title: The cyclic nucleotide gated channel subunit CNG-1 instructs behavioral outputs in Caenorhabditis elegans by coincidence detection of nutritional status and olfactory input.
abstract: In mammals, olfactory subsystems have been shown to express seven-transmembrane G-protein-coupled receptors (GPCRs) in a one-receptor-one-neuron pattern, whereas in Caenorhabditis elegans, olfactory sensory neurons express multiple G-protein coupled odorant receptors per olfactory sensory neuron. In both mammalian and C. elegans olfactory sensory neurons (OSNs), the process of olfactory adaptation begins within the OSN; this process of negative feedback within the mammalian OSN has been well described in mammals and enables activated OSNs to desensitize their response cell autonomously while attending to odors detected by separate OSNs. However, the mechanism that enables C. elegans to adapt to one odor and attend to another odor sensed by the same olfactory sensory neuron remains unclear. We found that the cyclic nucleotide gated channel subunit CNG-1 is required to promote cross adaptation responses between distinct olfactory cues. This change in sensitivity to a pair of odorants after persistent stimulation by just one of these odors is modulated by the internal nutritional state of the animal, and we find that this response is maintained across a diverse range of food sources for C. elegans. We also reveal that CNG-1 integrates food related cues for exploratory motor output, revealing that CNG-1 functions in multiple capacities to link nutritional information with behavioral output. Our data describes a novel model whereby CNG channels can integrate the coincidence detection of appetitive and olfactory information to set olfactory preferences and instruct behavioral outputs.
authors: Department of Biological Sciences, The George Washington University, Science and Engineering Hall 6000, 800 22nd St N.W., Washington DC, 20052, USA; Institute for Neuroscience, The George Washington University, 636 Ross Hall, 2300 I St. NW, Washington DC, 20052, USA.
authors: Chao
authors: C
authors: He
authors: UCSF Diabetes Center, Eli and Edythe Broad Center of Regeneration Medicine and Stem Cell Research, Department of Cell and Tissue Biology, University of California, San Francisco, CA 94143, USA.
authors: Svetlana
authors: S
authors: Altshuler-Keylin
authors: Department of Biological Sciences, The George Washington University, Science and Engineering Hall 6000, 800 22nd St N.W., Washington DC, 20052, USA; Institute for Neuroscience, The George Washington University, 636 Ross Hall, 2300 I St. NW, Washington DC, 20052, USA.
authors: David
authors: D
authors: Daniel
authors: Kavli Institute for Fundamental Neuroscience, Department of Cell and Tissue Biology, UCSF, 513 Parnassus Avenue HSW 717, UCSF, USA.
authors: Noelle D
authors: ND
authors: L'Etoile
authors: Department of Biological Sciences, The George Washington University, Science and Engineering Hall 6000, 800 22nd St N.W., Washington DC, 20052, USA; Institute for Neuroscience, The George Washington University, 636 Ross Hall, 2300 I St. NW, Washington DC, 20052, USA. Electronic address: damienoh@gwu.edu.
authors: Damien
authors: D
authors: O'Halloran
mesh_terms: D000818:Animals; D030801:Animals, Genetically Modified; D001522:Behavior, Animal / Q000502:physiology; D017173:Caenorhabditis elegans; D029742:Caenorhabditis elegans Proteins / Q000235:genetics / Q000378:metabolism*; D002633:Chemotaxis / Q000502:physiology*; D054815:Cyclic Nucleotide-Gated Cation Channels / Q000235:genetics / Q000378:metabolism*; D007473:Ion Channels / Q000235:genetics / Q000378:metabolism*; D009752:Nutritional Status; D009812:Odorants; D018034:Olfactory Receptor Neurons / Q000378:metabolism*; D018035:Receptors, Odorant / Q000378:metabolism; D012903:Smell / Q000502:physiology*
chemical_list: C502366:CNG-1 protein, C elegans; D029742:Caenorhabditis elegans Proteins; D054815:Cyclic Nucleotide-Gated Cation Channels; D007473:Ion Channels; D018035:Receptors, Odorant
keywords: Adaptation; C. elegans; CNG channel; Olfaction