Specialized synaptic pathway for chromatic signals beneath S-cone photoreceptors is common to human, Old and New World primates

Puller, Christian; Manookin, Michael B.; Neitz, Maureen; Neitz, Jay

doi:10.1364/josaa.31.00a189

Cited by 10 publications

(10 citation statements)

References 60 publications

(68 reference statements)

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“…This demonstrates a previously undiscovered, enhanced feedforward signaling mechanism between HII horizontal cells and cone bipolar cells that has evolved in primates for the purposes of color vision. 53 In subsequent experiments, as predicted by this hypothesis, the existence of other components of a GABA-mediated pathway was verified, including GABA receptors and the concomitant enrichment of the Na-K-Cl co-transporter with syntaxin-4. 54 The enrichment beneath S-cones reveals synapses for feedforward signaling between HII horizontal cells and S-cone bipolar cells.…”

Section: How the World Became Coloredmentioning

confidence: 65%

“…The two types of neurons, so produced, have chromatic responses aligned along roughly orthogonal axes. Now, as a solution to the problem of the origins of the unique hues, it is clear that feedforward from S-cones, via HII horizontal cells to L/M opponent midget bipolar cells 53,54 is capable of producing a subset of midget ganglion cells with responses that can account for human hue perception. The combinations of S-cone inputs to L/M opponent midget ganglion cells produces exactly the hue axes corresponding to phenomenological hues.…”

Section: Unique Huesmentioning

confidence: 99%

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Evolution of the circuitry for conscious color vision in primates

Neitz

2016

Eye

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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.

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Section: How the World Became Coloredmentioning

confidence: 65%

Section: Unique Huesmentioning

confidence: 99%

Evolution of the circuitry for conscious color vision in primates

Neitz

2016

Eye

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“…What was not appreciated previously was the possibility of a second synaptic pathway via HII horizontal cell feedforward from S-cones to a small subset of midget bipolar cells (Puller, Haverkamp, Neitz, & Neitz, 2014; Puller, Manookin, Neitz, & Neitz, 2014). This could account for why midget ganglion cells with S-cone input occur in much smaller numbers and with much weaker S cone input than the small bistratified cells (Martin & Lee, 2014).…”

Section: Modelsmentioning

confidence: 98%

“…Briefly, it proposes that human hue sensations are mediated by four different subclasses of midget ganglion cells which receive S cone input via a newly discovered feed-forward pathway from S cones via HII horizontal cells directly to midget bipolar cells (Puller, Haverkamp, Neitz, & Neitz, 2014; Puller, Manookin, Neitz, & Neitz, 2014). Specifically, we propose (a) that OFF-midget ganglion cells with S cone ON feed-forward (Puller, Manookin et al, 2014)) input and L cone centers serve the sensations of blue whereas (b) those with M centers serve sensations of red. And (c) ON-midgets with S cone OFF feed-forward input and L cones centers serve yellow whereas (d) those ON-midgets with S cone OFF feed-forward input and M centers are responsible for green sensations.…”

Section: Modelsmentioning

confidence: 99%

Circuitry to explain how the relative number of L and M cones shapes color experience

et al. 2016

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The wavelength of light that appears unique yellow is surprisingly consistent across people even though the ratio of middle (M) to long (L) wavelength sensitive cones is strikingly variable. This observation has been explained by normalization to the mean spectral distribution of our shared environment. Our purpose was to reconcile the nearly perfect alignment of everyone's unique yellow through a normalization process with the striking variability in unique green, which varies by as much as 60 nm between individuals. The spectral location of unique green was measured in a group of volunteers whose cone ratios were estimated with a technique that combined genetics and flicker photometric electroretinograms. In contrast to unique yellow, unique green was highly dependent upon relative cone numerosity. We hypothesized that the difference in neural architecture of the blue-yellow and red-green opponent systems in the presence of a normalization process creates the surprising dependence of unique green on cone ratio. We then compared the predictions of different theories of color vision processing that incorporate L and M cone ratio and a normalization process. The results of this analysis reveal that—contrary to prevailing notions--postretinal contributions may not be required to explain the phenomena of unique hues.

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“…In this model, hyperpolarization of S-cones would favor one pathway over the other and explain the observed shifts in hue perception reported here. One potential location where S-cone signals could be summed with L/M opponent pathways is in the outer retina 50 , where cones laterally influence the output of nearby receptors. Support for this site of lateral interaction was observed in the relationship between proximity to S-cones and the M-cones most likely to mediate a blue percept ( Figure 5).…”

Section: /12mentioning

confidence: 99%

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

Schmidt

Sabesan

Tuten

et al. 2018

Preprint

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Color vision requires the activity of cone photoreceptors to be compared in post-receptoral circuitry. Decades of psychophysical measurements have quantified the nature of these comparative interactions on a coarse scale. How such findings generalize to a cellular scale remains unclear. To answer that question, we quantified the influence of surrounding light on the appearance of spots targeted to individual cones. The eye's abberations were corrected with adaptive optics and its position was precisely tracked in real-time to compensate for natural movement. Subjects reported the color appearance of each spot. A majority of Land M-cones consistently gave rise to the sensation of white, while a smaller group repeatedly elicited hue sensations. When blue sensations were reported they were more likely mediated by M-than L-cones. Blue sensations were elicited from M-cones against a short-wavelength light that preferentially elevated the quantal catch in surrounding S-cones, while stimulation of the same cones against a white background elicited green sensations. In one of two subjects, proximity to S-cones increased the probability of blue reports when M-cones were probed. Thus, what is seen when an M-cone is probed appears to depend on the relative activity of cones at other locations in the mosaic.

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Specialized synaptic pathway for chromatic signals beneath S-cone photoreceptors is common to human, Old and New World primates

Cited by 10 publications

References 60 publications

Evolution of the circuitry for conscious color vision in primates

Evolution of the circuitry for conscious color vision in primates

Circuitry to explain how the relative number of L and M cones shapes color experience

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

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