Gerald H. Jacobs

THE DISTRIBUTION AND NATURE OF COLOUR VISION AMONG THE MAMMALS

1. An oft-cited view, derived principally from the writings of Gordon L. Walls, is that relatively few mammalian species have a capacity for colour vision. This review has evaluated that proposition in the light of recent research on colour vision and its mechanisms in mammals. 2. To yield colour vision a retina must contain two or more spectrally discrete types of photopigment. While this is a necessary condition, it is not a sufficient one. This means, in particular, that inferences about the presence of colour vision drawn from studies of photopigments, the precursors of photopigments, or from nervous system signals must be accepted with due caution. 3. Conjoint signals from rods and cones may be exploited by mammalian nervous systems to yield behavioural discriminations consistent with the formal definition of colour vision. Many mammalian retinas are relatively cone-poor, and thus there are abundant opportunities for such rod/cone interactions. Several instances were cited in which animals having (apparently) only one type of cone photopigment succeed at colour discriminations using such a mechanism. it is suggested that the exploitation of such a mechanism may not be uncommon among mammals. 4. Based on ideas drawn from natural history, Walls (1942) proposed that the receptors and photopigments necessary to support colour vision were lost during the nocturnal phase of mammalian history and then re-acquired during the subsequent mammalian radiations. Contemporary examination of photopigment genes along with the utilization of better techniques for identifying rods and cones suggest a different view, that the earliest mammals had retinas containing some cones and two types of cone photopigment. Thus the baseline mammalian colour vision is argued to be dichromacy. 5. A consideration of the broad range of mammalian niches and activity cycles suggests that many mammals are active during photic periods that would make a colour vision capacity potentially useful. 6. A systematic survey was presented that summarized the evidence for colour vision in mammals. Indications of the presence and nature of colour vision were drawn both from direct studies of colour vision and from studies of those retinal mechanisms that are most closely associated with the possession of colour vision. Information about colour vision can be adduced for species drawn from nine mammalian orders.(ABSTRACT TRUNCATED AT 400 WORDS)

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 λmax (wavelength of peak absorbance) close to 500 nm. In several animals, receptors were found that contained a short-wave pigment (mean λmax = 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 λmax 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 λmax = 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. But the spread of λmax values for individual cones was greater in the trichromatic squirrel monkeys than in the dichromats; and in the case of three, behaviourally deuteranomalous, trichromats there wasclear evidence that the distribution of λmax values was bimodal, suggesting photopigments at approximately 552 and 565 nm. The fourth, behaviourally protanomalous, trichrom at exhibited a spread of individual λmax values that ranged between 530 and 550 nm. Good quantitative agreement was found when the microspectrophoto-metrically measured absorbance spectra were used to predict the behavioural sensitivity of individual animals to long wavelengths. The concordance of the two sets of measurements places beyond question the existence of a polymorphism of colour vision in Saimiri sciureus and suggests that the behavioural variation arises from variation in the retinal photopigments. Heterozygous advantage may explain the polymorphism.

Evolution of colour vision in mammals

Colour vision allows animals to reliably distinguish differences in the distributions of spectral energies reaching the eye. Although not universal, a capacity for colour vision is sufficiently widespread across the animal kingdom to provide prima facie evidence of its importance as a tool for analysing and interpreting the visual environment. The basic biological mechanisms on which vertebrate colour vision ultimately rests, the cone opsin genes and the photopigments they specify, are highly conserved. Within that constraint, however, the utilization of these basic elements varies in striking ways in that they appear, disappear and emerge in altered form during the course of evolution. These changes, along with other alterations in the visual system, have led to profound variations in the nature and salience of colour vision among the vertebrates. This article concerns the evolution of colour vision among the mammals, viewing that process in the context of relevant biological mechanisms, of variations in mammalian colour vision, and of the utility of colour vision.

Emergence of Novel Color Vision in Mice Engineered to Express a Human Cone Photopigment

Changes in the genes encoding sensory receptor proteins are an essential step in the evolution of new sensory capacities. In primates, trichromatic color vision evolved after changes in X chromosome–linked photopigment genes. To model this process, we studied knock-in mice that expressed a human long-wavelength–sensitive (L) cone photopigment in the form of an X-linked polymorphism. Behavioral tests demonstrated that heterozygous females, whose retinas contained both native mouse pigments and human L pigment, showed enhanced long-wavelength sensitivity and acquired a new capacity for chromatic discrimination. An inherent plasticity in the mammalian visual system thus permits the emergence of a new dimension of sensory experience based solely on gene-driven changes in receptor organization.

Photopigments and Color Vision in the Nocturnal Monkey, Aotus

The owl monkey (Aotus trivirgatus) is the only nocturnal monkey. The photopigments of Aotus and the relationship between these photopigments and visual discrimination were examined through (1) an analysis of the flicker photometric electroretinogram (ERG), (2) psychophysical tests of visual sensitivity and color vision, and (3) a search for the presence of the photopigment gene necessary for the production of a short-wavelength sensitive (SWS) photopigment. Both electrophysiological and behavioral measurements indicate that in addition to a rod photopigment the retina of this primate contains only one other photopigment type--a cone pigment having a spectral peak ca 543 nm. Earlier results that suggested these monkeys can make crude color discriminations are interpreted as probably resulting from the joint exploitation of signals from rods and cones. Although Aotus has no functional SWS photopigment, hybridization analysis shows that Aotus has a pigment gene that is highly homologous to the human SWS photopigment gene.

Mutations in S-Cone Pigment Genes and the Absence of Colour Vision in Two Species of Nocturnal Primate

Most primates have short-wavelength sensitive (S) cones and one or more types of cone maximally sensitive in the middle to long wavelengths (M/L cones). These multiple cone types provide the basis for colour vision. Earlier experiments established that two species of nocturnal primate, the owl monkey (Aotus trivirgatus) and the bushbaby (Otolemur crassicaudatus), lack a viable population of S cones. Because the retinas of these species have only a single type of M/L cone, they lack colour vision. Both of these species have an S-cone pigment gene that is highly homologous to the human S-cone pigment gene. Examination of the nucleotide sequences of the S-cone pigment genes reveals that each species has deleterious mutational changes: in comparison to the sequence for the corresponding region of the human gene, exon 4 of the bushbaby S-cone pigment gene has a two nucleotide deletion and a single nucleotide insertion that produces a frame shift and results in the introduction of a stop codon. Exon 1 of the owl monkey S-cone pigment gene likewise contains deletions and insertions that produce a stop codon. The absence of colour vision in both of these nocturnal primates can thus be traced to defects in their S-cone pigment genes.

Influence of cone pigment coexpression on spectral sensitivity and color vision in the mouse

The mouse retina contains both middle-wavelength-sensitive (M) and ultraviolet-sensitive (UV) photopigments that are coexpressed in cones. To examine some potential visual consequences of cone pigment coexpression, spectral sensitivity functions were measured in mice (Mus musculus) using both the flicker electroretinogram (ERG) and behavioral discrimination tests. Discrimination tests were also employed to search for the presence of color vision in the mouse. Spectral sensitivity functions for the mouse obtained from ERG measurements and from psychophysical tests each reveal contributions from two classes of cone having peak sensitivities (lambda(max)) of approximately 360 and 509-512 nm. The relative contributions of the two pigment types to spectral sensitivity differ significantly in the two types of measurements with a relationship reversed from that often seen in mammals. Mice were capable of discriminating between some pairs of spectral stimuli under test conditions where luminance-related cues were irrelevant. Since mice can make dichromatic color discriminations, their visual systems must be able to exploit differences in the spectral absorption properties among the cones. Complete selective segregation of opsins into individual photoreceptors is apparently not a prerequisite for color vision.

Within-species variations in visual capacity among squirrel monkeys (Saimiri Sciureus): Color vision

Color vision was studied in 27 squirrel monkeys (Saimiri sciureus) of Peruvian origin (Roman Arch variety). Tests of wavelength discrimination and Rayleigh matching as well as a search for a spectral neutral point were carried out in a behavioral paradigm involving a three-alternative, forced-choice discrimination. Significant individual variations in color vision were found in this species. Some squirrel monkeys have trichromatic color vision, others are dichromats. Within each of these catagories there appear to be three subtypes. Each of these color vision phenotypes can be interpreted as reflecting the presence of a different combination of the types of cone photopigments known to characterize this species. There is a striking gender difference in squirrel monkey color vision; whereas both trichromatic and dichromatic female monkeys were found, all of the males tested were dichromats.

The topography of rod and cone photoreceptors in the retina of the ground squirrel

The distributions of rod and cone photoreceptors have been determined in the retina of the California ground squirrel, Spermophilus beecheyi. Retinas were fixed by perfusion and the rods and cones were detected with indirect immunofluorescence using opsin antibodies. Local densities were determined at 2-mm intervals across the entire retina, from which total numbers of each receptor type were estimated and isodensity distributions were constructed. The ground squirrel retina contains 7.5 million cones and 1.27 million rods. The peak density for the cones (49,550/mm2) is found in a horizontal strip of central retina 2 mm ventral to the elongated optic nerve head, falling gradually to half this value in the dorsal and ventral retinal periphery. Of the cones, there are 14 M cones for every S cone. S cone density is relatively flat across most of the retina, reaching a peak (4500/mm2) at the temporal end of the visual streak. There is one exception to this, however: S cone density climbs dramatically at the extreme dorso-nasal retinal margin (20,000/mm2), where the local ratio of S to M cones equals 1. Rod density is lowest in the visual streak, where the rods comprise less than 5% of the local photoreceptor population, increasing conspicuously in the ventral retina, where the rods achieve 30% of the local photoreceptor population (13,000/mm2). The functional importance of the change in S to M cone ratio at the dorsal circumference of the retina is compromised by the extremely limited portion of the visual field subserved by this retinal region. The significance for vision, if any, remains to be determined. By contrast, the change in rod/cone ratio between the dorsal and ventral halves of the retina indicates a conspicuous asymmetry in the ground squirrels visual system, suggesting a specialization for maximizing visual sensitivity under dim levels of illumination in the superior visual field.

Electroretinogram flicker photometry and its applications

The electroretinogram (ERG) has been a traditional tool for the measurement and the analysis of spectral sensitivity. With the appropriate choices of stimulus and measurement conditions, the ERG permits a noninvasive examination of photopigment complement and provides the means for studying the combination of spectral signals at various locations throughout the retina. There are a number of practical problems associated with making spectral measurements with the ERG. One approach to minimizing these problems is to exploit the advantages of a flicker-photometric procedure. We summarize a method used to conduct ERG flicker photometry and illustrate a range of problems to which this technique can be successfully applied.