A behavioral switch: cGMP and PKC signaling in olfactory neurons reverses odor preference in C. elegans.
Innate chemosensory preferences are often encoded by sensory neurons that are specialized for attractive or avoidance behaviors. Here, we show that one olfactory neuron in Caenorhabditis elegans, AWC(ON), has the potential to direct both attraction and repulsion. Attraction, the typical AWC(ON) behavior, requires a receptor-like guanylate cyclase GCY-28 that acts in adults and localizes to AWC(ON) axons. gcy-28 mutants avoid AWC(ON)-sensed odors; they have normal odor-evoked calcium responses in AWC(ON) but reversed turning biases in odor gradients. In addition to gcy-28, a diacylglycerol/protein kinase C pathway that regulates neurotransmission switches AWC(ON) odor preferences. A behavioral switch in AWC(ON) may be part of normal olfactory plasticity, as odor conditioning can induce odor avoidance in wild-type animals. Genetic interactions, acute rescue, and calcium imaging suggest that the behavioral reversal results from presynaptic changes in AWC(ON). These results suggest that alternative modes of neurotransmission can couple one sensory neuron to opposite behavioral outputs.
Tsunozaki
Makoto
M
Howard Hughes Medical Institute, Laboratory of Neural Circuits and Behavior, The Rockefeller University, New York, NY 10065, USA.
Chalasani
Sreekanth H
SH
Bargmann
Cornelia I
CI
D000818:Animals; D001070:Appetitive Behavior / Q000502:physiology; D001362:Avoidance Learning / Q000502:physiology*; D001522:Behavior, Animal / Q000502:physiology; D017173:Caenorhabditis elegans / Q000502:physiology*; D029742:Caenorhabditis elegans Proteins / Q000235:genetics* / Q000378:metabolism; D002633:Chemotaxis / Q000235:genetics / Q000502:physiology; D006162:Guanylate Cyclase / Q000235:genetics / Q000378:metabolism*; D009419:Nerve Tissue Proteins / Q000235:genetics; D009475:Neurons, Afferent / Q000378:metabolism*; D017346:Protein Serine-Threonine Kinases / Q000235:genetics / Q000378:metabolism; D015398:Signal Transduction / Q000502:physiology; D012903:Smell / Q000502:physiology*
D029742:Caenorhabditis elegans Proteins; D009419:Nerve Tissue Proteins; C532433:NSY-1 protein, C elegans; D017346:Protein Serine-Threonine Kinases; D006162:Guanylate Cyclase