Tetrachromatic color vision here refers to human color vision that relies on the presence of four types of retinal cone photopigment whose signals are processed independently. By analogy with the classical, psychophysical definition of human trichromacy , a tetrachromatic observer will require four primaries in a color-matching experiment to match any other color. In comparative studies of color vision, the term tetrachromacy usually refers to the presence of four distinct types of photoreceptor.
A distinction has been made between strong and weak tetrachromacy . In both cases, there are four types of cone in the retina, but only the former denotes behavioral tetrachromacy, where the cortex gains independent access to a fourth signal allowing the individual to perceive colors along a dimension denied to color-normal people.
Normal human color vision is trichromatic in that three variables or primary lights are needed to match any given color . Since 1802 , it has been thought that the basis of trichromacy is the presence in the retina of three types of “sensitive filament,” now commonly known as cone photoreceptors. According to the wavelength of maximum sensitivity, these cones are referred to as S (short-wave sensitive), M (middle-wave sensitive), and L (long-wave sensitive) cones.
To explain the existence of additional types of cone with different spectral sensitivities (M’ or L’), one needs to consider the genetics of the M and L cone photopigments. Nathans et al.  sequenced the M and L protein genes that are located in a tandem arrangement on the X chromosome and found a 98 % homology of their DNA. This has been taken as evidence for an evolutionarily recent duplication of an ancestral gene, followed by some degree of divergence of the sequences of the two original copies. Highly similar genes tend to misalign during meiosis and recombine in different ways. The most common outcome of this process is a gene product that consists of part L and part M gene. Importantly, such a hybrid gene will express a photopigment with a spectral sensitivity intermediate to the normal L and M cone photopigments (; for review see ).
A seminal paper by Mollon and colleagues  provides a useful analogy to human tetrachromacy. They studied variations of color vision in a basically dichromatic species of New World primates, the squirrel monkey. They discovered in the population pool a range of cone pigments with different spectral sensitivities and, more importantly, behavioral trichromacy in a subset of females. Though no genetic analyses were available at the time, the authors hypothesized correctly that the origin of these animals’ good color discrimination was genetic and afforded to them by heterozygosity at the X-linked locus.
X-Chromosome Inactivation and the Retinal Cone Mosaic
In females, during embryonic development, one of their two X chromosomes is silenced . This process is random with respect to the parental origin of the X chromosome, but once inactivation has taken place in a given cell, it is preserved in all daughter cells. Crucially for tetrachromacy, the different types of expressed photopigment will be segregated in different cone cells so that the retina of a carrier for, say, deuteranomaly will be a mosaic of normal and anomalous cones (S, M, L’, and L), and the size of the retinal cone patches will depend on the time of onset of X inactivation and the migration of cones in the developing retina. The analogous case exists for carriers of protanomaly (cPa) though they are much rarer in the population.
What Are the Necessary Conditions for Tetrachromacy?
It is known that there is a range of L pigments with different peak sensitivities and similarly a range of M pigments [9, 10]. In particular, a common polymorphism at site 180 in the L cone photopigment gives a ~4 nm spectral difference in sensitivity [4, 11]. In addition, some hybrid pigments may be present in lower optical density and thus have narrower absorption curves. How big a difference in absorption curve between, say, L and L’ is sufficient for tetrachromatic color vision? It may be significant that the strongest candidate for tetrachromacy identified so far (see below, ) has L and L’ cone photopigments with an estimated spectral difference of 12 nm.
Color vision does not simply depend on the number and type of retinal cone photopigment. In order to perceive colors and be able to discriminate between them, the inputs from different classes of cone need to be compared and two chromatic post-receptoral channels have been identified for this task (for discussion see ).
Prior to the 1980s the majority of scientists concerned with individual differences in human color vision and possible phenotypic manifestations of X-linked heterozygosity believed that female carriers of red-green deficiencies either shared a little in their sons’ disability or did not differ in any significant way from color-normal observers (for review see ). A different view was held by the Dutch physicist De Vries  who, in 1948, explicitly stated that the daughters of a Da father “must be tetrachromatic,” and that it should be possible to demonstrate (strong) tetrachromacy using color mixing experiments. That the existence of an additional cone type in the retina indeed has an effect on color matches was found by Nagy and colleagues 32 years later by demonstrating failure of the additivity law . According to this fundamental law of color matching for trichromats, the addition of a monochromatic light to an existing color match (here a match of a 546 nm and a 660 nm mixture ratio to a 588 nm reference light) should not upset the match even though the overall appearance might be different. Four carriers of an unidentified type, but no color-normal male or female control, changed their matches after chromatic adaptation. Since the carriers were nevertheless capable of making trichromatic matches, they would be classified as weak tetrachromats.
Methodological Issues and Results for Strong Tetrachromacy
Explicit tests for strong tetrachromacy must ensure that a fourth chromatic primary is provided in the middle- to long-wave range of the spectrum on which the tetrachromat can base her discriminations. Thus no ordinary RGB color monitor can be used for any test of this kind.
Ideal is a specifically designed colorimeter which allows inclusion and manipulation of the wavelength of n primary lights with independent control of luminance. It would also permit the precise specifications of spatial and temporal stimulus parameters. Such a system was used by Jordan et al.  for the identification of tetrachromats in a Rayleigh-type discrimination test. The stimuli used were in the spectral range from 556 nm to 670 nm, where S cones are insensitive. A triplet of three successive lights was presented. One light was a red-green mixture (546 + 670 nm) that could vary in the proportion of red, and the other two were a monochromatic yellow (590 nm). Observers were asked to identify the red-green mixture. Since all normal trichromats can make a dichromatic color match in this spectral range, they were expected to fail to detect the mixture light for some red-green mixture and some intensity of the monochromatic yellow. In contrast, a strong tetrachromat was predicted to always detect the mixture with her L’ (M’) cones. Only one out of 18 cDa (known as cDa29) and none of 7 cPa participants performed according to the prediction. As expected, all control subjects failed to discriminate. Since cDa29 could not make a trichromatic color match with only two primaries available in the Rayleigh region, she was classified as strong tetrachromat.
Another approach to explicitly test for strong tetrachromacy is to ask candidates to discriminate surface colors. The challenge here is that one needs to find stimuli that are metameric (indistinguishable) for normal observers, but look distinct to a tetrachromat. Such a test was designed to demonstrate that Da individuals are capable of making discriminations not achievable by normal observers  and cDa individuals ought to be able to make the same discriminations if their L vs (L + L’) channel is salient enough. Participants were asked to rate how distinct pairs of surface colors (two sets of different blue-yellow acrylic mixtures) looked . Multidimensional scaling (MDS) was then used to reconstruct the subjective color space for each observer. Four out of nine cDa observers were found to be able to make discriminations on this test, and their MDS solution correlated significantly with the theoretical L vs (L + L’) channel. One of these four carriers was cDa29. Molecular genetic analyses of saliva samples taken from these observers confirmed the existence of a hybrid gene for an L’ cone .
To provide the most conclusive evidence for strong tetrachromacy, a full set of color-matching functions is needed for selected candidates. This would allow direct derivation of the four-dimensional color space of four-cone individuals. Furthermore, the influence of factors such as cone ratios, cone optical density, and absorption by the ocular media must be considered in further tests.
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