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Biomedical subjects

J D Mollon

Publications and source records attributed to J D Mollon.

At least 19 recordsLinked to original sources

Adaptive evolution of color vision genes in higher primates.

The intron 4 sequences of the three polymorphic alleles at the X-linked color photo-pigment locus in the squirrel monkey and the marmoset reveal that the alleles in each species are exceptionally divergent. The data further suggest either that each triallelic system has arisen independently in these two New World monkey lineages, or that in each species at least seven deletions and insertions (14 in the two species) in intron 4 have been transferred and homogenized among the alleles by gene conversion or recombination. In either case, the alleles in each species apparently have persisted more than 5 million years and probably have been maintained by overdominant selection.

Alleles

Sequence and evolution of the blue cone pigment gene in Old and New World primates.

The sequences of the blue cone photopigments in the talapoin monkey (Miopithecus talapoin), an Old World primate, and in the marmoset (Callithrix jacchus), a New World monkey, are presented. Both genes are composed of 5 exons separated by 4 introns. In this respect, they are identical to the human blue gene, and intron sizes are also similar. Based on the level of amino acid identity, both monkey pigments are members of the S branch of pigments. Alignment of these sequences with the human gene requires the insertion/deletion of two separate codons in exon 1. The silent site divergence between these primate blue genes indicates a separation of the Old and New World primate lineages around 43 million years ago.

Amino Acid Sequence

Colour constancy influenced by contrast adaptation.

Visual sensitivity is controlled by at least two distinct types of adaptation: light adaptation adjusts sensitivity to the mean luminance and colour in the stimulus, and contrast adaptation adjusts sensitivity to the variations in luminance and colour. Light adaptation is thought to be important in maintaining the perceived colour of objects despite changes in illumination ('colour constancy'), compensating for the mean changes in the light reflected from scenes under different illuminants. But for naturalistic colour signals, we show here that changes in an illuminant can also alter colour contrasts in images (how colours are distributed around the mean) enough to alter the state of contrast adaptation. Thus perceived colour under different illuminants may also be noticeably influenced by contrast adaptation.

Adaptation, Ocular

The chemistry of John Dalton's color blindness.

John Dalton described his own color blindness in 1794. In common with his brother, he confused scarlet with green and pink with blue. Dalton supposed that his vitreous humor was tinted blue, selectively absorbing longer wavelengths. He instructed that his eyes should be examined after his death, but the examination revealed that the humors were perfectly clear. In experiments presented here, DNA extracted from his preserved eye tissue showed that Dalton was a deuteranope, lacking the middlewave photopigment of the retina. This diagnosis is shown to be compatible with the historical record of his phenotype, although it contradicts Thomas Young's belief that Dalton was a protanope.

Base Sequence

Rayleigh matches and unique green.

There are recurrent reports that Rayleigh matches are bimodally distributed in the colour-normal male population. Similar claims have been made for the distribution of the spectral locus of unique green. Moreover, a positive correlation has sometimes been reported between Rayleigh matches and unique green. Using a computer-controlled Maxwellian colorimeter and bias-free psychophysical methods, we measured both variables for 97 colour-normal male observers. We do not find a bimodal distribution either of Rayleight matches or of settings of unique green. Nor do we find any correlation between the two variables. However, we do observe a very significant relationship between the lightness of the subject's iris and the wavelength that he judges to be unique green.

Adaptation, Ocular

The influence of contrast adaptation on color appearance.

Most models of color vision assume that signals from the three classes of cone receptor are recoded into only three independent post-receptoral channels: one that encodes luminance and two that encode color. Stimuli that are equated for their effects on two of the channels should be discriminable only to the remaining channel, and are thus assumed to isolate the responses of single channels. We used an asymmetric matching task to examine whether such models can account for changes in color appearance following adaptation to contrast--to temporal variations in luminance and chromaticity around a fixed mean luminance and chromaticity. The experiments extend to suprathreshold color appearance the threshold adaptation paradigm of Krauskopf, Williams and Heeley [(1982) Vision Research, 32, 1123-1131]. Adaptation changes the perceived color of chromatic test stimuli both by reducing their saturation (contrast) and by changing their hue (direction within the equiluminant plane). The saturation losses are largest for test stimuli that lie along the chromatic axis defining the adapting modulation, while the hue changes are rotations away from the adapting direction and toward an orthogonal direction within the S and L-M plane. Similar selective changes in both perceived color and perceived lightness occur following adaptation to stimuli that covary in luminance and chromaticity. The selectivity of the aftereffects for multiple directions within color-luminance space is inconsistent with sensitivity changes in only three independent channels. These aftereffects suggest instead that color appearance depends on channels that can be selectively tuned to any color-luminance direction, and that there are no directions that invariably isolate responses in only a single channel. We use the perceived color changes to examine the spectral sensitivities of the chromatic channels and to estimate the distribution of channels. We also examine how adaptation alters the contrast-response function, how it affects reaction times for luminance and chromatic contrast, the extent to which the aftereffects exhibit interocular transfer, and the way in which the perceived color changes differ from those induced by conventional light adaptation.

Adaptation, Ocular

The spatial arrangement of cones in the primate fovea.

The retinae of Old World primates contain three classes of light-sensitive cone, which exhibit peak absorption in different spectral regions. But how are the different types of cone arranged in the hexagonal mosaic of the fovea? This question has often been answered with artists' impressions, but never with direct measurements. Staining for antibodies specific to the short-wave photopigment has revealed a sparse, semiregular array of cones; but nothing is known about the arrangement of the more numerous long- and middle-wave cones. Are they randomly distributed, with chance aggregations of one type, as Hartridge postulated in these columns nearly 50 years ago? Or do they exhibit a regular alteration, recalling the systematic mosaics seen in some non-mammalian species? Or, conversely, is there positive clumping of particular cone types, as might be expected if local patches of cones were descended from a single precursor cell? We have made direct microspectrophotometric measurements of patches of foveal retina from Old World monkeys, and report here that the distribution of long- and middle-wave cones is locally random. These two cone types are present in almost equal numbers, and not in the ratio of 2:1 that has been postulated for the human fovea.

Animals

Dichromats detect colour-camouflaged objects that are not detected by trichromats.

To explain the surprisingly high frequency of congenital red-green colour blindness, the suggestion has been made that dichromats might be at an advantage in breaking certain kinds of colour camouflage. We have compared the performance of dichromats and normal observers in a task in which texture is camouflaged by colour. The texture elements in a target area differed in either orientation or size from the background elements. In one condition, the texture elements were all of the same colour; in the camouflage condition they were randomly coloured red or green. For trichromats, it proved to be more difficult to detect the target region in the camouflage condition, even though colour was completely irrelevant to the task. Dichromats (n = 7) did not show this effect, and indeed performed better than trichromats in the camouflage condition. We conclude that colour can interfere with segregation based upon texture, and that dichromats are less susceptible to such interference.

Color Perception

Sequence divergence and copy number of the middle- and long-wave photopigment genes in Old World monkeys.

We have studied the sequence and organization of the genes for the middle-wave (MW) and long-wave (LW) cone photopigment genes in six species of Old World monkeys. Previous studies have shown that the MW and LW pigments of all six species exhibit peak sensitivities near 535 nm and 565 nm, respectively, and thus resemble the equivalent human pigments. In the case of man, the protein components of the MW and LW photopigments differ by 15 amino acids, although only seven of these differences involve non-homologous substitutions and are therefore candidates for a role in spectral tuning. Regions corresponding to exons 4 and 5 of these genes, and including five such candidate sites, were sequenced in the Old World monkeys. In contrast to the equivalent human genes, substitutions were found at two of these sites, position 233 and 309 of the MW gene in all six species. The role of amino acid substitutions in the spectral tuning of these photopigments is discussed. A comparison of the nucleotide sequences of the MW and LW genes provides evidence for sequence homogenization within species; the role of gene conversion in the evolution of these genes is discussed. The close juxtaposition and homology of the MW and LW genes on the X chromosome is thought to underlie the high frequency of colour vision defects in man and the presence in many individuals of extra copies of the MW gene. A study of a group of talapoin (Ceropithecus talapoin) monkeys has revealed a similar numerical polymorphism for this gene to that present in man. In contrast to the situation in man, where the MW and LW genes may contain a shortened first intron, restriction digests of genomic DNA showed that the size of this intron does not differ across the six species of Old World monkeys examined.

Amino Acid Sequence

The polymorphic photopigments of the marmoset: spectral tuning and genetic basis.

The marmoset (Callithrix jacchus jacchus), a South American monkey, is polymorphic for the middle- to long-wave cone photopigments: the three variant pigments have spectral peaks at 543, 556 and 563 nm. Comparisons of the deduced amino acid sequences of these pigments indicate that the variations in spectral sensitivity are associated with the presence or absence of hydroxyl-bearing residues at sites 180 and 285; but, in contrast to the additive hypothesis of Neitz et al. (1991), we propose that adjustments at site 233 may also be required to produce viable long-wave and middle-wave pigments. Within a family group of monkeys, we find that a restriction site polymorphism in the photopigment gene segregates in a way that is consistent with the single X-linked gene hypothesis previously proposed on the basis of the photopigment types present in male and female marmosets.

Amino Acid Sequence

The relationship between cone pigments and behavioural sensitivity in a New World monkey (Callithrix jacchus jacchus).

Microspectrophotometric measurements of visual pigments and behavioural measurements of spectral sensitivity are reported for individual marmosets from 3 family groups. The sex differences and polymorphism that characterise the long-wave cone pigments in this species are well reflected by variations in the behavioural sensitivities. With one exception, the pattern of inheritance is compatible with a genetic model in which the long-wave pigment is specified by a single polymorphic locus on the X-chromosome. Measurements are also reported for the spectral absorbance of the marmoset lens, and these are used to reconstruct short-wave behavioural sensitivity from the microspectrophotometric measurements of the short-wave cones.

Animals

A reduction in stimulus duration can improve wavelength discriminations mediated by short-wave cones.

Virtually all visual discriminations become less accurate when either the luminance or the duration of the stimulus is reduced. An exception is found for wavelength discriminations near 460 nm, where an increase in either luminance or duration can cause the threshold to rise. For flashes of 100 msec or less, the critical variable is the total energy of the flash (i.e. the product of retinal illuminance and flash duration), and wavelength discrimination is optimal at an intermediate value; higher stimulus energy causes discrimination to deteriorate. To explain these findings we suppose that discrimination in this region of the spectrum is mediated by a channel that draws opposed signals from the short-wavelength cones and from some combination of the middle- and long-wavelength cones, and that high stimulus energies cause saturation of this channel.

Adult

Changes in colour appearance following post-receptoral adaptation.

Current models of colour vision assume that colour is represented by activity in three independent post-receptoral channels: two encoding chromatic information and one encoding luminance. An important feature of these models is that variations in certain directions in colour space modulate the response of only one of the channels. We have tested whether such models can predict how colour appearance is altered by adaptation-induced changes in post-receptoral sensitivity. In contrast to the changes predicted by three independent channels, colour appearance is always distorted away from the direction in colour space to which the observer has adapted. This suggests that at the level at which the adaptation effects occur, there is no colour direction that invariably isolates only a single post-receptoral channel.

Adaptation, Physiological

Photosensitive and photostable pigments in the retinae of Old World monkeys.

Microspectrophotometric measurements of retinal receptors are reported for eight species of Old World monkey. Although the animals vary greatly in size, colourings and habitat, they all appear to be trichromats and the peak sensitivities of their cones invariably lie near 430, 535 and 565 nm. This consistent pattern contrasts with the results reported earlier for New World monkeys and with the results reported here for Tupaia glis. The trichromacy of frugivorous catarrhine monkeys may have co-evolved with a particular class of coloured fruit. Short-wave cones were rare in all species. The ratio of the numbers of middle-wave and long-wave cones varied between individual animals, but had an overall value close to unity. In the case of all the species examined here, we have recorded a photostable pigment in the inner segments of rods and cones. The latter pigment has a peak sensitivity close to 420 nm and an absorbance spectrum that is narrower than that of a photosensitive visual pigment.

Animals

"Tho' she kneel'd in that place where they grew..." The uses and origins of primate colour vision.

The disabilities experienced by colour-blind people show us the biological advantages of colour vision in detecting targets, in segregating the visual field and in identifying particular objects or states. Human dichromats have especial difficulty in detecting coloured fruit against dappled foliage that varies randomly in luminosity; it is suggested that yellow and orange tropical fruits have co-evolved with the trichromatic colour vision of Old World monkeys. It is argued that the colour vision of man and of the Old World monkeys depends on two subsystems that remain parallel and independent at early stages of the visual pathway. The primordial subsystem, which is shared with most mammals, depends on a comparison of the rates of quantum catch in the short- and middle-wave cones; this system exists almost exclusively for colour vision, although the chromatic signals carry with them a local sign that allows them to sustain several of the functions of spatiochromatic vision. The second subsystem arose from the phylogenetically recent duplication of a gene on the X-chromosome, and depends on a comparison of the rates of quantum catch in the long- and middle-wave receptors. At the early stages of the visual pathway, this chromatic information is carried by a channel that is also sensitive to spatial contrast. The New World monkeys have taken a different route to trichromacy: in species that are basically dichromatic, heterozygous females gain trichromacy as a result of X-chromosome inactivation, which ensures that different photopigments are expressed in two subsets of retinal photoreceptor.

Animals

Polymorphism of visual pigments in a callitrichid monkey.

Microspectrophotometric measurements of visual pigments have been obtained for a large sample of New World monkeys of the species Callithrix jacchus jacchus. These animals exhibit a polymorphism of visual pigments. The rods (Lmax 499 nm) and the short-wave receptors (Lmax 423 nm) appear to be common to all animals but individuals differ in the number and spectral position of pigments in the green-yellow spectral region. The latter pigments cluster near 545, 559 and 567 nm. Male monkeys draw one pigment from this set and female monkeys may draw one or two. The results are generally consistent with a genetic theory that postulates in Callithrix three possible alleles for a single locus in the X-chromosome. It appears that polymorphisms of cone pigments may be widespread among neotropical primates.

Animals