Cited by 26Neurobiology and Insect Physiology ResearchNeuroscience and Neuropharmacology ResearchMemory and Neural Mechanisms

Glia transmit negative valence information during aversive learning in Drosophila

Miyashita, Tomoyuki, Murakami, Kanako, Kikuchi, Emi, Ofusa, Kyouko, Mikami, Kyohei, Endo, Kentaro, Miyaji, Takaaki, Moriyama, Sawako +6 more·2023·Science

Abstract

During Drosophila aversive olfactory conditioning, aversive shock information needs to be transmitted to the mushroom bodies (MBs) to associate with odor information. We report that aversive information is transmitted by ensheathing glia (EG) that surround the MBs. Shock induces vesicular exocytosis of glutamate from EG. Blocking exocytosis impairs aversive learning, whereas activation of EG can replace aversive stimuli during conditioning. Glutamate released from EG binds to N -methyl- d -aspartate receptors in the MBs, but because of Mg 2+ block, Ca 2+ influx occurs only when flies are simultaneously exposed to an odor. Vesicular exocytosis from EG also induces shock-associated dopamine release, which plays a role in preventing formation of inappropriate associations. These results demonstrate that vesicular glutamate released from EG transmits negative valence information required for associative learning.

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Crossref · 10.1126/science.adf7429

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Authors
Miyashita, T., Murakami, K., Kikuchi, E., Ofusa, K., Mikami, K., Endo, K., Miyaji, T., Moriyama, S., Konno, K., Muratani, H., Moriyama, Y., Watanabe, M., Horiuchi, J., & Saitoe, M.
Affiliations
  • Tokyo Metropolitan Institute of Medical Science (JP)
  • Okayama University (JP)
  • Kurume University (JP)
  • Hokkaido University (JP)
  • University of Electro-Communications (JP)
Corresponding author
Saitoe, Minoru
Venue
Science
Published
2023-12-22
Volume
382
Issue
6677
Pages
eadf7429-eadf7429
ISSN
  • 0036-8075 (ISSN-L)
  • 1095-9203
OpenAlex
W4390046017
Cited by
26
References
63
Citations by year
2026: 5 · 2025: 9 · 2024: 9 · 2023: 1 · 2022: 2
FWCI
2.91
Type
journal article
Language
en
Open access
closed
Locations
  • Science (publishedVersion)
  • PubMed (publishedVersion)
Funders
Japan Society for the Promotion of Science (19H01013, 21K19338, 21K06403, 21K18238, 23K24791)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Keywords
ensheathing glia, mushroom body, vesicular glutamate release, NMDA receptor, dopamine release, negative valence, aversive learning, Drosophila, associative learning
MeSH terms
Animals, Avoidance Learning, Conditioning, Psychological, Drosophila, Drosophila melanogaster, Glutamates, Neuroglia, Odorants, Smell, Mushroom Bodies

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