S-cone photoreceptors in the primate retina are functionally distinct from L and M cones

Abstract

Daylight vision starts with signals in three classes of cone photoreceptors sensitive to short (S), middle (M), and long (L) wavelengths. Psychophysical studies show that perceptual sensitivity to rapidly varying inputs differs for signals originating in S cones versus L and M cones; notably, S-cone signals appear perceptually delayed relative to L- and M-cone signals. These differences could originate in the cones themselves or in the post-cone circuitry. To determine if the cones could contribute to these and related perceptual phenomena, we compared the light responses of primate S, M, and L cones. We found that S cones generate slower light responses than L and M cones, show much smaller changes in response kinetics as background-light levels increase, and are noisier than L and M cones. It will be important to incorporate these differences into descriptions of how cone signaling shapes human visual perception.

Cellular and molecular mechanisms of photoreceptor tuning for prey capture in larval zebrafish

“…For all we know, all sighted vertebrates have at least a mild form of an area temporalis or an area centralis, and in some species such as many primates as well as birds of prey and species of reptiles and fish, these specialised regions have further evolved into a fovea (Bringmann, 2019;Bringmann et al, 2018;Collin et al, 2000;Land, 2015). However, data on the possibility of regional tuning of photoreceptor function across most of these species remains outstanding with the notable exception of primates (Baudin et al, 2019;Sinha et al, 2017), mice (Baden et al, 2013b), and now zebrafish. In each of these latter three, cone-function has been found to be regionally tuned.…”

“…In many ways both the 'purpose' of functional tuning of SZ UV-cones as well as the underlying cellular and molecular mechanisms are reminiscent of differences between peripheral and foveal cones of the primate retina (Baudin et al, 2019;Curcio et al, 1990;Kemp et al, 1988;Mowat et al, 2008;Peng et al, 2019;Sinha et al, 2017). For example, in both zebrafish SZ UV-cones and in primate foveal cones outer segments are elongated (Curcio et al, 1990;Packer et al, 1989) and light-response kinetics are slowed (Baudin et al, 2019;Sinha et al, 2017). In the primate fovea, expression of rod-transducin gamma subunit has been discussed as one determinant of the slowed kinetics (Peng et al, 2019), which conceptually links with our finding of reduced levels of cone-transducin gamma subunit in zebrafish SZ cones.…”

“…Indeed, photoreceptor tuningeven within-typeis a fundamental property of vision in both invertebrates (Hardie, 1984;Sancer et al, 2019) and vertebrates (Baden et al, 2013b;Baudin et al, 2019;Sinha et al, 2017). Even primates make use of this trick: foveal cones have longer integration times than their peripheral counterparts, likely to boost their signal to noise ratio as in the foveal centre retinal ganglion cells do not spatially pool their inputs (Baudin et al, 2019;Sinha et al, 2017).…”

“…Indeed, photoreceptor tuningeven within-typeis a fundamental property of vision in both invertebrates (Hardie, 1984;Sancer et al, 2019) and vertebrates (Baden et al, 2013b;Baudin et al, 2019;Sinha et al, 2017). Even primates make use of this trick: foveal cones have longer integration times than their peripheral counterparts, likely to boost their signal to noise ratio as in the foveal centre retinal ganglion cells do not spatially pool their inputs (Baudin et al, 2019;Sinha et al, 2017). Understanding the mechanisms that underlie such functional tuning will be important for understanding how sensory systems can operate in the natural sensory world, and how they might have evolved to suit new sensory-ecological niches (Cronin et al, 2014;Lamb et al, 2007;Land and Nilsson, 2012;Yau and Hardie, 2009).…”

Voltage-clamp recordings of light responses from wild-type and mutant mouse cone photoreceptors

“…Although recent results from primate cones have greatly extended our understanding of normal cone function (Angueyra and Rieke, 2013;Sinha et al, 2017;Baudin et al, 2019), it would be useful to study cone photoresponses in a genetically tractable model where elements of phototransduction can be modified or deleted. The mouse retina offers these advantages, because genetic tools are available to explore mechanisms of phototransduction and other aspects of retinal function.…”