Dopamine and Glutamate Control Area-Restricted Search Behavior inCaenorhabditis elegans

Abstract

Area-restricted search (ARS) is a foraging strategy used by many animals to locate resources. The behavior is characterized by a timedependent reduction in turning frequency after the last resource encounter. This maximizes the time spent in areas in which resources are abundant and extends the search to a larger area when resources become scarce. We demonstrate that dopaminergic and glutamatergic signaling contribute to the neural circuit controlling ARS in the nematode Caenorhabditis elegans. Ablation of dopaminergic neurons eliminated ARS behavior, as did application of the dopamine receptor antagonist raclopride. Furthermore, ARS was affected by mutations in the glutamate receptor subunits GLR-1 and GLR-2 and the EAT-4 glutamate vesicular transporter. Interestingly, preincubation on dopamine restored the behavior in worms with defective dopaminergic signaling, but not in glr-1, glr-2, or eat-4 mutants. This suggests that dopaminergic and glutamatergic signaling function in the same pathway to regulate turn frequency. Both GLR-1 and GLR-2 are expressed in the locomotory control circuit that modulates the direction of locomotion in response to sensory stimuli and the duration of forward movement during foraging. We propose a mechanism for ARS in C. elegans in which dopamine, released in response to food, modulates glutamatergic signaling in the locomotory control circuit, thus resulting in an increased turn frequency.

Choline Transport and de novo Choline Synthesis Support Acetylcholine Biosynthesis in Caenorhabditis elegans Cholinergic Neurons

“…Although cho-1 mutants exhibit relatively coordinated movements in simple crawling or swimming assays, cholinergic output may be reduced to the point that more complex movement behaviors are affected. Changes in spontaneous reversal frequency are also observed in mutants with defects in glutamatergic or dopaminergic signaling (Hills et al 2004). Our observations on cho-1 mutants suggest that cholinergic signaling may also regulate reversal frequency.…”

A Caenorhabditis elegans allatostatin/galanin-like receptor NPR-9 inhibits local search behavior in response to feeding cues

“…When the food supply is exhausted turning frequency decreases and the search area is increased. Dopamine released in response to food modulates glutamate signaling to regulate ARS turn frequency (31). The overexpressed receptor appears to override the dopamine/glutamate signaling of ARS behavior, supporting the close relationship of NPR-9 to glutamate signaling.…”

The Robustness ofCaenorhabditis elegansMale Mating Behavior Depends on the Distributed Properties of Ray Sensory Neurons and Their Output through Core and Male-Specific Targets

“…Destination vectors used in this study were ccdBrev::ICE (pZL16) and ccdB::ChR2-YFP (pZL5 or pLR167). ccdBrev::ICE was made by digesting pdat-1::ICE (Hills et al, 2004) with Sma1 and Pst1, end-filling, and then inserting the ccdB C.1 cassette (Invitrogen) in the reverse orientation. ccdB::ChR2-YFP (pZL5) was made by digesting mec-4::ChR2(H13R)-YFP (Nagel et al, 2005) with HindIII and BamHI to remove the mec-4 promoter, end-filling, and then inserting the ccdB C.1 cassette.…”

“…To address this question, we specifically eliminated either A-or B-neurons and assessed the impact on mating. Because laser ablation of neuron processes at the ray tip is not sufficiently accurate to selectively target either the A-or B-neuron process within a ray, we eliminated each neuron type by alternative means: through genetically targeted expression of heterologous cell death genes or by killing cells with conventional laser ablation approaches in which the laser microbeam is aimed at the neuron cell body (Bargmann and Avery, 1995;Hills et al, 2004;Chelur and Chalfie, 2007).…”