Neuroligin tuning of pharyngeal pumping reveals extrapharyngeal modulation of feeding in Caenorhabditis elegans.

Abstract

The integration of distinct sensory modalities is essential for behavioural decision making. In Caenorhabditiselegans, this process is coordinated by neural circuits that integrate sensory cues from the environment to generate an appropriate behaviour at the appropriate output muscles. Food is a multimodal cue that impacts the microcircuits to modulate feeding and foraging drivers at the level of the pharyngeal and body wall muscle, respectively. When food triggers an upregulation in pharyngeal pumping, it allows the effective ingestion of food. Here, we show that a Celegans mutant in the single gene orthologous to human neuroligins, nlg-1, is defective in food-induced pumping. This was not due to an inability to sense food, as nlg-1 mutants were not defective in chemotaxis towards bacteria. In addition, we found that neuroligin is widely expressed in the nervous system, including AIY, ADE, ALA, URX and HSN neurons. Interestingly, despite the deficit in pharyngeal pumping, neuroligin was not expressed within the pharyngeal neuromuscular network, which suggests an extrapharyngeal regulation of this circuit. We resolved electrophysiologically the neuroligin contribution to the pharyngeal circuit by mimicking food-dependent pumping and found that the nlg-1 phenotype is similar to mutants impaired in GABAergic and/or glutamatergic signalling. We suggest that neuroligin organizes extrapharyngeal circuits that regulate the pharynx. These observations based on the molecular and cellular determinants of feeding are consistent with the emerging role of neuroligin in discretely impacting functional circuits underpinning complex behaviours.