Polarization Vision Research Articles

Insect Responses to Linearly Polarized Reflections: Orphan Behaviors Without Neural Circuits.

The e-vector orientation of linearly polarized light represents an important visual stimulus for many insects. Especially the detection of polarized skylight by many navigating insect species is known to improve their orientation skills. While great progress has been made towards describing both the anatomy and function of neural circuit elements mediating behaviors related to navigation, relatively little is known about how insects perceive non-celestial polarized light stimuli, like reflections off water, leaves, or shiny body surfaces. Work on different species suggests that these behaviors are not mediated by the “Dorsal Rim Area” (DRA), a specialized region in the dorsal periphery of the adult compound eye, where ommatidia contain highly polarization-sensitive photoreceptor cells whose receptive fields point towards the sky. So far, only few cases of polarization-sensitive photoreceptors have been described in the ventral periphery of the insect retina. Furthermore, both the structure and function of those neural circuits connecting to these photoreceptor inputs remain largely uncharacterized. Here we review the known data on non-celestial polarization vision from different insect species (dragonflies, butterflies, beetles, bugs and flies) and present three well-characterized examples for functionally specialized non-DRA detectors from different insects that seem perfectly suited for mediating such behaviors. Finally, using recent advances from circuit dissection in Drosophila melanogaster, we discuss what types of potential candidate neurons could be involved in forming the underlying neural circuitry mediating non-celestial polarization vision.

The Fly Sensitizing Pigment Enhances UV Spectral Sensitivity While Preventing Polarization-Induced Artifacts.

Microvillar photoreceptors are intrinsically capable of detecting the orientation of e-vector of linearly polarized light. They provide most invertebrates with an additional sensory channel to detect important features of their visual environment. However, polarization sensitivity (PS) of photoreceptors may lead to the detection of polarization-induced false colors and intensity contrasts. Most insect photoreceptors are thus adapted to have minimal PS. Flies have twisted rhabdomeres with microvilli rotated along the length of the ommatidia to reduce PS. The additional UV-absorbing sensitizing pigment on their opsin minimizes PS in the ultraviolet. We recorded voltage from Drosophila photoreceptors R1–6 to measure the spectral dependence of PS and found that PS in the UV is invariably negligible but can be substantial above 400 nm. Using modeling, we demonstrate that in R1–6 without the sensitizing pigment, PS in the UV (PSUV) would exceed PS in the visible part of the spectrum (PSVIS) by a factor PSUV/PSVIS = 1.2–1.8, as lower absorption of Rh1 rhodopsin reduces self-screening. We use polarimetric imaging of objects relevant to fly polarization vision to show that their degree of polarization outdoors is highest in the short-wavelength part of the spectrum. Thus, under natural illumination, the sensitizing pigment in R1–6 renders even those cells with high PS in the visible part unsuitable for proper polarization vision. We assume that fly ventral polarization vision can be mediated by R7 alone, with R1–6 serving as an unpolarized reference channel.

Polarized object detection in crabs: a two-channel system.

Many animal species take advantage of polarization vision for vital tasks such as orientation, communication and contrast enhancement. Previous studies have suggested that decapod crustaceans use a two-channel polarization system for contrast enhancement. Here, we characterize the polarization contrast sensitivity in a grapsid crab. We estimated the polarization contrast sensitivity of the animals by quantifying both their escape response and changes in heart rate when presented with polarized motion stimuli. The motion stimulus consisted of an expanding disk with an 82deg polarization difference between the object and the background. More than 90% of animals responded by freezing or trying to avoid the polarized stimulus. In addition, we co-rotated the electric vector (e-vector) orientation of the light from the object and background by increments of 30deg and found that the animals' escape response varied periodically with a 90deg period. Maximum escape responses were obtained for object and background e-vectors near the vertical and horizontal orientations. Changes in cardiac response showed parallel results but also a minimum response when e-vectors of object and background were shifted by 45deg with respect to the maxima. These results are consistent with an orthogonal receptor arrangement for the detection of polarized light, in which two channels are aligned with the vertical and horizontal orientations. It has been hypothesized that animals with object-based polarization vision rely on a two-channel detection system analogous to that of color processing in dichromats. Our results, obtained by systematically varying the e-vectors of object and background, provide strong empirical support for this theoretical model of polarized object detection.

Two visual systems in one eyestalk: The unusual optic lobe metamorphosis in the stomatopod Alima pacifica.

The compound eyes of adult stomatopod crustaceans have two to six ommatidial rows at the equator, called the midband, that are often specialized for color and polarization vision. Beneath the retina, this midband specialization is represented as enlarged optic lobe lamina cartridges and a hernia-like expansion in the medulla. We studied how the optic lobe transforms from the larvae, which possess typical crustacean larval compound eyes without a specialized midband, through metamorphosis into the adults with the midband in a two midband-row species Alima pacifica. Using histological staining, immunolabeling, and 3D reconstruction, we show that the last-stage stomatopod larvae possess double-retina eyes, in which the developing adult visual system forms adjacent to, but separate from, the larval visual system. Beneath the two retinas, the optic lobe also contains two sets of optic neuropils, comprising of a larval lamina, medulla, and lobula, as well as an adult lamina, medulla, and lobula. The larval eye and all larval optic neuropils degenerate and disappear approximately a week after metamorphosis. In stomatopods, the unique adult visual system and all optic neuropils develop alongside the larval system in the eyestalk of last-stage larvae, where two visual systems and two independent visual processing pathways coexist. © 2017 Wiley Periodicals, Inc. Develop Neurobiol 78: 3-14, 2018.

Why do horseflies need polarization vision for host detection? Polarization helps tabanid flies to select sunlit dark host animals from the dark patches of the visual environment.

Horseflies (Tabanidae) are polarotactic, being attracted to linearly polarized light when searching for water or host animals. Although it is well known that horseflies prefer sunlit dark and strongly polarizing hosts, the reason for this preference is unknown. According to our hypothesis, horseflies use their polarization sensitivity to look for targets with higher degrees of polarization in their optical environment, which as a result facilitates detection of sunlit dark host animals. In this work, we tested this hypothesis. Using imaging polarimetry, we measured the reflection–polarization patterns of a dark host model and a living black cow under various illumination conditions and with different vegetation backgrounds. We focused on the intensity and degree of polarization of light originating from dark patches of vegetation and the dark model/cow. We compared the chances of successful host selection based on either intensity or degree of polarization of the target and the combination of these two parameters. We show that the use of polarization information considerably increases the effectiveness of visual detection of dark host animals even in front of sunny–shady–patchy vegetation. Differentiation between a weakly polarizing, shady (dark) vegetation region and a sunlit, highly polarizing dark host animal increases the efficiency of host search by horseflies.

Bee cognition

Maeterlinck did not mean to suggest that honeybees rival humans in intelligence - rather he saw in the bee a qualitatively different form of intelligence, tailored to the challenges of a profoundly different kind of society and lifestyle. Insects are strange "aliens from inner space", with sensory and cognitive worlds wholly different from our own. The 19th century discovery that ants can detect ultraviolet light triggered a golden age in the exploration of the diversity of sensory systems of insects (and indeed other animals), identifying such abilities as magnetic compasses, electrosensitivity, polarization vision, and peculiar locations for sense organs such as the infrared sensors on the abdomens of some beetles or photoreceptors on the genitalia of some butterflies. Could insect minds be equally strange and diverse?

A vertebrate retina with segregated colour and polarization sensitivity.

Besides colour and intensity, some invertebrates are able to independently detect the polarization of light. Among vertebrates, such separation of visual modalities has only been hypothesized for some species of anchovies whose cone photoreceptors have unusual ultrastructure that varies with retinal location. Here, I tested this hypothesis by performing physiological experiments of colour and polarization discrimination using the northern anchovy, Engraulis mordax Optic nerve recordings showed that the ventro-temporal (VT), but not the ventro-nasal (VN), retina was polarization sensitive, and this coincided with the exclusive presence of polarization-sensitive photoreceptors in the VT retina. Spectral (colour) sensitivity recordings from the VN retina indicated the contribution of two spectral cone mechanisms to the optic nerve response, whereas only one contributed to the VT retina. This was supported by the presence of only one visual pigment in the VT retina and two in the VN retina, suggesting that only the VN retina was associated with colour sensitivity. Behavioural tests further demonstrated that anchovies could discriminate colour and the polarization of light using the ventral retina. Thus, in analogy with the visual system of some invertebrates, the northern anchovy has a retina with segregated retinal pathways for colour and polarization vision.

A Novel Display System Reveals Anisotropic Polarization Perception in the Motion Vision of the Butterfly Papilio xuthus.

While the linear polarization of light is virtually invisible to humans, many invertebrates' eyes can detect it. How this information is processed in the nervous system, and what behavioral function it serves, are in many cases unclear. One reason for this is the technical difficulty involved in presenting images or video containing polarization contrast, particularly if intensity and/or color contrast is also required. In this primarily methods-focused article, we present a novel technique based on projecting video through a synchronously rotating linear polarizer. This approach allows the intensity, angle of polarization, degree of linear polarization, and potentially also color of individual pixels to be controlled independently. We characterize the performance of our system, and then use it to investigate the relationship between polarization and motion vision in the swallowtail butterfly Papilio xuthus. Although this animal has photoreceptors sensitive to four different polarization angles, we find that its motion vision cannot distinguish between diagonally-polarized and unpolarized light. Furthermore, it responds more strongly to vertically-polarized moving objects than horizontally-polarized ones. This implies that Papilio's polarization-based motion detection employs either an unbalanced two-channel (dipolatic) opponent architecture, or possibly a single-channel (monopolatic) scheme without opponent mechanisms.

Bionic Orientation and Visual Enhancement With a Novel Polarization Camera

The remarkable polarization vision of animals provides a significant inspiration for robotic navigation and visual enhancement, as polarization pattern provides additional information besides spectral signatures. A novel bio-inspired polarization camera is proposed in this paper, which can realize real-time image-based polarization measurement. The composition of the system is described and the optimal estimation of the polarization state is derived based on the least square algorithm. This paper concentrates particularly on the camera orientation algorithms and visual enhancement methods with it. To estimate the camera’s heading angle with the skylight polarization pattern, the sun vector is established as an optimization problem of finding the minimum eigenvector. The solar meridian is also estimated from the degree of polarization pattern by detecting reflectional symmetry axes. The result shows that the measured polarization patterns are very close to the theory. The maximum orientation error of the proposed method based on angle of polarization is about 0.5°. The average error is 0.012° with standard deviation of 0.28°. Thus, the novel polarization camera could be used as sun compass. When observing scenes in distance, the polarization camera is used to decouple the airlight from the object radiance, which results in much better contrast. More importantly, the polarization information is helpful for scene identification and object detection. The result also shows that the polarization camera can reasonably cope with the semi-reflection problem.

Visual sensitivity and spatial resolution of the planktivorous fish, Atherinomorus forskalii (Atherinidae; Rüppell, 1838), to a polarized grating

Polarized light detection has been documented in only a small number of fish species. The benefit of polarization vision for fish is not fully understood, nor is the transduction mechanism that underlies it. Past studies proposed that one possible advantage of polarization vision is that it enhances the contrast of zooplankton targets by breaking their transparency. Here, we used an optomotor apparatus to test the responses of the planktivorous Hardyhead silverside fish Atherinomorus forskalii (Atherinidae) to vertical unpolarized (intensity) and polarized gratings. We also tested and compared the spatial and temporal resolutions of A. forskalii in the intensity and polarization domains. A. forskalii responded to the polarization pattern, but only under illumination that included ultraviolet-blue (λ>380nm) wavelengths. The spatial resolution of A. forskalii was measured as a minimum separable angle of 0.57° (a 1-mm prey viewed from 100-mm distance). The temporal resolution to unpolarized vs. polarized gratings was constant, at 33 and 10Hz respectively at most of the stripe widths tested. At the smallest stripe width tested (1mm=the minimal separable angle), which correlates with the size of prey typically consumed by these fish, the temporal resolution to the polarized grating increased to 42Hz. We conclude that A. forskalii is polarization sensitive, may use polarization vision to improve detection of its planktonic prey, and that polarization may be perceived by the fish via a separate visual pathway than intensity.

Can invertebrates see the e-vector of polarization as a separate modality of light?

ABSTRACTThe visual world is rich in linearly polarized light stimuli, which are hidden from the human eye. But many invertebrate species make use of polarized light as a source of valuable visual information. However, exploiting light polarization does not necessarily imply that the electric (e)-vector orientation of polarized light can be perceived as a separate modality of light. In this Review, I address the question of whether invertebrates can detect specific e-vector orientations in a manner similar to that of humans perceiving spectral stimuli as specific hues. To analyze e-vector orientation, the signals of at least three polarization-sensitive sensors (analyzer channels) with different e-vector tuning axes must be compared. The object-based, imaging polarization vision systems of cephalopods and crustaceans, as well as the water-surface detectors of flying backswimmers, use just two analyzer channels. Although this excludes the perception of specific e-vector orientations, a two-channel system does provide a coarse, categoric analysis of polarized light stimuli, comparable to the limited color sense of dichromatic, ‘color-blind’ humans. The celestial compass of insects employs three or more analyzer channels. However, that compass is multimodal, i.e. e-vector information merges with directional information from other celestial cues, such as the solar azimuth and the spectral gradient in the sky, masking e-vector information. It seems that invertebrate organisms take no interest in the polarization details of visual stimuli, but polarization vision grants more practical benefits, such as improved object detection and visual communication for cephalopods and crustaceans, compass readings to traveling insects, or the alert ‘water below!’ to water-seeking bugs.

Photoreceptor spectral tuning by colorful, multilayered facet lenses in long-legged fly eyes (Dolichopodidae)

The facet lenses of the compound eyes of long-legged flies (Dolichopodidae) feature a striking, interlaced coloration pattern, existing of alternating rows of green-yellow and orange-red reflecting facets, due to dielectric multilayers located distally in the facet lenses (Bernard and Miller. Invest Ophthalmol 7:416–434 (1968). We investigated this phenomenon in the dolichopodid Dolichopus nitidus by applying microspectrophotometry, electron microscopy and optical modeling. The measured narrow-band reflectance spectra, peaking at ~540 and ~590 nm with bandwidth ~105 nm, are well explained by a refractive index oscillating sinusoidally in six periods around a mean value of about 1.44 with amplitude 0.6. The facet lens reflectance spectra are associated with a spectrally restricted, reduced transmittance, which causes modified spectral sensitivities of the underlying photoreceptors. Based on the modeling and electroretinography of the dolichopodid Condylostylus japonicus we conjecture that the green and orange facets narrow the spectral bandwidths of blue and green central photoreceptors, respectively, thus possibly improving color and/or polarization vision.

The copepod Calanus spp. (Calanidae) is repelled by polarized light.

Both attraction and repulsion from linearly polarized light have been observed in zooplankton. A dichotomous choice experiment, consisting of plankton light traps deployed in natural waters at a depth of 30 m that projected either polarized or unpolarized light of the same intensity, was used to test the hypothesis that the North Atlantic copepod, Calanus spp., is linearly polarotactic. In addition, the transparency of these copepods, as they might be seen by polarization insensitive vs. sensitive visual systems, was measured. Calanus spp. exhibited negative polarotaxis with a preference ratio of 1.9:1. Their transparency decreased from 80% to 20% to 30% in the unpolarized, partially polarized, and electric (e-) vector orientation domains respectively - that is, these copepods would appear opaque and conspicuous to a polarization-sensitive viewer looking at them under conditions rich in polarized light. Since the only difference between the two plankton traps was the polarization cue, we conclude that Calanus spp. are polarization sensitive and exhibit negative polarotaxis at low light intensities (albeit well within the sensitivity range reported for copepods). We hypothesize that Calanus spp. can use polarization vision to reduce their risk of predation by polarization-sensitive predators and suggest that this be tested in future experiments.

A Bionic Polarization Navigation Sensor and Its Calibration Method.

The polarization patterns of skylight which arise due to the scattering of sunlight in the atmosphere can be used by many insects for deriving compass information. Inspired by insects’ polarized light compass, scientists have developed a new kind of navigation method. One of the key techniques in this method is the polarimetric sensor which is used to acquire direction information from skylight. In this paper, a polarization navigation sensor is proposed which imitates the working principles of the polarization vision systems of insects. We introduce the optical design and mathematical model of the sensor. In addition, a calibration method based on variable substitution and non-linear curve fitting is proposed. The results obtained from the outdoor experiments provide support for the feasibility and precision of the sensor. The sensor’s signal processing can be well described using our mathematical model. A relatively high degree of accuracy in polarization measurement can be obtained without any error compensation.

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.

Anatomical Reconstruction and Functional Imaging Reveal an Ordered Array of Skylight Polarization Detectors in Drosophila.

Many insects exploit skylight polarization as a compass cue for orientation and navigation. In the fruit fly, Drosophila melanogaster, photoreceptors R7 and R8 in the dorsal rim area (DRA) of the compound eye are specialized to detect the electric vector (e-vector) of linearly polarized light. These photoreceptors are arranged in stacked pairs with identical fields of view and spectral sensitivities, but mutually orthogonal microvillar orientations. As in larger flies, we found that the microvillar orientation of the distal photoreceptor R7 changes in a fan-like fashion along the DRA. This anatomical arrangement suggests that the DRA constitutes a detector for skylight polarization, in which different e-vectors maximally excite different positions in the array. To test our hypothesis, we measured responses to polarized light of varying e-vector angles in the terminals of R7/8 cells using genetically encoded calcium indicators. Our data confirm a progression of preferred e-vector angles from anterior to posterior in the DRA, and a strict orthogonality between the e-vector preferences of paired R7/8 cells. We observed decreased activity in photoreceptors in response to flashes of light polarized orthogonally to their preferred e-vector angle, suggesting reciprocal inhibition between photoreceptors in the same medullar column, which may serve to increase polarization contrast. Together, our results indicate that the polarization-vision system relies on a spatial map of preferred e-vector angles at the earliest stage of sensory processing. The fly's visual system is an influential model system for studying neural computation, and much is known about its anatomy, physiology, and development. The circuits underlying motion processing have received the most attention, but researchers are increasingly investigating other functions, such as color perception and object recognition. In this work, we investigate the early neural processing of a somewhat exotic sense, called polarization vision. Because skylight is polarized in an orientation that is rigidly determined by the position of the sun, this cue provides compass information. Behavioral experiments have shown that many species use the polarization pattern in the sky to direct locomotion. Here we describe the input stage of the fly's polarization-vision system.

仿生偏振视觉定位定向机理与实验

仿生偏振视觉定位定向机理与实验

Multiband Polarization Imaging

Multiband polarization imaging is an emerging sensing method that enables simultaneous acquisition of multiband spectral and multiangle polarization information of an object of interest in the scene. Spectral signatures of the light reflected from a target reveal the characteristics of the material composing the target while polarized light provides useful information on the surface features such as light scattering and specular reflection. In multiband spectral imaging, combined spectral and polarization information offers a comprehensive representation of an object utilizing complementary spectral and polarization information in visual sensing. Multiband polarization imaging has demonstrated a potential in the recognition of targets in challenging operating environments such as low-contrast and hazy conditions. This paper presents the concept and recent advances of multiband polarization imaging techniques, in particular, a bioinspired multiband polarization vision system. Applications of multiband polarization imaging in various fields include atmospheric observation, object detection and classification, medical diagnostics, surveillance, and 3D object reconstruction.

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.

Circularly Polarized Light as a Communication Signal in Mantis Shrimps

Animals that communicate using conspicuous body patterns face a trade-off between desired detection by intended receivers and undesired detection from eavesdropping predators, prey, rivals, or parasites. In some cases, this trade-off favors the evolution of signals that are both hidden from predators and visible to conspecifics. Animals may produce covert signals using a property of light that is invisible to those that they wish to evade, allowing them to hide in plain sight (e.g., dragonfish can see their own, otherwise rare, red bioluminescence). The use of the polarization of light is a good example of a potentially covert communication channel, as very few vertebrates are known to use polarization for object-based vision. However, even these patterns are vulnerable to eavesdroppers, as sensitivity to the linearly polarized component of light is widespread among invertebrates due to their intrinsically polarization sensitive photoreceptors. Stomatopod crustaceans appear to have gone one step further in this arms race and have evolved a sensitivity to the circular polarization of light, along with body patterns producing it. However, to date we have no direct evidence that any of these marine crustaceans use this modality to communicate with conspecifics. We therefore investigated circular polarization vision of the mantis shrimp Gonodactylaceus falcatus and demonstrate that (1) the species produces strongly circularly polarized body patterns, (2) they discriminate the circular polarization of light, and (3) that they use circular polarization information to avoid occupied burrows when seeking a refuge.