, V. N., Mathis, M. W., & Bethge, M. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0209-y · Cited by 5,187
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
Gustafsson, M. G. L., Shao, L., Carlton, P. M., Wang, R., Golubovskaya, I. N., Cande, W. Z., Agard, D. A., & Sedat, J. W. (2008) · Biophysical Journal · doi:10.1529/biophysj.107.120345 · Cited by 1,560
A toolbox of Cre-dependent optogenetic transgenic mice for light-induced activation and silencing
Madisen, L., Mao, T., Koch, H., Zhuo, J.-M., Berenyi, A., Fujisawa, S., Hsu, Y.-W. A., Garcia, A. J., Gu, X., Zanella, S., et al. (2012) · Nature Neuroscience · doi:10.1038/nn.3078 · Cited by 1,398
Nicotinic Acetylcholine Receptors and Nicotinic Cholinergic Mechanisms of the Central Nervous System
Dani, J. A., & Bertrand, D. (2007) · Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev.pharmtox.47.120505.105214 · Cited by 1,197
Berke, J. D. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0152-y · Cited by 904
Matsuda, W., Furuta, T., Nakamura, K. C., Hioki, H., Fujiyama, F., Arai, R., & Kaneko, T. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.4029-08.2009 · Cited by 865
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
Rossi, J., Balthasar, N., Olson, D., Scott, M., Berglund, E., Lee, C. E., Choi, M. J., Lauzon, D., Lowell, B. B., & Elmquist, J. K. (2011) · Cell Metabolism · doi:10.1016/j.cmet.2011.01.010 · Cited by 672
Rapid signalling in distinct dopaminergic axons during locomotion and reward
Howe, M. W., & Dombeck, D. A. (2016) · Nature · doi:10.1038/nature18942 · Cited by 618
Endogenous nicotinic cholinergic activity regulates dopamine release in the striatum
Zhou, F.-M., Liang, Y., & Dani, J. A. (2001) · Nature Neuroscience · doi:10.1038/nn769 · Cited by 585
Coincident but Distinct Messages of Midbrain Dopamine and Striatal Tonically Active Neurons
Morris, G., Arkadir, D., Nevet, A., Vaadia, E., & Bergman, H. (2004) · Neuron · doi:10.1016/j.neuron.2004.06.012 · Cited by 574
Dopamine neuron activity before action initiation gates and invigorates future movements
da Silva, J. A., Tecuapetla, F., Paixão, V., & Costa, R. M. (2018) · Nature · doi:10.1038/nature25457 · Cited by 574
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
Next-generation GRAB sensors for monitoring dopaminergic activity in vivo
Sun, F., Zhou, J., Dai, B., Qian, T., Zeng, J., Li, X., Zhuo, Y., Zhang, Y., Wang, Y., Cheng, Q., et al. (2020) · Nature Methods · doi:10.1038/s41592-020-00981-9 · Cited by 483
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
An optimized acetylcholine sensor for monitoring in vivo cholinergic activity
Jing, M., Li, Y., Zeng, J., Huang, P., Skirzewski, M., Kljakic, O., Peng, W., Qian, T., Tan, K., Zou, J., et al. (2020) · Nature Methods · doi:10.1038/s41592-020-0953-2 · Cited by 408
Le Novere, N., Zoli, M., & Changeux, J. (1996) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1996.tb01206.x · Cited by 385
Reward and choice encoding in terminals of midbrain dopamine neurons depends on striatal target
Parker, N. F., Cameron, C. M., Taliaferro, J. P., Lee, J., Choi, J. Y., Davidson, T. J., Daw, N. D., & Witten, I. B. (2016) · Nature Neuroscience · doi:10.1038/nn.4287 · Cited by 348
Dopamine neurons share common response function for reward prediction error
Eshel, N., Tian, J., Bukwich, M., & Uchida, N. (2016) · Nature Neuroscience · doi:10.1038/nn.4239 · Cited by 321
Spatial and temporal scales of dopamine transmission
Liu, C., Goel, P., & Kaeser, P. S. (2021) · Nature reviews. Neuroscience · doi:10.1038/s41583-021-00455-7 · Cited by 320
Dopamine Secretion Is Mediated by Sparse Active Zone-like Release Sites
Liu, C., Kershberg, L., Wang, J., Schneeberger, S., & Kaeser, P. S. (2018) · Cell · doi:10.1016/j.cell.2018.01.008 · Cited by 256
Grace, A. A., & Bunney, B. S. (1980) · Science · doi:10.1126/science.7433992 · Cited by 241
Giorguieff, M. F., Floc'h, M. L. L., Glowinski, J., & Besson, M. (1977) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)30804-9 · Cited by 237
Dodson, P. D., Dreyer, J. K., Jennings, K. A., Syed, E. C. J., Wade‐Martins, R., Cragg, S. J., Bolam, J. P., & Magill, P. J. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1515941113 · Cited by 195
Decker, E. R., & Dani, J. (1990) · Journal of Neuroscience · doi:10.1523/jneurosci.10-10-03413.1990 · Cited by 175
Baptista, D., Schmitz, Y., Mészáros, J., Merchant, P., Hu, G., Li, S., Henke, A., Lizardi-Ortiz, J. E., Karpowicz, R. J., Morgenstern, T. J., et al. (2016) · Nature Neuroscience · doi:10.1038/nn.4252 · Cited by 172
Jones, I. W., Bolam, J. P., & Wonnacott, S. (2001) · The Journal of Comparative Neurology · doi:10.1002/cne.1345 · Cited by 168
Synaptic Integration Mediated by Striatal Cholinergic Interneurons in Basal Ganglia Function
Kaneko, S., Hikida, T., Watanabe, D., Ichinose, H., Nagatsu, T., Kreitman, R. J., Pastan, I. H., & Nakanishi, S. (2000) · Science · doi:10.1126/science.289.5479.633 · Cited by 166
Wilson, C. J. (2005) · Neuron · doi:10.1016/j.neuron.2004.12.053 · Cited by 163
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
Slow integration leads to persistent action potential firing in distal axons of coupled interneurons
Sheffield, M. E. J., Best, T. K., Mensh, B. D., Kath, W. L., & Spruston, N. (2011) · Nature Neuroscience · doi:10.1038/nn.2728 · Cited by 125
Segregation of Axonal and Somatic Activity During Fast Network Oscillations
Dugladze, T., Schmitz, D., Whittington, M. A., Vida, I., & Gloveli, T. (2012) · Science · doi:10.1126/science.1222017 · Cited by 122
Dopamine-acetylcholine interaction in the rat striatum: A dual-labeling immunocytochemical study
Chang, H. T. (1988) · Brain Research Bulletin · doi:10.1016/0361-9230(88)90244-4 · Cited by 104
Parker, J. G., Zweifel, L. S., Clark, J. J., Evans, S. B., Phillips, P. E. M., & Palmiter, R. D. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1007827107 · Cited by 97
Dopamine Gates Action Potential Backpropagation in Midbrain Dopaminergic Neurons
Gentet, L. J., & Williams, S. R. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.5234-06.2007 · Cited by 91
Cai, Y., & Ford, C. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.11.053 · Cited by 90
Coordination of rapid cholinergic and dopaminergic signaling in striatum during spontaneous movement
Howe, M. W., Ridouh, I., Mascaro, A. L. A., Larios, A., Azcorra, M., & Dombeck, D. A. (2019) · eLife · doi:10.7554/elife.44903 · Cited by 84
Synapse and Active Zone Assembly in the Absence of Presynaptic Ca2+ Channels and Ca2+ Entry
Held, R. G., Liu, C., Ma, K., Ramsey, A. M., Tarr, T. B., de Nola, G., Wang, S. S. H., Wang, J., van den Maagdenberg, A. M. J. M., Schneider, T., et al. (2020) · Neuron · doi:10.1016/j.neuron.2020.05.032 · Cited by 84
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 70
Wang, L., Zhang, X., Xu, H., Zhou, L., Jiao, R., Liu, W., Zhu, F., Kang, X., Liu, B., Teng, S., et al. (2014) · The Journal of Physiology · doi:10.1113/jphysiol.2014.271825 · Cited by 46
Ritzau‐Jost, A., Tsintsadze, T. S., Krueger, M., Ader, J., Bechmann, I., Eilers, J., Barbour, B., Smith, S. M., & Hallermann, S. (2021) · Cell Reports · doi:10.1016/j.celrep.2020.108612 · Cited by 44
Visual-Induced Excitation Leads to Firing Pauses in Striatal Cholinergic Interneurons
Schulz, J. M., Oswald, M. J., & Reynolds, J. N. J. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.0661-11.2011 · Cited by 42
Conditional inactivation of theCacna1a gene in transgenic mice
Todorov, B., van de Ven, R. C. G., Kaja, S., Broos, L. A. M., Verbeek, S. J., Plomp, J. J., Ferrari, M. D., Frants, R. R., & van den Maagdenberg, A. M. J. M. (2006) · genesis · doi:10.1002/dvg.20255 · Cited by 35
Yang, J., Xiao, Y., Li, L., He, Q., Li, M., & Shu, Y. (2019) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2019.00317 · Cited by 29
Flagged first, then by citations
Research works printed but not linked: 1
- A. Pereverzev, M. Mikhna, R. Vajna, C. Gissel, M. Henry, M. Weiergräber, J. Hescheler, N. Smyth, T. Schneider, Disturbances in glucose-tolerance, insulin-release, and stress-induced hyperglycemia upon disruption of the Ca(v)2.3 (α1E) subunit of voltage-gated Ca2+ channels. Mol. Endocrinol. 16, 884–895 (2002). 11923483
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Unique functional responses differentially map onto genetic subtypes of dopamine neurons
Azcorra, M., Gaertner, Z. A., Davidson, C., He, Q., Kim, H., Nagappan, S., Hayes, C. K., Ramakrishnan, C., Fenno, L. E., Kim, Y. S., et al. (2023) · Nature Neuroscience · doi:10.1038/s41593-023-01401-9 · Cited by 172
Basal forebrain cholinergic signalling: development, connectivity and roles in cognition
Ananth, M. R., Rajebhosale, P., Kim, R., Talmage, D. A., & Role, L. W. (2023) · Nature Reviews Neuroscience · doi:10.1038/s41583-023-00677-x · Cited by 148
Improved green and red GRAB sensors for monitoring dopaminergic activity in vivo
Zhuo, Y., Luo, B., Yi, X., Dong, H., Miao, X., Wan, J., Williams, J. T., Campbell, M. G., Cai, R., Qian, T., et al. (2023) · Nature Methods · doi:10.1038/s41592-023-02100-w · Cited by 174
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
Metadata
- Authors
- Liu, C., Cai, X., Ritzau-Jost, A., Kramer, P. F., Li, Y., Khaliq, Z. M., Hallermann, S., & Kaeser, P. S.
- Affiliations
- Harvard University (US)
- Carl-Ludwig-Institute of Physiology, Faculty of Medicine, Leipzig University, Leipzig, Germany.
- National Institutes of Health (US)
- Peking University (CN)
- Leipzig University (DE)
- Corresponding author
- Liu, Changliang
- Kaeser, Pascal S.
- ORCID
- Venue
- Science
- Published
- 2022-03-25
- Volume
- 375
- Issue
- 6587
- Pages
- 1378-1385
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- PMC
- PMC9081985
- OpenAlex
- W4220904128
- Cited by
- 213
- References
- 45
- Citations by year
- 2026: 25 · 2025: 50 · 2024: 56 · 2023: 60 · 2022: 22
- FWCI
- 20.78
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health
- National Institute of Neurological Disorders and Stroke (P30NS072030, R01NS103484, R01NS083898, ZIANS003135)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (P50HD105351)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
- Keywords
- action potential generation, distal axons, dopamine release, acetylcholine, cholinergic neurons, nicotinic acetylcholine receptors, striatum, spontaneous neuronal activity, movement direction, axonal signaling
- MeSH terms
- Acetylcholine, Action Potentials, Animals, Axons, Corpus Striatum, Dopamine, Synaptic Transmission, Receptors, Nicotinic, Mice, Cholinergic Neurons
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