Achromatic Vision Research Articles

Flower colour and size-signals vary with altitude and resulting climate on the tropical-subtropical islands of Taiwan.

The diversity of flower colours in nature provides quantifiable evidence for how visitations by colour sensing insect pollinators can drive the evolution of angiosperm visual signalling. Recent research shows that both biotic and abiotic factors may influence flower signalling, and that harsher climate conditions may also promote salient signalling to entice scarcer pollinators to visit. In parallel, a more sophisticated appreciation of the visual task foragers face reveals that bees have a complex visual system that uses achromatic vision when moving fast, whilst colour vision requires slower, more careful inspection of targets. Spectra of 714 native flowering species across Taiwan from sea level to mountainous regions 3,300 m above sea level (a.s.l.) were measured. We modelled how the visual system of key bee pollinators process signals, including flower size. By using phylogenetically informed analyses, we observed that at lower altitudes including foothills and submontane landscapes, there is a significant relationship between colour contrast and achromatic signals. Overall, the frequency of flowers with high colour contrast increases with altitude, whilst flower size decreases. The evidence that flower colour signaling becomes increasingly salient in higher altitude conditions supports that abiotic factors influence pollinator foraging in a way that directly influences how flowering plants need to advertise.

Applying Resampling and Visualization Methods in Factor Analysis to Model Human Spatial Vision.

Studies have reported different numbers of spatial frequency channels for chromatic and achromatic vision. To resolve the difference, we performed factor analysis, a multivariate modeling technique, on population data of achromatic and chromatic sensitivity. In addition, we included resampling and visualization methods to evaluate models from factor analysis. These routines are complex but widely useful. Therefore we have archived our analysis routines by building smCSF, an open-source software package in R (https://smin95.github.io/dataviz/). Data of 103 normally-sighted adults were analyzed. They included blue-yellow, red-green, and achromatic contrast sensitivity. To obtain the confidence interval of relevant statistical parameters, factor analysis was performed using a resampling method. Then exploratory models were developed. We then performed model selections by fitting them against the empirical data and quantifying the quality of the fits. During the exploratory factor analysis, different statistical tests supported different factor models. These could partially be reasons for why there have been conflicting reports. However, after the confirmatory analysis, we found that a model that included two spatial channels was adequate to approximate the chromatic sensitivity data, whereas that with three channels was so for the achromatic sensitivity data. Our findings provide novel insights about the spatial channels for chromatic and achromatic contrast sensitivity from population data. Also, the analysis and visualization routines have been archived in a computational package to boost the transparency and replicability of science.

Poster Session II: Variation of cone spectral composition in the macula.

Cone spectral composition is central to the study of color vision and retinal development. There is a lack of information on the spatial distribution of L and M-cones in the macula given that there are no histological methods to separate them. To overcome this gap, cones were spectrally classified using adaptive optics OCT-based optoretinography in human subjects and their variation was described in the macula. To date, we have classified ~130000 total cones in 9 subjects across 79 regions of interest (ROI), with a maximum of 16 retinal eccentricities per subject spread along the 4 cardinal meridians. In 2 two subjects, the variation in cone spectral topography in both eyes was compared. The L: M cone ratio decreased in the foveal slope (0.4°- 1°) but remained relatively uniform in the parafovea from 1.5°- 10° eccentricity. The % S-cones and S-cone density were consistent with prior histology (Curcio et al. 1991). No significant differences were observed in the fellow eyes of the same subject or the distribution of cone types across the 4 cardinal meridians. Decreased L: M cone ratio in the foveal slope suggests earlier differentiation of M-cones than L-cones. The stable L: M cone ratio in the parafovea suggests that the greater fall off in chromatic versus achromatic vision with eccentricity is not explained by cone spectral composition, but is rather attributed to pooling in downstream neurons.

Achromatic Cues Are Important for Flower Visibility to Hawkmoths and Other Insects

Studies on animal colour vision typically focus on the chromatic aspect of colour, which is related to the spectral distribution, and disregard the achromatic aspect, which is related to the intensity (“brightness”) of a stimulus. Although the chromatic component of vision is often most reliable for object recognition because it is fairly context independent, the achromatic component may provide a reliable signal under specific conditions, for example at night when light intensity is low. Here we make a case for the importance of achromatic cues in plant-pollinator signalling, based on experimental data on naïve Deilephila elpenor and Macroglossum stellatarum hawkmoths, optical modelling and synthesising published experiments on bees, flies, butterflies and moths. Our experiments show that in ecologically relevant light levels hawkmoths express a strong preference for brighter stimuli. Published experiments suggest that for flower-visiting bees, butterflies, moths and flies, achromatic cues may be more important for object detection than often considered. Our optical modelling enabled disentangling the contribution of pigments and scattering structures to the flower’s achromatic contrast, and illustrates how flower anatomy and background are important mediating factors. We discuss our findings in the context of the often-assumed dichotomy between detection and discrimination, chromatic versus achromatic vision, and the evolution of floral visual signals.

Retinal organization and visual abilities for flower foraging in swallowtail butterflies.

Papilio butterflies' ability to forage for flowers relies upon multiple visual cues such as color, brightness, and motion. Papilio learns the color of rewarding flowers and detects it at a distance. Its color vision is based on four photoreceptor classes: UV, blue, green, and red, providing sensitive wavelength discrimination. These four receptor classes also contribute to the perception of brightness and polarization. Papilio's motion vision is based on a different set of receptors: green, red, and broad band. This implies that two visual pathways exist in Papilio. The contribution of several receptor classes not only for chromatic vision but also achromatic vision likely enhances the butterfly's ability to detect flowers in complex visual environments.

RNA sequencing analysis of the human retina and associated ocular tissues

The retina is a stratified layer of sensory neurons lining the posterior portion of the eye. In humans, fine detail and color vision are enabled by the macula, a central region of the retina dense in cone photoreceptors (PRs). Achromatic low light and peripheral vision are facilitated by rod PRs found with increasing density outside the macula in the peripheral retina. The outer retina is nourished by choroidal blood flow regulated by a single layer of intervening retinal pigment epithelial (RPE) cells. Existing human retinal transcriptome projects have been critical for studying aspects of retinal development and disease however, there are currently no publicly available data sets accurately describing the aging human central retina, peripheral retina, and supporting RPE/choroid. Here we used Illumina RNA sequencing (RNA-seq) analysis to characterize the mRNA transcriptome of rod and cone PR-enriched human retina as well as supporting macular RPE/choroid tissue. These data will be valuable to the vision research community for characterizing global changes in gene expression in clinically relevant ocular tissues.

Hummingbird vision.

Hummingbirds are widely recognized by their hovering flight. In this Quick guide, Altshuler and Wylie describe the visual specializations that allow for the hummingbird's flight abilities.

More than noise: context-dependent luminance contrast discrimination in a coral reef fish (Rhinecanthus aculeatus).

Achromatic (luminance) vision is used by animals to perceive motion, pattern, space and texture. Luminance contrast sensitivity thresholds are often poorly characterised for individual species and are applied across a diverse range of perceptual contexts using over-simplified assumptions of an animal's visual system. Such thresholds are often estimated using the receptor noise limited model (RNL). However, the suitability of the RNL model to describe luminance contrast perception remains poorly tested. Here, we investigated context-dependent luminance discrimination using triggerfish (Rhinecanthus aculeatus) presented with large achromatic stimuli (spots) against uniform achromatic backgrounds of varying absolute and relative contrasts. 'Dark' and 'bright' spots were presented against relatively dark and bright backgrounds. We found significant differences in luminance discrimination thresholds across treatments. When measured using Michelson contrast, thresholds for bright spots on a bright background were significantly higher than for other scenarios, and the lowest threshold was found when dark spots were presented on dark backgrounds. Thresholds expressed in Weber contrast revealed lower thresholds for spots darker than their backgrounds, which is consistent with the literature. The RNL model was unable to estimate threshold scaling across scenarios as predicted by the Weber-Fechner law, highlighting limitations in the current use of the RNL model to quantify luminance contrast perception. Our study confirms that luminance contrast discrimination thresholds are context dependent and should therefore be interpreted with caution.

Vision in an abundant North American bird: The Red-winged Blackbird

AbstractAvian vision is fundamentally different from human vision; however, even within birds there are substantial between-species differences in visual perception in terms of visual acuity, visual coverage, and color vision. However, there are not many species that have all these visual traits described, which can constrain our ability to study the evolution of visual systems in birds. To start addressing this gap, we characterized multiple traits of the visual system (visual coverage, visual acuity, centers of acute vision, and color vision) of the Red-winged Blackbird (Agelaius phoeniceus), one of the most abundant and studied birds in North America. We found that Red-winged Blackbirds have: wide visual coverage; one center of acute vision per eye (fovea) projecting fronto-laterally with high density of single and double cones, making it the center of both chromatic and achromatic vision; a wide binocular field that does not have the input of the centers of acute vision; and an ultraviolet sensitive visual system. With this information, we parameterized a Red-winged Blackbird-specific perceptual model considering different plumage patches. We found that the male red epaulet was chromatically conspicuous but with minimal achromatic signal, but the male yellow patch had a lower chromatic but a higher achromatic signal, which may be explained by the pigment composition of the feathers. However, the female epaulet was not visually conspicuous in both the chromatic and achromatic dimensions compared with other female feather patches. We discuss the implications of this visual system configuration relative to the foraging, antipredator, mate choice, and social behaviors of Red-winged Blackbirds. Our findings can be used for comparative studies as well as for making more species-specific predictions about different visual behaviors for future empirical testing.

Neural Mechanisms That Hide Individual Behavioral Differences: Evidence from Psychophysics and Neuroscience

In both theory and practice, individual behavioral differences can reveal details of underlying neural mechanisms, and this has been widely exploited in experimental psychology. However, under some circumstances, individual differences are conspicuous by their absence. Three illuminating examples are treated in this theoretical review: (1) In color vision, there is a surprising lack of variation in red–green color opponency, especially as studied using unique hues, given the huge variation of L:M-cone ratios in normal observers. (2) Conversely, in achromatic vision, individual differences in L:M-cone ratios can be studied by measuring spectral sensitivity (luminance efficiency) functions. However, contrary to reasonable expectations, parvo and magno mechanisms can give rise to indistinguishable spectral sensitivity functions, so individual variations in parvo and magno activation often cannot be studied via spectral sensitivity. (3) Similar convergences occur in neuroscience: in simulated and actual neuronal networks and in electrophysiological/functional imaging studies of intact animals/humans. Neuronal systems trained or developed to do the same tasks need not wind up with the same wiring or the exact same behavior. However, under some circumstances, their behaviors can become functionally similar. Markedly different neural mechanisms somehow yield similar behaviors, a result found in systems as different as motor behaviors in crustaceans and sensory behaviors in humans. Theoretically, similar neural mechanisms can result from different neural combinations, a response convergence which limits our ability to infer the origins of some perceptual channels. When expected individual differences do not manifest, this is a clue that something interesting is happening and a goad to further investigation.

Psychophysical Evaluation of Visual Functions of Ex-Alcoholic Subjects After Prolonged Abstinence.

Chronic alcohol abuse can lead to a brain damages, and the health status of alcoholics even after a long-term alcohol abstinence is a public health concern. The present study investigated the color vision and spatial luminance contrast sensitivity of a group of 17 ex-alcoholics (46.3 ± 6.7 years old) in long-term alcohol abstinence after having been previously under alcohol dependence for many years. We also investigated the association of impaired psychophysical performance in different tests we applied. The mean time of alcohol consumption was 16.9 ± 5.1 years and the mean abstinence period was 12.4 ± 8.5 years. Achromatic vision of all subjects was evaluated using spatial luminance contrast sensitivity function (CSF) test and color vision was evaluated using Mollon–Reffin color discrimination test (MR) and the Farnsworth–Munsell 100 hue arrangement test (FM100). Relative to controls, the spatial luminance contrast sensitivity was lower in 10/17 of the ex-alcoholic subjects. In the color vision tests, 11/16 ex-alcoholic subjects had impaired results compared to controls in the FM100 test and 13/14 subjects had color vision deficits measured in the MR test. Fourteen subjects performed all visual tests, three subjects had impaired results for all tests, seven subjects had impaired results in two tests, three subjects had visual deficit in one test, and one had normal results for all tests. The results showed the existence of functional deficits in achromatic and chromatic vision of subjects with history of chronic alcoholism after long abstinence. Most subjects had altered result in more than one test, especially in the color vision tests. The present investigation suggests that the damage in visual functions produced by abusive alcohol consumption is not reversed after long term alcohol abstinence.

Non-linear amplification of graded voltage signals in the first-order visual interneurons of the butterfly Papilio xuthus.

Lamina monopolar cells (LMCs) are the first-order visual interneurons of insects and crustacea, primarily involved in achromatic vision. Here, we investigated morphological and electrophysiological properties of LMCs in the butterfly Papilio xuthus Using intracellular recording coupled with dye injection, we found two types of LMCs. Cells with roundish terminals near the distal surface of the medulla demonstrating no or small depolarizing spikes were classified as L1/2. Cells with elongated terminals deep in the medulla that showed prominent spiking were classified as L3/4. The majority of LMCs of both types had broad spectral sensitivities, peaking between 480 and 570 nm. Depending on the experimental conditions, spikes varied from small to action potential-like events, with their amplitudes and rates decreasing as stimulus brightness increased. When the eye was stimulated with naturalistic contrast-modulated time series, spikes were reliably triggered by high-contrast components of the stimulus. Spike-triggered average functions showed that spikes emphasize rapid membrane depolarizations. Our results suggest that spikes are mediated by voltage-activated Na+ channels, which are mainly inactivated at rest. Strong local minima in the coherence functions of spiking LMCs indicate that the depolarizing conductance contributes to the amplification of graded responses even when detectable spikes are not evoked. We propose that the information transfer strategies of spiking LMCs change with light intensity. In dim light, both graded voltage signals and large spikes are used together without mutual interference, as a result of separate transmission bandwidths. In bright light, signals are non-linearly amplified by the depolarizing conductance in the absence of detectable spikes.

Testing a key assumption in animal communication: between-individual variation in female visual systems alters perception of male signals.

ABSTRACTVariation in male signal production has been extensively studied because of its relevance to animal communication and sexual selection. Although we now know much about the mechanisms that can lead to variation between males in the properties of their signals, there is still a general assumption that there is little variation in terms of how females process these male signals. Variation between females in signal processing may lead to variation between females in how they rank individual males, meaning that one single signal may not be universally attractive to all females. We tested this assumption in a group of female wild-caught brown-headed cowbirds (Molothrus ater), a species that uses a male visual signal (e.g. a wingspread display) to make its mate-choice decisions. We found that females varied in two key parameters of their visual sensory systems related to chromatic and achromatic vision: cone densities (both total and proportions) and cone oil droplet absorbance. Using visual chromatic and achromatic contrast modeling, we then found that this between-individual variation in visual physiology leads to significant between-individual differences in how females perceive chromatic and achromatic male signals. These differences may lead to variation in female preferences for male visual signals, which would provide a potential mechanism for explaining individual differences in mate-choice behavior.

Nonlinearity of contrast responses in human achromatic and color vision

Nonlinearity of contrast responses in human achromatic and color vision

Rainbow Enhancers Regulate Restrictive Transcription in Teleost Green, Red, and Blue Cones.

Photoreceptor-specific transcription of individual genes collectively constitutes the transcriptional profile that orchestrates the structural and functional characteristics of each photoreceptor type. It is challenging, however, to study the transcriptional specificity of individual photoreceptor genes because each gene's distinct spatiotemporal transcription patterns are determined by the unique interactions between a specific set of transcription factors and the gene's own cis-regulatory elements (CREs), which remain unknown for most of the genes. For example, it is unknown what CREs underlie the zebrafish mpp5bponli (ponli) and crumbs2b (crb2b) apical polarity genes' restrictive transcription in the red, green, and blue (RGB) cones in the retina, but not in other retinal cell types. Here we show that the intronic enhancers of both the ponli and crb2b genes are conserved among teleost species and that they share sequence motifs that are critical for RGB cone-specific transcription. Given their similarities in sequences and functions, we name the ponli and crb2b enhancers collectively rainbow enhancers. Rainbow enhancers may represent a cis-regulatory mechanism to turn on a group of genes that are commonly and restrictively expressed in RGB cones, which largely define the beginning of the color vision pathway.SIGNIFICANCE STATEMENT Dim-light achromatic vision and bright-light color vision are initiated in rod and several types of cone photoreceptors, respectively; these photoreceptors are structurally distinct from each other. In zebrafish, although quite different from rods and UV cones, RGB cones (red, green, and blue cones) are structurally similar and unite into mirror-symmetric pentamers (G-R-B-R-G) by adhesion. This structural commonality and unity suggest that a set of genes is commonly expressed only in RGB cones but not in other cells. Here, we report that the rainbow enhancers activate RGB cone-specific transcription of the ponli and crb2b genes. This study provides a starting point to study how RGB cone-specific transcription defines RGB cones' distinct functions for color vision.

Two-dimensional Neural Basis of Achromatic Vision in Invertebrates and Vertebrates

Two-dimensional Neural Basis of Achromatic Vision in Invertebrates and Vertebrates

What visual illusions tell us about underlying neural mechanisms and observer strategies for tackling the inverse problem of achromatic perception.

Research in lightness perception centers on understanding the prior assumptions and processing strategies the visual system uses to parse the retinal intensity distribution (the proximal stimulus) into the surface reflectance and illumination components of the scene (the distal stimulus—ground truth). It is agreed that the visual system must compare different regions of the visual image to solve this inverse problem; however, the nature of the comparisons and the mechanisms underlying them are topics of intense debate. Perceptual illusions are of value because they reveal important information about these visual processing mechanisms. We propose a framework for lightness research that resolves confusions and paradoxes in the literature, and provides insight into the mechanisms the visual system employs to tackle the inverse problem. The main idea is that much of the debate and confusion in the literature stems from the fact that lightness, defined as apparent reflectance, is underspecified and refers to three different types of judgments that are not comparable. Under stimulus conditions containing a visible illumination component, such as a shadow boundary, observers can distinguish and match three independent dimensions of achromatic experience: apparent intensity (brightness), apparent local intensity ratio (brightness-contrast), and apparent reflectance (lightness). In the absence of a visible illumination boundary, however, achromatic vision reduces to two dimensions and, depending on stimulus conditions and observer instructions, judgments of lightness are identical to judgments of brightness or brightness-contrast. Furthermore, because lightness judgments are based on different information under different conditions, they can differ greatly in their degree of difficulty and in their accuracy. This may, in part, explain the large variability in lightness constancy across studies.

Individual variation in cone photoreceptor density in house sparrows: implications for between-individual differences in visual resolution and chromatic contrast.

Between-individual variation has been documented in a wide variety of taxa, especially for behavioral characteristics; however, intra-population variation in sensory systems has not received similar attention in wild animals. We measured a key trait of the visual system, the density of retinal cone photoreceptors, in a wild population of house sparrows (Passer domesticus). We tested whether individuals differed from each other in cone densities given within-individual variation across the retina and across eyes. We further tested whether the existing variation could lead to individual differences in two aspects of perception: visual resolution and chromatic contrast. We found consistent between-individual variation in the densities of all five types of avian cones, involved in chromatic and achromatic vision. Using perceptual modeling, we found that this degree of variation translated into significant between-individual differences in visual resolution and the chromatic contrast of a plumage signal that has been associated with mate choice and agonistic interactions. However, there was no evidence for a relationship between individual visual resolution and chromatic contrast. The implication is that some birds may have the sensory potential to perform “better” in certain visual tasks, but not necessarily in both resolution and contrast simultaneously. Overall, our findings (a) highlight the need to consider multiple individuals when characterizing sensory traits of a species, and (b) provide some mechanistic basis for between-individual variation in different behaviors (i.e., animal personalities) and for testing the predictions of several widely accepted hypotheses (e.g., honest signaling).

Related but not alike: not all Hemiptera are attracted to yellow

Most innate responses to color stimuli lead herbivorous insects to orient to “green” and “yellow” surfaces. Early research showed that aphid orientation to plants is influenced by foliar pigments and leads them to alight on leaves of a specific physiological state regardless of whether or not it is their actual host. In this study, we quantified the color preferences of four psyllids specialized on young to recently expanded leaves of different Eucalyptus hosts presenting distinct between (inter-specific) and within canopy (ontogenic) optical characteristics. Color preferences of Ctenarytaina eucalypti and C. bipartita were similar to those observed in aphids with more frequent selection of yellow and green stimuli, consistent with the coloration of their host leaves. However, attraction of Anoeconeossa bundoorensis and Glycaspis brimblecombei to a red stimulus contrasts strongly with the literature for hemipteran and herbivorous insects generally for which attraction to red is peculiar. Interestingly, both red-attracted species occur on the same host eucalypt, which expresses anthocyanic (red) young leaves. Our experiments demonstrate that these two species are sensitive to long wavelength radiation. Behavioral work and modeling of putative “aphid-like” photoreceptors were conducted to investigate whether achromatic vision mediates perception of “red”. Our results do not provide strong evidence for an intensity-dependant type of attraction. Nevertheless, the current knowledge of photoreceptors in Hemiptera identifies the achromatic as the most likely mechanism for detecting long wavelengths. Thus, our findings highlight the need for physiological work with Psylloidea to dissect the mechanisms responsible for such atypical responses. We discuss the ecological implications of our work in relation to red foliar pigments in expanding leaves of perennial plants which differs greatly from the thoroughly studied aphid-autumnal leaves system involving senescing foliage.

Do American Goldfinches See Their World Like Passive Prey Foragers? A Study on Visual Fields, Retinal Topography, and Sensitivity of Photoreceptors

Several species of the most diverse avian order, Passeriformes, specialize in foraging on passive prey, although relatively little is known about their visual systems. We tested whether some components of the visual system of the American goldfinch (Spinus tristis), a granivorous bird, followed the profile of species seeking passive food items (small eye size relative to body mass, narrow binocular fields and blind areas, centrally located retinal specialization projecting laterally, ultraviolet-sensitive vision). We measured eye size, visual field configuration, the degree of eye movement, variations in the density of ganglion cells and cone photoreceptors, and the sensitivity of photoreceptor visual pigments and oil droplets. Goldfinches had relatively large binocular (46°) and lateral (134°) visual fields with a high degree of eye movement (66° at the plane of the bill). They had a single centrotemporally located fovea that projects laterally, but can be moved closer to the edge of the binocular field by converging the eyes. Goldfinches could also increase their panoramic vision by diverging their eyes while handling food items in head-up positions. The distribution of photoreceptors indicated that the highest density of single and double cones was surrounding the fovea, making it the center of chromatic and achromatic vision and motion detection. Goldfinches possessed a tetrachromatic ultraviolet visual system with visual pigment peak sensitivities of 399 nm (ultraviolet-sensitive cone), 442 nm (short-wavelength-sensitive cone), 512 nm (medium-wavelength-sensitive cone), and 580 nm (long-wavelength-sensitive cone). Overall, the visual system of American goldfinches showed characteristics of passive as well as active prey foragers, with a single-fovea configuration and a large degree of eye movement that would enhance food searching and handling with their relatively wide binocular fields.