A single neuron subset governs a single coactive neuron circuit in Hydra vulgaris, representing a possible ancestral feature of neural evolution

Abstract The last common ancestor of Bilateria and Cnidaria is believed to be one of the first animals to develop a nervous system over 500 million years ago. Many of the genes involved in the neural function of the advanced nervous system in Bilateria are well conserved in Cnidaria. Thus, the cnida...

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Autores principales:	Yukihiko Noro, Hiroshi Shimizu, Katsuhiko Mineta, Takashi Gojobori
Formato:	article
Lenguaje:	EN
Publicado:	Nature Portfolio 2021
Materias:	Medicine R Science Q
Acceso en línea:	https://doaj.org/article/44a467e2ebcf4b0ab0905de782e24818
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spelling	oai:doaj.org-article:44a467e2ebcf4b0ab0905de782e248182021-12-02T15:00:20ZA single neuron subset governs a single coactive neuron circuit in Hydra vulgaris, representing a possible ancestral feature of neural evolution10.1038/s41598-021-89325-x2045-2322https://doaj.org/article/44a467e2ebcf4b0ab0905de782e248182021-05-01T00:00:00Zhttps://doi.org/10.1038/s41598-021-89325-xhttps://doaj.org/toc/2045-2322Abstract The last common ancestor of Bilateria and Cnidaria is believed to be one of the first animals to develop a nervous system over 500 million years ago. Many of the genes involved in the neural function of the advanced nervous system in Bilateria are well conserved in Cnidaria. Thus, the cnidarian Hydra vulgaris is a good model organism for the study of the putative primitive nervous system in its last common ancestor. The diffuse nervous system of Hydra consists of several peptidergic neuron subsets. However, the specific functions of these subsets remain unclear. Using calcium imaging, here we show that the neuron subsets that express neuropeptide, Hym-176, function as motor circuits to evoke longitudinal contraction. We found that all neurons in a subset defined by the Hym-176 gene (Hym-176A) or its paralogs (Hym-176B) expression are excited simultaneously, followed by longitudinal contraction. This indicates not only that these neuron subsets have a motor function but also that a single molecularly defined neuron subset forms a single coactive circuit. This is in contrast with the bilaterian nervous system, where a single molecularly defined neuron subset harbors multiple coactive circuits, showing a mixture of neurons firing with different timings. Furthermore, we found that the two motor circuits, one expressing Hym-176B in the body column and the other expressing Hym-176A in the foot, are coordinately regulated to exert region-specific contraction. Our results demonstrate that one neuron subset is likely to form a monofunctional circuit as a minimum functional unit to build a more complex behavior in Hydra. This simple feature (one subset, one circuit, one function) found in Hydra may represent the simple ancestral condition of neural evolution.Yukihiko NoroHiroshi ShimizuKatsuhiko MinetaTakashi GojoboriNature PortfolioarticleMedicineRScienceQENScientific Reports, Vol 11, Iss 1, Pp 1-12 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Medicine R Science Q
spellingShingle	Medicine R Science Q Yukihiko Noro Hiroshi Shimizu Katsuhiko Mineta Takashi Gojobori A single neuron subset governs a single coactive neuron circuit in Hydra vulgaris, representing a possible ancestral feature of neural evolution
description	Abstract The last common ancestor of Bilateria and Cnidaria is believed to be one of the first animals to develop a nervous system over 500 million years ago. Many of the genes involved in the neural function of the advanced nervous system in Bilateria are well conserved in Cnidaria. Thus, the cnidarian Hydra vulgaris is a good model organism for the study of the putative primitive nervous system in its last common ancestor. The diffuse nervous system of Hydra consists of several peptidergic neuron subsets. However, the specific functions of these subsets remain unclear. Using calcium imaging, here we show that the neuron subsets that express neuropeptide, Hym-176, function as motor circuits to evoke longitudinal contraction. We found that all neurons in a subset defined by the Hym-176 gene (Hym-176A) or its paralogs (Hym-176B) expression are excited simultaneously, followed by longitudinal contraction. This indicates not only that these neuron subsets have a motor function but also that a single molecularly defined neuron subset forms a single coactive circuit. This is in contrast with the bilaterian nervous system, where a single molecularly defined neuron subset harbors multiple coactive circuits, showing a mixture of neurons firing with different timings. Furthermore, we found that the two motor circuits, one expressing Hym-176B in the body column and the other expressing Hym-176A in the foot, are coordinately regulated to exert region-specific contraction. Our results demonstrate that one neuron subset is likely to form a monofunctional circuit as a minimum functional unit to build a more complex behavior in Hydra. This simple feature (one subset, one circuit, one function) found in Hydra may represent the simple ancestral condition of neural evolution.
format	article
author	Yukihiko Noro Hiroshi Shimizu Katsuhiko Mineta Takashi Gojobori
author_facet	Yukihiko Noro Hiroshi Shimizu Katsuhiko Mineta Takashi Gojobori
author_sort	Yukihiko Noro
title	A single neuron subset governs a single coactive neuron circuit in Hydra vulgaris, representing a possible ancestral feature of neural evolution
title_short	A single neuron subset governs a single coactive neuron circuit in Hydra vulgaris, representing a possible ancestral feature of neural evolution
title_full	A single neuron subset governs a single coactive neuron circuit in Hydra vulgaris, representing a possible ancestral feature of neural evolution
title_fullStr	A single neuron subset governs a single coactive neuron circuit in Hydra vulgaris, representing a possible ancestral feature of neural evolution
title_full_unstemmed	A single neuron subset governs a single coactive neuron circuit in Hydra vulgaris, representing a possible ancestral feature of neural evolution
title_sort	single neuron subset governs a single coactive neuron circuit in hydra vulgaris, representing a possible ancestral feature of neural evolution
publisher	Nature Portfolio
publishDate	2021
url	https://doaj.org/article/44a467e2ebcf4b0ab0905de782e24818
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A single neuron subset governs a single coactive neuron circuit in Hydra vulgaris, representing a possible ancestral feature of neural evolution

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