Jess F. Deegan

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.

Uniformity of colour vision in Old World monkeys

It is often assumed that all Old World monkeys share the same trichromatic colour vision, but the evidence in support of this conclusion is sparse as only a small fraction of all Old World monkey species have been tested. To address this issue, spectral sensitivity functions were measured in animals from eight species of Old World monkey (five cercopithecine species, three colobine species) using a non–invasive electrophysiological technique. Each of the 25 animals so examined had spectrally well–separated middl– and long–wavelength cone pigments. Cone pigments maximally sensitive to short wavelengths were also detected, implying the presence of trichromatic colour vision. Direct comparisons of the spectral sensitivity functions of Old World monkeys suggest there are no significant variations in the spectral positions of the cone pigments underlying the trichromatic colour vision of Old World monkeys.

Opsin gene and photopigment polymorphism in a prosimian primate.

A recent genetic investigation found some species of prosimian to have an opsin gene polymorphism [Nature 402 (1999) 36]. In the present study the functional implications of this finding were explored in a correlated investigation of opsin genes and spectral sensitivity measurements of a diurnal prosimian, Coquerels sifaka (Propithecus verreauxi coquereli). Spectra recorded using electroretinogram (ERG) flicker photometry reveal a cone photopigment polymorphism paralleling an opsin gene polymorphism detected by molecular methods. This species has two middle-to-long-wavelength cone pigments with peak sensitivities of about 545 and 558 nm and a short-wavelength-sensitive cone with a peak at about 430 nm. The distribution of these pigments among animals predicts the presence of both dichromatic and trichromatic forms of color vision.

Photopigments and colour vision in New World monkeys from the family Atelidae

Most New World monkeys have an X–chromosome opsin gene polymorphism that produces a variety of different colour vision phenotypes. Howler monkeys (Alouatta), one of the four genera in the family Atelidae, lack this polymorphism. Instead, they have acquired uniform trichromatic colour vision similar to that of Old World monkeys, apes and people through opsin gene duplication. In order to determine whether closely related monkeys share this arrangement, spectral sensitivity functions that allow inferences about cone pigments were measured for 56 monkeys from two other Atelid genera, spider monkeys (Ateles) and woolly monkeys (Lagothrix). Unlike howler monkeys, both spider and woolly monkeys are polymorphic for their middle– and long–wavelength cone photopigments. However, they also differ from other polymorphic New World monkeys in having two rather than three possible types of middle– and long–wavelength cone pigments. This feature directly influences the relative numbers of dichromatic and trichromatic monkeys.

Cone pigment variations in four genera of new world monkeys.

Previous research revealed significant individual variations in opsin genes and cone photopigments in several species of platyrrhine (New World) monkeys and showed that these in turn can yield significant variations in color vision. To extend the understanding of the nature of color vision in New World monkeys, electroretinogram flicker photometry was used to obtain spectral sensitivity measurements from representatives of four platyrrhine genera (Cebus, Leontopithecus, Saguinus, Pithecia). Animals from each genus were found to be polymorphic for middle to long-wavelength (M/L) sensitive cones. The presence of a short-wavelength sensitive photopigment was established as well so these animals conform to the earlier pattern in predicting that all male monkeys are dichromats while, depending on their opsin gene array, individual females can be either dichromatic or trichromatic. Across subjects a total of five different M/L cone pigments were inferred with a subset of three of these present in each species.

Spectral Sensitivity, Photopigments, and Color Vision in the Guinea Pig (Cavia porcellus)

Behavioral discrimination tests and electroretinogram (ERG) flicker photometry were used to measure spectral sensitivity and to define the spectral mechanisms of the guinea pig (Cavia porcellus). Results from these 2 approaches converge to indicate that guinea pig retinas contain rods with peak sensitivity of about 494 nm and 2 classes of cone having peak sensitivities of about 429 nm and 529 nm. The presence of 2 classes of cones suggests a retinal basis for a color vision capacity. Behavioral tests of color vision were conducted that verified this prediction: Guinea pigs have dichromatic color vision with a spectral neutral point centered at about 480 nm. The cone pigment complement of the guinea pig is different from that known to characterize other rodents.

Sensitivity to ultraviolet light in the gerbil (Meriones unguiculatus): Characteristics and mechanisms

In earlier electrophysiological experiments on the Mongolian gerbil (Meriones unguiculatus) evidence was obtained to suggest that the retina of this rodent contains only a single type of cone. The cones were found to have peak sensitivity of about 493 nm. Gerbil rods have peak sensitivity of about 500 nm, yielding a Purkinje shift that is small in magnitude and reversed in direction from that conventionally found among mammals. In a series of experiments we extended electrophysiological and behavioral measurements to include UV stimulation and this reveals a second photopic mechanism. Several pieces of evidence suggest this second mechanism is a cone having peak sensitivity of about 360 nm. Results from adaptation experiments show that the sensitivities of the two cone mechanisms can be independently manipulated, and thus they presumably reflect the operation of two types of cone photopigment. The results from behavioral experiments verify that the gerbil UV mechanism provides information that can be used to make visual discriminations based on intensity differences. A test of color vision additionally suggests that the two cone pigments can support some color discriminations.

Spectral sensitivity of macaque monkeys measured with ERG flicker photometry

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.

Photopigments of dogs and foxes and their implications for canid vision

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.

Photopigment basis for dichromatic color vision in cows, goats, and sheep

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.