Electrical synapses between mushroom body neurons are critical for consolidated memory retrieval in Drosophila

Wei Huan Shyu, Wang Pao Lee, Meng Hsuan Chiang, Ching Ching Chang, Tsai Feng Fu, Hsueh Cheng Chiang, Tony Wu, Chia Lin Wu

Research output: Contribution to journalArticle

Abstract

Electrical synapses between neurons, also known as gap junctions, are direct cell membrane channels between adjacent neurons. Gap junctions play a role in the synchronization of neuronal network activity; however, their involvement in cognition has not been well characterized. Three-hour olfactory associative memory in Drosophila has two components: consolidated anesthesia-resistant memory (ARM) and labile anesthesia-sensitive memory (ASM). Here, we show that knockdown of the gap junction gene innexin5 (inx5) in mushroom body (MB) neurons disrupted ARM, while leaving ASM intact. Whole-mount brain immunohistochemistry indicated that INX5 protein was preferentially expressed in the somas, calyxes, and lobes regions of the MB neurons. Adult-stage-specific knockdown of inx5 in αβ neurons disrupted ARM, suggesting a specific requirement of INX5 in αβ neurons for ARM formation. Hyperpolarization of αβ neurons during memory retrieval by expressing an engineered halorhodopsin (eNpHR) also disrupted ARM. Administration of the gap junction blocker carbenoxolone (CBX) reduced the proportion of odor responsive αβ neurons to the training odor 3 hours after training. Finally, the α-branch-specific 3-hour ARM-specific memory trace was also diminished with CBX treatment and in inx5 knockdown flies. Altogether, our results suggest INX5 gap junction channels in αβ neurons for ARM retrieval and also provide a more detailed neuronal mechanism for consolidated memory in Drosophila.

Original languageEnglish
Article numbere1008153
JournalPLoS genetics
Volume15
Issue number5
DOIs
Publication statusPublished - 2019 Jan 1

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Electrical Synapses
Mushroom Bodies
mushroom bodies
mushroom
synapse
Drosophila
neurons
Neurons
anesthesia
Anesthesia
gap junctions
Gap Junctions
Carbenoxolone
odor
Halorhodopsins
odors
cognition
Carisoprodol
calyx
Ion Channels

All Science Journal Classification (ASJC) codes

  • Ecology, Evolution, Behavior and Systematics
  • Molecular Biology
  • Genetics
  • Genetics(clinical)
  • Cancer Research

Cite this

Shyu, Wei Huan ; Lee, Wang Pao ; Chiang, Meng Hsuan ; Chang, Ching Ching ; Fu, Tsai Feng ; Chiang, Hsueh Cheng ; Wu, Tony ; Wu, Chia Lin. / Electrical synapses between mushroom body neurons are critical for consolidated memory retrieval in Drosophila. In: PLoS genetics. 2019 ; Vol. 15, No. 5.
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Electrical synapses between mushroom body neurons are critical for consolidated memory retrieval in Drosophila. / Shyu, Wei Huan; Lee, Wang Pao; Chiang, Meng Hsuan; Chang, Ching Ching; Fu, Tsai Feng; Chiang, Hsueh Cheng; Wu, Tony; Wu, Chia Lin.

In: PLoS genetics, Vol. 15, No. 5, e1008153, 01.01.2019.

Research output: Contribution to journalArticle

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AU - Shyu, Wei Huan

AU - Lee, Wang Pao

AU - Chiang, Meng Hsuan

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AU - Fu, Tsai Feng

AU - Chiang, Hsueh Cheng

AU - Wu, Tony

AU - Wu, Chia Lin

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