Evolution of the circuitry for conscious color vision in primates

Abstract

There are many ganglion cell types and subtypes in our retina that carry color information. These have appeared at different times over the history of the evolution of the vertebrate visual system. They project to several different places in the brain and serve a variety of purposes allowing wavelength information to contribute to diverse visual functions. These include circadian photoentrainment, regulation of sleep and mood, guidance of orienting movements, detection and segmentation of objects. Predecessors to some of the circuits serving these purposes presumably arose before mammals evolved and different functions are represented by distinct ganglion cell types. However, while other animals use color information to elicit motor movements and regulate activity rhythms, as do humans, using phylogenetically ancient circuitry, the ability to appreciate color appearance may have been refined in ancestors to primates, mediated by a special set of ganglion cells that serve only that purpose. Understanding the circuitry for color vision has implications for the possibility of treating color blindness using gene therapy by recapitulating evolution. In addition, understanding how color is encoded, including how chromatic and achromatic percepts are separated is a step toward developing a complete picture of the diversity of ganglion cell types and their functions. Such knowledge could be useful in developing therapeutic strategies for blinding eye disorders that rely on stimulating elements in the retina, where more than 50 different neuron types are organized into circuits that transform signals from photoreceptors into specialized detectors many of which are not directly involved in conscious vision.

The spectral identity of foveal cones is preserved in hue perception

“…Firstly, do sensations from individually targeted L and M cones truly vary in saturation (amount of whiteness)? More specifically, do single-cone color percepts exist on a continuum, with each cone producing a mixture of hue and achromatic sensation (Wool et al, 2018) or is there a discrete subclass of cones wired specifically into chromatic or achromatic pathways (Neitz and Neitz, 2017)? In our prior work, subjects reported on their perception with only a single color name (Sabesan et al, 2016; Schmidt et al, 2018).…”

The spectral identity of foveal cones is preserved in hue perception

“…First, do sensations from individually targeted L and M cones truly vary in saturation (amount of whiteness)? More specifically, do single-cone color percepts exist on a continuum, with each cone producing a mixture of hue and achromatic sensation (Wool et al, 2018 ), or is there a discrete subclass of cones wired specifically into chromatic or achromatic pathways (Neitz & Neitz, 2017 )? In our prior work, subjects reported on their perception with only a single color name (Sabesan et al, 2016 ; Schmidt et al, 2018 ).…”

Sensations from a single M-cone depend on the activity of surrounding S-cones

“…Therefore, the main finding -that a relative increase in S-cone quantal catch is required to switch a spot targeted at an M-cone from green to blue -may be explained if M-cones participate in two spectrally opponent pathways that are differentially affected by light absorbed in S-cones. If S-cones contribute excitatory input to an OFF M-L pathway and inhibitory input to an ON M-L pathway, they would form an (S+M)-L circuit for blueness and an M-(L+S) circuit for greenness [32][33][34] . In this model, hyperpolarization of S-cone would favor one pathway over the other and explain the observed shifts in hue perception reported here.…”

“…contribute excitatory input to an OFF M-L pathway and inhibitory input to an ON M-L parvocellular pathway, they would form an (S+M)-L circuit for blueness and an M-(L+S) circuit for greenness 36,37,49 . In this model, hyperpolarization of S-cones would favor one pathway over the other and explain the observed shifts in hue perception reported here.…”