Thresholds of polarization vision in octopuses.

Polarization vision is widespread in nature, mainly among invertebrates, and is used for a range of tasks including navigation, habitat localization and communication. In marine environments, some species such as those from the Crustacea and Cephalopoda that are principally monochromatic, have evolved to use this adaptation to discriminate objects across the whole visual field, an ability similar to our own use of colour vision. The performance of these polarization vision systems varies, and the few cephalopod species tested so far have notably acute thresholds of discrimination. However, most studies to date have used artificial sources of polarized light that produce levels of polarization much higher than found in nature. In this study, the ability of octopuses to detect polarization contrasts varying in angle of polarization (AoP) was investigated over a range of different degrees of linear polarization (DoLP) to better judge their visual ability in more ecologically relevant conditions. The 'just-noticeable-differences' (JND) of AoP contrasts varied consistently with DoLP. These JND thresholds could be largely explained by their 'polarization distance', a neurophysical model that effectively calculates the level of activity in opposing horizontally and vertically oriented polarization channels in the cephalopod visual system. Imaging polarimetry from the animals' natural environment was then used to illustrate the functional advantage that these polarization thresholds may confer in behaviourally relevant contexts.

Computational simulation of human perception of spatially dependent patterns modulated by degree and angle of linear polarization.

Recent studies on polarization perception have shown that humans are sensitive to patterned stimuli modulated by either angle of linear polarization (AoP) or degree of polarization (DoP). Here, we present a model of human polarization sensitivity that incorporates both AoP and DoP as spatially dependent input variables. Applying the model to both sinusoidal- and square-wave-modulated DoP and AoP inputs, we demonstrate the theoretical similarities and differences generated by such inputs. Our model indicates the following: (i) edge boundaries between two adjacent areas of different linear polarization are preserved for both AoP- and DoP-modulated stimuli; and (ii) compared with DoP stimuli, AoP stimuli generate greater luminance changes at the photoreceptor level, suggesting that AoP-modulated patterns are potentially more salient than DoP patterns. The computational model is supported experimentally with an optical test of the model comprising a radial diattenuating polarizing filter and modified liquid crystal displays generating DoP- and AoP-modulated outputs. Psychophysical measures of human sensitivity confirm the increased salience of AoP- relative to DoP-modulated stimuli. These findings have practical application to the selection of DoP- and AoP-modulated stimuli for the investigation of macular function and macular pigment density in healthy and diseased eyes.

Haidinger's brushes elicited at varying degrees of polarization rapidly and easily assesses total macular pigmentation.

Macular pigments (MPs), by absorbing potentially toxic short-wavelength (400-500 nm) visible light, provide protection against photo-chemical damage thought to be relevant in the pathogenesis of age-related macular degeneration (AMD). A method of screening for low levels of MPs could be part of a prevention strategy for helping people to delay the onset of AMD. We introduce a new method for assessing MP density that takes advantage of the polarization-dependent absorption of blue light by MPs, which results in the entoptic phenomenon called Haidinger's brushes (HB). Subjects were asked to identify the direction of rotation of HB when presented with a circular stimulus illuminated with an even intensity of polarized white light in which the electric field vector was rotating either clockwise or anti-clockwise. By reducing the degree of polarization of the stimulus light, a threshold for perceiving HB (degree of polarization threshold) was determined and correlated (r2=0.66) to macular pigment optical density assessed using dual-wavelength fundus autofluoresence. The speed and ease of measurement of degree of polarization threshold makes it well suited for large-scale screening of macular pigmentation.

Polarisation vision: overcoming challenges of working with a property of light we barely see.

In recent years, the study of polarisation vision in animals has seen numerous breakthroughs, not just in terms of what is known about the function of this sensory ability, but also in the experimental methods by which polarisation can be controlled, presented and measured. Once thought to be limited to only a few animal species, polarisation sensitivity is now known to be widespread across many taxonomic groups, and advances in experimental techniques are, in part, responsible for these discoveries. Nevertheless, its study remains challenging, perhaps because of our own poor sensitivity to the polarisation of light, but equally as a result of the slow spread of new practices and methodological innovations within the field. In this review, we introduce the most important steps in designing and calibrating polarised stimuli, within the broader context of areas of current research and the applications of new techniques to key questions. Our aim is to provide a constructive guide to help researchers, particularly those with no background in the physics of polarisation, to design robust experiments that are free from confounding factors.

Correction to: Polarisation vision: overcoming challenges of working with a property of light we barely see.

In "Polarisation vision: overcoming challenges of working with a property of light we barely see" (Foster et al. 2018) we provide a basic description of how Stokes parameters can be estimated and used to calculate the angle of polarisation (AoP).

Computational simulation of Haidinger's brushes.

Haidinger's brushes (HB) are entoptic phenomena resulting from differential absorption of linear polarized light by the human macula. Computational models have assisted in understanding the behavior of these subjective phenomena but have been limited in their application. This study presents a revised computational model that incorporates known determinants of the form and behavior of HB. The model generates both static and animated simulations of HB that can be quantified by their density, contrast, and radial/circumferential extent. Measured physiological parameters are used to demonstrate the dependency of HB on macular pigment (MP) density, MP distribution, and ocular retardation. Physiological variations in these parameters explain the reported variations in the perception of HB.

Perceiving polarization with the naked eye: characterization of human polarization sensitivity.

Like many animals, humans are sensitive to the polarization of light. We can detect the angle of polarization using an entoptic phenomenon called Haidinger's brushes, which is mediated by dichroic carotenoids in the macula lutea. While previous studies have characterized the spectral sensitivity of Haidinger's brushes, other aspects remain unexplored. We developed a novel methodology for presenting gratings in polarization-only contrast at varying degrees of polarization in order to measure the lower limits of human polarized light detection. Participants were, on average, able to perform the task down to a threshold of 56%, with some able to go as low as 23%. This makes humans the most sensitive vertebrate tested to date. Additionally, we quantified a nonlinear relationship between presented and perceived polarization angle when an observer is presented with a rotatable polarized light field. This result confirms a previous theoretical prediction of how uniaxial corneal birefringence impacts the perception of Haidinger's brushes. The rotational dynamics of Haidinger's brushes were then used to calculate corneal retardance.We suggest that psychophysical experiments, based upon the perception of polarized light, are amenable to the production of affordable technologies for self-assessment and longitudinal monitoring of visual dysfunctions such as age-related macular degeneration.

Out of the blue: the evolution of horizontally polarized signals in Haptosquilla (Crustacea, Stomatopoda, Protosquillidae).

The polarization of light provides information that is used by many animals for a number of different visually guided behaviours. Several marine species, such as stomatopod crustaceans and cephalopod molluscs, communicate using visual signals that contain polarized information, content that is often part of a more complex multi-dimensional visual signal. In this work, we investigate the evolution of polarized signals in species of Haptosquilla, a widespread genus of stomatopod, as well as related protosquillids. We present evidence for a pre-existing bias towards horizontally polarized signal content and demonstrate that the properties of the polarization vision system in these animals increase the signal-to-noise ratio of the signal. Combining these results with the increase in efficacy that polarization provides over intensity and hue in a shallow marine environment, we propose a joint framework for the evolution of the polarized form of these complex signals based on both efficacy-driven (proximate) and content-driven (ultimate) selection pressures.

Corneal microprojections in coleoid cephalopods.

The cornea is the first optical element in the path of light entering the eye, playing a role in image formation and protection. Corneas of vertebrate simple camera-type eyes possess microprojections on the outer surface in the form of microridges, microvilli, and microplicae. Corneas of invertebrates, which have simple or compound eyes, or both, may be featureless or may possess microprojections in the form of nipples. It was previously unknown whether cephalopods (invertebrates with camera-type eyes like vertebrates) possess corneal microprojections and, if so, of what form. Using scanning electron microscopy, we examined corneas of a range of cephalopods and discovered nipple-like microprojections in all species. In some species, nipples were like those described on arthropod compound eyes, with a regular hexagonal arrangement and sizes ranging from 75 to 103 nm in diameter. In others, nipples were nodule shaped and irregularly distributed. Although terrestrial invertebrate nipples create an antireflective surface that may play a role in camouflage, no such optical function can be assigned to cephalopod nipples due to refractive index similarities of corneas and water. Their function may be to increase surface-area-to-volume ratio of corneal epithelial cells to increase nutrient, gas, and metabolite exchange, and/or stabilize the corneal mucous layer, as proposed for corneal microprojections of vertebrates.

High e-vector acuity in the polarisation vision system of the fiddler crab Uca vomeris.

Polarisation vision is used by a variety of species in many important tasks, including navigation and orientation (e.g. desert ant), communication and signalling (e.g. stomatopod crustaceans), and as a possible substitute for colour vision (e.g. cephalopod molluscs). Fiddler crabs are thought to possess the anatomical structures necessary to detect polarised light, and occupy environments rich in polarisation cues. Yet little is known about the capabilities of their polarisation sense. A modified polarisation-only liquid crystal display and a spherical rotating treadmill were combined to test the responses of fiddler crabs to moving polarisation stimuli. The species Uca vomeris was found to be highly sensitive to polarised light and detected stimuli differing in e-vector angle by as little as 3.2 deg. This represents the most acute behavioural sensitivity to polarised light yet measured for a crustacean. The occurrence of null points in their discrimination curve indicates that this species employs an orthogonal (horizontal/vertical) receptor array for the detection of polarised light.

The retinal wholemount technique: a window to understanding the brain and behaviour.

The accessibility of the vertebrate retina has provided the opportunity to assess various parameters of the visual abilities of a range of species. This thin but complex extension of the brain achieves a large proportion of the necessary visual processing of an optical image before information is delivered to the brain as neural impulses. Studies of the retina as a wholemount or a flattened sheet of neural tissue are abundant due to the large amount of information that can be analysed, as follows: the level of summation or convergence; the coverage, stratification and potential sites of synaptic connections; the spatial resolving power; the arrangement of neuronal arrays or mosaics; electrophysiological access for the recording of responses to visual stimuli; the spatial arrangement of cell dendritic fields; location of retinal 'blind spots' (optic nerve, falciform process and pecten); topographic differences in retinal cell sampling; spectral filters, and reflective structures. The present study examines all aspects of the wholemount technique, including enucleation, fixation, retinal extraction, flattening, staining, visualization of labelled cells and stereological mapping of cell density. Uniquely, it highlights the crucial technical and often species-specific differences encountered when examining a range of vertebrate taxa (fishes, reptiles, birds and mammals). This broad comparative approach will enable future studies to overcome technical difficulties, thus permitting larger conceptual questions to be posed regarding the diversity of visual tasks across phylogenetic boundaries.

Seeing polarization of light with the naked eye.

Many readers may know that scores of animal species sense the polarization of light for purposes including navigation, predation, and communication1. It is commonly thought that humans lack any sensitivity to polarization of light (e.g., Morehouse2). We hope to convince you otherwise by describing three examples where humans can detect polarization of light with the naked eye, by showing you how to see it yourself, and by describing its uses.

Polarization perception in humans: on the origin of and relationship between Maxwell's spot and Haidinger's brushes.

Under specific conditions of illumination and polarization, differential absorption of light by macular pigments is perceived as the entoptic phenomena of Maxwell's spot (MS) or Haidinger's brushes (HB). To simulate MS and HB, an existing computational model of polarization-dependent properties of the human macula was extended by incorporating neuronal adaptation to stabilized retinal images. The model predicted that polarized light modifies the appearance of MS leading to the perception of a novel phenomenon. The model also predicted a correlation between the observed diameters of MS and HB. Predictions were tested psychophysically in human observers, whose measured differences in the diameters of each entoptic phenomenon generated with depolarized and linearly polarized light were consistent with the model simulations. These findings support a common origin of each phenomenon, and are relevant to the clinical use of polarization stimuli in detecting and monitoring human eye disorders, including macular degeneration. We conclude: (i) MS and HB both result from differential light absorption through a radial diattenuator, compatible with the arrangement of macular pigments in Henle fibres; (ii) the morphology of MS is dependent on the degree of linear polarization; (iii) perceptual differences between MS and HB result from different states of neural adaptation.

Red fluorescence of the triplefin Tripterygion delaisi is increasingly visible against background light with increasing depth.

The light environment in water bodies changes with depth due to the absorption of short and long wavelengths. Below 10 m depth, red wavelengths are almost completely absent rendering any red-reflecting animal dark and achromatic. However, fluorescence may produce red coloration even when red light is not available for reflection. A large number of marine taxa including over 270 fish species are known to produce red fluorescence, yet it is unclear under which natural light environment fluorescence contributes perceptively to their colours. To address this question we: (i) characterized the visual system of Tripterygion delaisi, which possesses fluorescent irides, (ii) separated the colour of the irides into its reflectance and fluorescence components and (iii) combined these data with field measurements of the ambient light environment to calculate depth-dependent perceptual chromatic and achromatic contrasts using visual modelling. We found that triplefins have cones with at least three different spectral sensitivities, including differences between the two members of the double cones, giving them the potential for trichromatic colour vision. We also show that fluorescence contributes increasingly to the radiance of the irides with increasing depth. Our results support the potential functionality of red fluorescence, including communicative roles such as species and sex identity, and non-communicative roles such as camouflage.

Dynamic polarization vision in mantis shrimps.

Gaze stabilization is an almost ubiquitous animal behaviour, one that is required to see the world clearly and without blur. Stomatopods, however, only fix their eyes on scenes or objects of interest occasionally. Almost uniquely among animals they explore their visual environment with a series pitch, yaw and torsional (roll) rotations of their eyes, where each eye may also move largely independently of the other. In this work, we demonstrate that the torsional rotations are used to actively enhance their ability to see the polarization of light. Both Gonodactylus smithii and Odontodactylus scyllarus rotate their eyes to align particular photoreceptors relative to the angle of polarization of a linearly polarized visual stimulus, thereby maximizing the polarization contrast between an object of interest and its background. This is the first documented example of any animal displaying dynamic polarization vision, in which the polarization information is actively maximized through rotational eye movements.

Target Detection Is Enhanced by Polarization Vision in a Fiddler Crab.

We are constantly surprised by the ability of relatively simple animals to perform precise visually guided movements within complex visual scenes, often using eyes with limited resolution. Exceptional examples include the capture of airborne prey by dragonflies, the learning flights of bees and wasps, and the tracking of conspecifics by crabs on intertidal mudflats. Most studies have focused on how animals do this using sensitivity to intensity or color. However, it is increasingly evident that a third ability, polarization vision, may contribute to such tasks. In many insects, polarization-sensitive photoreceptors are confined within an area of the eye known as the dorsal rim, which detects the polarized sky pattern specifically for navigation. However, some animals, including fiddler crabs, are sensitive to the polarization of light across the majority of their image-forming eyes, potentially allowing them to use polarization information to increase perceived contrast for general visual tasks. Investigations into the use of polarization image-parsing by animals have largely been confined to laboratory settings under artificial lighting. This approach can occasionally mislead if the lighting conditions are different from natural. This study presents the first behavioral evidence from the natural context for a function of polarization image parsing. Using experimental manipulations in wild populations of the fiddler crab Uca stenodactylus, we provide evidence that these animals use their polarization vision to enhance contrast in their visual environment, thereby increasing their ability to detect and respond to objects on the mudflat surface.

Cyp27c1 Red-Shifts the Spectral Sensitivity of Photoreceptors by Converting Vitamin A1 into A2.

Some vertebrate species have evolved means of extending their visual sensitivity beyond the range of human vision. One mechanism of enhancing sensitivity to long-wavelength light is to replace the 11-cis retinal chromophore in photopigments with 11-cis 3,4-didehydroretinal. Despite over a century of research on this topic, the enzymatic basis of this perceptual switch remains unknown. Here, we show that a cytochrome P450 family member, Cyp27c1, mediates this switch by converting vitamin A1 (the precursor of 11-cis retinal) into vitamin A2 (the precursor of 11-cis 3,4-didehydroretinal). Knockout of cyp27c1 in zebrafish abrogates production of vitamin A2, eliminating the animal's ability to red-shift its photoreceptor spectral sensitivity and reducing its ability to see and respond to near-infrared light. Thus, the expression of a single enzyme mediates dynamic spectral tuning of the entire visual system by controlling the balance of vitamin A1 and A2 in the eye.

A fish eye out of water: epithelial surface projections on aerial and aquatic corneas of the 'four-eyed fish' Anableps anableps.

BACKGROUND: Vertebrate corneas feature a variety of microprojections, to which a tear film adheres. These microprojections are formed by folds in epithelial cell membranes, which increase surface area, stabilise the tear film and enhance movement of nutritional and waste products across cell membranes. Differences in corneal microprojections among vertebrates have been correlated with habitat and differ markedly between terrestrial and aquatic species. METHODS: This study investigated epithelial microprojections of both the aerial (dorsal) and aquatic (ventral) corneal surfaces of the 'four-eyed fish' Anableps anableps using scanning electron microscopy. RESULTS: The central region of the dorsal cornea, which projects above the water, had a density of 16,387 ± 3,995 cells per mm(2) , while the central region of the ventral cornea (underwater) had a density of 22,428 ± 6,387 cells per mm(2), a difference that suggests an environmental adaptation along the two visual axes. Both corneal surfaces were found to possess microridges rather than microvilli or microplicae characteristic of terrestrial/aerial vertebrates. Microridges were 142 ± 9 nm wide and did not differ (p = 0.757) between dorsal and ventral corneas. Microridges were consistently separated by a distance of 369 ± 9 nm across both corneas. CONCLUSION: Dorsal-ventral differences in corneal epithelial cell density in Anableps anableps suggest a difference in osmotic pressure of the two corneas. The modest differences in the microprojections indicate that the need to secure the tear film underlying each optical axis is of prime importance, due to the likelihood that a persistent layer of water normally covers both dorsal and ventral corneal surfaces and that maintaining a transparent optical pathway for vision is critical for a species prone to predation from both above and below the water's surface.

Behavioural relevance of polarization sensitivity as a target detection mechanism in cephalopods and fishes.

Aquatic habitats are rich in polarized patterns that could provide valuable information about the environment to an animal with a visual system sensitive to polarization of light. Both cephalopods and fishes have been shown to behaviourally respond to polarized light cues, suggesting that polarization sensitivity (PS) may play a role in improving target detection and/or navigation/orientation. However, while there is general agreement concerning the presence of PS in cephalopods and some fish species, its functional significance remains uncertain. Testing the role of PS in predator or prey detection seems an excellent paradigm with which to study the contribution of PS to the sensory assets of both groups, because such behaviours are critical to survival. We developed a novel experimental set-up to deliver computer-generated, controllable, polarized stimuli to free-swimming cephalopods and fishes with which we tested the behavioural relevance of PS using stimuli that evoke innate responses (such as an escape response from a looming stimulus and a pursuing behaviour of a small prey-like stimulus). We report consistent responses of cephalopods to looming stimuli presented in polarization and luminance contrast; however, none of the fishes tested responded to either the looming or the prey-like stimuli when presented in polarization contrast.