Ras acts as a molecular switch between two forms of consolidated memory in Drosophila

Jan 15, 2020Proceedings of the National Academy of Sciences of the United States of America

Ras protein controls two types of long-term memory in fruit flies

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Abstract

The Ras→Raf→ROCK pathway in mushroom body neurons suppresses anesthesia-resistant memory consolidation, allowing for the formation of long-term memories.

Inhibition of the ROCK pathway enhances anesthesia-resistant memory (ARM) but impairs long-term memory (LTM).
Postacquisition Ras activity negatively affects memory performance when increased optogenetically.
Knockdown of Ras leads to enhanced memory expression through increased ARM but eliminates protein synthesis-dependent LTM.
The effects observed are mediated by the downstream kinase Raf, while canonical extracellular signal-regulated kinase does not replicate these outcomes.
Constitutively active ROCK enhances ARM and inhibits long-term memory formation, indicating its critical role in memory processes.

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Long-lasting, consolidated memories require not only positive biological processes that facilitate long-term memories (LTM) but also the suppression of inhibitory processes that prevent them. The mushroom body neurons (MBn) instore protein synthesis-dependent LTM (PSD-LTM) as well as protein synthesis-independent, anesthesia-resistant memory (ARM). The formation of ARM inhibits PSD-LTM but the underlying molecular processes that mediate this interaction remain unknown. Here, we demonstrate that the Ras→Raf→rho kinase (ROCK) pathway in MBn suppresses ARM consolidation, allowing the formation of PSD-LTM. Our initial results revealed that the effects of Ras on memory are due to postacquisition processes.knockdown enhanced memory expression but had no effect on acquisition. Additionally, increasing Ras activity optogenetically after, but not before, acquisition impaired memory performance. The elevated memory produced byknockdown is a result of increased ARM. Whileknockdown enhanced the consolidation of ARM, it eliminated PSD-LTM. We found that these effects are mediated by the downstream kinase Raf. Similar to, knockdown ofenhanced ARM consolidation and impaired PSD-LTM. Surprisingly, knockdown of the canonical downstream extracellular signal-regulated kinase did not reproduce the phenotypes observed withandknockdown. Rather, Ras/Raf inhibition of ROCK was found to be responsible for suppressing ARM. Constitutively active ROCK enhanced ARM and impaired PSD-LTM, while decreasing ROCK activity rescued the enhanced ARM produced byknockdown. We conclude that MBn Ras/Raf inhibition of ROCK suppresses the consolidation of ARM, which permits the formation of PSD-LTM. Drosophila melanogaster Ras Ras Ras Ras Raf Ras Raf Ras

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Ras acts as a molecular switch between two forms of consolidated memory in Drosophila

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