Synaptic targets of functionally specialized R7 and R8 photoreceptors in the central eye and dorsal rim area of Drosophila

Color and polarization provide complementary information about the world and are detected by specialized photoreceptors. However, the downstream neural circuits that process these distinct modalities are incompletely understood in any animal. We have systematically reconstructed, using light and electron microscopy, the synaptic targets of the photoreceptors specialized to detect color and polarized light in Drosophila. We identified known and novel downstream targets that are selective for different wavelengths as well as for polarized light and followed their projections to other areas in the optic lobes and the central brain. Strikingly, photoreceptors in the polarization-sensitive dorsal rim area target fewer cell types, that lack strong connections to the lobula, a neuropil with a proposed role in color processing. Our reconstruction identifies shared wiring and modality-specific specializations for color and polarization vision, and provides a comprehensive view of the first steps of the pathways processing color and polarized light inputs.

Thresholds of polarization vision in octopuses

ABSTRACTPolarization 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.

Polarization contrasts and their effect on the gaze stabilisation of crustaceans

Many animals go to great lengths to stabilise their eyes relative to the visual scene and do so to enhance the localisation of moving objects and to functionally partition the visual system relative to the outside world. An important cue that is used to control these stabilisation movements is contrast within the visual surround. Previous studies on insects, spiders and fish have shown that gaze stabilisation is achromatic (= ‘colour-blind’), meaning that chromatic contrast alone (in the absence of apparent intensity contrasts) does not contribute to gaze stabilisation. Following the assumption that polarization vision is analogous in many ways to colour vision, the present study shows that five different crustacean species do not use the polarization of light alone for gaze stabilisation, despite being able to use this modality for detecting predator-like objects. This work therefore suggests that the gaze stabilisation in many crustaceans cannot be elicited by the polarization of light alone.

Spatial orientation of social caterpillars is influenced by polarized light

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.

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

ABSTRACTStomatopods, 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.

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

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.