Color vision in the tree shrew after removal of posterior neocortex.
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Groups of newborn human infants (N = 180) were habituated to large 16 degrees achromatic ("white") lights of varying luminance (0.35 to 1.16 log cd/m2) and then tested for recovery of habituation to 16 degrees green (dominant lambda = 545 nm), yellow (dominant lambda = 585 nm) or red (dominant lambda = 650 nm) lights which varied in the level of excitation purity (range = 32 to 83%). Results showed that newborns discriminated the chromatic stimuli from white only when excitation purity values exceeded at least 41% for 545-nm green, 47% for 650-nm red, and 65% for 585-nm yellow, limits much higher than those for adults (<1%). Taken together with the results from previous experiments, these saturation discrimination data (with the exception of the yellow data), provide some support for an expanded MacAdam ellipse model of early color discrimination (Brown, 1993; Teller & Lindsey, 1993). This helps reinforce the current view that neonates' vision is based on general rather than selective immaturities or inefficiencies within the requisite optical, photoreceptoral and neural mechanisms.
Budgerigars, Melopsittacus undulatus, were trained to discriminate monochromatic lights from mixtures of two comparison lights. The addition of small amounts of UV (365 nm) to blue or yellow lights dramatically changed the color for the birds. Hue matches showed the birds to be dichromatic both at long wavelengths (only P565 and P508 active) and at short wavelengths (only P370 and P445 active because of screening of P508 and P565 by cone oil droplets). In mid-spectrum (only P445 and P508 active), a hue match was achieved, but the results were more complicated because two opponent neural processes were activated. All observed hue matches were in quantitative agreement with calculations of relative quantum catch in the pairs of participating single cones and point to the presence of a minimum of three opponent neural processes. For the hue matches at mid- and short wavelengths, the calculations also predict peak values of absorbance of the cone oil droplets associated with P508 and P445. Relative intensity of the training light affected difficult matches at long but not short wavelengths, likely due to achromatic signals from the double cones. With suitable training, birds could make intensity discriminations at short wavelengths, where the double cones have diminished sensitivity.
In 1982, Horace Barlow considered the question of human trichromacy in the context of information theory: according to the Sampling Theorem, three types of receptors covering the visible spectrum (400-700 nm) might be sufficient to reconstruct the color signal. Although Barlow was led to reject the direct application of the Sampling Theorem to explain color dimensionality, the theoretical framework offers a fresh point of view for analyzing the color system in conjunction with the physical characteristics of natural color signals. This review aims to illustrate that if the strict mathematical reconstruction (as implied by the Sampling Theorem) is replaced by a pragmatic approximation of color signals, then trichromacy, with its subsequent opponent-color process, could be regarded as an optimization of color constancy abilities in the spectral environment of primates. Higher dimension systems (tetrachromacy) found in other species can also serve the purpose of color constancy optimization in environments where color signals exhibit a finer spectral structure.
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Cichlid fish of the East African Rift Lakes are renowned for their diversity and offer a unique opportunity to study adaptive changes in the visual system in rapidly evolving species flocks. Since color plays a significant role in mate choice, differences in visual sensitivities could greatly influence and even drive speciation of cichlids. Lake Malawi cichlids inhabiting rock and sand habitats have significantly different cone spectral sensitivities. By combining microspectrophotometry (MSP) of isolated cones, sequencing of opsin genes, and spectral analysis of recombinant pigments, we have established the cone complements of four species of Malawi cichlids. MSP demonstrated that each of these species predominately expresses three cone pigments, although these differ between species to give three spectrally different cone complements. In addition, rare populations of spectrally distinct cones were found. In total, seven spectral classes were identified. This was confirmed by opsin gene sequencing, expression, and in vitro reconstitution. The genes represent the four major classes of cone opsin genes that diverged early in vertebrate evolution. All four species possess a long-wave-sensitive (LWS), three spectrally distinct green-sensitive (RH2), a blue-sensitive (SWS2A), a violet-sensitive (SWS2B), and an ultraviolet-sensitive (SWS1) opsin. However, African cichlids determine their spectral sensitivity by differential expression of primarily only three of the seven available cone opsin genes. Phylogenetic analysis suggests that all percomorph fish have similar potential.
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Increment-threshold spectral sensitivity functions were determined during the dominance and suppression phases of binocular rivalry. The shapes of the functions obtained during the dominance phase exhibited three maxima at approximately 440, 530, and 610 nanometers and resembled functions obtained for nonrivalrous control conditions. However, the functions measured during suppression had a single broad peak near 555 nanometers and were adequately described by functions measured with flicker methods during nonrivalrous conditions. The results indicate that binocular rivalry differentially attenuates opponent-color information relative to achromatic information.
The coelacanth, a "living fossil," lives near the coast of the Comoros archipelago in the Indian Ocean. Living at a depth of about 200 m, the Comoran coelacanth receives only a narrow range of light, at about 480 nm. To detect the entire range of "color" at this depth, the coelacanth appears to use only two closely related paralogous RH1 and RH2 visual pigments with the optimum light sensitivities (lambdamax) at 478 nm and 485 nm, respectively. The lambdamax values are shifted about 20 nm toward blue compared with those of the corresponding orthologous pigments. Mutagenesis experiments show that each of these coadapted changes is fully explained by two amino acid replacements.
Males of two closely related, co-occurring species of Lycaena butterflies have dorsally blue (Lycaena heteronea) or red-orange plus ultraviolet (Lycaena rubidus) wings. Males are selectively territorial against conspecific males. Virgin females accept only conspecific males, probably chosen by wing color. Females are nonterritorial and spend most of their adult activity ovipositing on the correct larval food plants. Eyes of both species contain four spectral types of visual pigments (P360, P437, P500, and P568) but the distribution of these pigments within the receptor mosaic is quite different between both species and sexes. The ventral eye region of L. heteronea is tetrachromatic but that of L. rubidus is trichromatic, lacking the blue-sensitive visual pigment P437. The dorsal eye region of males of both species is dichromatic (P360 and P437). Visual-pigment spectra and wing-reflectance spectra are well matched for effective discrimination of wings of conspecific males from those of other species. The dorsal region of female eyes is trichromatic, containing P360, P437, and P568. The third visual pigment, P568, is important for long-range detection by ovipositing females of red coloration on Eriogonum and Rumex food plants. P568 has the same absorbance spectrum as the human red-cone and is considerably red-shifted compared to the P530 possessed by most insects. That the sexes and closely related species can have such major differences in distribution of visual pigments indicates that the visual system is as readily altered as wing coloration in the course of adaptive evolution.
It is known that the squirrel monkey, marmoset, and other related New World (NW) monkeys possess three high-frequency alleles at the single X-linked photopigment locus, and that the spectral sensitivity peaks of these alleles are within those delimited by the human red and green pigment genes. The three alleles in the squirrel monkey and marmoset have been sequenced previously. In this study, the three alleles were found and sequenced in the saki monkey, capuchin, and tamarin. Although the capuchin and tamarin belong to the same family as the squirrel monkey and marmoset, the saki monkey belongs to a different family and is one of the species that is most divergent from the squirrel monkey and marmoset, suggesting the presence of the triallelic system in many NW monkeys. The nucleotide sequences of these alleles from the five species studied indicate that gene conversion occurs frequently and has partially or completely homogenized intronic and exonic regions of the alleles in each species, making it appear that a triallelic system arose independently in each of the five species studied. Nevertheless, a detailed analysis suggests that the triallelic system arose only once in the NW monkey lineage, from a middle wavelength (green) opsin gene, and that the amino acid differences at functionally critical sites among alleles have been maintained by natural selection in NW monkeys for >20 million years. Moreover, the two X-linked opsin genes of howler monkeys (a NW monkey genus) were evidently derived from the incorporation of a middle (green) and a long wavelength (red) allele into one chromosome; these two genes together with the (autosomal) blue opsin gene would immediately enable even a male monkey to have trichromatic vision.
The coelacanth, a "living fossil," lives at a depth of about 200 m near the coast of the Comoros archipelago in the Indian Ocean and receives only a narrow range of light at about 480 nm. To see the entire range of "color" the Comoran coelacanth appears to use only rod-specific RH1 and cone-specific RH2 visual pigments, with the optimum light sensitivities (lambda max) at 478 nm and 485 nm, respectively. These blue-shifted lambda max values of RH1 and RH2 pigments are fully explained by independent double amino acid replacements E122Q/A292S and E122Q/M207L, respectively. More generally, currently available mutagenesis experiments identify only 10 amino acid changes that shift the lambda max values of visual pigments more than 5 nm. Among these, D83N, E1220, M207L, and A292S are associated strongly with the adaptive blue shifts in the lambda max values of RH1 and RH2 pigments in vertebrates.
When the monkey striate cortex is stained for the mitochondrial enzyme cytochrome oxidase a polka-dot pattern of patches or blobs is observed in layers 2 and 3 and more faintly in layers 5 and 6. In the macaque these blobs are aligned along the centers of ocular dominance columns. Cells within blobs lack the orientation selectivity and instead have the simpler concentric center-surround fields common in geniculate cells. Blob cells are specifically concerned with color and in particular with maintaining color constancy despite marked changes in the spectral content of the light source.
Three red/green blind observers (dichromats) performed a wavelength discrimination task over a wide range of intensity levels. As expected, discrimination failed in the entire red/green spectral range at the low intensities typically used in wavelength discrimination experiments, but at very high intensities (at or above 10,000 td) discrimination was well maintained into the red/green range. The following experiments demonstrate that dichromats are able to utilize signals from the blue-sensitive cones (S-cones) to mediate color discrimination throughout the spectrum at high intensities, and they provide an estimate of S-cone sensitivity throughout the visible spectrum.
Sexual selection often favors brighter and exaggerated traits, which also increase the risk of detection by predators. Signals that are preferentially conspicuous to conspecifics would reduce the predation cost of signaling and, therefore, might facilitate the evolution of stronger sexual and social signals. This selective signaling is possible if predators and prey have differently tuned sensory systems. By using a retinal model to compare reflectance from the plumages of Swedish songbirds to the reflectance of their natural backgrounds, we found their color badges to be significantly more conspicuous to other songbirds (which have a UV-tuned visual system) than to raptors and corvids (which have a violet-tuned system) in both coniferous and deciduous forests, consistent with an adaptive private communication system.
The author points out two errors in a reference in a paper by Elzinga and de Weert [J. Opt. Soc. Am. A 3, 1173 (1986)] and their failure to acknowledge the magnitude scaling aspect of B. C. Wilson's work [B. C. Wilson, Ph.D. dissertation (University of Michigan, Ann Arbor, Mich., 1964)].
A central unanswered question in phototransduction is how photosensitive molecules, visual pigments, regulate their absorption spectra. In nature, there exist various types of visual pigments that are adapted to diverse photic environments. To elucidate the molecular mechanisms involved in the adaptive selection of these pigments, we have to identify amino acid changes of pigments that are potentially important in changing the wavelength of maximal absorption (lambda max) and then determine the effects of these mutations on the shift in lambda max. The desired mutants can be constructed using site-directed mutagenesis, expressed in tissue culture cells, and the functional effect of virtually any such mutant can be rigorously determined. The availability of these cell/molecular methods makes vision an ideal model system in studying adaptive mechanisms at the molecular level. The identification of potentially important amino acid changes using evolutionary biological means is an indispensable step in elucidating the molecular mechanisms that underlie the spectral tuning of visual pigments.