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Featured ArticleResearch Articles, Cellular/Molecular

Regulation of Diacylglycerol Content in Olfactory Neurons Determines Forgetting or Retrieval of Olfactory Memory in Caenorhabditis elegans

Mary Arai, Itsuki Kurokawa, Hoshinosuke Arakane, Tomohiro Kitazono and Takeshi Ishihara
Journal of Neuroscience 26 October 2022, 42 (43) 8039-8053; DOI: https://doi.org/10.1523/JNEUROSCI.0090-22.2022
Mary Arai
1Department of Biology, Faculty of Science, Kyushu University, Fukuoka, 819-0395, Japan
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Itsuki Kurokawa
2Graduate School of Systems Life Sciences, Kyushu University, Fukuoka, 819-0395, Japan
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Hoshinosuke Arakane
1Department of Biology, Faculty of Science, Kyushu University, Fukuoka, 819-0395, Japan
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Tomohiro Kitazono
2Graduate School of Systems Life Sciences, Kyushu University, Fukuoka, 819-0395, Japan
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Takeshi Ishihara
1Department of Biology, Faculty of Science, Kyushu University, Fukuoka, 819-0395, Japan
2Graduate School of Systems Life Sciences, Kyushu University, Fukuoka, 819-0395, Japan
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Abstract

Proper management of memories by forgetting and retrieval is essential for animals to adapt their behavior to changing environments. To elucidate the mechanisms underlying forgetting, we use olfactory learning to an attractive odorant, diacetyl, in Caenorhabditis elegans hermaphrodites as a model. In this learning paradigm, the TIR-1/JNK-1 pathway in AWC sensory neurons accelerates forgetting of the olfactory memory, which is stored as a sensory memory trace in AWA sensory neurons. Our genetic screening revealed that increased neuronal diacylglycerol in the olfactory neuronal circuit, by mutations in diacylglycerol kinase-1, egl-30 or goa-1, Gq and Go type G-proteins, suppresses the forgetting defect in the behavior of tir-1 mutants, although the calcium imaging analyses of the olfactory neurons revealed that the sensory memory trace to the odorant was maintained. In contrast, the expression of a gain-of-function goa-1 gene exclusively in AWC neurons caused a forgetting defect in behavior, although their sensory memory trace declined. Furthermore, the behavioral analysis of animals applied with diacylglycerol analog and measurement of diacylglycerol content by fluorescent imaging suggested that diacylglycerol content in AWC is important for the proper forgetting. These findings raise a possibility that diacylglycerol signaling plays a crucial role in determining whether to forget or to recall in olfactory learning.

SIGNIFICANCE STATEMENT Forgetting and retrieval are important processes for proper management of memories, although the mechanisms underlying these processes remain largely unclear. We found that, in Caenorhabditis elegans, diacylglycerol signaling works in a forgetting mechanism downstream of TIR-1/JNK-1 pathway. Mutations that change diacylglycerol content in the olfactory neurons affect behavioral forgetting, although they did not alter the sensory memory trace. This suggests that diacylglycerol in specific neurons may determine the occurrence of retrieving, rather than modifying, the memory traces. Consistent with this hypothesis, application of diacylglycerol analog to animals suggests that diacylglycerol content until memory acquisition decides whether to retrieve or to forget the memory.

  • C. elegans
  • Ca2+ imaging
  • diacylglycerol
  • forgetting
  • memory retrieval
  • memory trace

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The Journal of Neuroscience: 42 (43)
Journal of Neuroscience
Vol. 42, Issue 43
26 Oct 2022
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Regulation of Diacylglycerol Content in Olfactory Neurons Determines Forgetting or Retrieval of Olfactory Memory in Caenorhabditis elegans
Mary Arai, Itsuki Kurokawa, Hoshinosuke Arakane, Tomohiro Kitazono, Takeshi Ishihara
Journal of Neuroscience 26 October 2022, 42 (43) 8039-8053; DOI: 10.1523/JNEUROSCI.0090-22.2022

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Regulation of Diacylglycerol Content in Olfactory Neurons Determines Forgetting or Retrieval of Olfactory Memory in Caenorhabditis elegans
Mary Arai, Itsuki Kurokawa, Hoshinosuke Arakane, Tomohiro Kitazono, Takeshi Ishihara
Journal of Neuroscience 26 October 2022, 42 (43) 8039-8053; DOI: 10.1523/JNEUROSCI.0090-22.2022
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Keywords

  • C. elegans
  • Ca2+ imaging
  • diacylglycerol
  • forgetting
  • memory retrieval
  • memory trace

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