Distinct retinal ganglion cell types in strictly subterranean, naturally microphthalmic mammals

Abstract

African mole-rats (Bathyergidae, Rodentia) are subterranean rodents that live in extensive dark underground tunnel systems and rarely emerge aboveground. They can discriminate between light and dark but show no overt visually driven behaviours except for light-avoidance responses. Their eyes and central visual system are strongly reduced but not degenerated. Here, we focus on retinal ganglion cells (RGCs). Sighted mammals have numerous RGC types with distinct morphological and functional properties that encode different aspects of a visual scene. We analysed the morphological diversity of 216 intracellularly dye-injected RGCs in the giant mole-rat (Fukomys mechowii) and 48 RGCs in Ansell's mole-rat (Fukomys anselli). Using a hierarchical cluster analysis on 11 morphological parameters, we show that both species possess at least five RGC types with distinct dendritic field sizes and branching patterns. These resemble some RGC types of the mouse and rat, but mole-rat RGCs feature overall sparser and more asymmetric branching patterns. The dendritic trees of most RGCs in all clusters are monostratified in the inner plexiform layer, but bistratified and multistratified/diffuse cells also exist. Thus, although RGC morphologies have become disorganized, the basic retinal organization principle of parallel information processing by distinct RGC types is retained.

Keywords: Fukomys; microphthalmia; mole-rats; ocular regression; retinal ganglion cells; subterranean mammals.