Cited by 162Neurobiology and Insect Physiology ResearchMemory and Neural MechanismsNeuroscience and Neuropharmacology Research

Reward signal in a recurrent circuit drives appetitive long-term memory formation

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Ichinose, Toshiharu, Aso, Yoshinori, Yamagata, Nobuhiro, Abe, Ayako, Rubin, Gerald M, Tanimoto, Hiromu·2015·eLife

Abstract

Dopamine signals reward in animal brains. A single presentation of a sugar reward to Drosophila activates distinct subsets of dopamine neurons that independently induce short- and long-term olfactory memories (STM and LTM, respectively). In this study, we show that a recurrent reward circuit underlies the formation and consolidation of LTM. This feedback circuit is composed of a single class of reward-signaling dopamine neurons (PAM-α1) projecting to a restricted region of the mushroom body (MB), and a specific MB output cell type, MBON-α1, whose dendrites arborize that same MB compartment. Both MBON-α1 and PAM-α1 neurons are required during the acquisition and consolidation of appetitive LTM. MBON-α1 additionally mediates the retrieval of LTM, which is dependent on the dopamine receptor signaling in the MB α/β neurons. Our results suggest that a reward signal transforms a nascent memory trace into a stable LTM using a feedback circuit at the cost of memory specificity.

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Authors
Ichinose, T., Aso, Y., Yamagata, N., Abe, A., Rubin, G. M., & Tanimoto, H.
Affiliations
  • Tohoku University (JP)
  • Howard Hughes Medical Institute (US)
Corresponding author
Tanimoto, Hiromu
Venue
eLife
Published
2015-11-17
Volume
4
Pages
e10719-e10719
ISSN
2050-084X (ISSN-L)
OpenAlex
W2179301060
Cited by
162
References
81
Citations by year
2026: 8 · 2025: 13 · 2024: 29 · 2023: 20 · 2022: 17 · 2021: 16 · 2020: 13 · 2019: 10 · 2018: 16 · 2017: 14 · 2016: 6
FWCI
5.60
Type
journal article
Language
en
Open access
Locations
  • eLife (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • Deutsche Forschungsgemeinschaft (DFG) (TA 552/5-1)
  • MEXT/JSPS KAKENHI (266646, 15K14307, 26840110, 25890003, 26250001, 26120705, 26119503)
  • Naito Foundation
  • Kurata Memorial Hitachi Science and Technology Foundation
  • Uehara Memorial Foundation
  • Howard Hughes Medical Institute (HHMI)
  • The Strategic Research Program for Brain Sciences
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords
dopamine, reward signaling, long-term memory, memory consolidation, memory retrieval, mushroom body, olfactory memory, Drosophila, memory specificity, dopamine receptor signaling
MeSH terms
Animals, Appetitive Behavior, Conditioning, Classical, Drosophila, Neural Pathways, Recurrence, Memory, Long-Term, Dopaminergic Neurons

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