TY - JOUR
T1 - NPY/NPF-related neuropeptide FLP-34 signals from serotonergic neurons to modulate aversive olfactory learning in Caenorhabditis elegans
AU - Fadda, Melissa
AU - De Fruyt, Nathan
AU - Borghgraef, Charline
AU - Watteyne, Jan
AU - Peymen, Katleen
AU - Vandewyer, Elke
AU - Galindo, Francisco J.Naranjo
AU - Kieswetter, Amanda
AU - Mirabeau, Olivier
AU - Chew, Yee Lian
AU - Beets, Isabel
AU - Schoofs, Liliane
PY - 2020/7/29
Y1 - 2020/7/29
N2 - 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.
AB - 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.
KW - Aversive learning
KW - Caenorhabditis elegans
KW - GPCR
KW - Neuropeptide Y
KW - Serotonin
UR - http://www.scopus.com/inward/record.url?scp=85088882437&partnerID=8YFLogxK
U2 - 10.1523/JNEUROSCI.2674-19.2020
DO - 10.1523/JNEUROSCI.2674-19.2020
M3 - Article
C2 - 32576621
AN - SCOPUS:85088882437
SN - 0270-6474
VL - 40
SP - 6018
EP - 6034
JO - Journal of Neuroscience
JF - Journal of Neuroscience
IS - 31
ER -