From Polarization Sensitivity to Polarization Vision

2000 ◽

Vol 355 (1401) ◽

pp. 1187-1190 ◽

Cited By ~ 32

Author(s):

Craig W. Hawryshyn

Keyword(s):

Polarized Light ◽

Spatial Arrangement ◽

Short Review ◽

Research Problem ◽

Polarization Sensitivity ◽

Polarization Vision ◽

Selective Reflection ◽

Mosaic Pattern ◽

Cone Mosaic ◽

Biophysical Mechanism

Polarization vision in vertebrates has been marked with significant controversy over recent decades. In the last decade, however, models from two laboratories have indicated that the spatial arrangement of photoreceptors provides the basis for polarization sensitivity.Work in my laboratory, in collaboration with I. Novales Flamarique and F. I. Harosi, has shown that polarization sensitivity depends on a well–defined square cone mosaic pattern and that the biophysical properties of the square cone mosaic probably account for polarization vision in the ultraviolet spectrum. The biophysical mechanism appears to be based on the selective reflection of axial–polarized light by the partitioning membrane, formed along the contact zone between the members of the double cones, onto neighbouring ultraviolet–sensitive cones. In this short review, I discuss the historical development of this research problem.

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Polarization vision in cuttlefish in a concealed communication channel?

Journal of Experimental Biology ◽

10.1242/jeb.199.9.2077 ◽

1996 ◽

Vol 199 (9) ◽

pp. 2077-2084

Author(s):

N Shashar ◽

P Rutledge ◽

T Cronin

Keyword(s):

Polarized Light ◽

Egg Laying ◽

Polarization Sensitivity ◽

Polarization Vision ◽

Microscopical Examination ◽

Polarization Pattern ◽

Behavioral Experiments ◽

Marine Animals ◽

Linearly Polarized ◽

Electron Microscopical

Polarization sensitivity is well documented in marine animals, but its function is not yet well understood. Of the cephalopods, squid and octopus are known to be sensitive to the orientation of polarization of incoming light. This sensitivity arises from the orthogonal orientation of neighboring photoreceptors. Electron microscopical examination of the retina of the cuttlefish Sepia officinalis L. revealed the same orthogonal structure, suggesting that cuttlefish are also sensitive to linearly polarized light. Viewing cuttlefish through an imaging polarized light analyzer revealed a prominent polarization pattern on the arms, around the eyes and on the forehead of the animals. The polarization pattern disappeared when individuals lay camouflaged on the bottom and also during extreme aggression display, attacks on prey, copulation and egg-laying behavior in females. In behavioral experiments, the responses of cuttlefish to their images reflected from a mirror changed when the polarization patterns of the reflected images were distorted. These results suggest that cuttlefish use polarization vision and display for intraspecific recognition and communication.

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Spatial orientation of social caterpillars is influenced by polarized light

Biology Letters ◽

10.1098/rsbl.2020.0736 ◽

2021 ◽

Vol 17 (2) ◽

Author(s):

Mizuki Uemura ◽

Andrej Meglič ◽

Myron P. Zalucki ◽

Andrea Battisti ◽

Gregor Belušič

Keyword(s):

Visual System ◽

Spatial Orientation ◽

Polarized Light ◽

Thaumetopoea Pityocampa ◽

Polarization Sensitivity ◽

Polarization Vision ◽

Anatomical Analysis ◽

Skylight Polarization ◽

Rugged Surface ◽

Anatomical Evidence

Processionary caterpillars of Thaumetopoea pityocampa (in Europe) and Ochrogaster lunifer (in Australia) (Lepidoptera: Notodontidae) form single files of larvae crawling head-to-tail when moving to feeding and pupation sites. We investigated if the processions are guided by polarization vision. The heading orientation of processions could be manipulated with linear polarizing filters held above the leading caterpillar. Exposure to changes in the angle of polarization around the caterpillars resulted in corresponding changes in heading angles. Anatomical analysis indicated specializations for polarization vision of stemma I in both species. Stemma I has a rhabdom with orthogonal and aligned microvilli, and an opaque and rugged surface, which are optimizations for skylight polarization vision, similar to the dorsal rim of adult insects. Stemmata II-VI have a smooth and shiny surface and lobed rhabdoms with non-orthogonal and non-aligned microvilli; they are thus optimized for general vision with minimal polarization sensitivity. Behavioural and anatomical evidence reveal that polarized light cues are important for larval orientation and can be robustly detected with a simple visual system.

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Two chiral types of randomly rotated ommatidia are distributed across the retina of the flathead oak borer Coraebus undatus (Coleoptera: Buprestidae)

Journal of Experimental Biology ◽

10.1242/jeb.225920 ◽

2020 ◽

Vol 223 (14) ◽

pp. jeb225920 ◽

Cited By ~ 2

Author(s):

Andrej Meglič ◽

Marko Ilić ◽

Carmen Quero ◽

Kentaro Arikawa ◽

Gregor Belušič

Keyword(s):

Color Vision ◽

Photoreceptor Cell ◽

The Body ◽

Polarization Sensitivity ◽

Compound Eyes ◽

Polarization Vision ◽

Intracellular Recordings ◽

Cell Responses ◽

Ommatidial Rotation

ABSTRACTJewel beetles are colorful insects, which use vision to recognize their conspecifics and can be lured with colored traps. We investigated the retina and coloration of one member of this family, the flathead oak borer Coraebus undatus using microscopy, spectrometry, polarimetry, electroretinography and intracellular recordings of photoreceptor cell responses. The compound eyes are built of a highly unusual mosaic of mirror-symmetric or chiral ommatidia that are randomly rotated along the body axes. Each ommatidium has eight photoreceptors, two of them having rhabdomeres in tiers. The eyes contain six spectral classes of photoreceptors, peaking in the UV, blue, green and red. Most photoreceptors have moderate polarization sensitivity with randomly distributed angular maxima. The beetles have the necessary retinal substrate for complex color vision, required to recognize conspecifics and suitable for a targeted design of color traps. However, the jewel beetle array of freely rotated ommatidia is very different from the ordered mosaic in insects that have object-directed polarization vision. We propose that ommatidial rotation enables the cancelling out of polarization signals, thus allowing stable color vision, similar to the rhabdomeric twist in the eyes of flies and honeybees.

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The molecular basis of mechanisms underlying polarization vision

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2010.0206 ◽

2011 ◽

Vol 366 (1565) ◽

pp. 627-637 ◽

Cited By ~ 48

Author(s):

Nicholas W. Roberts ◽

Megan L. Porter ◽

Thomas W. Cronin

Keyword(s):

Protein Interactions ◽

Cell Types ◽

Phase Behaviour ◽

Polarization Sensitivity ◽

Polarization Vision ◽

Membrane Phase ◽

Protein Protein Interactions ◽

Molecular Ordering ◽

Underlying Mechanisms ◽

Long Range Ordering

The underlying mechanisms of polarization sensitivity (PS) have long remained elusive. For rhabdomeric photoreceptors, questions remain over the high levels of PS measured experimentally. In ciliary photoreceptors, and specifically cones, little direct evidence supports any type of mechanism. In order to promote a greater interest in these fundamental aspects of polarization vision, we examined a varied collection of studies linking membrane biochemistry, protein–protein interactions, molecular ordering and membrane phase behaviour. While initially these studies may seem unrelated to polarization vision, a common narrative emerges. A surprising amount of evidence exists demonstrating the importance of protein–protein interactions in both rhabdomeric and ciliary photoreceptors, indicating the possible long-range ordering of the opsin protein for increased PS. Moreover, we extend this direction by considering how such protein paracrystalline organization arises in all cell types from controlled membrane phase behaviour and propose a universal pathway for PS to occur in both rhabdomeric and cone photoreceptors.

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Polarization Vision

Visual Ecology ◽

10.23943/princeton/9780691151847.003.0008 ◽

2014 ◽

Author(s):

Thomas W. Cronin ◽

Sönke Johnsen ◽

N. Justin Marshall ◽

Eric J. Warrant

Keyword(s):

Central Nervous System ◽

Polarized Light ◽

Polarization Sensitivity ◽

Natural Scenes ◽

Polarization Vision ◽

Natural Behavior ◽

Remarkable Feature ◽

Celestial Navigation ◽

The Central Nervous System ◽

Light Stimuli

This chapter explores how polarization sensitivity is achieved in animals and how it is used in natural behavior. Arthropods are famous for their polarization sensitivity, but other animals, including vertebrates are also capable of this. A remarkable feature of some insect systems is that the sky pattern is genetically imprinted into the neural arrangements, all the way through to the central nervous system. However, celestial navigation is not the only use to which animals can put polarization vision. Other functions may include communication, contrast enhancement, and camouflage breaking. Polarized light stimuli are abundant in nature. Although no important source of light is polarized, light may become polarized when it is scattered or reflected. These two fundamental principles produce abundant polarized light in natural scenes, which explains why polarization vision is so common.

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Polarization Vision—Overcoming Challenges of Working with a Property of Light We Barely See

10.1101/207217 ◽

2017 ◽

Author(s):

James J. Foster ◽

Shelby E. Temple ◽

Martin J. How ◽

Ilse M. Daly ◽

Camilla R. Sharkey ◽

...

Keyword(s):

Animal Species ◽

Experimental Methods ◽

Polarization Sensitivity ◽

Polarization Vision ◽

Confounding Factors ◽

New Techniques ◽

Taxonomic Groups ◽

Polarization Of Light ◽

Sensory Ability ◽

Key Questions

AbstractIn recent years, the study of polarization 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 polarization can be controlled, presented and measured. Once thought to be limited to only a few animal species, polarization 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 polarization 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 polarized 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 polarization, to design robust experiments that are free from confounding factors.

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

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1910807116 ◽

2019 ◽

Vol 116 (43) ◽

pp. 21843-21853 ◽

Cited By ~ 10

Author(s):

Andrej Meglič ◽

Marko Ilić ◽

Primož Pirih ◽

Aleš Škorjanc ◽

Martin F. Wehling ◽

...

Keyword(s):

Division Of Labor ◽

Compound Eye ◽

Polarization Sensitivity ◽

Polarization Vision ◽

Electron Microscopic ◽

Visual Guidance ◽

Differential Signal ◽

Green Component ◽

Host Detection

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.

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