Search

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, inCaenorhabditis elegansadult hermaphrodites:C. elegansspecifically enhances chemotaxis to butanone by preexposure to butanone and food. Mutant analysis revealed that this plasticity requires the AWCONolfactory 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 AWCONneuron. Butanone enhancement also required the functions of Bardet-Biedl syndrome genes in the AWCONneuron 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 AWCONolfactory 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.

The enhancement of sensory responses after prior exposure to a stimulus is a fundamental mechanism of neural function in animals. Its molecular basis, however, has not been studied in as much depth as the reduction of sensory responses, such as adaptation or habituation. We report here that the avoidance behavior of the nematodeCaenorhabditis elegansin response to repellent odors (2-nonanone or 1-octanol) is enhanced rather than reduced after preexposure to the odors. This enhancement effect of preexposure was maintained for at least 1 h after the conditioning. The enhancement of 2-nonanone avoidance was not dependent on the presence or absence of food during conditioning, which generally functions as a strong positive or negative unconditioned stimulus in the animals. These results suggest that the enhancement is acquired as a type of nonassociative learning. In addition, genetic and pharmacological analyses revealed that the enhancement of 2-nonanone avoidance requires dopamine signaling via D2-like dopamine receptor DOP-3, which functions in a pair of RIC interneurons to regulate the enhancement. Because dopamine signaling has been tightly linked with food-related information to modulate various behaviors ofC. elegans, it may play different role in the regulation of the enhancement of 2-nonanone avoidance. Thus, our data suggest a new genetic and pharmacological paradigm for nonassociative enhancement of neural responses that is regulated by dopamine signaling.