Multiple signaling pathways coordinately regulate forgetting of olfactory adaptation through control of sensory responses in caenorhabditis elegans

Tomohiro Kitazono, Sayuri Hara-Kuge, Osamu Matsuda, Akitoshi Inoue, Manabi Fujiwara, Takeshi Ishihara

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Abstract

Forgetting memories is important for animals to properly respond to continuously changing environments. To elucidate the mechanisms of forgetting, we used one of the behavioral plasticities of Caenorhabditis elegans hermaphrodite, olfactory adaptation to an attractive odorant, diacetyl, as a simple model of learning. In C. elegans, the TIR-1/JNK-1 pathway accelerates forgetting of olfactory adaptation by facilitating neural secretion from AWC sensory neurons. In this study, to identify the downstream effectors of the TIR-1/JNK-1 pathway, we conducted a genetic screen for suppressors of the gain-of-function mutant of tir-1 (ok1052), which shows excessive forgetting. Our screening showed that three proteins—a membrane protein, MACO-1; a receptor tyrosine kinase, SCD-2; and its putative ligand, HEN-1—regulated forgetting downstream of the TIR-1/JNK-1 pathway. We further demonstrated that MACO-1 and SCD-2/HEN-1 functioned in parallel genetic pathways, and only MACO-1 regulated forgetting of olfactory adaptation to isoamyl alcohol, which is an attractive odorant sensed by different types of sensory neurons. In olfactory adaptation, odor-evoked Ca2+ responses in olfactory neurons are attenuated by conditioning and recovered thereafter. A Ca2+ imaging study revealed that this attenuation is sustained longer in maco-1 and scd-2 mutant animals than in wild-type animals like the TIR-1/JNK-1 pathway mutants. Furthermore, temporal silencing by histamine-gated chloride channels revealed that the neuronal activity of AWC neurons after conditioning is important for proper forgetting. We propose that distinct signaling pathways, each of which has a specific function, may coordinately and temporally regulate forgetting by controlling sensory responses.

Original languageEnglish
Pages (from-to)10240-10251
Number of pages12
JournalJournal of Neuroscience
Volume37
Issue number42
DOIs
Publication statusPublished - Oct 18 2017

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MAP Kinase Signaling System
Caenorhabditis elegans
Sensory Receptor Cells
TYK2 Kinase
Neurons
Diacetyl
Chloride Channels
Wild Animals
Histamine
Membrane Proteins
Learning
Ligands
Odorants
Conditioning (Psychology)

All Science Journal Classification (ASJC) codes

  • Neuroscience(all)

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Multiple signaling pathways coordinately regulate forgetting of olfactory adaptation through control of sensory responses in caenorhabditis elegans. / Kitazono, Tomohiro; Hara-Kuge, Sayuri; Matsuda, Osamu; Inoue, Akitoshi; Fujiwara, Manabi; Ishihara, Takeshi.

In: Journal of Neuroscience, Vol. 37, No. 42, 18.10.2017, p. 10240-10251.

Research output: Contribution to journalArticle

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