NPY/NPF-related neuropeptide FLP-34 signals from serotonergic neurons to modulate aversive olfactory learning in Caenorhabditis elegans

Melissa Fadda, Nathan De Fruyt, Charline Borghgraef, Jan Watteyne, Katleen Peymen, Elke Vandewyer, Francisco J.Naranjo Galindo, Amanda Kieswetter, Olivier Mirabeau, Yee Lian Chew, Isabel Beets, Liliane Schoofs

Research output: Contribution to journalArticlepeer-review

2 Citations (Scopus)

Abstract

Aversive learning is fundamental for animals to increase chances of survival. In addition to classical neurotransmitters, neuropeptides have emerged to modulate such complex behaviors. Among them, neuropeptide Y (NPY) is well known to promote aversive memory acquisition in mammals. Here we identify an NPY/neuropeptide F (NPF)-related neuropeptide system in Caenorhabditis elegans and show that this FLP-34/NPR-11 system is required for learning negative associations, a process that is reminiscent of NPY signaling in mammals. The Caenorhabditis elegans NPY/NPF ortholog FLP-34 displays conserved structural hallmarks of bilaterian-wide NPY/NPF neuropeptides. We show that it is required for aversive olfactory learning after pairing diacetyl with the absence of food, but not for appetitive olfactory learning in response to butanone. To mediate diacetyl learning and thus integrate the aversive food context with the diacetyl odor, FLP-34 is released from serotonergic neurons and signals through its evolutionarily conserved NPY/NPF GPCR, NPR-11, in downstream AIA interneurons. NPR-11 activation in the AIA integration center results in avoidance of a previously attractive stimulus. This study opens perspectives for a deeper understanding of stress conditions in which aversive learning results in excessive avoidance.

Original languageEnglish
Pages (from-to)6018-6034
Number of pages17
JournalJournal of Neuroscience
Volume40
Issue number31
DOIs
Publication statusPublished - 29 Jul 2020
Externally publishedYes

Keywords

  • Aversive learning
  • Caenorhabditis elegans
  • GPCR
  • Neuropeptide Y
  • Serotonin

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