Self-organizing circuit assembly through spatiotemporally coordinated neuronal migration within geometric constraints.

<h4>Background</h4>Neurons are dynamically coupled with each other through neurite-mediated adhesion during development. Understanding the collective behavior of neurons in circuits is important for understanding neural development. While a number of genetic and activity-dependent factor...

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Autores principales:	Yi Sun, Zhuo Huang, Kaixuan Yang, Wenwen Liu, Yunyan Xie, Bo Yuan, Wei Zhang, Xingyu Jiang
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2011
Materias:	Medicine R Science Q
Acceso en línea:	https://doaj.org/article/d12bb244d2ac4d0caa20b20c3e97dd60
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spelling	oai:doaj.org-article:d12bb244d2ac4d0caa20b20c3e97dd602021-11-18T07:33:42ZSelf-organizing circuit assembly through spatiotemporally coordinated neuronal migration within geometric constraints.1932-620310.1371/journal.pone.0028156https://doaj.org/article/d12bb244d2ac4d0caa20b20c3e97dd602011-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/22132234/?tool=EBIhttps://doaj.org/toc/1932-6203<h4>Background</h4>Neurons are dynamically coupled with each other through neurite-mediated adhesion during development. Understanding the collective behavior of neurons in circuits is important for understanding neural development. While a number of genetic and activity-dependent factors regulating neuronal migration have been discovered on single cell level, systematic study of collective neuronal migration has been lacking. Various biological systems are shown to be self-organized, and it is not known if neural circuit assembly is self-organized. Besides, many of the molecular factors take effect through spatial patterns, and coupled biological systems exhibit emergent property in response to geometric constraints. How geometric constraints of the patterns regulate neuronal migration and circuit assembly of neurons within the patterns remains unexplored.<h4>Methodology/principal findings</h4>We established a two-dimensional model for studying collective neuronal migration of a circuit, with hippocampal neurons from embryonic rats on Matrigel-coated self-assembled monolayers (SAMs). When the neural circuit is subject to geometric constraints of a critical scale, we found that the collective behavior of neuronal migration is spatiotemporally coordinated. Neuronal somata that are evenly distributed upon adhesion tend to aggregate at the geometric center of the circuit, forming mono-clusters. Clustering formation is geometry-dependent, within a critical scale from 200 µm to approximately 500 µm. Finally, somata clustering is neuron-type specific, and glutamatergic and GABAergic neurons tend to aggregate homo-philically.<h4>Conclusions/significance</h4>We demonstrate self-organization of neural circuits in response to geometric constraints through spatiotemporally coordinated neuronal migration, possibly via mechanical coupling. We found that such collective neuronal migration leads to somata clustering, and mono-cluster appears when the geometric constraints fall within a critical scale. The discovery of geometry-dependent collective neuronal migration and the formation of somata clustering in vitro shed light on neural development in vivo.Yi SunZhuo HuangKaixuan YangWenwen LiuYunyan XieBo YuanWei ZhangXingyu JiangPublic Library of Science (PLoS)articleMedicineRScienceQENPLoS ONE, Vol 6, Iss 11, p e28156 (2011)
institution	DOAJ
collection	DOAJ
language	EN
topic	Medicine R Science Q
spellingShingle	Medicine R Science Q Yi Sun Zhuo Huang Kaixuan Yang Wenwen Liu Yunyan Xie Bo Yuan Wei Zhang Xingyu Jiang Self-organizing circuit assembly through spatiotemporally coordinated neuronal migration within geometric constraints.
description	<h4>Background</h4>Neurons are dynamically coupled with each other through neurite-mediated adhesion during development. Understanding the collective behavior of neurons in circuits is important for understanding neural development. While a number of genetic and activity-dependent factors regulating neuronal migration have been discovered on single cell level, systematic study of collective neuronal migration has been lacking. Various biological systems are shown to be self-organized, and it is not known if neural circuit assembly is self-organized. Besides, many of the molecular factors take effect through spatial patterns, and coupled biological systems exhibit emergent property in response to geometric constraints. How geometric constraints of the patterns regulate neuronal migration and circuit assembly of neurons within the patterns remains unexplored.<h4>Methodology/principal findings</h4>We established a two-dimensional model for studying collective neuronal migration of a circuit, with hippocampal neurons from embryonic rats on Matrigel-coated self-assembled monolayers (SAMs). When the neural circuit is subject to geometric constraints of a critical scale, we found that the collective behavior of neuronal migration is spatiotemporally coordinated. Neuronal somata that are evenly distributed upon adhesion tend to aggregate at the geometric center of the circuit, forming mono-clusters. Clustering formation is geometry-dependent, within a critical scale from 200 µm to approximately 500 µm. Finally, somata clustering is neuron-type specific, and glutamatergic and GABAergic neurons tend to aggregate homo-philically.<h4>Conclusions/significance</h4>We demonstrate self-organization of neural circuits in response to geometric constraints through spatiotemporally coordinated neuronal migration, possibly via mechanical coupling. We found that such collective neuronal migration leads to somata clustering, and mono-cluster appears when the geometric constraints fall within a critical scale. The discovery of geometry-dependent collective neuronal migration and the formation of somata clustering in vitro shed light on neural development in vivo.
format	article
author	Yi Sun Zhuo Huang Kaixuan Yang Wenwen Liu Yunyan Xie Bo Yuan Wei Zhang Xingyu Jiang
author_facet	Yi Sun Zhuo Huang Kaixuan Yang Wenwen Liu Yunyan Xie Bo Yuan Wei Zhang Xingyu Jiang
author_sort	Yi Sun
title	Self-organizing circuit assembly through spatiotemporally coordinated neuronal migration within geometric constraints.
title_short	Self-organizing circuit assembly through spatiotemporally coordinated neuronal migration within geometric constraints.
title_full	Self-organizing circuit assembly through spatiotemporally coordinated neuronal migration within geometric constraints.
title_fullStr	Self-organizing circuit assembly through spatiotemporally coordinated neuronal migration within geometric constraints.
title_full_unstemmed	Self-organizing circuit assembly through spatiotemporally coordinated neuronal migration within geometric constraints.
title_sort	self-organizing circuit assembly through spatiotemporally coordinated neuronal migration within geometric constraints.
publisher	Public Library of Science (PLoS)
publishDate	2011
url	https://doaj.org/article/d12bb244d2ac4d0caa20b20c3e97dd60
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Self-organizing circuit assembly through spatiotemporally coordinated neuronal migration within geometric constraints.

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