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The Journal of Neuroscience, January 24, 2007, 27(4):741-750; doi:10.1523/JNEUROSCI.4312-06.2007

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Development/Plasticity/Repair
Caenorhabditis elegans Integrates the Signals of Butanone and Food to Enhance Chemotaxis to Butanone

Ichiro Torayama, Takeshi Ishihara, and Isao Katsura

Structural Biology Center, National Institute of Genetics, and Department of Genetics, The Graduate University for Advanced Studies, Mishima 411-8540, Japan

Correspondence should be addressed to Isao Katsura, Structural Biology Center, National Institute of Genetics, Mishima 411-8540, Japan. Email: ikatsura{at}lab.nig.ac.jp

Behavioral plasticity induced by the integration of two sensory signals, such as associative learning, is an important issue in neuroscience, but its evolutionary origin and diversity have not been explored sufficiently. We report here a new type of such behavioral plasticity, which we call butanone enhancement, in Caenorhabditis elegans adult hermaphrodites: C. elegans specifically enhances chemotaxis to butanone by preexposure to butanone and food. Mutant analysis revealed that this plasticity requires the AWC^ON olfactory neuron, whose fate is known to be determined by the NSY-1/ASK1 MAPKKK (mitogen-activated protein kinase kinase kinase) cascade as well as the DAF-11 and ODR-1 guanylyl cyclases. These proteins also control many aspects of olfactory sensation/plasticity in AWC neurons and seem to provide appropriate cellular conditions for butanone enhancement in the AWC^ON neuron. Butanone enhancement also required the functions of Bardet-Biedl syndrome genes in the AWC^ON neuron but not other genes that control ciliary transport. Furthermore, preexposure to butanone and the odor of food was enough for the enhancement of butanone chemotaxis. These results suggest that the AWC^ON olfactory neuron may conduct a behavioral plasticity resembling associative learning and that the functions of Bardet-Biedl syndrome genes in sensory cilia may play an important role in this plasticity.

Key words: C. elegans; olfactory neuron; learning; Bardet-Biedl syndrome; chemotaxis; sensory cilia

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Received Oct. 3, 2006; revised Dec. 4, 2006; accepted Dec. 5, 2006.

Correspondence should be addressed to Isao Katsura, Structural Biology Center, National Institute of Genetics, Mishima 411-8540, Japan. Email: ikatsura{at}lab.nig.ac.jp

Related articles in J. Neurosci.:

Butanone: The Memory of a Scent

Eiji Kodama and Paola Jurado
J. Neurosci. 2007 27: 5267-5268. [Full Text]  

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