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J D Mollon

Publications and source records attributed to J D Mollon.

At least 19 recordsLinked to original sources

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

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

Tyndall's paradox of hue discrimination.

We confirm a remarkable but forgotten property of human color vision that was described over 50 years ago by Tyndall [J. Opt. Soc. Am 23, 12 (1933)]: if wavelength discrimination is measured in the region of 455 nm, the sensitivity of the eye improves when a large fraction of the monochromatic light in each half of the matching field is replaced by white light that is common to the two halves. We demonstrate that a similar facilitation also occurs when the shortwave monochromatic components are held constant in luminance and a long-wave desaturant of increasing luminance is added to the shortwave discrimanda. We relate these phenomena to the properties of postreceptoral visual channels.

Color Perception

Polymorphism of photopigments in the squirrel monkey: a sixth phenotype.

We describe here a trichromatic type of squirrel monkey that resembles Old World monkeys in having two well-separated photopigments in the red-green part of the spectrum; the cones of this phenotype have peak sensitivities close to 430, 536 and 564 nm. The existence of such animals is predicted by a genetic model that postulates three alleles for a single locus on the X-chromosome of the squirrel monkey. The three alleles correspond to three different photopigments in the red-green spectral range. A male monkey, or a homozygous female, will be dichromatic, combining short-wave cones with just one of the cone types in the red-green range. But a female monkey, if heterozygous at the locus, draws any two of the three alleles from the set. X-chromosome inactivation ensures that the two alleles are expressed in different subpopulations of retinal cone, giving the monkey the basis for trichromatic colour vision. This model requires three trichromatic types of female squirrel monkey. The photopigment complements of two types have previously been reported and microspectrophotometric data are now given for the third type. Behaviourally, this third type of trichromat gives precise Rayleigh matches that are intermediate between those of the other two types of trichromat. The polymorphism of photopigments in the squirrel monkey may be maintained by the heterozygous advantage enjoyed by the trichromatic females. This would be an instructive instance of heterozygous advantage because it is a case where X-chromosome inactivation plays a crucial role in segregating the two different gene-products into different cells.

Animals

Transient tritanopia of a second kind.

Using a psychophysical method that allows the tracking of very rapid changes in sensitivity, we demonstrate an anomaly in the time-course of light adaptation for the short-wave mechanism: after the onset of a yellow (581 nm) field of approximately 10(5.3) td the threshold for short-wave targets does not recover monotonically but continues to rise for several seconds before falling to its equilibrium value. The phenomenon is absent when the adapting field has a wavelength of 511 nm and has been adjusted to give a similar equilibrium value for the short-wave threshold.

Adaptation, Ocular

Two types of trichromatic squirrel monkey share a pigment in the red-green spectral region.

Microspectrophotometric measurements have been obtained for individual photoreceptors from four female squirrel monkeys (Saimiri sciureus) that had been shown behaviourally to be trichromatic. Relative to a normal human observer, two of the monkeys required more red light for a Rayleigh match; the other two required more green light than a normal human observer. In the red-green spectral region, the first type of monkey was found to have two cone pigments with peak sensitivities at approximately 536 and 549 nm, whereas the second type was found to have pigments with peak sensitivities at approximately 549 and 564 nm. By maximum likelihood estimation it was shown that the microspectrophotometric data could be described by a model that assumed only three underlying distributions, two of which were present in each type of monkey. The fit of this model was as good as one in which a "double normal" distribution was fitted individually to the data for each animal. This result is consistent with a genetic theory that postulates in Saimiri three possible alleles for a single locus on the X-chromosome; the heterozygous female enjoys trichromacy because Lyonisation ensures that only one photopigment is manufactured in any given cone.

Animals

Variations of colour vision in a New World primate can be explained by polymorphism of retinal photopigments.

The squirrel monkey (Saimiri sciureus) exhibits a polymorphism of colour vision: some animals are dichromatic, some trichromatic, and within each of these classes there are subtypes that resemble the protan and deutan variants of human colour vision. For each of ten individual monkeys we have obtained (i) behavioural measurements of colour vision and (ii) microspectrophotometric measurements of retinal photopigments. The behavioural tests, carried out in Santa Barbara, included wavelength discrimination, Rayleigh matches, and increment sensitivity at 540 and 640 nm. The microspectrophotometric measurements were made in London, using samples of fresh retinal tissue and a modified Liebman microspectrophotometer: the absorbance spectra for single retinal cells were obtained by passing a monochromatic measuring beam through the outer segments of individual rods and cones. The two types of data, behavioural and microspectrophotometric, were obtained independently and were handed to a third party before being interchanged between experimenters. From all ten animals, a rod pigment was recorded with lambda max (wavelength of peak absorbance) close to 500 nm. In several animals, receptors were found that contained a short-wave pigment (mean lambda max = 433.5 nm): these violet-sensitive receptors were rare, as in man and other primate species. In the middle- to long-wave part of the spectrum, there appear to be at least three possible Saimiri photopigments (with lambda max values at about 537,550 and 565 nm) and individual animals draw either one or two pigments from this set, giving dichromatic or trichromatic colour vision. Thus, those animals that behaviourally resembled human protanopes exhibited only one pigment in the red-green range, with lambda max = 537 nm; other behaviourally dichromatic animals had single pigments lying at longer wavelengths and these were the animals that behaviourally had higher sensitivity to long wavelengths. Four of the monkeys were behaviourally judged to be trichromatic. None of the latter animals exhibited the two widely separated pigments (close to 535 and 567 nm) that are found in the middle- and long-wave cones of macaque monkeys.(ABSTRACT TRUNCATED AT 400 WORDS)

Animals

Human visual pigments: microspectrophotometric results from the eyes of seven persons.

The material for this work was obtained from seven eyes removed because of malignant growths. Foveal and parafoveal samples of the retinas were taken and transverse measurements were made of the absorbance spectra of the outer segments of the rods and cones, using a Liebman microspectrophotometer. Four kinds of spectra were obtained with absorbance peaks at the following wavelengths: rods, 496.3 +/- 2.3 nm (n = 39); red cones, 558.4 +/- 5.2 nm (n = 58); green cones, 530.8 +/- 3.5 nm (n = 45); blue cones, 419.0 +/- 3.6 nm (n = 5). The distribution of the peaks was unimodal for the rods. For the red and green cones, however, there was evidence for bimodal distributions, with sub-population maxima at 563.2 +/- 3.1 nm (n = 27) and 554.2 +/- 2.3 nm (n = 31) for the reds and at 533.7 +/- 2.1 nm (n = 23) and 527.8 +/- 1.8 nm (n = 22) for the greens. A substantial difference in mean spectral location of the red cones was observed between patient 1 (561 nm) and patient 4 (553 nm). Both patients were classified as normal trichromats by all clinical tests of colour vision but there was a clear difference in their relative sensitivities to long-wave fields. In both direction and magnitude, this difference proved to be that required by the microspectrophotometric results.

Humans