title: Dissecting the signaling mechanisms underlying recognition and preference of food odors.
abstract: Food is critical for survival. Many animals, including the nematode Caenorhabditis elegans, use sensorimotor systems to detect and locate preferred food sources. However, the signaling mechanisms underlying food-choice behaviors are poorly understood. Here, we characterize the molecular signaling that regulates recognition and preference between different food odors in C. elegans. We show that the major olfactory sensory neurons, AWB and AWC, play essential roles in this behavior. A canonical Gα-protein, together with guanylate cyclases and cGMP-gated channels, is needed for the recognition of food odors. The food-odor-evoked signal is transmitted via glutamatergic neurotransmission from AWC and through AMPA and kainate-like glutamate receptor subunits. In contrast, peptidergic signaling is required to generate preference between different food odors while being dispensable for the recognition of the odors. We show that this regulation is achieved by the neuropeptide NLP-9 produced in AWB, which acts with its putative receptor NPR-18, and by the neuropeptide NLP-1 produced in AWC. In addition, another set of sensory neurons inhibits food-odor preference. These mechanistic logics, together with a previously mapped neural circuit underlying food-odor preference, provide a functional network linking sensory response, transduction, and downstream receptors to process complex olfactory information and generate the appropriate behavioral decision essential for survival.
authors.affiliation: Department of Organismic and Evolutionary Biology, Center for Brain Science, Harvard University, Cambridge, Massachusetts 02138, and.
authors.forename: Gareth
authors.initials: G
authors.lastname: Harris
authors.affiliation: Department of Organismic and Evolutionary Biology, Center for Brain Science, Harvard University, Cambridge, Massachusetts 02138, and.
authors.forename: Yu
authors.initials: Y
authors.lastname: Shen
authors.affiliation: Department of Organismic and Evolutionary Biology, Center for Brain Science, Harvard University, Cambridge, Massachusetts 02138, and.
authors.forename: Heonick
authors.initials: H
authors.lastname: Ha
authors.affiliation: Institute of Genetics and Biophysics of the National Research Council, 80131 Naples, Italy.
authors.forename: Alessandra
authors.identifier: http://orcid.org/0000-0002-5143-8681
authors.initials: A
authors.lastname: Donato
authors.affiliation: Department of Organismic and Evolutionary Biology, Center for Brain Science, Harvard University, Cambridge, Massachusetts 02138, and.
authors.forename: Samuel
authors.initials: S
authors.lastname: Wallis
authors.affiliation: Department of Organismic and Evolutionary Biology, Center for Brain Science, Harvard University, Cambridge, Massachusetts 02138, and.
authors.forename: Xiaodong
authors.initials: X
authors.lastname: Zhang
authors.affiliation: Department of Organismic and Evolutionary Biology, Center for Brain Science, Harvard University, Cambridge, Massachusetts 02138, and yzhang@oeb.harvard.edu.
authors.forename: Yun
authors.initials: Y
authors.lastname: Zhang
mesh_terms: D000818:Animals; D017173:Caenorhabditis elegans; D005502:Food / Q000145:classification; D005518:Food Preferences / Q000502:physiology*; D009415:Nerve Net / Q000502:physiology*; D009812:Odorants; D018034:Olfactory Receptor Neurons / Q000502:physiology*; D021641:Recognition, Psychology / Q000502:physiology*; D012903:Smell / Q000502:physiology*; D009435:Synaptic Transmission / Q000502:physiology*
keywords: glutamatergic transmission; neuropeptide signaling; olfactory sensory neurons; olfactory sensory signaling; preference of food odors