Abstract

The retina communicates with the brain using ≥30 parallel channels, each carried by axons of distinct types of retinal ganglion cells. In every mammalian retina one finds so-called "alpha" ganglion cells (αRGCs), identified by their large cell bodies, stout axons, wide and mono-stratified dendritic fields, and high levels of neurofilament protein. In the mouse, three αRGC types have been described based on responses to light steps: On-sustained, Off-sustained, and Off-transient. Here we employed a transgenic mouse line that labels αRGCs in the live retina, allowing systematic targeted recordings. We characterize the three known types and identify a fourth, with On-transient responses. All four αRGC types share basic aspects of visual signaling, including a large receptive field center, a weak antagonistic surround, and absence of any direction selectivity. They also share a distinctive waveform of the action potential, faster than that of other RGC types. Morphologically, they differ in the level of dendritic stratification within the IPL, which accounts for their response properties. Molecularly, each type has a distinct signature. A comparison across mammals suggests a common theme, in which four large-bodied ganglion cell types split the visual signal into four channels arranged symmetrically with respect to polarity and kinetics.

Highlights

  • The retina communicates visual information to the brain through the action potentials of retinal ganglion cells (RGCs)

  • Four alpha ganglion cell types in mouse retina osteopontin, which are markers of αRGCs [16,25]. Each of these markers labels only a small fraction of all RGCs, yet their overlap was extensive (S1 Fig): ~77% of the YFP-positive RGCs in KCNG4-cre;thy1-stop-YFP1 mice were SMI-positive and 92% were osteopontin-positive; 80% of the SMI-32 positive neurons and 73% of the osteopontin-positive neurons were YFP positive. These features suggest that the RGCs labeled in KCNG4-cre;thy1-stopYFP1 mice are primarily αRGCs

  • All GFP-positive neurons were RFP positive, demonstrating that CB2-GFP-labeled cells were KCNG4-cre-positive (Fig 9F). Together these results indicate that the αRGCs labeled in KCNG4-cre mice include those labeled in TYW7 and CB2-GFP mice, consistent with our hypothesis that the KCNG4-cre line labels all αRGCs, and that all αRGCs are osteopontin-positive

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Summary

Introduction

The retina communicates visual information to the brain through the action potentials of retinal ganglion cells (RGCs). This population of neurons consists of more than thirty distinct types, each of which covers the retina to reliably encode its part of the visual message [1,2]. Among the best recognized are the so-called alpha ganglion cells (αRGCs) Their physiological characteristics vary from species to species (reviewed in [3]), they are recognizable as a distinct morphological class by their large cell bodies, stout dendrites and axons, large mono-stratified dendritic arbors, and high levels of neurofilament proteins [4,5]. Alpha RGCs share certain physiological properties, such as a short response latency and fast conducting

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