A Gustatory Neural Circuit of<i>Caenorhabditis elegans</i>Generates Memory-Dependent Behaviors in Na⁺Chemotaxis

Abstract

Animals show various behaviors in response to environmental chemicals. These behaviors are often plastic depending on previous experiences. <i>Caenorhabditis elegans</i>, which has highly developed chemosensory system with a limited number of sensory neurons, is an ideal model for analyzing the role of each neuron in innate and learned behaviors. Here, we report a new type of memory-dependent behavioral plasticity in Na⁺ chemotaxis generated by the left member of bilateral gustatory neuron pair ASE (ASEL neuron). When worms were cultivated in the presence of Na⁺, they showed positive chemotaxis toward Na⁺, but when cultivated under Na⁺-free conditions, they showed no preference regarding Na⁺ concentration. Both channelrhodopsin-2 (ChR2) activation with blue light and up-steps of Na⁺ concentration activated ASEL only after cultivation with Na⁺, as judged by increase in intracellular Ca²⁺ Under cultivation conditions with Na⁺, photoactivation of ASEL caused activation of its downstream interneurons AIY and AIA, which stimulate forward locomotion, and inhibition of its downstream interneuron AIB, which inhibits the turning/reversal behavior, and overall drove worms toward higher Na⁺ concentrations. We also found that the Gq signaling pathway and the neurotransmitter glutamate are both involved in the behavioral response generated by ASEL.<b>SIGNIFICANCE STATEMENT</b> Animals have acquired various types of behavioral plasticity during their long evolutionary history. <i>Caenorhabditis elegans</i> prefers odors associated with food, but plastically changes its behavioral response according to previous experience. Here, we report a new type of behavioral response generated by a single gustatory sensory neuron, the ASE-left (ASEL) neuron. ASEL did not respond to photostimulation or upsteps of Na⁺ concentration when worms were cultivated in Na⁺-free conditions; however, when worms were cultivated with Na⁺, ASEL responded and inhibited AIB to avoid turning and stimulated AIY and AIA to promote forward locomotion, which collectively drove worms toward higher Na⁺ concentrations. Glutamate and the Gq signaling pathway are essential for driving worms toward higher Na⁺ concentrations.