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Neuropeptidergic integration of behavior in Trichoplax adhaerens, an animal without synapses

Trichoplax adhaerens is a flat, millimeter-sized marine animal that adheres to surfaces and grazes on algae. Trichoplax displays a repertoire of different feeding behaviors despite the apparent absence of a true nervous system with electrical or chemical synapses. It glides along surfaces to find fo...

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Autores principales: Senatore, Adriano, Reese, Thomas S., Smith, Carolyn L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Company of Biologists Ltd 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5612019/
https://www.ncbi.nlm.nih.gov/pubmed/28931721
http://dx.doi.org/10.1242/jeb.162396
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author Senatore, Adriano
Reese, Thomas S.
Smith, Carolyn L.
author_facet Senatore, Adriano
Reese, Thomas S.
Smith, Carolyn L.
author_sort Senatore, Adriano
collection PubMed
description Trichoplax adhaerens is a flat, millimeter-sized marine animal that adheres to surfaces and grazes on algae. Trichoplax displays a repertoire of different feeding behaviors despite the apparent absence of a true nervous system with electrical or chemical synapses. It glides along surfaces to find food, propelled by beating cilia on cells at its ventral surface, and pauses during feeding by arresting ciliary beating. We found that when endomorphin-like peptides are applied to an animal, ciliary beating is arrested, mimicking natural feeding pauses. Antibodies against these neuropeptides label cells that express the neurosecretory proteins and voltage-gated calcium channels implicated in regulated secretion. These cells are embedded in the ventral epithelium, where they comprise only 4% of the total, and are concentrated around the edge of the animal. Each bears a cilium likely to be chemosensory and used to detect algae. Trichoplax pausing during feeding or spontaneously in the absence of food often induce their neighbors to pause as well, even neighbors not in direct contact. Pausing behavior propagates from animal to animal across distances much greater than the signal that diffuses from just one animal, so we presume that the peptides secreted from one animal elicit secretion from nearby animals. Signal amplification by peptide-induced peptide secretion explains how a small number of sensory secretory cells lacking processes and synapses can evoke a wave of peptide secretion across the entire animal to globally arrest ciliary beating and allow pausing during feeding.
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spelling pubmed-56120192017-10-13 Neuropeptidergic integration of behavior in Trichoplax adhaerens, an animal without synapses Senatore, Adriano Reese, Thomas S. Smith, Carolyn L. J Exp Biol Research Article Trichoplax adhaerens is a flat, millimeter-sized marine animal that adheres to surfaces and grazes on algae. Trichoplax displays a repertoire of different feeding behaviors despite the apparent absence of a true nervous system with electrical or chemical synapses. It glides along surfaces to find food, propelled by beating cilia on cells at its ventral surface, and pauses during feeding by arresting ciliary beating. We found that when endomorphin-like peptides are applied to an animal, ciliary beating is arrested, mimicking natural feeding pauses. Antibodies against these neuropeptides label cells that express the neurosecretory proteins and voltage-gated calcium channels implicated in regulated secretion. These cells are embedded in the ventral epithelium, where they comprise only 4% of the total, and are concentrated around the edge of the animal. Each bears a cilium likely to be chemosensory and used to detect algae. Trichoplax pausing during feeding or spontaneously in the absence of food often induce their neighbors to pause as well, even neighbors not in direct contact. Pausing behavior propagates from animal to animal across distances much greater than the signal that diffuses from just one animal, so we presume that the peptides secreted from one animal elicit secretion from nearby animals. Signal amplification by peptide-induced peptide secretion explains how a small number of sensory secretory cells lacking processes and synapses can evoke a wave of peptide secretion across the entire animal to globally arrest ciliary beating and allow pausing during feeding. The Company of Biologists Ltd 2017-09-15 /pmc/articles/PMC5612019/ /pubmed/28931721 http://dx.doi.org/10.1242/jeb.162396 Text en © 2017. Published by The Company of Biologists Ltd http://creativecommons.org/licenses/by/3.0This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Article
Senatore, Adriano
Reese, Thomas S.
Smith, Carolyn L.
Neuropeptidergic integration of behavior in Trichoplax adhaerens, an animal without synapses
title Neuropeptidergic integration of behavior in Trichoplax adhaerens, an animal without synapses
title_full Neuropeptidergic integration of behavior in Trichoplax adhaerens, an animal without synapses
title_fullStr Neuropeptidergic integration of behavior in Trichoplax adhaerens, an animal without synapses
title_full_unstemmed Neuropeptidergic integration of behavior in Trichoplax adhaerens, an animal without synapses
title_short Neuropeptidergic integration of behavior in Trichoplax adhaerens, an animal without synapses
title_sort neuropeptidergic integration of behavior in trichoplax adhaerens, an animal without synapses
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5612019/
https://www.ncbi.nlm.nih.gov/pubmed/28931721
http://dx.doi.org/10.1242/jeb.162396
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