Abstract
Pheromone responses are highly context dependent. For example, the C. elegans pheromone ascaroside C9 (ascr#3) is repulsive to wild-type hermaphrodites, attractive to wild-type males, and usually neutral to "social" hermaphrodites with reduced activity of the npr-1 neuropeptide receptor gene. We show here that these distinct behavioral responses arise from overlapping push-pull circuits driven by two classes of pheromone-sensing neurons. The ADL sensory neurons detect C9 and, in wild-type hermaphrodites, drive C9 repulsion through their chemical synapses. In npr-1 mutant hermaphrodites, C9 repulsion is reduced by the recruitment of a gap junction circuit that antagonizes ADL chemical synapses. In males, ADL sensory responses are diminished; in addition, a second pheromone-sensing neuron, ASK, antagonizes C9 repulsion. The additive effects of these antagonistic circuit elements generate attractive, repulsive, or neutral pheromone responses. Neuronal modulation by circuit state and sex, and flexibility in synaptic output pathways, may permit small circuits to maximize their adaptive behavioral outputs.
Copyright © 2012 Elsevier Inc. All rights reserved.
Publication types
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Research Support, N.I.H., Extramural
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Research Support, Non-U.S. Gov't
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Research Support, U.S. Gov't, Non-P.H.S.
MeSH terms
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Analysis of Variance
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Animals
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Animals, Genetically Modified
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Caenorhabditis elegans / drug effects*
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Caenorhabditis elegans / physiology
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Caenorhabditis elegans Proteins / genetics
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Calcium / metabolism
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Complement C9 / pharmacology
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Dose-Response Relationship, Drug
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Drug Interactions
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Escape Reaction / drug effects
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Escape Reaction / physiology
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Female
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Green Fluorescent Proteins / genetics
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Green Fluorescent Proteins / metabolism
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Immunologic Factors
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Luminescent Proteins / genetics
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Luminescent Proteins / metabolism
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Male
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Mutation / genetics
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Nerve Net / drug effects
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Nerve Net / physiology
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Nerve Tissue Proteins / genetics
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Neural Pathways / drug effects
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Neural Pathways / physiology
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Neurons / classification
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Neurons / drug effects
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Neurons / physiology*
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Neurotransmitter Agents / metabolism*
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Neurotransmitter Agents / pharmacology
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Pheromones / metabolism
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Pheromones / pharmacology*
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Reaction Time / drug effects
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Reaction Time / genetics
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Receptors, Neuropeptide Y / genetics
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Receptors, Odorant / genetics
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Sex Characteristics*
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Synapses / classification
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Synapses / drug effects*
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Synapses / genetics
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TRPV Cation Channels
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Transient Receptor Potential Channels / genetics
Substances
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Caenorhabditis elegans Proteins
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Complement C9
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Immunologic Factors
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Luminescent Proteins
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NPR-1 protein, C elegans
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Nerve Tissue Proteins
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Neurotransmitter Agents
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OSM-9 protein, C elegans
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Pheromones
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Receptors, Neuropeptide Y
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Receptors, Odorant
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TRPV Cation Channels
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Transient Receptor Potential Channels
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fluorescent protein 583
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odr-7 protein, C elegans
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Green Fluorescent Proteins
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Calcium