Ultrastructural characteristics and synaptic connectivity of photoreceptors in the simplex retina of Little skate ( Leucoraja erinacea ).

The retinas of the vast majority of vertebrate species are termed "duplex" - that is, they contain both rod and cone photoreceptor neurons in different ratios. The retina of Little skate ( Leucoraja erinacea ) is a rarity among vertebrates because it contains only a single photoreceptor cell type and is thus "simplex". This unique retina provides us with an important comparative model and an exciting opportunity to study retinal circuitry within the context of a visual system with a single photoreceptor cell type. What is perhaps even more intriguing is the fact that the Leucoraja retina is able use that single photoreceptor cell type to function under both scotopic and photopic ranges of illumination. Although some ultrastructural characteristics of skate photoreceptors have been examined previously, leading to a general description of them as "rods" largely based on outer segment morphology and rhodopsin expression, a detailed study of the fine anatomy of the entire cell and its synaptic connectivity is still lacking. To address this gap in knowledge, we performed serial block-face electron microscopy imaging and examined the structure of skate photoreceptors and their post-synaptic partners. We find that skate photoreceptors exhibit unusual ultrastructural characteristics that are either common to rods or cones in other vertebrates (e.g., outer segment architecture, synaptic ribbon number, terminal extensions), or are somewhere in between those of a typical vertebrate rod or cone (e.g., number of invaginating contacts, clustering of multiple ribbons over a single synaptic invagination). We suggest that some of the ultrastructural characteristics we observe may play a role in the ability of the skate retina to function across scotopic and photopic ranges of illumination. Our findings have the potential to reveal as yet undescribed principles of vertebrate retinal design. Significance Statement The vast majority of vertebrate retinas are duplex and have mixed rod-cone populations of photoreceptors. The processing of visual information in a duplex retina is separated between rods and cones, which mediate function under scotopic and photopic lighting conditions, respectively. However, the cartilaginous fish Little skate ( Leucoraja erinacea ) has a simplex retina, comprised solely of one photoreceptor cell type. Skate photoreceptors are unusual because they have the ability to retain function over a full range of illumination. We know little about the ultrastructural anatomy of the skate retina, and we hypothesize that functional plasticity can be traced back to morphological adaptations at the level of photoreceptors and downstream circuitry, thus illuminating new pathways for the processing of visual information among vertebrates.