Abstract
SummaryPhotoreception in the mammalian retina is not restricted to rods and cones but extends to a small number of intrinsically photoreceptive retinal ganglion cells (ipRGCs), expressing the photopigment melanopsin [1–4]. ipRGCs are known to support various accessory visual functions including circadian photoentrainment and pupillary reflexes. However, despite anatomical and physiological evidence that they contribute to the thalamocortical visual projection [5–7], no aspect of visual discrimination has been shown to rely upon ipRGCs. Based on their currently known roles, we hypothesized that ipRGCs may contribute to distinguishing brightness. This percept is related to an object's luminance—a photometric measure of light intensity relevant for cone photoreceptors. However, the perceived brightness of different sources is not always predicted by their respective luminance [8–12]. Here, we used parallel behavioral and electrophysiological experiments to first show that melanopsin contributes to brightness discrimination in both retinally degenerate and fully sighted mice. We continued to use comparable paradigms in psychophysical experiments to provide evidence for a similar role in healthy human subjects. These data represent the first direct evidence that an aspect of visual discrimination in normally sighted subjects can be supported by inner retinal photoreceptors.
Highlights
Behavioral Assays of Brightness Discrimination in Mice One prediction of the hypothesis that intrinsically photoreceptive retinal ganglion cells contribute to assessing brightness is that this aspect of visual discrimination should survive complete loss of outer retinal photoreceptors. ipRGCs remain functional and can support a variety of accessory visual responses in mice lacking rods and cones [13]
At the ages employed here, rd/rd cl mice are essentially rodless and coneless [14]. We tested their ability to make visual discriminations in a trapezoid Y water maze in which the mouse was trained to swim toward a lit target to reach an escape platform (Figure 1A)
It is important to raise a couple of caveats to that conclusion. We find that both species can use melanopsin to inform assessments of brightness, imperceptible visual qualities can elicit perceptual biases [34]
Summary
In order to maximize the melanopic excitation achievable with the metamer approach, we aimed to circumvent rod-based responses by working at background light levels sufficiently bright to saturate rods
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