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Afferent modulation of dopamine neuron firing differentially regulates tonic and phasic dopamine transmission

Floresco, Stan B, West, Anthony R, Ash, Brian, Moore, Holly, Grace, Anthony A·2003·Nature Neuroscience

DOI 10.1038/nn1103

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Abstract

The mesolimbic dopamine system is centrally involved in reward and goal-directed behavior, and it has been implicated in multiple psychiatric disorders. Understanding the mechanism by which dopamine participates in these activities requires comprehension of the dynamics of dopamine release. Here we report dissociable regulation of dopamine neuron discharge by two separate afferent systems in rats; inhibition of pallidal afferents selectively increased the population activity of dopamine neurons, whereas activation of pedunculopontine inputs increased burst firing. Only the increase in population activity increased ventral striatal dopamine efflux. After blockade of dopamine reuptake, however, enhanced bursting increased dopamine efflux three times more than did enhanced population activity. These results provide insight into multiple regulatory systems that modulate dopamine system function: burst firing induces massive synaptic dopamine release, which is rapidly removed by reuptake before escaping the synaptic cleft, whereas increased population activity modulates tonic extrasynaptic dopamine levels that are less influenced by reuptake.

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Authors: Floresco, S. B., West, A. R., Ash, B., Moore, H., & Grace, A. A.
Affiliations: University of Pittsburgh (US)
Corresponding author: Floresco, Stan B
Grace, Anthony A
ORCID: Floresco, Stan B
West, Anthony R
Moore, Holly
Grace, Anthony A
Venue: Nature Neuroscience
Publisher: Springer Science and Business Media LLC
Published: 2003-08-03
Volume: 6
Issue: 9
Pages: 968-973
ISSN: 1097-6256 (ISSN-L)
1546-1726
DOI: 10.1038/nn1103
OpenAlex: W1994984635
Cited by: 1,106
References: 40
Citations by year: 2026: 23 · 2025: 33 · 2024: 37 · 2023: 33 · 2022: 49 · 2021: 43 · 2020: 46 · 2019: 50 · 2018: 67 · 2017: 44 · 2016: 61 · 2015: 54 · 2014: 73 · 2013: 55 · 2012: 60
FWCI: 13.17
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
Locations: Nature Neuroscience (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health
National Institute of Mental Health (F32MH011305)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
Keywords: dopaminergic neurons, mesolimbic dopamine system, pedunculopontine nucleus, burst firing, tonic dopamine release, dopamine reuptake, ventral striatum, dopamine efflux, population activity, reward
MeSH terms: Afferent Pathways, Animals, Dopamine, Male, Mesencephalon, Synaptic Transmission, Neurons, Nucleus Accumbens, Rats, Sprague-Dawley, Ventral Tegmental Area, GABA Antagonists, Rats

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Afferent modulation of dopamine neuron firing differentially regulates tonic and phasic dopamine transmission

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