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Control of Locomotory Behavior of Caenorhabditis elegans by the Immunoglobulin Superfamily Protein RIG-3.

ABSTRACT: Cell surface immunoglobulin superfamily (IgSF) proteins play important roles in the development and function of the nervous system . Here we define the role of a Caenorhabditis elegans IgSF protein, RIG-3, in the function of the AVA command interneuron. This study reveals that RIG-3 regulates the abundance of the glutamate receptor subunit, GLR-1, in the AVA command interneuron and also regulates reversal behavior in C. elegans The mutant strain lacking rig-3 (rig-3 (ok2156)) shows increased reversal frequency during local search behaviors. Genetic and behavioral experiments suggest that RIG-3 functions through GLR-1 to regulate reversal behavior. We also show that the increased reversal frequency seen in rig-3 mutants is dependent on the increase in GLR-1 abundance at synaptic inputs to AVA, suggesting that RIG-3 alters the synaptic strength of incoming synapses through GLR-1 Consistent with the imaging experiments, altered synaptic strength was also reflected in increased calcium transients in rig-3 mutants when compared to wild-type control animals. Our results further suggest that animals lacking rig-3 show increased AVA activity, allowing the release of FLP-18 neuropeptide from AVA, which is an activity-dependent signaling molecule. Finally, we show that FLP-18 functions through the neuropeptide receptor, NPR-5, to modulate reversal behavior in C. elegans.

SUBMITTER: Bhardwaj A

PROVIDER: S-EPMC6944407 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The nematode Caenorhabditis elegans provides a unique opportunity to interrogate the neural basis of behavior at single neuron resolution. In C. elegans, neural circuits that control behaviors can be formulated based on its complete neural connection map, and easily assessed by applying advanced genetic tools that allow for modulation in the activity of specific neurons. Importantly, C. elegans exhibits several elaborate behaviors that can be empirically quantified and analyzed, thus providing a means to assess the contribution of specific neural circuits to behavioral output. Particularly, locomotory behavior can be recorded and analyzed with computational and mathematical tools. Here, we describe a robust single worm-tracking system, which is based on the open-source Python programming language, and an analysis system, which implements path-related algorithms. Our tracking system was designed to accommodate worms that explore a large area with frequent turns and reversals at high speeds. As a proof of principle, we used our tracker to record the movements of wild-type animals that were freshly removed from abundant bacterial food, and determined how wild-type animals change locomotory behavior over a long period of time. Consistent with previous findings, we observed that wild-type animals show a transition from area-restricted local search to global search over time. Intriguingly, we found that wild-type animals initially exhibit short, random movements interrupted by infrequent long trajectories. This movement pattern often coincides with local/global search behavior, and visually resembles Lévy flight search, a search behavior conserved across species. Our mathematical analysis showed that while most of the animals exhibited Brownian walks, approximately 20% of the animals exhibited Lévy flights, indicating that C. elegans can use Lévy flights for efficient food search. In summary, our tracker and analysis software will help analyze the neural basis of the alteration and transition of C. elegans locomotory behavior in a food-deprived condition.

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Control of Locomotory Behavior of Caenorhabditis elegans by the Immunoglobulin Superfamily Protein RIG-3.

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