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Neuroligin tuning of pharyngeal pumping reveals an extrapharyngeal modulation of Caenorhabditis elegans feeding

Neuroligin tuning of pharyngeal pumping reveals an extrapharyngeal modulation of Caenorhabditis elegans feeding
Neuroligin tuning of pharyngeal pumping reveals an extrapharyngeal modulation of Caenorhabditis elegans feeding
The integration of distinct sensory modalities is essential for behavioural decision making. In C. elegans 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 on the microcircuits to modulating 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 C. elegans mutant in the single orthologous gene of human neuroligins, nlg-1, is defective in food induced pumping. This is not explained by an inability to sense food, as nlg-1 mutants are not defective in chemotaxis towards bacteria. In addition, we show that neuroligin is widely expressed in the nervous system including AIY, ADE, ALA, URX and HSN neurones. Interestingly, despite the deficit in pharyngeal pumping neuroligin is not expressed within the pharyngeal neuromuscular network, which suggests an extrapharyngeal regulation of this circuit. We resolve electrophysiologically the neuroligin contribution to the pharyngeal circuit by mimicking a food-dependent pumping, and show 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.
0022-0949
1-11
Calahorro, Fernando
dddfa373-d3cc-433f-8851-9ca37f2f3950
Keefe, Francesca
07c7cc98-405c-4d3e-a593-e4e059ddc575
Dillon, James
f406e30a-3ad4-4a53-80db-6694bab5e3ed
Holden-dye, Lindy
8032bf60-5db6-40cb-b71c-ddda9d212c8e
O'connor, Vincent
8021b06c-01a0-4925-9dde-a61c8fe278ca
Calahorro, Fernando
dddfa373-d3cc-433f-8851-9ca37f2f3950
Keefe, Francesca
07c7cc98-405c-4d3e-a593-e4e059ddc575
Dillon, James
f406e30a-3ad4-4a53-80db-6694bab5e3ed
Holden-dye, Lindy
8032bf60-5db6-40cb-b71c-ddda9d212c8e
O'connor, Vincent
8021b06c-01a0-4925-9dde-a61c8fe278ca

Calahorro, Fernando, Keefe, Francesca, Dillon, James, Holden-dye, Lindy and O'connor, Vincent (2019) Neuroligin tuning of pharyngeal pumping reveals an extrapharyngeal modulation of Caenorhabditis elegans feeding. The Journal of Experimental Biology, 222 ((Pt 3)), 1-11, [jeb.189423]. (doi:10.1242/jeb.189423).

Record type: Article

Abstract

The integration of distinct sensory modalities is essential for behavioural decision making. In C. elegans 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 on the microcircuits to modulating 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 C. elegans mutant in the single orthologous gene of human neuroligins, nlg-1, is defective in food induced pumping. This is not explained by an inability to sense food, as nlg-1 mutants are not defective in chemotaxis towards bacteria. In addition, we show that neuroligin is widely expressed in the nervous system including AIY, ADE, ALA, URX and HSN neurones. Interestingly, despite the deficit in pharyngeal pumping neuroligin is not expressed within the pharyngeal neuromuscular network, which suggests an extrapharyngeal regulation of this circuit. We resolve electrophysiologically the neuroligin contribution to the pharyngeal circuit by mimicking a food-dependent pumping, and show 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.

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jeb.189423.full - Accepted Manuscript
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Accepted/In Press date: 7 December 2018
e-pub ahead of print date: 17 December 2018
Published date: 8 February 2019

Identifiers

Local EPrints ID: 427850
URI: http://eprints.soton.ac.uk/id/eprint/427850
ISSN: 0022-0949
PURE UUID: d89a4bc5-f9a1-45f7-96b3-8457b170803c
ORCID for Fernando Calahorro: ORCID iD orcid.org/0000-0003-0659-7728
ORCID for Lindy Holden-dye: ORCID iD orcid.org/0000-0002-9704-1217

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Date deposited: 30 Jan 2019 17:30
Last modified: 18 Feb 2021 17:21

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