Spectral sensitivity of cone vision in the diurnal murid Rhabdomys pumilio.

Annette E Allen,Anthony A Vugler,Joshua W Mouland,Beatriz Baño-Otálora,Glen Jeffery,Jessica Rodgers,Timothy M Brown,Robert J Lucas,Ronald H Douglas

doi:10.1242/jeb.215368

Abstract

ABSTRACTAn animal's temporal niche – the time of day at which it is active – is known to drive a variety of adaptations in the visual system. These include variations in the topography, spectral sensitivity and density of retinal photoreceptors, and changes in the eye's gross anatomy and spectral transmission characteristics. We have characterised visual spectral sensitivity in the murid rodent Rhabdomys pumilio (the four-striped grass mouse), which is in the same family as (nocturnal) mice and rats but exhibits a strong diurnal niche. As is common in diurnal species, the R. pumilio lens acts as a long-pass spectral filter, providing limited transmission of light <400 nm. Conversely, we found strong sequence homologies with the R. pumilio SWS and MWS opsins and those of related nocturnal species (mice and rats) whose SWS opsins are maximally sensitive in the near-UV. We continued to assess in vivo spectral sensitivity of cone vision using electroretinography and multi-channel recordings from the visual thalamus. These revealed that responses across the human visible range could be adequately described by those of a single pigment (assumed to be MWS opsin) maximally sensitive at ∼500 nm, but that sensitivity in the near-UV required inclusion of a second pigment whose peak sensitivity lay well into the UV range (λmax<400 nm, probably ∼360 nm). We therefore conclude that, despite the UV-filtering effects of the lens, R. pumilio retains an SWS pigment with a UV-A λmax. In effect, this somewhat paradoxical combination of long-pass lens and UV-A λmax results in narrow-band sensitivity for SWS cone pathways in the UV-A range.

Highlights

The vast majority of mammalian retinas contain three classes of photoreceptor: the outerretinal rods and cones, that mediate form vision in dim and bright conditions, respectively; and the inner-retinal intrinsically-photosensitive retinal ganglion cells, which contribute a lower spatiotemporal resolution representation of the visual environment supporting aspects of vision as well as an array of non-image forming light responses
When aligned against the corresponding opsin sequence from multiple other rodent species (Mus musculus, Rattus norvegicus, Octodon degus, Meriones ungiuculatus, Ictidomys tridecemlineatus and Cavia porcellus), Rhabdomys opsins showed highest sequence homology with mouse and rat, (~96% and 97% respectively) as predicted for the phylogeny of these species (Blanga-Kanfi et al 2009)
When we examined known spectral tuning sites, we found the Rhabdomys sequences were most similar to rats and mice

Summary

Introduction

The vast majority of mammalian retinas contain three classes of photoreceptor: the outerretinal rods and cones, that mediate form vision in dim and bright conditions, respectively; and the inner-retinal intrinsically-photosensitive retinal ganglion cells (ipRGCs), which contribute a lower spatiotemporal resolution representation of the visual environment supporting aspects of vision as well as an array of non-image forming light responses (e.g. photoentrainment of the circadian clock). These photoreceptors allow organisms to sense and respond to light across the broad variations in illumination that they would commonly encounter in the natural world. Sometimes that increased density is apparent across the entire retina (such as in the thirteen-lined ground squirrel (Kryger et al 1998)), but it may occur in spatially localised regions, such as the primate fovea (reviewed by (Ahnelt and Kolb 2000))

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