Opponent colour coding is a universal strategy to evaluate the photoreceptor inputs in Hymenoptera

Summary Behavioural tests were carried out with 9 hymenopteran insect species, which ranked certain sets of coloured stimuli according to their subjective similarity to a previously memorized stimulus. Kendall's coefficient is employed for the analysis of correlation between these similarity rankings and the colour distance rankings predicted by various models of neural colour computation. The models are based on the measured spectral sensitivities of photoreceptor colour types and use a variety of simple colour coding systems to derive hypothetical colour distances. The correlation between the predictions of the models and the behavioural results serves as a measure for the likelihood of existence of a colour coding system. In all species, the similarity rankings can be best explained by assuming that colour is coded on a perceptual level by two colour opponent mechanisms. Brightness differences are ignored, indicating that an intensity-coding sub-system is not used in colour discrimination by the insects investigated. The weighting factors of the colour opponent mechanisms differ between species in detail, but not in the principles involved. It is thus possible to employ a standard measure of perceptual colour distance (colour hexagon distance) to predict the capacities of colour discrimination adequately in all the tested insects.     

Trichromacy, opponent colours coding and optimum colour information transmission in the retina

This paper presents a systematic analysis of the role of opponent type processing in colour vision and the relation between opponent type colour transformations and the initial three colour mechanisms. It is shown that efficient information transmission is achieved by a transformation of the initial three colour mechanisms into an achromatic and two opponent chromatic channels. The derivation of the transformation is dependent solely on criteria from information theory. Thus it provides a logical rationale reconciling opponent type processing as an optimal necessary step after the initial three colour mechanisms, unifying respectively the Hering and Young-Helmholtz approaches to colour vision. The effects of chromatic adaptation on the spectral response of the achromatic and two chromatic channels are discussed from the point of view of information theory. It is argued that adaptation serves as a dynamic readjustment of these responses, necessary to meet criteria of efficient colour information transmission. The results are confronted with empirical observations to test the principles of the theory and the relation to other theories is discussed. Within the same framework the issue of trichromacy is discussed. It is argued that a broad class of typical colour spectra can effectively be represented by three significant degrees of freedom that make up a trichromatic system.     

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 and three colobine species) using a non-invasive electrophysiological technique. Each of the 25 animals examined had spectrally well-separated middle- 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.     

Patterns of chromatic information processing in the lobula of the honeybee, Apis mellifera L

The honeybee, Apis mellifera L., is one of the living creatures that has its colour vision proven through behavioural tests. Previous studies of honeybee colour vision has emphasized the relationship between the spectral sensitivities of photoreceptors and colour discrimination behaviour. The current understanding of the neural mechanisms of bee colour vision is, however, rather limited. The present study surveyed the patterns of chromatic information processing of visual neurons in the lobula of the honeybee, using intracellular recording stimulated by three light-emitting diodes, whose emission spectra approximately match the spectral sensitivity peaks of the honeybee. The recorded visual neurons can be divided into two groups: non-colour opponent cells and colour opponent cells. The non-colour opponent cells comprise six types of broad-band neurons and four response types of narrow-band neurons. The former might detect brightness of the environment or function as chromatic input channels, and the latter might supply specific chromatic input. Amongst the colour opponent cells, the principal neural mechanism of colour vision, eight response types were recorded. The receptive fields of these neurons were not centre surround as observed in primates. Some recorded neurons with tonic post-stimulus responses were observed, however, suggesting temporal defined spectral opponency may be part of the colour-coding mechanisms.     

Colour choices of naive bumble bees and their implications for colour perception

The innate preferences of inexperienced bumble bees, Bombus terrestris, for floral colour stimuli were studied using artificial flowers. The artificial flowers provided a colour pattern and consisted of a star-shaped corolla and of central colour patches similar to the nectar guide of natural flowers. The innate choice behaviour was assessed in terms of the number of approach flights from some distance towards the artificial flowers and the percentage of approach flights terminating in antennal contact with the floral guide. The colours of the floral guide, the corolla and the background were varied. It was shown that the innate flower colour preference in bumble bees has two components. 1. The frequency of approaches from a distance is correlated with the colour difference between the corolla and the background against which it is presented. If the corolla colour was constant but its background colour varied, the relative attractiveness of the corolla increased with its colour difference to the background. The colour difference assessment underlying this behaviour on a perceptual basis can be attained by means of colour opponent coding, a system well-established in Hymenoptera. 2. The frequency of antennal contacts with the floral guides relative to that of approach flights cannot be accounted for by colour opponent coding alone. Whether the approach flights are interrupted, or whether they end in an antennal contact with the nectar guide is strongly dependent on the direction (sign) of the colour difference, not only its magnitude. The choice behaviour requires a unique perceptual dimension, possibly that of colour saturation or that of hue perception comparable to components of colour perception in humans.     

An account of responses of spectrally opponent neurons in macaque lateral geniculate nucleus to successive contrast

Coloured surfaces in the normal environment may be brighter or dimmer than the mean adaptation level. Changes in the firing rate of cells of the parvocellular layers of macaque lateral geniculate nucleus were studied with such stimuli; chromatic mixtures briefly replaced a white adaptation field. This paradigm is therefore one of successive contrast. Families of intensity-response curves for different wavelengths were measured. When taking sections at different luminance ratios through these families of curves, strongly opponent cells displayed spectrally selective responses at low luminance ratios, while weakly opponent cells had higher chromatic thresholds and responded well to stimuli at higher luminance ratios, brighter than the adaptation field. Strength of cone opponency, defined as the weight of the inhibitory cone mechanism relative to the excitatory one, was thus related to the range of intensity in which cells appeared to operate most effectively. S-cone inputs, as tested with lights lying along tritanopic confusion lines, could either be excitatory or inhibitory. Families of curves for different wavelengths can be simulated mathematically for a given cell by a simple model by using known cone absorption spectra. Hyperbolic response functions relate cone absorption to the output signals of the three cone mechanisms, which are assumed to interact linearly. Parameters from the simulation provided estimates of strength of cone opponency and cone sensitivity which were shown to be continuously distributed. Cell activity can be related to cone excitation in a trichromatic colour space with the help of the model, to give an indication of suprathreshold coding of colour and lightness.     

Broad spectral sensitivities in the honeybee's photoreceptors limit colour constancy

Colour constancy allows for visual systems to be view stimuli independent of changes in spectral illumination. Chromatic adaptation is likely to be an important mechanism in colour constancy and can be explained by use of the von Kries coefficient law. Chromatic adaptation is compared for the honeybee and three hypothetical visual systems. It is shown that the spectral breadth and asymmetry of photoreceptors in the honeybee may limit colour constancy. In particular, it is demonstrated that the absorption of short-wavelength radiation by the cis-band of chromophore is responsible for a poorer correction for bee colours rich in ultraviolet reflectance. The results are discussed in relation to theoretical considerations of von Kries colour constancy and the physiology of eye design in some other species for which colour constancy has been demonstrated. Accepted: 14 August 1999     

A temporal red-green opponent mechanism

A mechanistic model is presented that describes the temporal behaviour of a red-green colour opponent channel such as has been investigated for the macaque monkey. The model incorporates luminanceand chromaticity-adaptation mechanisms. Receptive field properties such as retardation and attenuation of the surround signals with respect to the center signals of the colour opponent channel are also included. The model predicts temporal psychophysical chromaticity thresholds and temporal electrophysiological red-green colour opponent ganglion cell behaviour with a reasonable degree of success.     

Fruits, foliage and the evolution of primate colour vision

Primates are apparently unique amongst the mammals in possessing trichromatic colour vision. However, not all primates are trichromatic. Amongst the haplorhine (higher) primates, the catarrhines possess uniformly trichromatic colour vision, whereas most of the platyrrhine species exhibit polymorphic colour vision, with a variety of dichromatic and trichromatic phenotypes within the population. It has been suggested that trichromacy in primates and the reflectance functions of certain tropical fruits are aspects of a coevolved seed-dispersal system: primate colour vision has been shaped by the need to find coloured fruits amongst foliage, and the fruits themselves have evolved to be salient to primates and so secure dissemination of their seeds. We review the evidence for and against this hypothesis and we report an empirical test: we show that the spectral positioning of the cone pigments found in trichromatic South American primates is well matched to the task of detecting fruits against a background of leaves. We further report that particular trichromatic platyrrhine phenotypes may be better suited than others to foraging for particular fruits under particular conditions of illumination; and we discuss possible explanations for the maintenance of polymorphic colour vision amongst the platyrrhines.     

The spectral input systems of hymenopteran insects and their receptor-based colour vision

Summary Spectral sensitivity functions S() of single photoreceptor cells in 43 different hymenopteran species were measured intracellularly with the fast spectral scan method. The distribution of maximal sensitivity values (_max) shows 3 major peaks at 340 nm, 430 nm and 535 nm and a small peak at 600 nm. Predictions about the colour vision systems of the different hymenopteran species are derived from the spectral sensitivities by application of a receptor model of colour vision and a model of two colour opponent channels. Most of the species have a trichromatic colour vision system. Although the S() functions are quite similar, the predicted colour discriminability curves differ in their relative height of best discriminability in the UV-blue or bluegreen area of the spectrum, indicating that relatively small differences in the S() functions may have considerable effects on colour discriminability. Four of the hymenopteran insects tested contain an additional R-receptor with maximal sensitivity around 600 nm. The R-receptor of the solitary bee Callonychium petuniae is based on a pigment (P596) with a long _max, whereas in the sawfly Tenthredo campestris the G-receptor appears to act as filter to a pigment (P570), shifting its _max value to a longer wavelength and narrowing its bandwidth. Evolutionary and life history constraints (e.g. phylogenetic relatedness, social or solitary life, general or specialized feeding behaviour) appear to have no effect on the S() functions. The only effect is found in UV receptors, for which _max values at longer wavelengths are found in bees flying predominantly within the forest.     

On the trichromatic and opponent-process theories: an article by E. Schr?dinger

A translation of Schr?dinger's paper, 'On the relation of the tetrachromatic theory to the trichromatic theory' (1925), is accompanied by a commentary. Schr?dinger applies a projective transformation to a standard chromaticity diagram, to demonstrate the common geometry of the chromaticity diagrams derived from the trichromatic and opponent-process theories of color vision.     

Chromatic induction: Responses of neurophysiological double opponent units?

Equations have been derived that improve the quantification of sensory equidistant colour and lightness differences. This has been achieved by a physiological approach involving non-linear responses of cone mechanisms and two subsequent stages of linear opponent transformation to describe the Munsell System (Seim and Valberg, 1980). Using the formulation for the first opponent stage, colours induced into an achromatic center field by a chromatic surround varying in purity, are shown to follow the same power function of the opponent coordinates for all hues. By analogy, a physiological model for colour coding and colour induction is offered. Double opponent neurones with spatially antagonistic, spectrally opponent and symmetric receptive fields constitute the units of the model. Colour induction is related to lateral excitation and colour differences to response differences of these units.     

A new interpretation of flower guide colouration: Absorption of ultraviolet light enhances colour saturation

In melittophilous plants the colour pattern of the flowers, as perceived by bumblebees, is a gradient of centripetally increasing spectral purity. This pattern serves as a signal for innate flower recognition in naive bumblebees permitting orientation to flowers and landing on flowers. Structures which make up the total signal pattern can include the background (e.g., green leaves), corollas, and stamens or floral guides. How various colour parameters, such as dominant wavelength, intensity, and spectral purity influence the colour signal pattern of flowers is analyzed. The process of strong absorption of ultraviolet light is shown to be a mechanism for the enhancement of spectral purity in flower guides. The importance of other mechanisms is also demonstrated. The presence of a gradient of centripetally increasing spectral purity in floral colour patterns as perceived by a bumblebee's eyes is demonstrated by a comparison of the spectral reflectance in different parts of the flower and a representation of colour loci in the colour triangle.     

Acquisition of color opponent representation by a three-layered neural network model

This paper discusses color representation in the visual system by analysis of a three-layered neural network model. The model incorporates physiological knowledge of color representation at the sensor level (broad-band trichromatic representation by cones) and the higher level (narrow-band color representation by color-coded cells in V4). We trained the model to perform a mapping between these color representations by the back propagation algorithm and analyzed the acquired characteristics of the hidden units. It turned out that the hidden units learned characteristics similar to those of the color opponent cells found in the visual system. It was concluded that the R-G and Y-B color opponent representations reflect the efficiency of the color representation in the visual system from investigations on the efficiency of color representation in the hidden layer and on the capability of the color recognition task of the model.     

Modelling of the vertebrate visual system 3. topological analysis of the cone mosaic

Spatial organization of the cone mosaic of the generalized vertebrate retina consists of rows of red and green cones alternating with rows of blue and blank cones. Cone inputs to retinal elements are defined spatially by red and green unit hexagons. Topological analysis entails determining for each cone in the mosaic the number of each cone type present in the unit hexagon which the activated cone can influence via electrical coupling between cones and/or stray light. Only weighted inputs in one-half of a sextant of the unit hexagon need be designated, since all other weighted inputs can be determined by rules giving systematic transformations of all cone types from one sextant to another: these rules arise from symmetries of the cone mosaic. Four retinal types are possible depending on replacement of blank cones by specific cone types; three cone-dominant retinas, where all blank cones are replaced by a specific cone type, and two forms of a trichromatic retina, where blank cones are replaced by equal numbers of red and green cones. The weighted input is the sum of individual cone type contributions and depends on the number of each cone type in the unit hexagon which can influence the cone in question. Weighted inputs for cone-dominant retinas are readily found by replacing blank cones with the proper cone type, while weighted inputs for trichromatic retinas require use of a specified cone mosaic to determine extra red and green cones. Receptive field size of post-cone elements as well as overlap of the center and surround fields of annular organized receptive fields of retinal elements increased with increasing values for attenuation factors.     

Optimum probabilistic processing in colour perception. I. Colour discrimination.

A comprehensive account of wavelength discrimination and colour saturation discrimination is given in terms of optimum probabilistic signal detection. The theory is a logical deduction from statistical estimation theory of the visual estimate of the spectral parameters of the stimulus. In place of geometrical concepts associated with colour-space geometry, stimulus discriminability is determined by optimum decision rules given by likelihood ratio tests on statistics that are postulated for the trichromatic responses. The classical line element theory and its formulations are deduced to be discriminability measures between signals. The different mathematical forms of classical theory are shown to correspond to different statistical constraints.     

Behavioural evidence for colour vision in stomatopod crustaceans

If an organism can be taught to respond in a particular way to a wavelength of light, irrespective of that light's intensity, then it must be able to perceive the colour of the stimulus. No marine invertebrate has yet been shown to have colour vision. Stomatopod crustaceans (mantis shrimps) are colourful animals and their eyes have many adaptations which indicate that they are capable of such spectral analysis. We adopted an associative learning paradigm to attempt to demonstrate colour vision. Stomatopods readily learnt to choose some colours from arrays of greys, even when the correct choice colours were darker than the ones they had been trained to. Possible mechanisms underlying colour vision in these animals, and their ecological significance are discussed. A simple model is presented which may help interpret the complex-stomatopod colour vision system and explain some of the learning anomalies.Abbreviations ND neutral density - OD optical density - R8 Retinular cell 8 - R1–7 Retinular cells 1–7 - R1D Distally placed R1–7 retinular cells in mid-band row 1 - e.g. R1P Proximally placed R1–7 retinular cells in mid-band row 1 - D/P Estimate of chromatic signal ratio     

Simultaneous and successive colour discrimination in the honeybee (Apis mellifera)

The colour discrimination of individual free-flying honeybees (Apis mellifera) was tested with simultaneous and successive viewing conditions for a variety of broadband reflectance stimuli. For simultaneous viewing bees used form vision to discriminate patterned target stimuli from homogeneous coloured distractor stimuli, and for successive discrimination bees were required to discriminate between homogeneously coloured stimuli. Bees were significantly better at a simultaneous discrimination task, and we suggest this is explained by the inefficiency with which the bees brain can code and retrieve colour information from memory when viewing stimuli successively. Using simultaneous viewing conditions bees discriminated between the test stimuli at a level equivalent to 1 just-noticeable-difference for human colour vision. Discrimination of colours by bees with simultaneous viewing conditions exceeded previous estimates of what is possible considering models of photoreceptor noise measured in bees, which suggests spatial and/or temporal summation of colour signals for fine discrimination tasks. The results show that when behavioural experiments are used to collect data about the mechanisms facilitating colour discrimination in animals, it is important to consider the effects of the stimulus viewing conditions on results.     

Non-random association of opsin alleles in wild groups of red-bellied tamarins (Saguinus labiatus) and maintenance of the colour vision polymorphism

The remarkable X-linked colour vision polymorphism observed in many New World primates is thought to be maintained by balancing selection. Behavioural tests support a hypothesis of heterozygote advantage, as heterozygous females (with trichromatic vision) exhibit foraging benefits over homozygous females and males (with dichromatic vision) when detecting ripe fruit on a background of leaves. Whilst most studies to date have examined the functional relevance of polymorphic colour vision in the context of foraging behaviour, alternative hypotheses proposed to explain the polymorphism have remained unexplored. In this study we examine colour vision polymorphism, social group composition and breeding success in wild red-bellied tamarins Saguinus labiatus. We find that the association of males and females within tamarin social groups is non-random with respect to colour vision genotype, with identified mating partners having the greatest allelic diversity. The observed distribution of alleles may be driven by inbreeding avoidance and implies an important new mechanism for maintaining colour vision polymorphism. This study also provides the first preliminary evidence that wild trichromatic females may have increased fitness compared with dichromatic counterparts, as measured by breeding success and longevity.     

Unidirectionality of floral colour changes

Many angiosperms have arranged their flowers in inflorescences forming a distinct signalling unit to flower visitors. In some species, the flowers of inflorescences undergo a temporal colour change corresponding exactly to a change in the reward status. Based on information obtained from the spectral reflection curves of pre-change and postchage colours of flower corollas and/or floral guides, it was possible to demonstrate that the colour phase associated with reward closely corresponds to the visual stimuli which trigger behavioural responses of inexperienced flower visitors, and that the colour phase associated with less reward corresponds to visual stimuli less attractive to naïve flower visitors. Reciprocal colour changes were not observed. It is to be assumed that the unidirectionality of floral colour changes is an adaptation of angiosperms aimed at the guidance of first-time flower visitors. Signalling reward to inexperienced flower visitors is an additional function of floral colour changes. The main function of floral colour changes, however, is to provide cues with which the flower visitors can learn to associate one colour phase with reward.