Date Published: July 28, 2017
Publisher: Public Library of Science
Author(s): Brenna Krieger, Mu Qiao, David L. Rousso, Joshua R. Sanes, Markus Meister, Steven Barnes.
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.
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). Although their physiological characteristics vary from species to species (reviewed in ), 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 also share certain physiological properties, such as a short response latency and fast conducting axons [6–8]. Thus the αRGCs are among the first to signal a new stimulus to the brain. Furthermore, the visual response of αRGCs involves a pronounced nonlinearity prior to summation over the receptive field center [9,10], owing in large part to rectification at the bipolar cell synapse . RGCs with alpha-like morphology have now been confirmed in the retinas of over 30 mammalian species including humans . This striking evolutionary conservation suggests that they play an essential role in visual processing.
This study extends our understanding of αRGCs, which form perhaps the fastest pathway for visual information to reach the brain. We showed here that αRGCs in the mouse express a shared set of molecular markers that facilitate their targeted study (Fig 3 and ) and a shared physiological feature, the shape of the action potential, that distinguishes them from other types of ganglion cells (Fig 7). Most importantly, we show that there exist not three but four types of αRGCs and that they cover the space of both function and morphology in a beautifully symmetric arrangement (Figs 1, 2, 4, 5 and 6). Finally we identify specific genetic markers that allow for the identification of three out of four of these types (Figs 8–11).