Analysis of growth cone extension in standardized coordinates highlights self-organization rules during wiring of the Drosophila visual system

A fascinating question in neuroscience is how ensembles of neurons, originating from different locations, extend to the proper place and by the right time to create precise circuits. Here, we investigate this question in the Drosophila visual system, where photoreceptors re-sort in the lamina to for...

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Autores principales:	Weiyue Ji, Lani F. Wu, Steven J. Altschuler
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2021
Materias:	Genetics QH426-470
Acceso en línea:	https://doaj.org/article/93927ab673724840b11ce01ebb009188
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spelling	oai:doaj.org-article:93927ab673724840b11ce01ebb0091882021-11-11T06:17:55ZAnalysis of growth cone extension in standardized coordinates highlights self-organization rules during wiring of the Drosophila visual system1553-73901553-7404https://doaj.org/article/93927ab673724840b11ce01ebb0091882021-11-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8565740/?tool=EBIhttps://doaj.org/toc/1553-7390https://doaj.org/toc/1553-7404A fascinating question in neuroscience is how ensembles of neurons, originating from different locations, extend to the proper place and by the right time to create precise circuits. Here, we investigate this question in the Drosophila visual system, where photoreceptors re-sort in the lamina to form the crystalline-like neural superposition circuit. The repeated nature of this circuit allowed us to establish a data-driven, standardized coordinate system for quantitative comparison of sparsely perturbed growth cones within and across specimens. Using this common frame of reference, we investigated the extension of the R3 and R4 photoreceptors, which is the only pair of symmetrically arranged photoreceptors with asymmetric target choices. Specifically, we found that extension speeds of the R3 and R4 growth cones are inherent to their cell identities. The ability to parameterize local regularity in tissue organization facilitated the characterization of ensemble cellular behaviors and dissection of mechanisms governing neural circuit formation. Author summary One of the most fascinating questions in neuroscience is how complex neural circuits form. Here, we investigate self-organization principles during neuronal development in the visual circuit of fruit flies. We utilized the regularity of the tissue environment to establish a developmental coordinate system during wiring, which allowed us to uncover a role for cell identity in governing neuronal growth cone extension speed. Our study highlights the importance of velocity control in the precise formation of complex neuronal circuits, as well as the use of developmental coordinates in identifying ensemble behaviors of tissue patterning.Weiyue JiLani F. WuSteven J. AltschulerPublic Library of Science (PLoS)articleGeneticsQH426-470ENPLoS Genetics, Vol 17, Iss 11 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Genetics QH426-470
spellingShingle	Genetics QH426-470 Weiyue Ji Lani F. Wu Steven J. Altschuler Analysis of growth cone extension in standardized coordinates highlights self-organization rules during wiring of the Drosophila visual system
description	A fascinating question in neuroscience is how ensembles of neurons, originating from different locations, extend to the proper place and by the right time to create precise circuits. Here, we investigate this question in the Drosophila visual system, where photoreceptors re-sort in the lamina to form the crystalline-like neural superposition circuit. The repeated nature of this circuit allowed us to establish a data-driven, standardized coordinate system for quantitative comparison of sparsely perturbed growth cones within and across specimens. Using this common frame of reference, we investigated the extension of the R3 and R4 photoreceptors, which is the only pair of symmetrically arranged photoreceptors with asymmetric target choices. Specifically, we found that extension speeds of the R3 and R4 growth cones are inherent to their cell identities. The ability to parameterize local regularity in tissue organization facilitated the characterization of ensemble cellular behaviors and dissection of mechanisms governing neural circuit formation. Author summary One of the most fascinating questions in neuroscience is how complex neural circuits form. Here, we investigate self-organization principles during neuronal development in the visual circuit of fruit flies. We utilized the regularity of the tissue environment to establish a developmental coordinate system during wiring, which allowed us to uncover a role for cell identity in governing neuronal growth cone extension speed. Our study highlights the importance of velocity control in the precise formation of complex neuronal circuits, as well as the use of developmental coordinates in identifying ensemble behaviors of tissue patterning.
format	article
author	Weiyue Ji Lani F. Wu Steven J. Altschuler
author_facet	Weiyue Ji Lani F. Wu Steven J. Altschuler
author_sort	Weiyue Ji
title	Analysis of growth cone extension in standardized coordinates highlights self-organization rules during wiring of the Drosophila visual system
title_short	Analysis of growth cone extension in standardized coordinates highlights self-organization rules during wiring of the Drosophila visual system
title_full	Analysis of growth cone extension in standardized coordinates highlights self-organization rules during wiring of the Drosophila visual system
title_fullStr	Analysis of growth cone extension in standardized coordinates highlights self-organization rules during wiring of the Drosophila visual system
title_full_unstemmed	Analysis of growth cone extension in standardized coordinates highlights self-organization rules during wiring of the Drosophila visual system
title_sort	analysis of growth cone extension in standardized coordinates highlights self-organization rules during wiring of the drosophila visual system
publisher	Public Library of Science (PLoS)
publishDate	2021
url	https://doaj.org/article/93927ab673724840b11ce01ebb009188
work_keys_str_mv	AT weiyueji analysisofgrowthconeextensioninstandardizedcoordinateshighlightsselforganizationrulesduringwiringofthedrosophilavisualsystem AT lanifwu analysisofgrowthconeextensioninstandardizedcoordinateshighlightsselforganizationrulesduringwiringofthedrosophilavisualsystem AT stevenjaltschuler analysisofgrowthconeextensioninstandardizedcoordinateshighlightsselforganizationrulesduringwiringofthedrosophilavisualsystem
_version_	1718439513877905408

Analysis of growth cone extension in standardized coordinates highlights self-organization rules during wiring of the Drosophila visual system

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