Teneurin-3 Specifies Morphological and Functional Connectivity of Retinal Ganglion Cells in the Vertebrate Visual System

A striking feature of the CNS is the precise wiring of its neuronal connections. During vertebrate visual system development, different subtypes of retinal ganglion cells (RGCs) form specific connections with their corresponding synaptic partners. However, the underlying molecular mechanisms remain...

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Main Authors: Paride Antinucci, Nikolas Nikolaou, Martin P. Meyer, Robert Hindges
Format: Article
Language:English
Published: Elsevier 2013-11-01
Series:Cell Reports
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124713005688
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author Paride Antinucci
Nikolas Nikolaou
Martin P. Meyer
Robert Hindges
author_facet Paride Antinucci
Nikolas Nikolaou
Martin P. Meyer
Robert Hindges
author_sort Paride Antinucci
collection DOAJ
description A striking feature of the CNS is the precise wiring of its neuronal connections. During vertebrate visual system development, different subtypes of retinal ganglion cells (RGCs) form specific connections with their corresponding synaptic partners. However, the underlying molecular mechanisms remain to be fully elucidated. Here, we report that the cell-adhesive transmembrane protein Teneurin-3 (Tenm3) is required by zebrafish RGCs for acquisition of their correct morphological and functional connectivity in vivo. Teneurin-3 is expressed by RGCs and their presynaptic amacrine and postsynaptic tectal cell targets. Knockdown of Teneurin-3 leads to RGC dendrite stratification defects within the inner plexiform layer, as well as mistargeting of dendritic processes into outer portions of the retina. Moreover, a subset of RGC axons exhibits tectal laminar arborization errors. Finally, functional analysis of RGCs targeting the tectum reveals a selective deficit in the development of orientation selectivity after Teneurin-3 knockdown. These results suggest that Teneurin-3 plays an instructive role in the functional wiring of the vertebrate visual system.
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spelling doaj.art-bb01cbf53c7f427d852c99fb36ef290b2022-12-22T00:26:59ZengElsevierCell Reports2211-12472013-11-015358259210.1016/j.celrep.2013.09.045Teneurin-3 Specifies Morphological and Functional Connectivity of Retinal Ganglion Cells in the Vertebrate Visual SystemParide Antinucci0Nikolas Nikolaou1Martin P. Meyer2Robert Hindges3MRC Centre for Developmental Neurobiology, King’s College London, Guy’s Campus, London SE1 1UL, UKMRC Centre for Developmental Neurobiology, King’s College London, Guy’s Campus, London SE1 1UL, UKMRC Centre for Developmental Neurobiology, King’s College London, Guy’s Campus, London SE1 1UL, UKMRC Centre for Developmental Neurobiology, King’s College London, Guy’s Campus, London SE1 1UL, UKA striking feature of the CNS is the precise wiring of its neuronal connections. During vertebrate visual system development, different subtypes of retinal ganglion cells (RGCs) form specific connections with their corresponding synaptic partners. However, the underlying molecular mechanisms remain to be fully elucidated. Here, we report that the cell-adhesive transmembrane protein Teneurin-3 (Tenm3) is required by zebrafish RGCs for acquisition of their correct morphological and functional connectivity in vivo. Teneurin-3 is expressed by RGCs and their presynaptic amacrine and postsynaptic tectal cell targets. Knockdown of Teneurin-3 leads to RGC dendrite stratification defects within the inner plexiform layer, as well as mistargeting of dendritic processes into outer portions of the retina. Moreover, a subset of RGC axons exhibits tectal laminar arborization errors. Finally, functional analysis of RGCs targeting the tectum reveals a selective deficit in the development of orientation selectivity after Teneurin-3 knockdown. These results suggest that Teneurin-3 plays an instructive role in the functional wiring of the vertebrate visual system.http://www.sciencedirect.com/science/article/pii/S2211124713005688
spellingShingle Paride Antinucci
Nikolas Nikolaou
Martin P. Meyer
Robert Hindges
Teneurin-3 Specifies Morphological and Functional Connectivity of Retinal Ganglion Cells in the Vertebrate Visual System
Cell Reports
title Teneurin-3 Specifies Morphological and Functional Connectivity of Retinal Ganglion Cells in the Vertebrate Visual System
title_full Teneurin-3 Specifies Morphological and Functional Connectivity of Retinal Ganglion Cells in the Vertebrate Visual System
title_fullStr Teneurin-3 Specifies Morphological and Functional Connectivity of Retinal Ganglion Cells in the Vertebrate Visual System
title_full_unstemmed Teneurin-3 Specifies Morphological and Functional Connectivity of Retinal Ganglion Cells in the Vertebrate Visual System
title_short Teneurin-3 Specifies Morphological and Functional Connectivity of Retinal Ganglion Cells in the Vertebrate Visual System
title_sort teneurin 3 specifies morphological and functional connectivity of retinal ganglion cells in the vertebrate visual system
url http://www.sciencedirect.com/science/article/pii/S2211124713005688
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