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 and brightness coding in the central nervous system: theoretical aspects and visual evoked potentials to homogeneous red and green stimuli

We designed visual evoked potentials experiments to study the differential aspects of colour and brightness coding in man. The substitution of equally bright red and green stimuli for a background yellow was investigated and compared with different luminance increments and decrements of red and green. A dominant N87 component was found for a colour change from yellow to brighter red colours, which was less pronounced for green and absent for yellow luminance changes. It is also absent for pure red luminance increments and green luminance changes, but reappears with red luminance decrements or red-offset. The data are discussed within the framework of a new concept of how the visual system fuses red-green information and black-white border information. Retinal X-cells can transmit colour and high spatial frequency achromatic information simultaneously by encoding only the presence of edges (a.c.) for the black-white stimuli and the presence of both edges (a.c.) and uniform areas of colour (d.c.) for red-green stimuli. Phylogenetically this kind of information transmission enables colour vision to be implemented in a retina such as the cat's by adding only a second class of cones. Barlow's economy principle will be violated for colour in the periphery, but restored early in the striate cortex where there is an early decoding of the combined chromatic and achromatic information by the concentric double opponent cells. The N87 behaviour correlates with the proposed discharge of peripheral X-type cells, but not with the discharge of cortical double opponent concentric or simple cells, which no longer respond to homogeneous colour stimuli. It is suggested that N87 may be generated by geniculate afferents in the dendritic arborization of cortical cells, reflecting the behaviour of peripheral units, and thus the violation of the economy principle, rather than the next step in cortical processing. The early cortical restoration of the economy principle is supported by the absence of any further dissociated behaviour for colour and brightness in later components.     

Using digital photography to study animal coloration

In understanding how visual signals function, quantifying the components of those patterns is vital. With the ever-increasing power and availability of digital photography, many studies are utilizing this technique to study the content of animal colour signals. Digital photography has many advantages over other techniques, such as spectrometry, for measuring chromatic information, particularly in terms of the speed of data acquisition and its relatively cheap cost. Not only do digital photographs provide a method of quantifying the chromatic and achromatic content of spatially complex markings, but also they can be incorporated into powerful models of animal vision. Unfortunately, many studies utilizing digital photography appear to be unaware of several crucial issues involved in the acquisition of images, notably the nonlinearity of many cameras' responses to light intensity, and biases in a camera's processing of the images towards particular wavebands. In the present study, we set out step-by-step guidelines for the use of digital photography to obtain accurate data, either independent of any particular visual system (such as reflection values), or for particular models of nonhuman visual processing (such as that of a passerine bird). These guidelines include how to: (1) linearize the camera's response to changes in light intensity; (2) equalize the different colour channels to obtain reflectance information; and (3) produce a mapping from camera colour space to that of another colour space (such as photon catches for the cone types of a specific animal species).  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 90 , 211–237.     

Visual Ecology and Perception of Coloration Patterns by Domestic Chicks

This article suggests how we might understand the way potential predators see coloration patterns used in aposematism and visual mimicry. We start by briefly reviewing work on evolutionary function of eyes and neural mechanisms of vision. Often mechanisms used for achromatic vision are accurately modeled as adaptations for detection and recognition of the generality of optical stimuli, rather than specific stimuli such as biological signals. Colour vision is less well understood, but for photoreceptor spectral sensitivities of birds and hymenopterans there is no evidence for adaptations to species-specific stimuli, such as those of food or mates. Turning to experimental work, we investigate how achromatic and chromatic stimuli are used for object recognition by foraging domestic chicks (Gallus gallus). Chicks use chromatic and achromatic signals in different ways: discrimination of large targets uses (chromatic) colour differences, and chicks remember chromatic signals accurately. However, detection of small targets, and discrimination of visual textures requires achromatic contrast. The different roles of chromatic and achromatic information probably reflect their utility for object recognition in nature. Achromatic (intensity) variation exceeds chromatic variation, and hence is more informative about change in reflectance – for example, object borders, while chromatic signals yield more information about surface reflectance (object colour) under variable illumination. This revised version was published online in July 2006 with corrections to the Cover Date.     

Development of contrast sensitivity and acuity of the infant colour system

We have monitored the development of infant colour vision by measuring chromatic contrast sensitivity and acuity in eight young infants over a period of 6 months. Steady-state visual evoked potentials (VEPS) were recorded in response to both chromatic (red-green) and luminance (red-black or green-black) patterns that were reversed in contrast over time. For most infants, no response could be obtained to chromatic stimuli of any size or contrast before 5 weeks of age, although luminance stimuli of 20% contrast gave reliable responses at that age. When responses to chromatic stimuli first appeared, they could be obtained only with stimuli of very low spatial frequency, 20 times lower than the acuity for luminance stimuli. Both contrast sensitivity and acuity for chromatic stimuli increased steadily, more rapidly than for luminance stimuli. As the spectral selectivities of infant cones are similar to those of adults, the difference in rate of development of luminance and chromatic contrast sensitivity and acuity stimuli probably reflects neural development of the infant colour system.     

No rainbow for grey bamboo sharks: evidence for the absence of colour vision in sharks from behavioural discrimination experiments

Despite convincing data collected by microspectrophotometry and molecular biology, rendering sharks colourblind cone monochromats, the question of whether sharks can perceive colour had not been finally resolved in the absence of any behavioural experiments compensating for the confounding factor of brightness. The present study tested the ability of juvenile grey bamboo sharks to perceive colour in an experimental design based on a paradigm established by Karl von Frisch using colours in combination with grey distractor stimuli of equal brightness. Results showed that contrasts but no colours could be discriminated. Blue and yellow stimuli were not distinguished from a grey distractor stimulus of equal brightness but could be distinguished from distractor stimuli of varying brightness. In addition, different grey stimuli were distinguished significantly above chance level from one another. In conclusion, the behavioural results support the previously collected physiological data on bamboo sharks, which mutually show that the grey bamboo shark, like several marine mammals, is a cone monochromate and colourblind.     

Visual modelling suggests a weak relationship between the evolution of ultraviolet vision and plumage coloration in birds

Birds have sophisticated colour vision mediated by four cone types that cover a wide visual spectrum including ultraviolet (UV) wavelengths. Many birds have modest UV sensitivity provided by violet‐sensitive (VS) cones with sensitivity maxima between 400 and 425 nm. However, some birds have evolved higher UV sensitivity and a larger visual spectrum given by UV‐sensitive (UVS) cones maximally sensitive at 360–370 nm. The reasons for VS–UVS transitions and their relationship to visual ecology remain unclear. It has been hypothesized that the evolution of UVS‐cone vision is linked to plumage colours so that visual sensitivity and feather coloration are ‘matched’. This leads to the specific prediction that UVS‐cone vision enhances the discrimination of plumage colours of UVS birds while such an advantage is absent or less pronounced for VS‐bird coloration. We test this hypothesis using knowledge of the complex distribution of UVS cones among birds combined with mathematical modelling of colour discrimination during different viewing conditions. We find no support for the hypothesis, which, combined with previous studies, suggests only a weak relationship between UVS‐cone vision and plumage colour evolution. Instead, we suggest that UVS‐cone vision generally favours colour discrimination, which creates a nonspecific selection pressure for the evolution of UVS cones.     

Colour processing in complex environments: insights from the visual system of bees

Colour vision enables animals to detect and discriminate differences in chromatic cues independent of brightness. How the bee visual system manages this task is of interest for understanding information processing in miniaturized systems, as well as the relationship between bee pollinators and flowering plants. Bees can quickly discriminate dissimilar colours, but can also slowly learn to discriminate very similar colours, raising the question as to how the visual system can support this, or whether it is simply a learning and memory operation. We discuss the detailed neuroanatomical layout of the brain, identify probable brain areas for colour processing, and suggest that there may be multiple systems in the bee brain that mediate either coarse or fine colour discrimination ability in a manner dependent upon individual experience. These multiple colour pathways have been identified along both functional and anatomical lines in the bee brain, providing us with some insights into how the brain may operate to support complex colour discrimination behaviours.     

Vision in elasmobranchs and their relatives: 21st century advances

This review identifies a number of exciting new developments in the understanding of vision in cartilaginous fishes that have been made since the turn of the century. These include the results of studies on various aspects of the visual system including eye size, visual fields, eye design and the optical system, retinal topography and spatial resolving power, visual pigments, spectral sensitivity and the potential for colour vision. A number of these studies have covered a broad range of species, thereby providing valuable information on how the visual systems of these fishes are adapted to different environmental conditions. For example, oceanic and deep-sea sharks have the largest eyes amongst elasmobranchs and presumably rely more heavily on vision than coastal and benthic species, while interspecific variation in the ratio of rod and cone photoreceptors, the topographic distribution of the photoreceptors and retinal ganglion cells in the retina and the spatial resolving power of the eye all appear to be closely related to differences in habitat and lifestyle. Multiple, spectrally distinct cone photoreceptor visual pigments have been found in some batoid species, raising the possibility that at least some elasmobranchs are capable of seeing colour, and there is some evidence that multiple cone visual pigments may also be present in holocephalans. In contrast, sharks appear to have only one cone visual pigment. There is evidence that ontogenetic changes in the visual system, such as changes in the spectral transmission properties of the lens, lens shape, focal ratio, visual pigments and spatial resolving power, allow elasmobranchs to adapt to environmental changes imposed by habitat shifts and niche expansion. There are, however, many aspects of vision in these fishes that are not well understood, particularly in the holocephalans. Therefore, this review also serves to highlight and stimulate new research in areas that still require significant attention.     

Behavioural evidence of sex-linked colour vision polymorphism in the squirrel monkey Saimiri ustus

Squirrel monkeys, like most Neotropical primates, display a sex-linked colour vision polymorphism. Here we assess the colour perception of 8 Saimiri ustus by a behavioural paradigm using Munsell colour chips as discriminating stimuli. A random variation in brightness assured that discriminations were based on colour rather than brightness cues. Results indicate that all males showed random performances when presented with stimuli which, in previous experiments with human colour-blind individuals and dichromatic non-human primates, proved to be difficult to discriminate. Females behaved as trichromats. The different phenotypes in S. ustus may offer diverse advantages in feeding ecology and are in agreement with the existence of vision polymorphism, as described for other species of squirrel monkeys.     

Opponent and nonopponent contributions to the zebrafish electroretinogram using heterochromatic flicker photometry

While some lower vertebrates, such as zebrafish, do not appear to possess anatomically separate pathways of processing visual information (such as M-pathways and P-pathways), it is believed that separate processing of the visual stimulus (such as luminance and chromatic processing) is a basic requirement of vertebrate vision. In this study, spectral sensitivity functions were obtained from electroretinogram responses to heterochromatic flicker photometry stimuli at several flicker rates, including a low flicker rate (2 Hz), in an attempt to predominantly stimulate chromatic processes and a high flicker rate (16 Hz), in an attempt to predominantly stimulate luminance processes. In addition, chromatic adaptation was used to isolate and examine the temporal properties of the different cone-type contributions to the electroretinogram response. Spectral sensitivity functions based on responses to heterochromatic stimuli of a low flicker rate appeared to receive both opponent and nonopponent contributions; however, when the stimulus flicker rate was high, spectral sensitivity appeared to be a function of only nonopponent mechanisms. Also, the differences in cone contributions to the spectral sensitivity functions across the different flicker rates appear to be related to the temporal properties of the cone contributions to the electroretinogram response.     

Colour vision in billfish

Members of the billfish family are highly visual predatory teleosts inhabiting the open ocean. Little is known about their visual abilities in detail, but past studies have indicated that these fishes were likely to be monochromats. This study, however, presents evidence of two anatomically distinct cone types in billfish. The cells are arranged in a regular mosaic pattern of single and twin cones as in many fishes, and this arrangement suggests that the different cone types also show different spectral sensitivity, which is the basis for colour vision. First measurements using microspectrophotometry (MSP) revealed a peak absorption of the rod pigment at 484 nm, indicating that MSP, despite technical difficulties, will be a decisive tool in proving colour vision in these offshore fishes. When hunting, billfish such as the sailfish flash bright blue bars on their sides. This colour reflects largely in ultraviolet (UV) light at 350 nm as revealed by spectrophotometric measurements. Billfish lenses block light of wavelengths below 400 nm, presumably rendering the animal blind to the UV component of its own body colour. Interestingly, at least two prey species of billfish have lenses transmitting light in the UV waveband and are therefore likely to perceive a large fraction of the UV peak found in the blue bar of the sailfish. The possible biological significance of this finding is discussed.     

Bat Eyes Have Ultraviolet-Sensitive Cone Photoreceptors

Mammalian retinae have rod photoreceptors for night vision and cone photoreceptors for daylight and colour vision. For colour discrimination, most mammals possess two cone populations with two visual pigments (opsins) that have absorption maxima at short wavelengths (blue or ultraviolet light) and long wavelengths (green or red light). Microchiropteran bats, which use echolocation to navigate and forage in complete darkness, have long been considered to have pure rod retinae. Here we use opsin immunohistochemistry to show that two phyllostomid microbats, Glossophaga soricina and Carollia perspicillata, possess a significant population of cones and express two cone opsins, a shortwave-sensitive (S) opsin and a longwave-sensitive (L) opsin. A substantial population of cones expresses S opsin exclusively, whereas the other cones mostly coexpress L and S opsin. S opsin gene analysis suggests ultraviolet (UV, wavelengths <400 nm) sensitivity, and corneal electroretinogram recordings reveal an elevated sensitivity to UV light which is mediated by an S cone visual pigment. Therefore bats have retained the ancestral UV tuning of the S cone pigment. We conclude that bats have the prerequisite for daylight vision, dichromatic colour vision, and UV vision. For bats, the UV-sensitive cones may be advantageous for visual orientation at twilight, predator avoidance, and detection of UV-reflecting flowers for those that feed on nectar.     

Dichromatic Colour Vision in Wallabies as Characterised by Three Behavioural Paradigms

Despite lacking genetic evidence of a third cone opsin in the retina of any Australian marsupial, most species tested so far appear to be trichromatic. In the light of this, we have re-examined colour vision of the tammar wallaby which had previously been identified as a dichromat. Three different psychophysical tests, based on an operant conditioning paradigm, were used to confirm that colour perception in the wallaby can be predicted and conclusively explained by the existence of only two cone types. Firstly, colour-mixing experiments revealed a Confusion Point between the three primary colours of a LCD monitor that can be predicted by the cone excitation ratio of the short- and middle-wavelength sensitive cones. Secondly, the wavelength discrimination ability in the wallaby, when tested with monochromatic stimuli, was found to be limited to a narrow range between 440 nm and 500 nm. Lastly, an experiment designed to test the wallaby’s ability to discriminate monochromatic lights from a white light provided clear evidence for a Neutral Point around 485 nm where discrimination consistently failed. Relative colour discrimination seemed clearly preferred but it was possible to train a wallaby to perform absolute colour discriminations. The results confirm the tammar wallaby as a dichromat, and so far the only behaviourally confirmed dichromat among the Australian marsupials.     

The machinery of colour vision

Some fundamental principles of colour vision, deduced from perceptual studies, have been understood for a long time. Physiological studies have confirmed the existence of three classes of cone photoreceptors, and of colour-opponent neurons that compare the signals from cones, but modern work has drawn attention to unexpected complexities of early organization: the proportions of cones of different types vary widely among individuals, without great effect on colour vision; the arrangement of different types of cones in the mosaic seems to be random, making it hard to optimize the connections to colour-opponent mechanisms; and new forms of colour-opponent mechanisms have recently been discovered. At a higher level, in the primary visual cortex, recent studies have revealed a simpler organization than had earlier been supposed, and in some respects have made it easier to reconcile physiological and perceptual findings.     

Colour spaces in ecology and evolutionary biology

The recognition that animals sense the world in a different way than we do has unlocked important lines of research in ecology and evolutionary biology. In practice, the subjective study of natural stimuli has been permitted by perceptual spaces, which are graphical models of how stimuli are perceived by a given animal. Because colour vision is arguably the best‐known sensory modality in most animals, a diversity of colour spaces are now available to visual ecologists, ranging from generalist and basic models allowing rough but robust predictions on colour perception, to species‐specific, more complex models giving accurate but context‐dependent predictions. Selecting among these models is most often influenced by historical contingencies that have associated models to specific questions and organisms; however, these associations are not always optimal. The aim of this review is to provide visual ecologists with a critical perspective on how models of colour space are built, how well they perform and where their main limitations are with regard to their most frequent uses in ecology and evolutionary biology. We propose a classification of models based on their complexity, defined as whether and how they model the mechanisms of chromatic adaptation and receptor opponency, the nonlinear association between the stimulus and its perception, and whether or not models have been fitted to experimental data. Then, we review the effect of modelling these mechanisms on predictions of colour detection and discrimination, colour conspicuousness, colour diversity and diversification, and for comparing the perception of colour traits between distinct perceivers. While a few rules emerge (e.g. opponent log–linear models should be preferred when analysing very distinct colours), in general model parameters still have poorly known effects. Colour spaces have nonetheless permitted significant advances in ecology and evolutionary biology, and more progress is expected if ecologists compare results between models and perform behavioural experiments more routinely. Such an approach would further contribute to a better understanding of colour vision and its links to the behavioural ecology of animals. While visual ecology is essentially a transfer of knowledge from visual sciences to evolutionary ecology, we hope that the discipline will benefit both fields more evenly in the future.     

Optimum probabilistic processing in colour perception. II. Colour vision as template matching.

A statistical approach to account for psychophysical phenomena in human colour vision is presented. The central visual processor is viewed as an optimum recognizer of stochastic patterns supplied by the periphery. The processor makes an optimum estimate of the spectral parameters of the stimulus, given the wavelength filter characteristics of the periphery, the stochastic nature of the information and an internal template to which the external stimulus is matched. The estimate is constrained in ways inferred from empirical phenomena. Subjective brightness of monochromatic stimuli and related constant brightness manifolds in the colour space constitute the constraint for brightness estimation. Results analogous and in accord with those of earlier line element theories are obtained. The Bezold-Brücke hue shift constitutes the basic constraint for hue estimation. The hue estimate involves interrelation between the fields in the experiment. Similarities and differences both in basic conceptions and results introduced by the template matching notions are discussed.     

Selection on quantitative colour variation in Centaurea cyanus: the role of the pollinator's visual system

Even though the importance of selection for trait evolution is well established, we still lack a functional understanding of the mechanisms underlying phenotypic selection. Because animals necessarily use their sensory system to perceive phenotypic traits, the model of sensory bias assumes that sensory systems are the main determinant of signal evolution. Yet, it has remained poorly known how sensory systems contribute to shaping the fitness surface of selected individuals. In a greenhouse experiment, we quantified the strength and direction of selection on floral coloration in a population of cornflowers exposed to bumblebees as unique pollinators during 4 days. We detected significant selection on the chromatic and achromatic (brightness) components of floral coloration. We then studied whether these patterns of selection are explicable by accounting for the visual system of the pollinators. Using data on bumblebee colour vision, we first showed that bumblebees should discriminate among quantitative colour variants. The observed selection was then compared to the selection predicted by psychophysical models of bumblebee colour vision. The achromatic but not the chromatic channel of the bumblebee's visual system could explain the observed pattern of selection. These results highlight that (i) pollinators can select quantitative variation in floral coloration and could thus account for a gradual evolution of flower coloration, and (ii) stimulation of the visual system represents, at least partly, a functional mechanism potentially explaining pollinators' selection on floral colour variants.     

The contribution of single and double cones to spectral sensitivity in budgerigars during changing light conditions

Bird colour vision is mediated by single cones, while double cones and rods mediate luminance vision in bright and dim light, respectively. In daylight conditions, birds use colour vision to discriminate large objects such as fruit and plumage patches, and luminance vision to detect fine spatial detail and motion. However, decreasing light intensity favours achromatic mechanisms and eventually, in dim light, luminance vision outperforms colour vision in all visual tasks. We have used behavioural tests in budgerigars (Melopsittacus undulatus) to investigate how single cones, double cones and rods contribute to spectral sensitivity for large (3.4°) static monochromatic stimuli at light intensities ranging from 0.08 to 63.5 cd/m². We found no influences of rods at any intensity level. Single cones dominate the spectral sensitivity function at intensities above 1.1 cd/m², as predicted by a receptor noise-limited colour discrimination model. Below 1.1 cd/m², spectral sensitivity is lower than expected at all wavelengths except 575 nm, which corresponds to double cone function. We suggest that luminance vision mediated by double cones restores visual sensitivity when single cone sensitivity quickly decreases at light intensities close to the absolute threshold of colour vision.