Abstract
SummaryA 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.
Highlights
In the vertebrate retina, retinal ganglion cells (RGCs) develop stereotypic dendritic arborization patterns and make specific synaptic connections with amacrine and bipolar cells in the inner plexiform layer (IPL) (Masland, 2012)
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
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
Summary
Retinal ganglion cells (RGCs) develop stereotypic dendritic arborization patterns and make specific synaptic connections with amacrine and bipolar cells in the inner plexiform layer (IPL) (Masland, 2012). The formation of such precise connections is critical for the processing of visual information and the generation of feature selectivity in RGCs (Gollisch and Meister, 2010; Wassle, 2004). Our understanding of the molecular mechanisms that specify connections within the retina and between the retina and retinorecipient nuclei in the brain, is still far from complete
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