Gustatory plasticity in C. elegans involves integration of negative cues and NaCl taste mediated by serotonin, dopamine, and glutamate

Abstract

While naïve Caenorhabditis elegans individuals are attracted to 0.1-200 mM NaCl, they become strongly repelled by these NaCl concentrations after prolonged exposure to 100 mM NaCl. We call this behavior gustatory plasticity. Here, we show that C. elegans displays avoidance of low NaCl concentrations only when pre-exposure to NaCl is combined with a negative stimulus, e.g., a repellent, or in the absence of food. By testing serotonin and/or dopamine signaling mutants and rescue by exogenously supplying these neurotransmitters, we found that serotonin and dopamine play a role during the plasticity response, while serotonin is also required during development. In addition, we also show that glutamate plays an important role in the response to NaCl, both in chemoattraction to NaCl and in gustatory plasticity. Thus, C. elegans can associate NaCl with negative stimuli using dopaminergic, serotonergic, and glutamatergic neurotransmission. Finally, we show that prolonged starvation enhances gustatory plasticity and can induce avoidance of NaCl in most gustatory plasticity mutants tested. Only mutation of the glutamate-gated Cl − channel gene avr-15 affected starvation-enhanced gustatory plasticity. These results suggest that starvation induces avoidance of NaCl largely independent of the normal gustatory plasticity mechanism.

An elegant mind: Learning and memory in Caenorhabditis elegans

“…The pairing of starvation with NaCl must have caused the aversion because animals starved on plates without NaCl did not develop it, nor did unstarved worms on NaCl containing plates. In addition to starvation, Hukema et al (2008) demonstrated that worms could also learn to associate NaCl with aversive stimuli (glycerol or undiluted benzaldehyde).The switch of NaCl from attractant to repellent occurred gradually (maximizing after 4 h of starvation) and was readily reversible, within an hour if worms were starved in the absence of NaCl and within 10 min if NaCl was presented with food. Saeki et al (2001) showed that learned aversion to NaCl generalized to other water-soluble attractants sensed by ASE, including cAMP, biotin, and lysine, suggesting that the changes were occurring at the cellular rather than the receptor level.…”

“…3). Hukema et al (2008) implicated serotonergic, dopaminergic, and glutamatergic signaling in this process.…”

Chronic nicotine exposure augments gustatory plasticity inCaenorhabditis elegans:involvement of dopamine signaling

“…2(A) and (B)). It is well known that nematodes show an avoidance response to NaCl after pre-exposure to this chemical without food, 18,38,39) whereas NaCl is an attractant for the nematodes. This gustatory plasticity represents a simple form of associative learning.…”

“…39) In salt-associative learning, involvement of both serotonin and dopamine as a component of food signaling and insulin-like signaling pathways is reported. 15,32,39) In the present study, bas-1, tph-1, and cat-2 mutants subjected to nicotine−/NaCl+ treatment displayed gustatory plasticity (Figs.…”

Glutamate-gated Chloride Channels

“…AVR-15 is also widely expressed in the nervous system but, in addition, is found in muscle cells of the pharynx (29, 55) along with GLC-2 (56). Mutations in avr-15 affect gustatory plasticity (57) and, along with avr-14, mediate mechanosensory inhibition of pharyngeal pumping (58). GLC-3 is expressed in the AIY interneuron, where it receives inputs from the AWC and AFD neurons, regulating the worm's responses to odors (59) and temperature (60), respectively.…”