Cognitive components of color vision in honey bees: how conditioning variables modulate color learning and discrimination

Since the demonstration of color vision in honey bees 100 years ago by Karl von Frisch, appetitive conditioning to color targets has been used as the principal way to access behavioral aspects of bee color vision. Yet, analyses on how conditioning parameters affect color perception remained scarce. Conclusions on bee color vision have often been made without referring them to the experimental context in which they were obtained, and thus presented as absolute facts instead of realizing that subtle variations in conditioning procedures might yield different results. Here, we review evidence showing that color learning and discrimination in bees are not governed by immutable properties of their visual system, but depend on how the insects are trained and thus learn a task. The use of absolute or differential conditioning protocols, the presence of aversive reinforcement in differential conditioning and the degrees of freedom of motor components determine dramatic variations in color discrimination. We, thus, suggest top-down attentional modulation of color vision to explain the changes in color learning and discrimination reviewed here. We discuss the possible neural mechanisms of this modulation and conclude that color vision experiments require a careful consideration of how training parameters shape behavioral responses.     

The Heterozygote Superiority Hypothesis for Polymorphic Color Vision Is Not Supported by Long-Term Fitness Data from Wild Neotropical Monkeys

The leading explanatory model for the widespread occurrence of color vision polymorphism in Neotropical primates is the heterozygote superiority hypothesis, which postulates that trichromatic individuals have a fitness advantage over other phenotypes because redgreen chromatic discrimination is useful for foraging, social signaling, or predator detection. Alternative explanatory models predict that dichromatic and trichromatic phenotypes are each suited to distinct tasks. To conclusively evaluate these models, one must determine whether proposed visual advantages translate into differential fitness of trichromatic and dichromatic individuals. We tested whether color vision phenotype is a significant predictor of female fitness in a population of wild capuchins, using longterm 26 years survival and fertility data. We found no advantage to trichromats over dichromats for three fitness measures fertility rates, offspring survival and maternal survival. This finding suggests that a selective mechanism other than heterozygote advantage is operating to maintain the color vision polymorphism. We propose that attention be directed to field testing the alternative mechanisms of balancing selection proposed to explain opsin polymorphism nichedivergence, frequencydependence and mutual benefit of association. This is the first indepth, longterm study examining the effects of color vision variation on survival and reproductive success in a naturallyoccurring population of primates.     

Color and luminance contrasts attract independent attention

Paying attention can improve vision in many ways, including some very basic functions such as contrast discrimination, a task that probably reflects very early levels of visual processing. Electrophysiological, psychophysical, and imaging studies on humans as well as single recordings in monkey show that attention can modulate the neuronal response at an early stage of visual processing, probably by acting on the response gain. Here, we measure incremental contrast thresholds for luminance and color stimuli to derive the contrast response of early neural mechanisms and their modulation by attention. We show that, for both cases, attention improves contrast discrimination, probably by multiplicatively increasing the gain of the neuronal response to contrast. However, the effects of attention are highly specific to the visual modality: concurrent attention to a competing luminance, but not chromatic pattern, greatly impedes luminance contrast discrimination; and attending to a competing chromatic, but not luminance, task impedes color contrast discrimination. Thus, the effects of attention are highly modality specific, implying separate attentional resources for different fundamental visual attributes at early stages of visual processing.     

Behavioral research in pigeons with ARENA: An Automated Remote Environmental Navigation Apparatus

Three experiments established the effectiveness of an Automated Remote Environmental Navigation Apparatus (ARENA) developed in our lab to study behavioral processes in pigeons. The technology utilizes one or more wireless modules, each capable of presenting colored lights as visual stimuli to signal reward and of detecting subject peck responses. In Experiment 1, subjects were instrumentally shaped to peck at a single ARENA module following an unsuccessful autoshaping procedure. In Experiment 2, pigeons were trained with a simultaneous discrimination procedure during which two modules were illuminated different colors; pecks to one color (S+) were reinforced while pecks to the other color (S−) were not. Pigeons learned to preferentially peck the module displaying the S+. In Experiment 3, two modules were lit the same color concurrently from a set of six colors in a conditional discrimination task. For three of the colors pecks to the module in one location (e.g., upper quadrant) were reinforced while for the remaining colors pecks at the other module (e.g., lower quadrant) were reinforced. After learning this discrimination, the color-reinforced location assignments were reversed. Pigeons successfully acquired the reversal. ARENA is an automated system for open-field studies and a more ecologically valid alternative to the touchscreen.     

Olfactory discrimination: when vision matters?

Many previous studies have attempted to investigate the effect of visual cues on olfactory perception in humans. The majority of this research has only looked at the modulatory effect of color, which has typically been explained in terms of multisensory perceptual interactions. However, such crossmodal effects may equally well relate to interactions taking place at a higher level of information processing as well. In fact, it is well-known that semantic knowledge can have a substantial effect on people's olfactory perception. In the present study, we therefore investigated the influence of visual cues, consisting of color patches and/or shapes, on people's olfactory discrimination performance. Participants had to make speeded odor discrimination responses (lemon vs. strawberry) while viewing a red or yellow color patch, an outline drawing of a strawberry or lemon, or a combination of these color and shape cues. Even though participants were instructed to ignore the visual stimuli, our results demonstrate that the accuracy of their odor discrimination responses was influenced by visual distractors. This result shows that both color and shape information are taken into account during speeded olfactory discrimination, even when such information is completely task irrelevant, hinting at the automaticity of such higher level visual-olfactory crossmodal interactions.     

Effects of maternal occupational exposure to organic solvents on offspring visual functioning: a prospective controlled study

BACKGROUND: Previous studies in adults and animals with high level exposure to organic solvents suggested impairments in visual functioning. The objective of this pilot study was to examine the effects of maternal occupational exposure to organic solvents during pregnancy on offspring color vision and visual acuity, the development of which may be especially vulnerable to organic solvent exposure. METHODS: We conducted a prospective cohort study of 32 offspring of women who were exposed occupationally to organic solvents during pregnancy compared with 27 nonexposed children. Monocular and binocular color vision and visual acuity were assessed using the Minimalist Test and the Cardiff Cards, respectively. Children with known hereditary color vision loss were excluded. RESULTS: Solvent-exposed children had significantly higher error scores on red-green and blue-yellow color discrimination, as well as poorer visual acuity compared with the control group. Exposure index (an estimated measure of exposure intensity) was not significantly related to color discrimination or visual acuity score. Despite excluding all children with a known family history of color vision loss, clinical red-green color vision loss was found among 3 of the 32 exposed children compared with none of the matched controls. CONCLUSIONS: These preliminary findings suggest that occupational exposure to organic solvents during pregnancy is associated with an increased risk of color vision and visual acuity impairment in offspring. The importance of routine visual function screening in risk assessment after prenatal exposure to chemicals warrants further attention.     

Animal visual systems and the evolution of color patterns: sensory processing illuminates signal evolution

Abstract Animal color pattern phenotypes evolve rapidly. What influences their evolution? Because color patterns are used in communication, selection for signal efficacy, relative to the intended receiver's visual system, may explain and predict the direction of evolution. We investigated this in bowerbirds, whose color patterns consist of plumage, bower structure, and ornaments and whose visual displays are presented under predictable visual conditions. We used data on avian vision, environmental conditions, color pattern properties, and an estimate of the bowerbird phylogeny to test hypotheses about evolutionary effects of visual processing. Different components of the color pattern evolve differently. Plumage sexual dimorphism increased and then decreased, while overall (plumage plus bower) visual contrast increased. The use of bowers allows relative crypsis of the bird but increased efficacy of the signal as a whole. Ornaments do not elaborate existing plumage features but instead are innovations (new color schemes) that increase signal efficacy. Isolation between species could be facilitated by plumage but not ornaments, because we observed character displacement only in plumage. Bowerbird color pattern evolution is at least partially predictable from the function of the visual system and from knowledge of different functions of different components of the color patterns. This provides clues to how more constrained visual signaling systems may evolve.     

Spatial heterogeneity in the perception of face and form attributes

The identity of an object is a fixed property, independent of where it appears, and an effective visual system should capture this invariance [1-3]. However, we now report that the perceived gender of a face is strongly biased toward male or female at different locations in the visual field. The spatial pattern of these biases was distinctive and stable for each individual. Identical neutral faces looked different when they were presented simultaneously at locations maximally biased to opposite genders. A similar effect was observed for perceived age of faces. We measured the magnitude of this perceptual heterogeneity for four other visual judgments: perceived aspect ratio, orientation discrimination, spatial-frequency discrimination, and color discrimination. The effect was sizeable for the aspect ratio task but substantially smaller for the other three tasks. We also evaluated perceptual heterogeneity for facial gender and orientation tasks at different spatial scales. Strong heterogeneity was observed even for the orientation task when tested at small scales. We suggest that perceptual heterogeneity is a general property of visual perception and results from undersampling of the visual signal at spatial scales that are small relative to the size of the receptive fields associated with each visual attribute.     

Orbeli's experimental work on color discrimination in dogs

In the 1900's, L.A. Orbeli, on I.P. Pavlov's request, attempted to establish color discrimination in dogs. Previous experiments used the motor discrimination method and gave inconsistent results. In contrast, Orbeli used the salivary conditional reflex method, which he considered to be more precise than the method that relied on erratic movements of a dog. After experimentation that lasted about one and a half years, Orbeli failed to establish color discrimination. When subsequent experiments by Russians and Germans yielded positive results with the motor discrimination method, Orbeli switched to this method and also obtained positive results. These findings were confirmed by most subsequent experiments on color discrimination in dogs. The utility of Pavlovian conditioning in sensory experimentation was not universally justified and its importance was greater in the study of learning.     

Influence of stimuli size on color discrimination in capuchin monkeys

Large-field trichromacy is a general feature of protanope and deuteranope humans, provided that the stimuli size extends to an 8 degrees visual angle. In this study we compared the performance of five male and three female tufted capuchin monkeys (Cebus apella) in discriminating pairs of Munsell color papers. Human subjects were also studied in two-choice discrimination tests, using the same stimuli and apparatus employed for the monkeys. The results show that although the dichromatic humans showed improved discrimination with larger versions of the stimuli, the dichromatic monkeys exhibited the same performance for both stimuli sizes. Thus, Cebus apella apparently do not present large-field trichromacy-at least for the conditions in the present experiments.     

The normalized segment classification model: A new tool to compare spectral reflectance curves

1. Color patterns are complex traits under selective pressures from conspecifics, mutualists, and antagonists. To evaluate the salience of a pattern or the similarity between colors, several visual models are available. Color discrimination models estimate the perceptual difference between any two colors. Their application to a diversity of taxonomic groups has become common in the literature to answer behavioral, ecological, and evolutionary questions. To use these models, we need information about the visual system of our beholder species. However, many color patterns are simultaneously subject to selective pressures from different species, often from different taxonomic groups, with different visual systems. Furthermore, we lack information about the visual system of many species, leading ecologists to use surrogate values or theoretical estimates for model parameters.
2. Here, we present a modification of the segment classification method proposed by Endler (Biological Journal of the Linnean Society, 1990 41, 315–352): the normalized segment classification model (NSC). We explain its logic and use, exploring how NSC differs from other visual models. We also compare its predictions with available experimental data.
3. Even though the NSC model includes no information about the visual system of the receiver species, it performed better than traditional color discrimination models when predicting the output of some behavioral tasks. Although vision scientists define color as independent of stimulus brightness, a likely explanation for the goodness of fit of the NSC model is that its distance measure depends on brightness differences, and achromatic information can influence the decision‐making process of animals when chromatic information is missing.
4. Species‐specific models may be insufficient for the study of color patterns in a community context. The NSC model offers a species‐independent solution for color analyses, allowing us to calculate color differences when we ignore the intended viewer of a signal or when different species impose selective pressures on the signal.

     

Unconscious letter discrimination is enhanced by association with conscious color perception in visual form agnosia

Adaptive behavior guided by unconscious visual cues occurs in patients with various kinds of brain damage as well as in normal observers, all of whom can process visual information of which they are fully unaware [1] [2] [3] [4] [5] [6] [7] [8]. Little is known on the possibility that unconscious vision is influenced by visual cues that have access to consciousness [9]. Here we report a 'blind' letter discrimination induced through a semantic interaction with conscious color processing in a patient who is agnosic for visual shapes, but has normal color vision and visual imagery. In seeing the initial letters of color names printed in different colors, it is normally easier to name the print color when it is congruent with the initial letter of the color name than when it is not [10]. The patient could discriminate the initial letters of the words 'red' and 'green' printed in the corresponding colors significantly above chance but without any conscious accompaniment, whereas he performed at chance with the reverse color-letter mapping as well as in standard tests of letter reading. We suggest that the consciously perceived colors activated a representation of the corresponding word names and their component letters, which in turn brought out a partially successful, unconscious processing of visual inputs corresponding to the activated letter representations.     

视觉通道中颜色与形状特征的识别

本文利用计算机设计新的心理物理实验,研究人类视觉系统的颜色、形状通道和对颜色的识别反应,证实视觉系统的颜色通道和形状通道是独立并行的.对颜色反应还进行视觉诱发电位测试,结果与心理物理实验基本一致.最后,提出颜色通道与形状通道间信息相互统一的假说模型.     

Spatial, colour and contrast response characteristics of mechanisms which mediate discrimination of pattern orientation and magnification

We have measured response times for the detection of a single target presented against a set of reference elements which are characterised by combinations of four different stimulus parameters; colour, contrast polarity, magnification and orientation. The aim of the experiments was to determine the response characteristics of visual mechanisms which mediate target detection through the discrimination of orientation and magnification. In the first experiments, we determined sensitivity to differences in colour and contrast polarity, and show that the mechanisms responsible for the discrimination of orientation and of magnification are both selective in their responses to colour and to contrast polarity. There are, nonetheless, residual interactions between patterns of different contrast polarities and between those of different colour, and in the latter case, weak interactions persist under equiluminance conditions. In a second set of experiments, we examined the interactions between orientation and magnification. We conclude that the responses of visual mechanisms which mediate target detection through discrimination of orientation are markedly dependent on stimulus magnification whereas those which mediate detection through discrimination of magnification are, in contrast, relatively insensitive to stimulus orientation.     

The reconstruction of the perceptual spaces of brightness and color on the basis of visual evoked potentials and their comparison with the data from behavioral trials

The visual evoked potentials to a change in color stimuli were studied. The amplitude of the N85 component was correlated with color discrimination. In cases when the brightness of one color was fixed and that of the other one changed, the amplitude dynamics of N85 was V-shaped with the minimum corresponding to the point of equal brightness of both colors. The N85 amplitude in this point serves as a measure of discrimination between stimuli chromaticity. The perceptual color space in rabbit (possessing two cone pigments) was constructed in accordance with the amplitudes of N85 to color change. This space represented a hypersphere in the four-dimensional Euclidean space. The perceptual spaces for brightness and color reconstructed on the basis of conditioning probabilities and N85 amplitudes evoked by replacement of colored and achromatic stimuli were shown to coincide. This suggests the common mechanism of the vector color coding.     

BUTTERFLY EYESPOTS: THE GENETICS AND DEVELOPMENT OF THE COLOR RINGS

The butterfly Bicyclus anynana has a series of distal eyespots on its wings. Each eyespot is composed of a white pupil, a black disc, and a gold outer ring. We applied artificial selection to the large dorsal eyespot on the forewing to produce a line with the gold ring reduced or absent (BLACK) and another line with a reduced black disc and a broad gold ring (GOLD). High heritabilities, coupled with a rapid response to selection, produced two lines of butterflies with very different phenotypes. Other eyespots showed a correlated change in the proportion of their color rings. Surgical experiments were performed on pupal wings from the different lines at the time of eyespot pattern specification. They showed that the additive genetic variance for this trait was in the response of the wing epidermis to signaling from the organizing cells at the eyespot center (the focus). This response was found to vary across different regions of the wing and also between the sexes. The particular eyespot color composition found for each sex, as well as the maintenance of the high genetic variation, are discussed with reference to the ecology of the butterfly, sexual selection, and visual selection by predators.     

Behavioral evidence of color vision deficiency in a protanomalia chimpanzee (<Emphasis Type="Italic">Pan troglodytes</Emphasis>)

Although color vision deficiency is very rare among Old World monkeys and apes, one male chimpanzee (Lucky) was identified as protanomalous by genetic and physiological analyses. This study assessed behavioral phenotypes of Lucky and four chimpanzees with normal color vision by discrimination task using the modified Ishihara pseudo-isochromatic plates. Lucky could not discriminate the stimuli that the other chimpanzees could. This is the first behavioral evidence of color vision deficiency in chimpanzees. Electronic Publication     

Sensory discrimination and the incipient advantage of mutations

Perception follows logarithmic or power functions, rather than linear functions, of stimulus intensity. A small increment in stimulus strength can be sufficient to elicit discrimination between individuals of different phenotypes when the initial stimulus magnitude is near zero. This may confer an incipient advantage to the mutation that caused it. The psychophysics of signal receivers may be a good predictor of the extent of phenotypic changes. For example, slight similarities in color of Batesian mimics to their distasteful model can be sufficient to cause predators to reject the mimics. Color changes produced by single mutations in incipient Batesian mimics should be more extensive in mimicry complexes where the predators are less sensitive to color differences.     

A retinal substrate for colour discrimination in crabs

Summary In crabs, there is behavioural evidence for colour discrimination from the portunidCarcinus and severalUca species, but in the same and related species only a single visual pigment has been found in the rhabdoms by microspectrophotometry. Micro-electrode recordings of the spectral sensitivity of single portunid photoreceptors may throw some light on this apparent inconsistency. Large changes in spectral sensitivity occur with light adaptation in the crabScylla serrata. Selective adaptation experiments rule out the possibility that the changes may be caused by the presence of a number of visual pigments or of antenna pigments. The results suggest that inScylla the absorption of a single visual pigment type is modified by different coloured filters in different photoreceptors and that this makes colour discrimination possible.     

The critical cue in pattern discrimination for the honey bee: Color or form?

When honey bees approach blossoms, they are attracted by the color and form of the goal in their visual field, and they use these cues for a successful revisit. Their visual system receives cues by two main types of parallel channels behind the retina; one channel for colors, and a monochrome channel for the orientation and edge of the item in their visual field. In the integration process of these 2 channels, the priority and interaction between them are significant due to the fact that these chromatic and achromatic signals coexist naturally. To investigate this issue, we trained bees to detect form and color and then tested them with combinations of opposite patterns. We observed that the bees chose the correct color but the wrong form pattern in the above experiment as well as for other manipulations as follows. The effect of the color training for the blue reward pattern differed from that of the green reward pattern. The color pattern choices tended to be more correct if blue was the target during the training process, indicating that the chromatic signal was the main cue in pattern discrimination. In other words, color tended to be the decisive factor in a conflicting situation. In addition, the color blue was preferred over the color green, indicating that color preference was involved in visual recognition.