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Dopamine Neurons Control Striatal Cholinergic Neurons via Regionally Heterogeneous Dopamine and Glutamate Signaling
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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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Malave, L. B., Zuelke, D. R., Uribe‐Cano, S., Starikov, L., Rebholz, H., Friedman, E., Qin, C., Li, Q., Bézard, E., & Kottmann, A. H. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.03.09.983759
Dopamine and Opioid regulation of amygdala function
Patel, S. (2020) · The Sydney eScholarship Repository (The University of Sydney)
Fleming, W., Lee, J., Briones, B. A., Bolkan, S. S., & Witten, I. B. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.08.29.458113
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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