Abstract
SummaryThe orientation of visual stimuli is a salient feature of visual scenes. In vertebrates, the first neural processing steps generating orientation selectivity take place in the retina. Here, we dissect an orientation-selective circuit in the larval zebrafish retina and describe its underlying synaptic, cellular, and molecular mechanisms. We genetically identify a class of amacrine cells (ACs) with elongated dendritic arbors that show orientation tuning. Both selective optogenetic ablation of ACs marked by the cell-adhesion molecule Teneurin-3 (Tenm3) and pharmacological interference with their function demonstrate that these cells are critical components for orientation selectivity in retinal ganglion cells (RGCs) by being a source of tuned GABAergic inhibition. Moreover, our morphological analyses reveal that Tenm3+ ACs and orientation-selective RGCs co-stratify their dendrites in the inner plexiform layer, and that Tenm3+ ACs require Tenm3 to acquire their correct dendritic stratification. Finally, we show that orientation tuning is present also among bipolar cell presynaptic terminals. Our results define a neural circuit underlying orientation selectivity in the vertebrate retina and characterize cellular and molecular requirements for its assembly.
Highlights
The detection of oriented visual stimuli is a key neural computation performed by visual systems of many animals
In tenm3 knockout mutant (tenm3KO) mutants, a 14-bp deletion in the exon encoding the transmembrane domain of Tenm3 leads to a reading frameshift and, subsequently, to a premature stop codon causing the loss of the entire extracellular domain (Figures 1C and S1A–S1F)
We found that 4 days post-fertilization tenm3KO mutants have a large decrease in both the number of orientation selective (OS) voxels (Figure 1E) and the proportion of orientation-selective RGC (OSGC) output relative to the whole population of responsive voxels (Figure 1F)
Summary
The detection of oriented visual stimuli is a key neural computation performed by visual systems of many animals. Orientation selectivity is present among retinal ganglion cells (RGCs) [10, 13], the sole retinal output neurons, and amacrine cells (ACs) [13, 14], a class of inhibitory neurons that modulate and shape RGC responses. It is presently unclear how orientation selectivity emerges in these cells and whether they form a distinct retinal circuit, partially due to the lack of specific molecular markers allowing targeted labeling and manipulations
Sign-in/Register to view highlights & summary Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a callDisclaimer: All third-party content on this website/platform is and will remain the property of their respective owners and is provided on "as is" basis without any warranties, express or implied. Use of third-party content does not indicate any affiliation, sponsorship with or endorsement by them. Any references to third-party content is to identify the corresponding services and shall be considered fair use under The CopyrightLaw.
