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The Journal of Neuroscience, February 4, 2004, 24(5):1217-1225; doi:10.1523/JNEUROSCI.1569-03.2004

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Cellular/Molecular
Dopamine and Glutamate Control Area-Restricted Search Behavior in Caenorhabditis elegans

Thomas Hills, Penelope J. Brockie, and Andres V. Maricq

Department of Biology, University of Utah, Salt Lake City, Utah 84112-0840

Area-restricted search (ARS) is a foraging strategy used by many animals to locate resources. The behavior is characterized by a time-dependent 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.

Key words: glutamate receptor; dopaminergic signaling; area-restricted search; locomotion; neural circuit; Caenorhabditis elegans; glr-1; glr-2; eat-4; cat-2

Received June 23, 2003; revised November 25, 2003; accepted December 8, 2003.




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