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All mammalian cone photopigments are derived from the operation of representatives from two opsin gene families (SWS1 and LWS in marsupial and eutherian mammals; SWS2 and LWS in monotremes), a process that produces cone pigments with respective peak sensitivities in the short and middle-to-long wavelengths. With the exception of a number of primate taxa, the modal pattern for mammals is to have two types of cone photopigment, one drawn from each of the gene families. In recent years, it has been discovered that the SWS1 opsin genes of a widely divergent collection of eutherian mammals have accumulated mutational changes that render them nonfunctional. This alteration reduces the retinal complements of these species to a single cone type, thus rendering ordinary color vision impossible. At present, several dozen species from five mammalian orders have been identified as falling into this category, but the total number of mammalian species that have lost short-wavelength cones in this way is certain to be much larger, perhaps reaching as high as 10% of all species. A number of circumstances that might be used to explain this widespread cone loss can be identified. Among these, the single consistent fact is that the species so affected are nocturnal or, if they are not technically nocturnal, they at least feature retinal organizations that are typically associated with that lifestyle. At the same time, however, there are many nocturnal mammals that retain functional short-wavelength cones. Nocturnality thus appears to set the stage for loss of functional SWS1 opsin genes in mammals, but it cannot be the sole circumstance.

Thirty years ago virtually everything known about primate color vision derived from psychophysical studies of normal and color-defective humans and from physiological investigations of the visual system of the macaque monkey, the most popular of human surrogates for this purpose. The years since have witnessed much progress toward the goal of understanding this remarkable feature of primate vision. Among many advances, investigations focused on naturally occurring variations in color vision in a wide range of nonhuman primate species have proven to be particularly valuable. Results from such studies have been central to our expanding understanding of the interrelationships between opsin genes, cone photopigments, neural organization, and color vision. This work is also yielding valuable insights into the evolution of color vision.

X-linked photopigment polymorphism produces six different color vision phenotypes in most species of New World monkey. In the subfamily Callitrichinae, the three M/L alleles underlying these different phenotypes are present at unequal frequencies suggesting that selective pressures other than heterozygous-advantage operate on these alleles. Earlier we investigated this hypothesis with functional substitution, a technique using a computer monitor to simulate colors as they would appear to humans with monkey visual pigments (Visual Neuroscience 21:217-222, 2004). The stimuli were derived from measurements of ecologically relevant fruit and foliage. We found that discrimination performance depended on the relative spectral positioning of the substituted M and L pigment pair. Here we have undertaken a systematic examination of two simulation parameters--test field luminance and stimulus duration. Discriminability of the fruit colors depended on which phenotype was simulated but only at short stimulus durations and/or low luminances. Under such conditions, phenotypes with the larger pigment peak separations performed better. At longer durations and higher luminances, differences in performance across different substitutions tended to disappear. The stimuli used in this experiment were analyzed with several color discrimination models. There was limited agreement among the predictions made by these models regarding the capabilities of animals with different pigment pairs and none predicted the dependence of discrimination on changes in luminance and stimulus duration.

Platyrrhine monkeys typically have only a single X-chromosome opsin gene. Alleles of this gene code for multiple versions of middle- to long-wavelength cone photopigments. X-chromosome inactivation provides heterozygous females with a retinal mosaic of cones containing either of two types of M and L pigment, thus establishing the photopigment basis for trichromatic color vision. This study examined the proportions of L and M cones created by this process. For that purpose, electroretinogram flicker photometry was used to obtain complete spectral sensitivity functions from 60 heterozygous female monkeys drawn from seven genera of platyrrhine monkeys. To obtain estimates of cone proportions, these functions were subsequently fit with linear combinations of L and M cone fundamentals that were derived from similar recordings made on conspecific animals having only one type of M/L pigment. Consistent with a random X-chromosome inactivation process, the average L:M cone weighting across the sample was close to unity. At the same time, there were significant individual variations in L:M cone proportions. The genesis of this variation and its implications for seeing are discussed.

Transgenic coneless mice were initially developed to study retinal function in the absence of cones. In coneless mice created by expressing an attenuated diphtheria toxin under the control of flanking sequences from the human L-cone opsin gene, a small number of cones (3-5% of the normal complement) survive in a retina that otherwise appears structurally quite normal. These cones predominantly ( approximately 87% of the total) contain UV-sensitive photopigment. ERG recordings, photoreceptor labeling, and behavioral measurements were conducted on coneless and wild-type mice to better understand how the nature of this alteration in receptor complement impacts vision. Signals from the small residual population of UV cones are readily detected in the flicker ERG where they yield signal amplitudes at saturation that are roughly proportional to the number of surviving cones. Behavioral measurements show that rod-based vision in coneless mice does not differ significantly from that of wild-type mice, nor does their rod system show any evidence of age-related deterioration. Coneless mice are able to make accurate rod-based visual discriminations at light levels well in excess of those required to reach cone threshold in wild-type mice.

Most platyrrhine monkeys have a triallelic M/L opsin gene polymorphism that underlies significant individual variations in color vision. A survey of the frequencies of these polymorphic genes suggests that the three alleles occur with equal frequency among squirrel monkeys (subfamily Cebinae), but are not equally frequent in a number of species from the subfamily Callitrichinae. This departure from equal frequency in the Callitrichids should slightly increase the ratio of dichromats to trichromats in the population and significantly alter the relative representation of the three possible dichromatic and trichromatic phenotypes. A particular feature of the inequality is that it leads to a relative increase in the number of trichromats whose M/L pigments have the largest possible spectral separation. To assess whether these trichromatic phenotypes are equally well equipped to make relevant visual discriminations, psychophysical experiments were run on human observers. A technique involving the functional substitution of photopigments was used to simulate the discrimination between fruits among a background of leaves. The goal of the simulation was to reproduce in the cones of human observers excitations equivalent to those produced in monkey cones as the animals view fruit. Three different viewing conditions were examined involving variations in the relative luminances of fruit and leaves and the spectrum of the illuminant. In all cases, performance was best for simulated trichromacies including M/L pigments with the largest spectral separation. Thus, the inequality of opsin gene frequency in Callitrichid monkeys may reflect adaptive pressures.

The spectral mechanisms of the ferret (Mustela putorious furo) were studied with electroretinogram (ERG) flicker photometry. Variations in adaptation state and flicker rate were used to define corneally based spectral sensitivities for the three classes of receptor present in the retina of this mustelid-rods (lambdamax = 505 nm), S cones (430 nm), and L cones (558 nm). The retinal distributions of the two classes of cone were determined using opsin antibody labeling. Ferret retinas contain a total of about 1.3 million cones with L cones outnumbering S cones in a ratio of approximately 14:1. ERGs were also recorded using 18.75-Hz flickering stimuli that were designed to isolate signals from individual cone classes. The contrast/response functions for signals originating from both S and L cones were linear over low-to-moderate levels of contrast, but with greatly different slopes for the two cone types. The L:S contrast gain ratio derived from a comparison of these slopes, as well as inferences drawn from another experiment in which responses to various combinations of L- and S-cone activation were analyzed, suggest that contributions of these two cone types to the flicker ERG have a relative weighting of about 4:1 to 5:1 (L/S).

Results from earlier experiments indicate that different species of rodent vary both in the number of cone types found in their retinas and in the spectral sensitivities of the cone pigments. These features have now been examined in two types of hamster commonly used for research purposes: Syrian golden hamsters (Mesocricetus auratus) and Siberian dwarf hamsters (Phodopus sungorus). Electroretinogram (ERG) flicker photometry, behavioral discrimination tasks, and opsin antibody labeling were used to investigate hamster photoreceptors and their visual consequences. Results from the three approaches support the following conclusions: (1) The retinas of both species have an abundant population of rods containing a photopigment with peak sensitivity of about 498-500 nm; (2) Siberian dwarf hamsters have two classes of cone: one with maximum sensitivity in the ultraviolet (c. 360 nm), the other with peak sensitivity closely similar to that of its rod; and (3) Syrian golden hamsters have a class of cone with peak sensitivity at about 506 nm, but they lack a second cone type. Implications of these alternative arrangements are discussed.

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 squirrel's visual system, suggesting a specialization for maximizing visual sensitivity under dim levels of illumination in the superior visual field.

Electroretinogram (ERG) flicker photometry was used to measure the spectral properties of cones in three common ungulates-cattle (Bos taurus), goats (Capra hircus), and sheep (Ovis aries). Two cone mechanisms were identified in each species. The location of peak sensitivity of an S-cone mechanism varied from about 444 to 455 nm for the three species; analogous values for an M/L-cone were tightly clumped at about 552-555 nm. Each of these three species has the requisite photopigment basis for dichromatic color vision and they are, thus, similar to other ungulates examined earlier.

Macaque monkeys are widely used as a model species for investigations of the biology of human vision. Previous measurements suggest that the cone-based spectral sensitivity of these two primates is greatly similar, but perhaps not identical. We measured the photopic spectral sensitivity of 42 male macaque monkeys from two species (Macaca mulatta, M. fascicularis) using an objective index, electroretinogram flicker photometry. The variations among individuals and between the two species were very small and there was no evidence for any significant cone pigment polymorphism in this sample. There are small but systematic differences in spectral sensitivity between macaque monkeys and equivalently tested human subjects--the monkeys were slightly more sensitive to short wavelengths (< 520 nm) and slightly less sensitive to wavelengths longer than this value. The results obtained from the curve fitting of standard photopigment absorption spectra to the spectral-sensitivity functions suggest that the difference between human and macaque monkey spectral sensitivity principally reflects differences in the relative proportions of the long- and middle-wavelength cones in the retinas of the two species.

About 3% of all mouse photoreceptors are cones. An earlier electrophysiological study indicated that there were two classes of cone in the mouse retina having peak sensitivities (lambda max) of about 360 nm and 511 nm. Recent immunocytochemical results show there are two types of cones that have distinctive regional segregation patterns. We used regional stimulation of the retina in conjunction with electroretinogram (ERG) flicker photometry to see if the two cone types identified electrophysiologically are regionalized in a fashion suggested by the anatomical results. We find they are. Relative sensitivity to ultraviolet and visible light stimulation qualitatively parallels that predicted by immunocytochemical labelling. One result of this remarkable regionalization of cone types is that the mouse retina is relatively more sensitive to ultraviolet light stimulation when that light is directed toward the ventral half of the retina.

Electroretinogram (ERG) flicker photometry was used to examine the photopigment complements of representatives of four genera of Canid: domestic dog (Canis familiaris), Island gray fox (Urocyon littoralis), red fox (Vulpes vulpes), and Arctic fox (Alopex lagopus). These four genera share a common cone pigment complement; each has one cone pigment with peak sensitivity of about 555 nm and a second cone pigment with peak at 430-435 nm. These pigment measurements accord well with the conclusions of an earlier investigation of color vision in the dog, and this fact allows some predictions about color vision in the wild canids. An additional set of measurements place the peak of the dog rod pigment at about 508 nm.

Behavioral and electrophysiological methods were used to measure sensitivity to flickering lights in a dichromatic species, the California ground squirrel (Spermophilus beecheyi). Discrimination tests were used to determine spectral sensitivity at stimulus frequencies from 5-50 Hz and increment threshold spectral sensitivity. The contributions of retinal mechanisms to these capacities were assessed by recording the responses of optic nerve fibers to temporally modulated monochromatic lights. In the ground squirrel, as in the human, the shape of the spectral-sensitivity function depends on the temporal frequency of the stimulus. Results from single-unit recording show that all of the classes of optic nerve fibers in the ground squirrel are highly phase-locked to the stimulus for modulation rates as high as 50 Hz. Neither the responses of photoreceptors nor any class of optic nerve fiber can singly account for the behavioral results. The electrophysiological results are also counter to models which propose that temporally dependent changes in the spectral sensitivity of spectrally opponent fibers account for the behavior. The temporal resolution of the optic nerve fibers exceeds that of the behaving animal suggesting that retinal mechanisms do not limit behavioral temporal resolution.

The presence of rod and cone photoreceptors has traditionally been linked to well-defined classes of visual capacity by the generalization known as duplicity theory. This paper summarizes results obtained from studies of vision and the visual system in ground squirrels (Spermophilus sp.) that reveal instances where structure/function linkages depart from expectations based in duplicity theory. The details of these exceptions are reviewed and their possible mechanisms discussed.

The color vision of three domestic dogs was examined in a series of behavioral discrimination experiments. Measurements of increment-threshold spectral sensitivity functions and direct tests of color matching indicate that the dog retina contains two classes of cone photopigment. These two pigments are computed to have spectral peaks of about 429 nm and 555 nm. The results of the color vision tests are all consistent with the conclusion that dogs have dichromatic color vision.

Ungulates have been classified as having arrhythmic eyes in the sense that they contain features appropriate both to diurnal and nocturnal life. The former is typically associated with multiple classes of cones and a color-vision capacity. To see if an arrhythmic animal has these features, the number of cone classes was determined and the spectra of these cones were measured in a common ungulate, the domestic pig (Sus scrofa). Examination with electroretinogram (ERG) flicker photometry revealed the presence of two classes of cones in the pig's eye having average maximum sensitivity (lambda max) at 439 nm and 556 nm, respectively. This ungulate thus has the requisite retinal basis for dichromatic color vision.