title: Decoding a neural circuit controlling global animal state in C. elegans.
abstract: Brains organize behavior and physiology to optimize the response to threats or opportunities. We dissect how 21% O2, an indicator of surface exposure, reprograms C. elegans' global state, inducing sustained locomotory arousal and altering expression of neuropeptides, metabolic enzymes, and other non-neural genes. The URX O2-sensing neurons drive arousal at 21% O2 by tonically activating the RMG interneurons. Stimulating RMG is sufficient to switch behavioral state. Ablating the ASH, ADL, or ASK sensory neurons connected to RMG by gap junctions does not disrupt arousal. However, disrupting cation currents in these neurons curtails RMG neurosecretion and arousal. RMG signals high O2 by peptidergic secretion. Neuropeptide reporters reveal neural circuit state, as neurosecretion stimulates neuropeptide expression. Neural imaging in unrestrained animals shows that URX and RMG encode O2 concentration rather than behavior, while the activity of downstream interneurons such as AVB and AIY reflect both O2 levels and the behavior being executed.
authors.affiliation: Laboratory of Molecular Biology, Cambridge, United Kingdom.
authors.forename: Patrick
authors.initials: P
authors.lastname: Laurent
authors.affiliation: Laboratory of Molecular Biology, Cambridge, United Kingdom.
authors.forename: Zoltan
authors.initials: Z
authors.lastname: Soltesz
authors.affiliation: Cell Biology Division, MRC Laboratory of Molecular Biology, Cambridge, United Kingdom.
authors.forename: Geoffrey M
authors.identifier: http://orcid.org/0000-0001-9825-4241
authors.initials: GM
authors.lastname: Nelson
authors.affiliation: Laboratory of Molecular Biology, Cambridge, United Kingdom.
authors.forename: Changchun
authors.initials: C
authors.lastname: Chen
authors.affiliation: Laboratory of Molecular Biology, Cambridge, United Kingdom.
authors.forename: Fausto
authors.initials: F
authors.lastname: Arellano-Carbajal
authors.affiliation: Laboratory of Molecular Biology, Cambridge, United Kingdom.
authors.forename: Emmanuel
authors.initials: E
authors.lastname: Levy
authors.affiliation: Laboratory of Molecular Biology, Cambridge, United Kingdom.
authors.forename: Mario
authors.initials: M
authors.lastname: de Bono
mesh_terms: D000818:Animals; D030801:Animals, Genetically Modified; D001143:Arousal / Q000235:genetics; D001522:Behavior, Animal; D017173:Caenorhabditis elegans / Q000166:cytology / Q000187:drug effects* / Q000235:genetics / Q000378:metabolism; D029742:Caenorhabditis elegans Proteins / Q000235:genetics / Q000378:metabolism; D002118:Calcium / Q000378:metabolism; D017629:Gap Junctions / Q000187:drug effects / Q000378:metabolism; D005786:Gene Expression Regulation; D007395:Interneurons / Q000166:cytology / Q000187:drug effects* / Q000378:metabolism; D017136:Ion Transport; D008124:Locomotion / Q000235:genetics; D009415:Nerve Net / Q000187:drug effects* / Q000378:metabolism; D009419:Nerve Tissue Proteins / Q000235:genetics / Q000378:metabolism; D009479:Neuropeptides / Q000235:genetics / Q000378:metabolism; D010100:Oxygen / Q000494:pharmacology*; D015221:Potassium Channels / Q000235:genetics / Q000378:metabolism; D017476:Receptors, Neuropeptide Y / Q000235:genetics / Q000378:metabolism; D011984:Sensory Receptor Cells / Q000166:cytology / Q000187:drug effects* / Q000378:metabolism; D015398:Signal Transduction; D050916:TRPV Cation Channels / Q000235:genetics / Q000378:metabolism
chemical_list: D029742:Caenorhabditis elegans Proteins; C583030:Flp-2 protein, C elegans; C468272:NPR-1 protein, C elegans; D009419:Nerve Tissue Proteins; D009479:Neuropeptides; C464590:OCR-2 protein, C elegans; D015221:Potassium Channels; D017476:Receptors, Neuropeptide Y; D050916:TRPV Cation Channels; D010100:Oxygen; D002118:Calcium
keywords: C. elegans; TRPV; caenorhabditis; gap junctions; neural circuit; neuroscience; optogenetics