Polarization-sensitive Photoreceptors Research Articles

Stable flies sense and behaviorally respond to the polarization of light

Insects use their polarization-sensitive photoreceptors in a variety of ecological contexts including host-foraging. Here, we investigated the effect of polarized light on host foraging by the blood-feeding stable fly, Stomoxys calcitrans, a pest of livestock. Electroretinogram recordings with chromatic adaptation demonstrated that the spectral sensitivity of stable flies resembles that of other calyptrate flies. Histological studies of the flies' compound eye revealed differences in microvillar arrangement of ommatidial types, assumed to be pale and yellow, with the yellow R7 and pale R8 photoreceptors having the greatest polarization sensitivity. In behavioural experiments, stable flies preferred to alight on horizontally polarized stimuli with a high degree of linear polarization. This preferential response disappeared when either ultraviolet (UV) or human-visible wavelengths were omitted from light stimuli. Removing specific wavelength bands further revealed that the combination of UV (330-400nm) and blue (400-525nm) wavelength bands was sufficient to enable polarized light discrimination by flies. These findings enhance our understanding of polarization vision and foraging behavior among hematophagous insects and should inform future trap designs.

Neural processing of linearly and circularly polarized light signal in a mantis shrimp Haptosquilla pulchella.

Stomatopods, or mantis shrimp, are the only animal group known to possess circular polarization vision along with linear polarization vision. By using the rhabdomere of a distally located photoreceptor as a wave retarder, the eyes of mantis shrimp are able to convert circularly polarized light into linearly polarized light. As a result, their circular polarization vision is based on the linearly polarized light-sensitive photoreceptors commonly found in many arthropods. To investigate how linearly and circularly polarized light signals might be processed, we presented a dynamic polarized light stimulus while recording from photoreceptors or lamina neurons in intact mantis shrimp Haptosquilla pulchella The results indicate that all the circularly polarized light-sensitive photoreceptors also showed differential responses to the changing e-vector angle of linearly polarized light. When stimulated with linearly polarized light of varying e-vector angle, most photoreceptors produced a concordant sinusoidal response. In contrast, some lamina neurons doubled the response frequency in reacting to linearly polarized light. These responses resembled a rectified sum of two-channel linear polarization-sensitive photoreceptors, indicating that polarization visual signals are processed at or before the first optic lobe. Noticeably, within the lamina, there was one type of neuron that showed a steady depolarization response to all stimuli except right-handed circularly polarized light. Together, our findings suggest that, between the photoreceptors and lamina neurons, linearly and circularly polarized light may be processed in parallel and differently from one another.

Cellular and synaptic adaptations of neural circuits processing skylight polarization in the fly.

Specialized ommatidia harboring polarization-sensitive photoreceptors exist in the 'dorsal rim area' (DRA) of virtually all insects. Although downstream elements have been described both anatomically and physiologically throughout the optic lobes and the central brain of different species, little is known about their cellular and synaptic adaptations and how these shape their functional role in polarization vision. We have previously shown that in the DRA of Drosophila melanogaster, two distinct types of modality-specific 'distal medulla' cell types (Dm-DRA1 and Dm-DRA2) are post-synaptic to long visual fiber photoreceptors R7 and R8, respectively. Here we describe additional neuronal elements in the medulla neuropil that manifest modality-specific differences in the DRA region, including DRA-specific neuronal morphology, as well as differences in the structure of pre- or post-synaptic membranes. Furthermore, we show that certain cell types (medulla tangential cells and octopaminergic neuromodulatory cells) specifically avoid contacts with polarization-sensitive photoreceptors. Finally, while certain transmedullary cells are specifically absent from DRA medulla columns, other subtypes show specific wiring differences while still connecting the DRA to the lobula complex, as has previously been described in larger insects. This hints towards a complex circuit architecture with more than one pathway connecting polarization-sensitive DRA photoreceptors with the central brain.

Horsefly object-directed polarotaxis is mediated by a stochastically distributed ommatidial subtype in the ventral retina

The ventral compound eye of many insects contains polarization-sensitive photoreceptors, but little is known about how they are integrated into visual functions. In female horseflies, polarized reflections from animal fur are a key stimulus for host detection. To understand how polarization vision is mediated by the ventral compound eye, we investigated the band-eyed brown horsefly Tabanus bromius using anatomical, physiological, and behavioral approaches. Serial electron microscopic sectioning of the retina and single-cell recordings were used to determine the spectral and polarization sensitivity (PS) of photoreceptors. We found 2 stochastically distributed subtypes of ommatidia, analogous to pale and yellow of other flies. Importantly, the pale analog contains an orthogonal analyzer receptor pair with high PS, formed by an ultraviolet (UV)-sensitive R7 and a UV- and blue-sensitive R8, while the UV-sensitive R7 and green-sensitive R8 in the yellow analog always have low PS. We tested horsefly polarotaxis in the field, using lures with controlled spectral and polarization composition. Polarized reflections without UV and blue components rendered the lures unattractive, while reflections without the green component increased their attractiveness. This is consistent with polarotaxis being guided by a differential signal from polarization analyzers in the pale analogs, and with an inhibitory role of the yellow analogs. Our results reveal how stochastically distributed sensory units with modality-specific division of labor serve as separate and opposing input channels for visual guidance.

Polarization Vision: Targets of Polarization-Sensitive Photoreceptors in the Drosophila Visual System.

Insects can perceive the polarization pattern in the sky and use the information to navigate: a new study has delineated neural circuitry immediately downstream of the polarization detectors in the dorsal rim area of the Drosophila retina, which is devoted to the task of polarization vision.

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.

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.

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.

Genetic Dissection of Photoreceptor Subtype Specification by the Drosophila melanogaster Zinc Finger Proteins Elbow and No ocelli

The elbow/no ocelli (elb/noc) complex of Drosophila melanogaster encodes two paralogs of the evolutionarily conserved NET family of zinc finger proteins. These transcriptional repressors share a conserved domain structure, including a single atypical C2H2 zinc finger. In flies, Elb and Noc are important for the development of legs, eyes and tracheae. Vertebrate NET proteins play an important role in the developing nervous system, and mutations in the homolog ZNF703 human promote luminal breast cancer. However, their interaction with transcriptional regulators is incompletely understood. Here we show that loss of both Elb and Noc causes mis-specification of polarization-sensitive photoreceptors in the ‘dorsal rim area’ (DRA) of the fly retina. This phenotype is identical to the loss of the homeodomain transcription factor Homothorax (Hth)/dMeis. Development of DRA ommatidia and expression of Hth are induced by the Wingless/Wnt pathway. Our data suggest that Elb/Noc genetically interact with Hth, and we identify two conserved domains crucial for this function. Furthermore, we show that Elb/Noc specifically interact with the transcription factor Orthodenticle (Otd)/Otx, a crucial regulator of rhodopsin gene transcription. Interestingly, different Elb/Noc domains are required to antagonize Otd functions in transcriptional activation, versus transcriptional repression. We propose that similar interactions between vertebrate NET proteins and Meis and Otx factors might play a role in development and disease.

Does reflection polarization by plants influence colour perception in insects? Polarimetric measurements applied to a polarization-sensitive model retina of Papilio butterflies.

Using imaging polarimetry, we have measured some typical reflection-polarization patterns of plant surfaces (leaves and flowers) under different illuminations. Using a quantitative model to determine photon absorptions in the weakly polarization-sensitive (PS approximately 2) photoreceptors of Papilio butterflies, we have calculated the influence of reflection polarization on the colours of leaves and flowers perceived by PAPILIO: Compared with a retina containing polarization-blind colour receptors, the colour loci of specularly reflecting and, thus, strongly polarizing areas on a plant are slightly shifted, which could cause the perception of false colours. However, the colour of specularly reflecting surfaces is strongly masked by white glare, which may prevent the perception of polarization-induced hue shifts. Although the perception of polarizational false colours by Papilio butterflies was previously demonstrated with artificial, strongly colour-saturated and totally linearly polarized stimuli, we expect that the weak polarization sensitivity of Papilio photoreceptors hardly influences colour perception under natural conditions.

A specialized dorsal rim area for polarized light detection in the compound eye of the scarab beetle Pachysoma striatum

Many animals have been shown to use the pattern of polarized light in the sky as an optical compass. Specialised photoreceptors are used to analyse this pattern. We here present evidence for an eye design suitable for polarized skylight navigation in the flightless desert scarab Pachysoma striatum. Morphological and electrophysiological studies show that an extensive part of the dorsal eye is equivalent to the dorsal rim area used for polarized light navigation in other insects. A polarization-sensitivity of 12.8 (average) can be recorded from cells sensitive to the ultraviolet spectrum of light. Features commonly known to increase the visual fields of polarization-sensitive photoreceptors, or to decrease their spatial resolution, are not found in the eye of this beetle. We argue that in this insect an optically unspecialised area for polarized light detection allows it not be used exclusively for polarized light navigation.

Spatial integration in polarization-sensitive interneurones of crickets: a survey of evidence, mechanisms and benefits

Many insects exploit the polarization pattern of the sky for compass orientation in navigation or cruising-course control. Polarization-sensitive neurones (POL1-neurones) in the polarization vision pathway of the cricket visual system have wide visual fields of approximately 60 degrees diameter, i.e. these neurones integrate information over a large area of the sky. This results from two different mechanisms. (i) Optical integration; polarization vision is mediated by a group of specialized ommatidia at the dorsal rim of the eye. These ommatidia lack screening pigment, contain a wide rhabdom and have poor lens optics. As a result, the angular sensitivity of the polarization-sensitive photoreceptors is very wide (median approximately 20 degrees ). (ii) Neural integration; each POL1-neurone receives input from a large number of dorsal rim photoreceptors with diverging optical axes. Spatial integration in POL1-neurones acts as a spatial low-pass filter. It improves the quality of the celestial polarization signal by filtering out cloud-induced local disturbances in the polarization pattern and increases sensitivity.

Detectors for polarized skylight in insects: a survey of ommatidial specializations in the dorsal rim area of the compound eye.

Apart from the sun, the polarization pattern of the sky offers insects a reference for visual compass orientation. Using behavioral experiments, it has been shown in a few insect species (field crickets, honey bees, desert ants, and house flies) that the detection of the oscillation plane of polarized skylight is mediated exclusively by a group of specialized ommatidia situated at the dorsal rim of the compound eye (dorsal rim area). The dorsal rim ommatidia of these species share a number physiological properties that make them especially suitable for polarization vision: each ommatidium contains two sets of homochromatic, strongly polarization-sensitive photoreceptors with orthogonally-arranged analyzer orientations. The physiological specialization of the dorsal rim area goes along with characteristic changes in ommatidial structure, providing actual anatomical hallmarks of polarized skylight detection, that are readily detectable in histological sections of compound eyes. The presence of anatomically specialized dorsal rim ommatidia in many other insect species belonging to a wide range of different orders indicates that polarized skylight detection is a common visual function in insects. However, fine-structural disparities in the design of dorsal rim ommatidia of different insect groups indicate that polarization vision arose polyphyletically in the insects.

Detectors for polarized skylight in insects: a survey of ommatidial specializations in the dorsal rim area of the compound eye

Apart from the sun, the polarization pattern of the sky offers insects a reference for visual compass orientation. Using behavioral experiments, it has been shown in a few insect species (field crickets, honey bees, desert ants, and house flies) that the detection of the oscillation plane of polarized skylight is mediated exclusively by a group of specialized ommatidia situated at the dorsal rim of the compound eye (dorsal rim area). The dorsal rim ommatidia of these species share a number physiological properties that make them especially suitable for polarization vision: each ommatidium contains two sets of homochromatic, strongly polarization-sensitive photoreceptors with orthogonally-arranged analyzer orientations. The physiological specialization of the dorsal rim area goes along with characteristic changes in ommatidial structure, providing actual anatomical hallmarks of polarized skylight detection, that are readily detectable in histological sections of compound eyes. The presence of anatomically specialized dorsal rim ommatidia in many other insect species belonging to a wide range of different orders indicates that polarized skylight detection is a common visual function in insects. However, fine-structural disparities in the design of dorsal rim ommatidia of different insect groups indicate that polarization vision arose polyphyletically in the insects. Microsc. Res. Tech. 47:368–379, 1999. © 1999 Wiley-Liss, Inc.

How polarization-sensitive interneurones of crickets see the polarization pattern of the sky: a field study with an opto-electronic model neurone

Many insects gain directional information from the polarization pattern of the sky. Polarization vision is mediated by the specialized ommatidia of the dorsal rim area of the compound eye, which contains highly polarization-sensitive photoreceptors. In crickets Gryllus campestris, polarized light information conveyed by the dorsal rim ommatidia was found to be processed by polarization-opponent interneurones (POL-neurones). In this study, a field-proof opto-electronic model of a POL-neurone was constructed that implements the physiological properties of cricket POL-neurones as measured by previous electrophysiological experiments in the laboratory. Using this model neurone, both the strength of the celestial polarization signal and the directional information available to POL-neurones were assessed under a variety of meteorological conditions. We show that the polarization signal as experienced by cricket POL-neurones is very robust, both because of the special filtering properties of these neurones (polarization-antagonism, spatial low-pass, monochromacy) and because of the relatively stable e-vector pattern of the sky.

Polarization-sensitive photoreceptors of different spectral types in the compound eye of waterstriders

Polarization-sensitive photoreceptors of different spectral types in the compound eye of waterstriders

Polarization-Sensitive Photoreceptors of Different Spectral Types in the Compound Eye of Waterstriders

Polarization-Sensitive Photoreceptors of Different Spectral Types in the Compound Eye of Waterstriders

Polarization-opponent interneurons in the insect visual system

Recent behavioural experiments dealing with the mechanism of polarized skylight navigation in bees indicated that processing of e-vector information in the visual system involves antagonistic interaction between polarization-sensitive photoreceptors1,2. Here we report electrophysiological recordings from polarization-opponent interneurons in the optic lobe of crickets. These neurons receive antagonistic input from polarization sensitive photoreceptors with orthogonally arranged analyser orientations. Although polarization-sensitive interneurons have previously been reported from the visual system of crabs3 and goldfish4,5, this is the first demonstration of polarization-opponent units.