Suppression of Dopamine Neurons Mediates Reward

Massive activation of dopamine neurons is critical for natural reward and drug abuse. In contrast, the significance of their spontaneous activity remains elusive. In Drosophila melanogaster, depolarization of the protocerebral anterior medial (PAM) cluster dopamine neurons en masse signals reward to...

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Bibliographic Details
Published in:PLoS biology 2016-12, Vol.14 (12), p.e1002586-e1002586
Main Authors: Yamagata, Nobuhiro, Hiroi, Makoto, Kondo, Shu, Abe, Ayako, Tanimoto, Hiromu
Format: Article
Language:English
Subjects:
Animals
Biology and Life Sciences
Brain research
Dopamine
Dopaminergic Neurons - metabolism
Dopaminergic Neurons - physiology
Drosophila melanogaster
Drug abuse
Experiments
Funding
Health aspects
Heterogeneity
Inactivation
Ingestion
Insects
Laboratories
Life sciences
Medicine and Health Sciences
Mesencephalon - cytology
Mesencephalon - metabolism
Mushroom Bodies - metabolism
Neural circuitry
Neurons
Neuropeptides
Peptides - physiology
Physical Sciences
Research and Analysis Methods
Reward
Signal Transduction
Social Sciences
Sugar
University graduates
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Summary:Massive activation of dopamine neurons is critical for natural reward and drug abuse. In contrast, the significance of their spontaneous activity remains elusive. In Drosophila melanogaster, depolarization of the protocerebral anterior medial (PAM) cluster dopamine neurons en masse signals reward to the mushroom body (MB) and drives appetitive memory. Focusing on the functional heterogeneity of PAM cluster neurons, we identified that a single class of PAM neurons, PAM-γ3, mediates sugar reward by suppressing their own activity. PAM-γ3 is selectively required for appetitive olfactory learning, while activation of these neurons in turn induces aversive memory. Ongoing activity of PAM-γ3 gets suppressed upon sugar ingestion. Strikingly, transient inactivation of basal PAM-γ3 activity can substitute for reward and induces appetitive memory. Furthermore, we identified the satiety-signaling neuropeptide Allatostatin A (AstA) as a key mediator that conveys inhibitory input onto PAM-γ3. Our results suggest the significance of basal dopamine release in reward signaling and reveal a circuit mechanism for negative regulation.
ISSN:1545-7885
1544-9173
1545-7885
DOI:10.1371/journal.pbio.1002586