­The Retinal Basis of Vertebrate Color Vision

Abstract

Vertebrate color vision is evolutionarily ancient. Jawless fish evolved four main spectral types of cone photoreceptor, almost certainly complemented by retinal circuits to process chromatic opponent signals. Subsequent evolution of photoreceptors and visual pigments are now documented for many vertebrate lineages and species, giving insight into evolutionary variation and ecological adaptation of color vision. We look at organization of the photoreceptor mosaic and the functions different types of cone in teleost fish, primates, and birds and reptiles. By comparison less is known about the underlying neural processing. Here we outline the diversity of vertebrate color vision and summarize our understanding of how spectral information picked up by animal photoreceptor arrays is adapted to natural signals. We then turn to the question of how spectral information is processed in the retina. Here, the quite well known and comparatively ‘simple’ system of mammals such as mice and primates reveals some evolutionarily conserved features such as the mammalian BlueON system which compares short and long wavelength receptors signals. We then survey our current understanding of the more complex circuits of fish, amphibians, birds and reptiles. Together, these clades make up more than 90% of vertebrate species, yet we know disturbingly little about their neural circuits for colour vision beyond the photoreceptors. Here, long-standing work on goldfish, freshwater turtles and other species is being complemented by new insights gained from the experimentally amendable retina of zebrafish. From this body of work, one thing is clear: The retinal basis of colour vision in non-mammalian vertebrates is substantially richer compared to mammals: Diverse and complex spectral tunings are established at the level of the cone output via horizontal cell feedforward circuits. From here, zebrafish use cone-selective wiring in bipolar cells to set-up color opponent synaptic layers in the inner retina, which in turn lead a large diversity of color-opponent channels for transmission to the brain. However, while we are starting to build an understanding of the richness of spectral properties in some of these species’ retinal neurons, little is known about inner retinal connectivity and cell-type identify.  To gain an understanding of their actual circuits, and thus to build a more generalised understanding of the vertebrate retinal basis of color vision, it will be paramount to expand ongoing efforts in deciphering the retinal circuits of non-mammalian models.