Stereoscopic artificial compound eyes for spatiotemporal perception in three-dimensional space.

Arthropods' eyes are effective biological vision systems for object tracking and wide field of view because of their structural uniqueness; however, unlike mammalian eyes, they can hardly acquire the depth information of a static object because of their monocular cues. Therefore, most arthropods rely on motion parallax to track the object in three-dimensional (3D) space. Uniquely, the praying mantis (Mantodea) uses both compound structured eyes and a form of stereopsis and is capable of achieving object recognition in 3D space. Here, by mimicking the vision system of the praying mantis using stereoscopically coupled artificial compound eyes, we demonstrated spatiotemporal object sensing and tracking in 3D space with a wide field of view. Furthermore, to achieve a fast response with minimal latency, data storage/transportation, and power consumption, we processed the visual information at the edge of the system using a synaptic device and a federated split learning algorithm. The designed and fabricated stereoscopic artificial compound eye provides energy-efficient and accurate spatiotemporal object sensing and optical flow tracking. It exhibits a root mean square error of 0.3 centimeter, consuming only approximately 4 millijoules for sensing and tracking. These results are more than 400 times lower than conventional complementary metal-oxide semiconductor-based imaging systems. Our biomimetic imager shows the potential of integrating nature's unique design using hardware and software codesigned technology toward capabilities of edge computing and sensing.

Looking across the gap: Understanding the evolution of eyes and vision among insects.

The compound eyes of insects exhibit stunning variation in size, structure, and function, which has allowed these animals to use their vision to adapt to a huge range of different environments and lifestyles, and evolve complex behaviors. Much of our knowledge of eye development has been learned from Drosophila, while visual adaptations and behaviors are often more striking and better understood from studies of other insects. However, recent studies in Drosophila and other insects, including bees, beetles, and butterflies, have begun to address this gap by revealing the genetic and developmental bases of differences in eye morphology and key new aspects of compound eye structure and function. Furthermore, technical advances have facilitated the generation of high-resolution connectomic data from different insect species that enhances our understanding of visual information processing, and the impact of changes in these processes on the evolution of vision and behavior. Here, we review these recent breakthroughs and propose that future integrated research from the development to function of visual systems within and among insect species represents a great opportunity to understand the remarkable diversification of insect eyes and vision.

Fabrication of a light screen-aperture integrated flexible thin film micro-lens array for a biomimetic superposition compound eye.

Micro-lens array, an artificial compound eye vision system, provides a wide field of view and multi-perspective view. However, it has not been adopted as a computer vision application due to its limited visible range and high optical interference. In this research, a novel fabrication method for the flexible polydimethylsiloxane micro-lens array with a polytetrafluoroethylene light screen-aperture integrated layer was established by the simple protrusion method. The integrated layer provided longer visible range by one meter while maintaining the wide field-of-view of 100 °. The resulting images were used for obtaining depth information of a target as an example and for analyzing the rectangular and hexagonal arrangements of the micro-lenses for the future applications. With the improved visual range, wide field-of-view and flexibility, the fabricated micro-lens array can be applied to the small and curved CMOS image sensors in the future.

Evidence for UV-green dichromacy in the basal hymenopteran Sirex noctilio (Siricidae).

A precondition for colour vision is the presence of at least two spectral types of photoreceptors in the eye. The order Hymenoptera is traditionally divided into the Apocrita (ants, bees, wasps) and the Symphyta (sawflies, woodwasps, horntails). Most apocritan species possess three different photoreceptor types. In contrast, physiological studies in the Symphyta have reported one to four photoreceptor types. To better understand the evolution of photoreceptor diversity in the Hymenoptera, we studied the Symphyta Sirex noctilio, which belongs to the superfamily Siricoidea, a closely related group of the Apocrita suborder. Our aim was to (i) identify the photoreceptor types of the compound eye by electroretinography (ERG), (ii) characterise the visual opsin genes of S. noctilio by genomic comparisons and phylogenetic analyses and (iii) analyse opsin mRNA expression. ERG measurements revealed two photoreceptor types in the compound eye, maximally sensitive to 527 and 364 nm. In addition, we identified three opsins in the genome, homologous to the hymenopteran green or long-wavelength sensitive (LW) LW1, LW2 and ultra-violet sensitive (UV) opsin genes. The LW1 and UV opsins were found to be expressed in the compound eyes, and LW2 and UV opsins in the ocelli. The lack of a blue or short-wavelength sensitive (SW) homologous opsin gene and a corresponding receptor suggests that S. noctilio is a UV-green dichromate.

Semper's cells in the insect compound eye: Insights into ocular form and function.

The arthropod compound eye represents one of two major eye types in the animal kingdom and has served as an essential experimental paradigm for defining fundamental mechanisms underlying sensory organ formation, function, and maintenance. One of the most distinguishing features of the compound eye is the highly regular array of lens facets that define individual eye (ommatidial) units. These lens facets are produced by a deeply conserved quartet of cuticle-secreting cells, called Semper cells (SCs). Also widely known as cone cells, SCs were originally identified for their secretion of the dioptric system, i.e. the corneal lens and underlying crystalline cones. Additionally, SCs are now known to execute a diversity of patterning and glial functions in compound eye development and maintenance. Here, we present an integrated account of our current knowledge of SC multifunctionality in the Drosophila compound eye, highlighting emerging gene regulatory modules that may drive the diverse roles for these cells. Drawing comparisons with other deeply conserved retinal glia in the vertebrate single lens eye, this discussion speaks to glial cell origins and opens new avenues for understanding sensory system support programs.

The role of Ire1 in Drosophila eye pigmentation revealed by an RNase dead allele.

Ire1 is an endoplasmic reticulum (ER) transmembrane RNase that cleaves substrate mRNAs to help cells adapt to ER stress. Because there are cell types with physiological ER stress, loss of Ire1 results in metabolic and developmental defects in diverse organisms. In Drosophila, Ire1 mutants show developmental defects at early larval stages and in pupal eye photoreceptor differentiation. These Drosophila studies relied on a single Ire1 loss of function allele with a Piggybac insertion in the coding sequence. Here, we report that an Ire1 allele with a specific impairment in the RNase domain, H890A, unmasks previously unrecognized Ire1 phenotypes in Drosophila eye pigmentation. Specifically, we found that the adult eye pigmentation is altered, and the pigment granules are compromised in Ire1H890A homozygous mosaic eyes. Furthermore, the Ire1H890A mutant eyes had dramatically reduced Rhodopsin-1 protein levels. Drosophila eye pigment granules are most notably associated with late endosome/lysosomal defects. Our results indicate that the loss of Ire1, which would impair ER homeostasis, also results in altered adult eye pigmentation.

An overview on trilobite eyes and their functioning.

Great progress has been made during the last decades in understanding visual systems of arthropods living today. Thus it seems worthwhile to review what is known about structure and function of the eyes of trilobites, the most important group of marine arthropods during the Paleozoic. There are three types of compound eyes in trilobites. The oldest and most abundant is the so-called holochroal eye. The sensory system represents a typical apposition eye, and all units are covered by one cornea in common. The so-called abathochroal eye (only in eodiscid trilobites) consists of small lenses, each individually covered by a thin cuticular cornea. The schizochroal eye is represented just in the suborder Phacopina, and probably is a highly specialized visual system. We discuss the calcitic character of trilobite lenses, the phylogenetic relevance of the existence of crystalline cones in trilobites, and consider adaptations of trilobite's compound eyes to different ecological constraints. The aim of this article is to give a resumé of what is known so far about trilobite vision, and to open perspectives to what still might be done.

The Compound Eye Possesses a Self-Sustaining Circadian Oscillator in the Cricket Gryllus bimaculatus.

Many insects show daily and circadian changes in morphology and physiology in their compound eye. In this study, we investigated whether the compound eye had an intrinsic circadian rhythm in the cricket Gryllus bimaculatus. We found that clock genes period (per), timeless (tim), cryptochrome 2 (cry2), and cycle (cyc) were rhythmically expressed in the compound eye under 12-h light/12-h dark cycles (LD 12:12) and constant darkness (DD) at a constant temperature. After the optic nerves were severed (ONX), a weak but significant rhythmic expression persisted for per and tim under LD 12:12, while under DD, tim and cyc showed rhythmic expression. We also found that more than half of the ONX compound eyes exhibited weak but significant circadian electroretinographic rhythms. These results clearly demonstrate that the cricket compound eye possesses an intrinsic circadian oscillator which can drive the circadian light sensitivity rhythm in the eye, and that the circadian clock in the optic lobe exerts its influence on the oscillator in the eye.

Evolution of Insect Color Vision: From Spectral Sensitivity to Visual Ecology.

Color vision is widespread among insects but varies among species, depending on the spectral sensitivities and interplay of the participating photoreceptors. The spectral sensitivity of a photoreceptor is principally determined by the absorption spectrum of the expressed visual pigment, but it can be modified by various optical and electrophysiological factors. For example, screening and filtering pigments, rhabdom waveguide properties, retinal structure, and neural processing all influence the perceived color signal. We review the diversity in compound eye structure, visual pigments, photoreceptor physiology, and visual ecology of insects. Based on an overview of the current information about the spectral sensitivities of insect photoreceptors, covering 221 species in 13 insect orders, we discuss the evolution of color vision and highlight present knowledge gaps and promising future research directions in the field.

Surf and turf vision: Patterns and predictors of visual acuity in compound eye evolution.

Eyes have the flexibility to evolve to meet the ecological demands of their users. Relative to camera-type eyes, the fundamental limits of optical diffraction in arthropod compound eyes restrict the ability to resolve fine detail (visual acuity) to much lower degrees. We tested the capacity of several ecological factors to predict arthropod visual acuity, while simultaneously controlling for shared phylogenetic history. In this study, we have generated the most comprehensive review of compound eye visual acuity measurements to date, containing 385 species that span six of the major arthropod classes. An arthropod phylogeny, made custom to this database, was used to develop a phylogenetically-corrected generalized least squares (PGLS) linear model to evaluate four ecological factors predicted to underlie compound eye visual acuity: environmental light intensity, foraging strategy (predator vs. non-predator), horizontal structure of the visual scene, and environmental medium (air vs. water). To account for optical constraints on acuity related to animal size, body length was also included, but this did not show a significant effect in any of our models. Rather, the PGLS analysis revealed that the strongest predictors of compound eye acuity are described by a combination of environmental medium, foraging strategy, and environmental light intensity.

Ommochrome pathway genes kynurenine 3-hydroxylase and cardinal participate in eye pigmentation in Plutella xylostella.

BACKGROUND: Eye pigmentation genes have been utilized as visible markers for constructing genetic control prototypes in several insect vectors of human disease. Here, orthologs of two ommochrome pathway genes, kynurenine 3-hydroxylase (kmo) and cardinal, were investigated in Plutella xylostella, a globally distributed, economically important pest of Brassica crops. RESULTS: Both somatic mosaic and germline mutations were efficiently created using the CRISPR/Cas9 system, and null mutant strains of Pxkmo and Pxcardinal were obtained. A frame-shift mutation in Pxkmo caused yellow compound eyes at adult stage while an in-frame mutation lacking two amino acids resulted in a hypomorphic red eye phenotypes. In contrast, Pxcardinal-deficient moths with a frame-shift mutation exhibited yellow eye pigmentation in newly emerged adults which turned to red as the adults aged. Additionally, differences were observed in the coloration of larval ocelli, brains and testes in Pxkmo and Pxcardinal yellow-eye mutant lines. CONCLUSIONS: Our work identifies the important roles of Pxkmo and Pxcardinal in P. xylostella eye pigmentation and provides tools for future genetic manipulation of this important crop pest.

The visual neuroecology of anisoptera.

Dragonflies belong to the oldest known lineage of flying animals, found across the globe around streams, ponds and forests. They are insect predators, specialising in ambush attack as aquatic larvae and rapid pursuit as adults. Dragonfly adults hunt amidst swarms in conditions that confuse many predatory species, and exhibit capture rates above 90%. Underlying the performance of such a remarkable predator is a finely tuned visual system capable of tracking targets amidst distractors and background clutter. The dragonfly performs a complex repertoire of flight behaviours, from near-motionless hovering to acute turns at high speeds. Here, we review the optical, neuronal, and behavioural adaptations that underlie the dragonflies' ability to achieve such remarkable predatory success.

Divergent sensory investment mirrors potential speciation via niche partitioning across Drosophila.

The examination of phylogenetic and phenotypic characteristics of the nervous system, such as behavior and neuroanatomy, can be utilized as a means to assess speciation. Recent studies have proposed a fundamental tradeoff between two sensory organs, the eye and the antenna. However, the identification of ecological mechanisms for this observed tradeoff have not been firmly established. Our current study examines several monophyletic species within the obscura group, and asserts that despite their close relatedness and overlapping ecology, they deviate strongly in both visual and olfactory investment. We contend that both courtship and microhabitat preferences support the observed inverse variation in these sensory traits. Here, this variation in visual and olfactory investment seems to provide relaxed competition, a process by which similar species can use a shared environment differently and in ways that help them coexist. Moreover, that behavioral separation according to light gradients occurs first, and subsequently, courtship deviations arise.

Specializations in the compound eye of Talitrus saltator (Crustacea, Amphipoda).

We investigated the eye regionalization in Talitrus saltator by morphological, electrophysiological and behavioural experiments. Each ommatidium possesses five radially arranged retinular cells producing a square fused rhabdom by R1-R4 cells; the smaller R5 exists between R1 and R4. The size of R5 rhabdomere is larger in the dorsal part and becomes smaller in the median and ventral parts of the eye. Spectral-sensitivity by electroretinograms were recorded from dorsal or ventral parts of the eye. The dorsal part possesses maxima at green and UV-blue region. The main response region in the ventral part is only from UV (390 nm) to blue (430 nm) decreasing at longer wavelengths. To evaluate the sandhoppers' celestial orientation, their eyes were painted black either in the dorsal or ventral part, under the natural sky or a blue filter with or without the vision of the sun. Sandhoppers with the dorsal region of the eyes painted and tested under the screened sun were more dispersed and their directions varied more than in other groups of individuals. Sandhoppers with this area of the eye obscured display considerable difficulties to head in a specific direction. This work suggests the existence of regional specializations in the eye of T. saltator.

Color vision in insects: insights from Drosophila.

Color vision is an important sensory capability that enhances the detection of contrast in retinal images. Monochromatic animals exclusively detect temporal and spatial changes in luminance, whereas two or more types of photoreceptors and neuronal circuitries for the comparison of their responses enable animals to differentiate spectral information independent of intensity. Much of what we know about the cellular and physiological mechanisms underlying color vision comes from research on vertebrates including primates. In insects, many important discoveries have been made, but direct insights into the physiology and circuit implementation of color vision are still limited. Recent advances in Drosophila systems neuroscience suggest that a complete insect color vision circuitry, from photoreceptors to behavior, including all elements and computations, can be revealed in future. Here, we review fundamental concepts in color vision alongside our current understanding of the neuronal basis of color vision in Drosophila, including side views to selected other insects.

Bioinspired Zoom Compound Eyes Enable Variable-Focus Imaging.

Natural compound eyes provide the inspiration for developing artificial optical devices that feature a large field of view (FOV). However, the imaging ability of artificial compound eyes is generally based on the large number of ommatidia. The lack of a tunable imaging mechanism significantly limits the practical applications of artificial compound eyes, for instance, distinguishing targets at different distances. Herein, we reported zoom compound eyes that enable variable-focus imaging by integrating a deformable poly(dimethylsiloxane) (PDMS) microlens array (MLA) with a microfluidic chamber. The thin and soft PDMS MLA was fabricated by soft lithography using a hard template prepared by a combined technology of femtosecond laser processing and wet etching. As compared with other mechanical machining strategies, our combined technology features high flexibility, efficiency, and uniformity, as well as designable processing capability, since the size, distribution, and arrangement of the ommatidia can be well controlled during femtosecond laser processing. By tuning the volume of water injected into the chamber, the PDMS MLA can deform from a planar structure to a hemispherical shape, evolving into a tunable compound eye of variable FOV up to 180°. More importantly, the tunable chamber can functionalize as the main zoom lens for tunable imaging, which endows the compound eye with the additional capability of distinguishing targets at different distances. Its focal length can be turned from 3.03 mm to infinity with an angular resolution of 3.86 × 10-4 rad. This zoom compound eye combines the advantages of monocular eyes and compound eyes together, holding great promise for developing advanced micro-optical devices that enable large FOV and variable-focus imaging.

Spectral organization of the compound eye of a migrating nymphalid, the chestnut tiger butterfly Parantica sita.

Several butterflies of family Nymphalidae perform long-distance migration. Extensive studies of migration in the iconic monarch butterfly Danaus plexippus have revealed that vision plays a crucial role in migratory orientation. Differences in the migratory patterns of butterflies suggest that not all species are exposed to the same visual conditions and yet, little is known about how the visual system varies across migratory species. Here, we used intracellular electrophysiology, dye injection and electron microscopy to assess the spectral and polarization properties of the photoreceptors of a migrating nymphalid, Parantica sita Our findings reveal three spectral classes of photoreceptors including ultraviolet, blue and green receptors. The green receptor class contains three subclasses, which are broad, narrow and double-peaking green receptors. Ultraviolet and blue receptors are sensitive to polarized light parallel to the dorso-ventral axis of the animal, while the variety of green receptors are sensitive to light polarized at 45 deg, 90 deg and 135 deg away from the dorso-ventral axis. The polarization sensitivity ratio is constant across spectral receptor classes at around 1.8. Although P. sita has a typical nymphalid eye with three classes of spectral receptors, subtle differences exist among the eyes of migratory nymphalids, which may be genus specific.

Light input pathways to the circadian clock of insects with an emphasis on the fruit fly Drosophila melanogaster.

Light is the most important Zeitgeber for entraining animal activity rhythms to the 24-h day. In all animals, the eyes are the main visual organs that are not only responsible for motion and colour (image) vision, but also transfer light information to the circadian clock in the brain. The way in which light entrains the circadian clock appears, however, variable in different species. As do vertebrates, insects possess extraretinal photoreceptors in addition to their eyes (and ocelli) that are sometimes located close to (underneath) the eyes, but sometimes even in the central brain. These extraretinal photoreceptors contribute to entrainment of their circadian clocks to different degrees. The fruit fly Drosophila melanogaster is special, because it expresses the blue light-sensitive cryptochrome (CRY) directly in its circadian clock neurons, and CRY is usually regarded as the fly's main circadian photoreceptor. Nevertheless, recent studies show that the retinal and extraretinal eyes transfer light information to almost every clock neuron and that the eyes are similarly important for entraining the fly's activity rhythm as in other insects, or more generally spoken in other animals. Here, I compare the light input pathways between selected insect species with a focus on Drosophila's special case.

A new method for mapping spatial resolution in compound eyes suggests two visual streaks in fiddler crabs.

Visual systems play a vital role in guiding the behaviour of animals. Understanding the visual information animals are able to acquire is therefore key to understanding their visually mediated decision making. Compound eyes, the dominant eye type in arthropods, are inherently low-resolution structures. Their ability to resolve spatial detail depends on sampling resolution (interommatidial angle) and the quality of ommatidial optics. Current techniques for estimating interommatidial angles are difficult, and generally require in vivo measurements. Here, we present a new method for estimating interommatidial angles based on the detailed analysis of 3D micro-computed tomography images of fixed samples. Using custom-made MATLAB software, we determined the optical axes of individual ommatidia and projected these axes into the 3D space around the animal. The combined viewing directions of all ommatidia, estimated from geometrical optics, allowed us to estimate interommatidial angles and map the animal's sampling resolution across its entire visual field. The resulting topographic representations of visual acuity match very closely the previously published data obtained from both fiddler and grapsid crabs. However, the new method provides additional detail that was not previously detectable and reveals that fiddler crabs, rather than having a single horizontal visual streak as is common in flat-world inhabitants, probably have two parallel streaks located just above and below the visual horizon. A key advantage of our approach is that it can be used on appropriately preserved specimens, allowing the technique to be applied to animals such as deep-sea crustaceans that are inaccessible or unsuitable for in vivo approaches.

Optic lobe organization in stomatopod crustacean species possessing different degrees of retinal complexity.

Stomatopod crustaceans possess tripartite compound eyes; upper and lower hemispheres are separated by an equatorial midband of several ommatidial rows. The organization of stomatopod retinas is well established, but their optic lobes have been studied less. We used histological staining, immunolabeling, and fluorescent tracer injections to compare optic lobes in two 6-row midband species, Neogonodactylus oerstedii and Pseudosquilla ciliata, to those in two 2-row midband species, Squilla empusa and Alima pacifica. Compared to the 6-row species, we found structural differences in all optic neuropils in both 2-row species. Photoreceptor axons from 2-row midband ommatidia supply two sets of lamina cartridges; however, conspicuous spaces lacking lamina cartridges are observed in locations corresponding to where the cartridges of the upper four ommatidial rows of 6-row species would exist. The tripartite arrangement and enlarged projections containing fibers associated with the two rows of midband ommatidia can be traced throughout the entire optic lobe. However, 2-row species lack some features of medullar and lobular neuropils in 6-row species. Our results support the hypothesis that 2-row midband species are derived from a 6-row ancestor, and suggest specializations in the medulla and lobula found solely in 6-row species are important for color and polarization analysis.