Design considerations for the enhancement of human color vision by breaking binocular redundancy.
ABSTRACT: To see color, the human visual system combines the response of three types of cone cells in the retina-a compressive process that discards a significant amount of spectral information. Here, we present designs based on thin-film optical filters with the goal of enhancing human color vision by breaking its inherent binocular redundancy, providing different spectral content to each eye. We fabricated a set of optical filters that "splits" the response of the short-wavelength cone between the two eyes in individuals with typical trichromatic vision, simulating the presence of approximately four distinct cone types. Such an increase in the number of effective cone types can reduce the prevalence of metamers-pairs of distinct spectra that resolve to the same tristimulus values. This technique may result in an enhancement of spectral perception, with applications ranging from camouflage detection and anti-counterfeiting to new types of artwork and data visualization.
Project description:The first step in the evolution of primate trichromatic color vision was the expression of a third cone class not present in ancestral mammals. This observation motivates a fundamental question about the evolution of any sensory system: how is it possible to detect and exploit the presence of a novel sensory class? We explore this question in the context of primate color vision. We present an unsupervised learning algorithm capable of both detecting the number of spectral cone classes in a retinal mosaic and learning the class of each cone using the inter-cone correlations obtained in response to natural image input. The algorithm's ability to classify cones is in broad agreement with experimental evidence about functional color vision for a wide range of mosaic parameters, including those characterizing dichromacy, typical trichromacy, anomalous trichromacy, and possible tetrachromacy.
Project description:Synaptic interactions to extract information about wavelength, and thus color, begin in the vertebrate retina with three classes of light-sensitive cells: rod photoreceptors at low light levels, multiple types of cone photoreceptors that vary in spectral sensitivity, and intrinsically photosensitive ganglion cells that contain the photopigment melanopsin. When isolated from its neighbors, a photoreceptor confounds photon flux with wavelength and so by itself provides no information about color. The retina has evolved elaborate color opponent circuitry for extracting wavelength information by comparing the activities of different photoreceptor types broadly tuned to different parts of the visible spectrum. We review studies concerning the circuit mechanisms mediating opponent interactions in a range of species, from tetrachromatic fish with diverse color opponent cell types to common dichromatic mammals where cone opponency is restricted to a subset of specialized circuits. Distinct among mammals, primates have reinvented trichromatic color vision using novel strategies to incorporate evolution of an additional photopigment gene into the foveal structure and circuitry that supports high-resolution vision. Color vision is absent at scotopic light levels when only rods are active, but rods interact with cone signals to influence color perception at mesopic light levels. Recent evidence suggests melanopsin-mediated signals, which have been identified as a substrate for setting circadian rhythms, may also influence color perception. We consider circuits that may mediate these interactions. While cone opponency is a relatively simple neural computation, it has been implemented in vertebrates by diverse neural mechanisms that are not yet fully understood.
Project description:Color vision in birds is mediated by four types of cone photoreceptors whose maximal sensitivities (?max) are evenly spaced across the light spectrum. In the course of avian evolution, the ?max of the most shortwave-sensitive cone, SWS1, has switched between violet (?max > 400 nm) and ultraviolet (?max < 380 nm) multiple times. This shift of the SWS1 opsin is accompanied by a corresponding short-wavelength shift in the spectrally adjacent SWS2 cone. Here, we show that SWS2 cone spectral tuning is mediated by modulating the ratio of two apocarotenoids, galloxanthin and 11’,12’-dihydrogalloxanthin, which act as intracellular spectral filters in this cell type. We propose an enzymatic pathway that mediates the differential production of these apocarotenoids in the avian retina, and we use color vision modeling to demonstrate how correlated evolution of spectral tuning is necessary to achieve even sampling of the light spectrum and thereby maintain near-optimal color discrimination.
Project description:Color vision in marsupials has recently emerged as a particularly interesting case among mammals. It appears that there are both dichromats and trichromats among closely related species. In contrast to primates, marsupials seem to have evolved a different type of trichromacy that is not linked to the X-chromosome. Based on microspectrophotometry and retinal whole-mount immunohistochemistry, four trichromatic marsupial species have been described: quokka, quenda, honey possum, and fat-tailed dunnart. It has, however, been impossible to identify the photopigment of the third cone type, and genetically, all evidence so far suggests that all marsupials are dichromatic. The tammar wallaby is the only Australian marsupial to date for which there is no evidence of a third cone type. To clarify whether the wallaby is indeed a dichromat or trichromatic like other Australian marsupials, we analyzed the number of cone types in the "dichromatic" wallaby and the "trichromatic" dunnart. Employing identical immunohistochemical protocols, we confirmed that the wallaby has only two cone types, whereas 20-25% of cones remained unlabeled by S- and LM-opsin antibodies in the dunnart retina. In addition, we found no evidence to support the hypothesis that the rod photopigment (rod opsin) is expressed in cones which would have explained the absence of a third cone opsin gene. Our study is the first comprehensive and quantitative account of color vision in Australian marsupials where we now know that an unexpected diversity of different color vision systems appears to have evolved.
Project description:The color vision of most platyrrhine primates is determined by alleles at the polymorphic X-linked locus coding for the opsin responsible for the middle- to long-wavelength (M/L) cone photopigment. Females who are heterozygous at the locus have trichromatic vision, whereas homozygous females and all males are dichromatic. This study characterized the opsin alleles in a wild population of the socially monogamous platyrrhine monkey Callicebus brunneus (the brown titi monkey), a primate that an earlier study suggests may possess an unusual number of alleles at this locus and thus may be a subject of special interest in the study of primate color vision. Direct sequencing of regions of the M/L opsin gene using feces-, blood-, and saliva-derived DNA obtained from 14 individuals yielded evidence for the presence of three functionally distinct alleles, corresponding to the most common M/L photopigment variants inferred from a physiological study of cone spectral sensitivity in captive Callicebus.
Project description:Primate trichromatic colour vision has been hypothesized to be well tuned for detecting variation in facial coloration, which could be due to selection on either signal wavelengths or the sensitivities of the photoreceptors themselves. We provide one of the first empirical tests of this idea by asking whether, when compared with other visual systems, the information obtained through primate trichromatic vision confers an improved ability to detect the changes in facial colour that female macaque monkeys exhibit when they are proceptive. We presented pairs of digital images of faces of the same monkey to human observers and asked them to select the proceptive face. We tested images that simulated what would be seen by common catarrhine trichromatic vision, two additional trichromatic conditions and three dichromatic conditions. Performance under conditions of common catarrhine trichromacy, and trichromacy with narrowly separated LM cone pigments (common in female platyrrhines), was better than for evenly spaced trichromacy or for any of the dichromatic conditions. These results suggest that primate trichromatic colour vision confers excellent ability to detect meaningful variation in primate face colour. This is consistent with the hypothesis that social information detection has acted on either primate signal spectral reflectance or photoreceptor spectral tuning, or both.
Project description:Human color vision is achieved by mixing neural signals from cone photoreceptors sensitive to different wavelengths of light. The spatial arrangement and proportion of these spectral types in the retina set fundamental limits on color perception, and abnormal or missing types are responsible for color vision loss. Imaging provides the most direct and quantitative means to study these photoreceptor properties at the cellular scale in the living human retina, but remains challenging. Current methods rely on retinal densitometry to distinguish cone types, a prohibitively slow process. Here, we show that photostimulation-induced optical phase changes occur in cone cells and carry substantial information about spectral type, enabling cones to be differentiated with unprecedented accuracy and efficiency. Moreover, these phase dynamics arise from physiological activity occurring on dramatically different timescales (from milliseconds to seconds) inside the cone outer segment, thus exposing the phototransduction cascade and subsequent downstream effects. We captured these dynamics in cones of subjects with normal color vision and a deuteranope, and at different macular locations by: (<i>i</i>) marrying adaptive optics to phase-sensitive optical coherence tomography to avoid optical blurring of the eye, (<i>ii</i>) acquiring images at high speed that samples phase dynamics at up to 3 KHz, and (<i>iii</i>) localizing phase changes to the cone outer segment, where photoactivation occurs. Our method should have broad appeal for color vision applications in which the underlying neural processing of photoreceptors is sought and for investigations of retinal diseases that affect cone function.
Project description:What is color vision for? Here we compared the extent to which memory modulates color appearance of objects and faces. Participants matched the colors of stimuli illuminated by low-pressure sodium light, which renders scenes monochromatic. Matches for fruit were not predicted by stimulus identity. In contrast, matches for faces were predictable, but surprising: faces appeared green and looked sick. The paradoxical face-color percept could be explained by a Bayesian observer model constrained by efficient coding. The color-matching data suggest that the face-color prior is established by visual signals arising from the recently evolved L-M cone system, not the older S-cone channel. Taken together, the results show that when retinal mechanisms of color vision are impaired, the impact of memory on color perception is greatest for face color, supporting the idea that trichromatic color plays an important role in social communication.
Project description:<h4>Background</h4>Color vision plays a critical role in visual behavior. An animal's capacity for color vision rests on the presence of differentially sensitive cone photoreceptors. Spectral sensitivity is a measure of the visual responsiveness of these cones at different light wavelengths. Four classes of cone pigments have been identified in vertebrates, but in teleost fishes, opsin genes have undergone gene duplication events and thus can produce a larger number of spectrally distinct cone pigments. In this study, we examine the question of large-scale variation in color vision with respect to individual, sex and species that may result from differential expression of cone pigments. Cichlid fishes are an excellent model system for examining variation in spectral sensitivity because they have seven distinct cone opsin genes that are differentially expressed.<h4>Results</h4>To examine the variation in the number of cones that participate in cichlid spectral sensitivity, we used whole organism electrophysiology, opsin gene expression and empirical modeling. Examination of over 100 spectral sensitivity curves from 34 individuals of three species revealed that (1) spectral sensitivity of individual cichlids was based on different subsets of four or five cone pigments, (2) spectral sensitivity was shaped by multiple cone interactions and (3) spectral sensitivity differed between species and correlated with foraging mode and the spectral reflectance of conspecifics. Our data also suggest that there may be significant differences in opsin gene expression between the sexes.<h4>Conclusions</h4>Our study describes complex opponent and nonopponent cone interactions that represent the requisite neural processing for color vision. We present the first comprehensive evidence for pentachromatic color vision in vertebrates, which offers the potential for extraordinary spectral discrimination capabilities. We show that opsin gene expression in cichlids, and possibly also spectral sensitivity, may be sex-dependent. We argue that females and males sample their visual environment differently, providing a neural basis for sexually dimorphic visual behaviour. The diversification of spectral sensitivity likely contributes to sensory adaptations that enhance the contrast of transparent prey and the detection of optical signals from conspecifics, suggesting a role for both natural and sexual selection in tuning color vision.
Project description:The howler monkeys (Alouatta sp.) are the only New World primates to exhibit routine trichromacy. Both males and females have three cone photopigments. However, in contrast to Old World monkeys, Alouatta has a locus control region upstream of each opsin gene on the X-chromosome and this might influence the retinal organization underlying its color vision. Post-mortem microspectrophotometry (MSP) was performed on the retinae of two male Alouatta to obtain rod and cone spectral sensitivities. The MSP data were consistent with only a single opsin being expressed in each cone and electrophysiological data were consistent with this primate expressing full trichromacy. To study the physiological organization of the retina underlying Alouatta trichromacy, we recorded from retinal ganglion cells of the same animals used for MSP measurements with a variety of achromatic and chromatic stimulus protocols. We found MC cells and PC cells in the Alouatta retina with similar properties to those previously found in the retina of other trichromatic primates. MC cells showed strong phasic responses to luminance changes and little response to chromatic pulses. PC cells showed strong tonic response to chromatic changes and small tonic response to luminance changes. Responses to other stimulus protocols (flicker photometry; changing the relative phase of red and green modulated lights; temporal modulation transfer functions) were also similar to those recorded in other trichromatic primates. MC cells also showed a pronounced frequency double response to chromatic modulation, and with luminance modulation response saturation accompanied by a phase advance between 10-20 Hz, characteristic of a contrast gain mechanism. This indicates a very similar retinal organization to Old-World monkeys. Cone-specific opsin expression in the presence of a locus control region for each opsin may call into question the hypothesis that this region exclusively controls opsin expression.