Neuropeptide feedback modifies odor-evoked dynamics in Caenorhabditis elegans olfactory neurons.
Many neurons release classical transmitters together with neuropeptide co-transmitters whose functions are incompletely understood. Here we define the relationship between two transmitters in the olfactory system of C. elegans, showing that a neuropeptide-to-neuropeptide feedback loop alters sensory dynamics in primary olfactory neurons. The AWC olfactory neuron is glutamatergic and also expresses the peptide NLP-1. Worms with nlp-1 mutations show increased AWC-dependent behaviors, suggesting that NLP-1 limits the normal response. The receptor for NLP-1 is the G protein-coupled receptor NPR-11, which acts in postsynaptic AIA interneurons. Feedback from AIA interneurons modulates odor-evoked calcium dynamics in AWC olfactory neurons and requires INS-1, a neuropeptide released from AIA. The neuropeptide feedback loop dampens behavioral responses to odors on short and long timescales. Our results point to neuronal dynamics as a site of behavioral regulation and reveal the ability of neuropeptide feedback to remodel sensory networks on multiple timescales.
Chalasani
Sreekanth H
SH
Howard Hughes Medical Institute, The Rockefeller University, New York, New York, USA.
Kato
Saul
S
Albrecht
Dirk R
DR
Nakagawa
Takao
T
Abbott
L F
LF
Bargmann
Cornelia I
CI
D000222:Adaptation, Physiological / Q000187:drug effects / Q000235:genetics; D000818:Animals; D030801:Animals, Genetically Modified; D001522:Behavior, Animal; D017173:Caenorhabditis elegans / Q000033:anatomy & histology / Q000235:genetics; D029742:Caenorhabditis elegans Proteins / Q000235:genetics; D002118:Calcium / Q000378:metabolism; D002461:Cell Line, Transformed; D004305:Dose-Response Relationship, Drug; D025461:Feedback, Physiological / Q000187:drug effects / Q000502:physiology*; D018698:Glutamic Acid / Q000494:pharmacology; D006801:Humans; D008959:Models, Neurological; D009154:Mutation / Q000235:genetics; D017711:Nonlinear Dynamics; D009812:Odorants; D009833:Olfactory Pathways / Q000166:cytology*; D010455:Peptides / Q000235:genetics / Q000494:pharmacology*; D017476:Receptors, Neuropeptide Y / Q000235:genetics / Q000502:physiology; D011984:Sensory Receptor Cells / Q000187:drug effects* / Q000502:physiology; D013997:Time Factors; D014162:Transfection / Q000379:methods
D029742:Caenorhabditis elegans Proteins; D010455:Peptides; D017476:Receptors, Neuropeptide Y; D018698:Glutamic Acid; D002118:Calcium