Synaptic targets of photoreceptors specialized to detect color and skylight polarization in 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. Using electron microscopy, we have systematically reconstructed the synaptic targets of the photoreceptors specialized to detect color and skylight polarization in Drosophila, and we have used light microscopy to confirm many of our findings. We identified known and novel downstream targets that are selective for different wavelengths or polarized light, and followed their projections to other areas in the optic lobes and the central brain. Our results revealed many synapses along the photoreceptor axons between brain regions, new pathways in the optic lobes, and spatially segregated projections to central brain regions. Strikingly, photoreceptors in the polarization-sensitive dorsal rim area target fewer cell types, and lack strong connections to the lobula, a neuropil involved 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.

Visual system characterization of the obligate bat ectoparasite Trichobius frequens (Diptera: Streblidae).

As an obligate ectoparasite of bats, the bat fly Trichobius frequens (Diptera: Streblidae) inhabits the same subterranean environment as their nocturnal bat hosts. In this study, we characterize the macromorphology, optical architecture, rhabdom anatomy, photoreceptor absorbance, and opsin expression of the significantly reduced visual system in T. frequens resulting from evolution in the dark. The eyes develop over a 21-22 day pupal developmental period, with pigmentation appearing on pupal day 11. After eclosion as an adult, T. frequens eyes consist of on average 8 facets, each overlying a fused rhabdom consisting of anywhere from 11 to 18 estimated retinula cells. The dimensions of the facets and fused rhabdoms are similar to those measured in other nocturnal insects. T. frequens eyes are functional as shown by expression of a Rh1 opsin forming a visual pigment with a peak sensitivity to 487 nm, similar to other dipteran Rh1 opsins. Future studies will evaluate how individuals with such reduced capabilities for spatial vision as well as sensitivity still capture enough visual information to use flight to maneuver through dark habitats.

The brachyceran de novo gene PIP82, a phosphorylation target of aPKC, is essential for proper formation and maintenance of the rhabdomeric photoreceptor apical domain in Drosophila.

The Drosophila apical photoreceptor membrane is defined by the presence of two distinct morphological regions, the microvilli-based rhabdomere and the stalk membrane. The subdivision of the apical membrane contributes to the geometrical positioning and the stereotypical morphology of the rhabdomeres in compound eyes with open rhabdoms and neural superposition. Here we describe the characterization of the photoreceptor specific protein PIP82. We found that PIP82's subcellular localization demarcates the rhabdomeric portion of the apical membrane. We further demonstrate that PIP82 is a phosphorylation target of aPKC. PIP82 localization is modulated by phosphorylation, and in vivo, the loss of the aPKC/Crumbs complex results in an expansion of the PIP82 localization domain. The absence of PIP82 in photoreceptors leads to misshapped rhabdomeres as a result of misdirected cellular trafficking of rhabdomere proteins. Comparative analyses reveal that PIP82 originated de novo in the lineage leading to brachyceran Diptera, which is also characterized by the transition from fused to open rhabdoms. Taken together, these findings define a novel factor that delineates and maintains a specific apical membrane domain, and offers new insights into the functional organization and evolutionary history of the Drosophila retina.

Identification of Genes Required for Apical Protein Trafficking in Drosophila Photoreceptor Cells.

Drosophila melanogaster photoreceptor cells are highly polarized epithelial cells. Their apical membrane is further subdivided into the stalk membrane and the light-sensing rhabdomere. The photo-pigment Rhodopsin1 (Rh1) localizes to the rhabdomere, whereas the apical determinant Crumbs (Crb) is enriched at the stalk membrane. The proteoglycan Eyes shut (Eys) is secreted through the apical membrane into an inter-rhabdomeral space. Rh1, Crb, and Eys are essential for the development of photoreceptor cells, normal vision, and photoreceptor cell survival. Human orthologs of all three proteins have been linked to retinal degenerative diseases. Here, we describe an RNAi-based screen examining the importance of 237 trafficking-related genes in apical trafficking of Eys, Rh1, and Crb. We found 28 genes that have an effect on the localization and/or levels of these apical proteins and analyzed several factors in more detail. We show that the Arf GEF protein Sec71 is required for biosynthetic traffic of both apical and basolateral proteins, that the exocyst complex and the microtubule-based motor proteins dynein and kinesin promote the secretion of Eys and Rh1, and that Syntaxin 7/Avalanche controls the endocytosis of Rh1, Eys, and Crb.

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.

Syndapin constricts microvillar necks to form a united rhabdomere in Drosophila photoreceptors.

Drosophila photoreceptors develop from polarized epithelial cells that have apical and basolateral membranes. During morphogenesis, the apical membranes subdivide into a united bundle of photosensory microvilli (rhabdomeres) and a surrounding supporting membrane (stalk). By EMS-induced mutagenesis screening, we found that the F-Bin/Amphiphysin/Rvs (F-BAR) protein syndapin is essential for apical membrane segregation. The analysis of the super-resolution microscopy, STORM and the electron microscopy suggest that syndapin localizes to the neck of the microvilli at the base of the rhabdomere. Syndapin and moesin are required to constrict the neck of the microvilli to organize the membrane architecture at the base of the rhabdomere, to exclude the stalk membrane. Simultaneous loss of syndapin along with the microvilli adhesion molecule chaoptin significantly enhanced the disruption of stalk-rhabdomere segregation. However, loss of the factors involving endocytosis do not interfere. These results indicated syndapin is most likely functioning through its membrane curvature properties, and not through endocytic processes for stalk-rhabdomere segregation. Elucidation of the mechanism of this unconventional domain formation will provide novel insights into the field of cell biology.

Serial electron microscopic reconstruction of the drosophila larval eye: Photoreceptors with a rudimentary rhabdomere of microvillar-like processes.

Photoreceptor cells (PRCs) across the animal kingdom are characterized by a stacking of apical membranes to accommodate the high abundance of photopigment. In arthropods and many other invertebrate phyla PRC membrane stacks adopt the shape of densely packed microvilli that form a structure called rhabdomere. PRCs and surrounding accessory cells, including pigment cells and lens-forming cells, are grouped in stereotyped units, the ommatidia. In larvae of holometabolan insects, eyes (called stemmata) are reduced in terms of number and composition of ommatidia. The stemma of Drosophila (Bolwig organ) is reduced to a bilateral cluster of subepidermal PRCs, lacking all other cell types. In the present paper we have analyzed the development and fine structure of the Drosophila larval PRCs. Shortly after their appearance in the embryonic head ectoderm, PRC precursors delaminate and lose expression of apical markers of epithelial cells, including Crumbs and several centrosome-associated proteins. In the early first instar larva, PRCs show an expanded, irregularly shaped apical surface that is folded into multiple horizontal microvillar-like processes (MLPs). Apical PRC membranes and MLPs are covered with a layer of extracellular matrix. MLPs are predominantly aligned along an axis that extends ventro-anteriorly to dorso-posteriorly, but vary in length, diameter, and spacing. Individual MLPs present a "beaded" shape, with thick segments (0.2-0.3 µm diameter) alternating with thin segments (>0.1 µm). We show that loss of the glycoprotein Chaoptin, which is absolutely essential for rhabdomere formation in the adult PRCs, does not lead to severe abnormalities in larval PRCs.

Using micro-CT techniques to explore the role of sex and hair in the functional morphology of bumblebee (Bombus terrestris) ocelli.

Many insects have triplets of camera type eyes, called ocelli, whose function remains unclear for most species. Here, we investigate the ocelli of the bumblebee, Bombus terrestris, using reconstructed 3D data from X-ray microtomography scans combined with computational ray-tracing simulations. This method enables us, not only to predict the visual fields of the ocelli, but to explore for the first time the effect that hair has on them as well as the difference between worker female and male ocelli. We find that bumblebee ocellar fields of view are directed forward and dorsally, incorporating the horizon as well as the sky. There is substantial binocular overlap between the median and lateral ocelli, but no overlap between the two lateral ocelli. Hairs in both workers and males occlude the ocellar field of view, mostly laterally in the worker median ocellus and dorsally in the lateral ocelli. There is little to no sexual dimorphism in the ocellar visual field, suggesting that in B. terrestris they confer no advantage to mating strategies. We compare our results with published observations for the visual fields of compound eyes in the same species as well as with the ocellar vision of other bee and insect species.

Electron microscopic observation of photoreceptor cells in directly inserted anesthetized Drosophila into a high-pressure freezing unit.

The high-pressure freezing (HPF) technique is known to cryofix water-containing materials with little ice-crystal formation in deep depths compared with other freezing techniques. In this study, HPF for anesthetized living Drosophila was performed by placing them directly on the carrier of the HPF unit and exposing them to light. Frozen Drosophila were freeze substituted, and their compound eyes were examined by transmission electron microscopy. The ultrastructures of ommatidia composed of photoreceptor cells were well preserved. The location of the cytoplasmic organelles inside the photoreceptor cells was observed. In some photoreceptor cells in ommatidia of the light-exposed Drosphila, the cytoplasmic small granules were localized nearer the base of rhabdomeres, compared with those of the nonlight-exposed Drosophila. Thus, HPF with the direct insertion of living Drosophila under light exposure into the HPF machine enabled us to examine changes to functional structures of photoreceptor cells that occur within seconds.

Temporal and spatial order of photoreceptor and glia projections into optic lobe in Drosophila.

Photoreceptor (PR) axons project from the retina to the optic lobe in brain and form a precise retinotopic map in the Drosophila visual system. Yet the role of retinal basal glia in the retinotopic map formation is not previously known. We examined the formation of the retinotopic map by marking single PR pairs and following their axonal projections. In addition to confirming previous studies that the spatial information is preserved from the retina to the optic stalk and then to the optic lamina, we found that the young PR R3/4 axons transiently overshoot and then retract to their final destination, the lamina plexus. We then examined the process of wrapping glia (WG) membrane extension in the eye disc and showed that the WG membrane extensions also follow the retinotopic map. We show that the WG is important for the proper spatial distribution of PR axons in the optic stalk and lamina, suggesting an active role of wrapping glia in the retinotopic map formation.

The giant butterfly-moth Paysandisia archon has spectrally rich apposition eyes with unique light-dependent photoreceptor dynamics.

The palm borer moth Paysandisia archon (Burmeister, 1880) (fam. Castniidae) is a large, diurnally active palm pest. Its compound eyes consist of ~ 20,000 ommatidia and have apposition optics with interommatidial angles below 1°. The ommatidia contain nine photoreceptor cells and appear structurally similar to those in nymphalid butterflies. Two morphological ommatidial types were identified. Using the butterfly numbering scheme, in type I ommatidia, the distal rhabdom consists exclusively of the rhabdomeres of photoreceptors R1-2; the medial rhabdom has contributions from R1-8. The rhabdom in type II ommatidia is distally split into two sub-rhabdoms, with contributions from photoreceptors R2, R3, R5, R6 and R1, R4, R7, R8, respectively; medially, only R3-8 and not R1-2 contribute to the fused rhabdom. In both types, the pigmented bilobed photoreceptors R9 contribute to the rhabdom basally. Their nuclei reside in one of the lobes. Upon light adaptation, in both ommatidial types, the rhabdoms secede from the crystalline cones and pigment granules invade the gap. Intracellular recordings identified four photoreceptor classes with peak sensitivities in the ultraviolet, blue, green and orange wavelength regions (at 360, 465, 550, 580 nm, respectively). We discuss the eye morphology and optics, the photoreceptor spectral sensitivities, and the adaptation to daytime activity from a phylogenetic perspective.

The V-ATPase V1 subunit A1 is required for rhodopsin anterograde trafficking in Drosophila.

Synthesis and maturation of the light sensor, rhodopsin, are critical for the maintenance of light sensitivity and for photoreceptor homeostasis. In Drosophila, the main rhodopsin, Rh1, is synthesized in the endoplasmic reticulum and transported to the rhabdomere through the secretory pathway. In an unbiased genetic screen for factors involved in rhodopsin homeostasis, we identified mutations in vha68-1, which encodes the vacuolar proton-translocating ATPase (V-ATPase) catalytic subunit A isoform 1 of the V1 component. Loss of vha68-1 in photoreceptor cells disrupted post-Golgi anterograde trafficking of Rh1, reduced light sensitivity, increased secretory vesicle pH, and resulted in incomplete Rh1 deglycosylation. In addition, vha68-1 was required for activity-independent photoreceptor cell survival. Importantly, vha68-1 mutants exhibited phenotypes similar to those exhibited by mutations in the V0 component of V-ATPase, vha100-1. These data demonstrate that the V1 and V0 components of V-ATPase play key roles in post-Golgi trafficking of Rh1 and that Drosophila may represent an important animal model system for studying diseases associated with V-ATPase dysfunction.

Diversity and common themes in the organization of ocelli in Hymenoptera, Odonata and Diptera.

We show in a comparative analysis that distinct retinal specializations in insect ocelli are much more common than previously realized and that the rhabdom organization of ocellar photoreceptors is extremely diverse. Hymenoptera, Odonata and Diptera show prominent equatorial fovea-like indentations of the ocellar retinae, where distal receptor endings are furthest removed from the lens surface and receptor densities are highest. In contrast, rhabdomere arrangements are very diverse across insect groups: in Hymenoptera, with some exceptions, pairs of ocellar retinular cells form sheet-like rhabdoms that form elongated rectangular shapes in cross-section, with highly aligned microvilli directions perpendicular to the long axis of cross-sections. This arrangement makes most ocellar retinular cells in Hymenoptera sensitive to the direction of polarized light. In dragonflies, triplets of retinular cells form a y-shaped fused rhabdom with microvilli directions oriented at 60° to each other. In Dipteran ocellar retinular cells microvilli directions are randomised, which destroys polarization sensitivity. We suggest that the differences in ocellar organization between insect groups may reflect the different head attitude control systems that have evolved in these insect groups, but possibly also differences in the mode of locomotion and in the need for celestial compass information.

Regulated Alternative Splicing of Drosophila Dscam2 Is Necessary for Attaining the Appropriate Number of Photoreceptor Synapses.

How the brain makes trillions of synaptic connections using a genome of only 20,000 genes is a major question in modern neuroscience. Alternative splicing is one mechanism that can increase the number of proteins produced by each gene, but its role in regulating synapse formation is poorly understood. In Drosophila, photoreceptors form a synapse with multiple postsynaptic elements including lamina neurons L1 and L2. L1 and L2 express distinct isoforms of the homophilic repulsive protein Dscam2, and since these isoforms cannot bind to each other, cell-specific expression has been proposed to be necessary for preventing repulsive interactions that could disrupt the synapse. Here, we show that the number of synapses are reduced in flies that express only one isoform, and L1 and L2 dendritic morphology is perturbed. We propose that these defects result from inappropriate interactions between L1 and L2 dendrites. We conclude that regulated Dscam2 alternative splicing is necessary for the proper assembly of photoreceptor synapses.

Unique Temporal Expression of Triplicated Long-Wavelength Opsins in Developing Butterfly Eyes.

Following gene duplication events, the expression patterns of the resulting gene copies can often diverge both spatially and temporally. Here we report on gene duplicates that are expressed in distinct but overlapping patterns, and which exhibit temporally divergent expression. Butterflies have sophisticated color vision and spectrally complex eyes, typically with three types of heterogeneous ommatidia. The eyes of the butterfly Papilio xuthus express two green- and one red-absorbing visual pigment, which came about via gene duplication events, in addition to one ultraviolet (UV)- and one blue-absorbing visual pigment. We localized mRNAs encoding opsins of these visual pigments in developing eye disks throughout the pupal stage. The mRNAs of the UV and blue opsin are expressed early in pupal development (pd), specifying the type of the ommatidium in which they appear. Red sensitive photoreceptors first express a green opsin mRNA, which is replaced later by the red opsin mRNA. Broadband photoreceptors (that coexpress the green and red opsins) first express the green opsin mRNA, later change to red opsin mRNA and finally re-express the green opsin mRNA in addition to the red mRNA. Such a unique temporal and spatial expression pattern of opsin mRNAs may reflect the evolution of visual pigments and provide clues toward understanding how the spectrally complex eyes of butterflies evolved.

Microsaccadic sampling of moving image information provides Drosophila hyperacute vision.

Small fly eyes should not see fine image details. Because flies exhibit saccadic visual behaviors and their compound eyes have relatively few ommatidia (sampling points), their photoreceptors would be expected to generate blurry and coarse retinal images of the world. Here we demonstrate that Drosophila see the world far better than predicted from the classic theories. By using electrophysiological, optical and behavioral assays, we found that R1-R6 photoreceptors' encoding capacity in time is maximized to fast high-contrast bursts, which resemble their light input during saccadic behaviors. Whilst over space, R1-R6s resolve moving objects at saccadic speeds beyond the predicted motion-blur-limit. Our results show how refractory phototransduction and rapid photomechanical photoreceptor contractions jointly sharpen retinal images of moving objects in space-time, enabling hyperacute vision, and explain how such microsaccadic information sampling exceeds the compound eyes' optical limits. These discoveries elucidate how acuity depends upon photoreceptor function and eye movements.

A biomimetic fly photoreceptor model elucidates how stochastic adaptive quantal sampling provides a large dynamic range.

Light intensities (photons s-1  µm-2 ) in a natural scene vary over several orders of magnitude from shady woods to direct sunlight. A major challenge facing the visual system is how to map such a large dynamic input range into its limited output range, so that a signal is neither buried in noise in darkness nor saturated in brightness. A fly photoreceptor has achieved such a large dynamic range; it can encode intensity changes from single to billions of photons, outperforming man-made light sensors. This performance requires powerful light adaptation, the neural implementation of which has only become clear recently. A computational fly photoreceptor model, which mimics the real phototransduction processes, has elucidated how light adaptation happens dynamically through stochastic adaptive quantal information sampling. A Drosophila R1-R6 photoreceptor's light sensor, the rhabdomere, has 30,000 microvilli, each of which stochastically samples incoming photons. Each microvillus employs a full G-protein-coupled receptor signalling pathway to adaptively transduce photons into quantum bumps (QBs, or samples). QBs then sum the macroscopic photoreceptor responses, governed by four quantal sampling factors (limitations): (i) the number of photon sampling units in the cell structure (microvilli), (ii) sample size (QB waveform), (iii) latency distribution (time delay between photon arrival and emergence of a QB), and (iv) refractory period distribution (time for a microvillus to recover after a QB). Here, we review how these factors jointly orchestrate light adaptation over a large dynamic range.

Not flying blind: a comparative study of photoreceptor function in flying and non-flying cockroaches.

Flying is often associated with superior visual performance, as good vision is crucial for detection and implementation of rapid visually guided aerial movements. To understand the evolution of insect visual systems it is therefore important to compare phylogenetically related species with different investments in flight capability. Here, we describe and compare morphological and electrophysiological properties of photoreceptors from the habitually flying green cockroach Panchlora nivea and the American cockroach Periplaneta americana, which flies only at high ambient temperatures. In contrast to Periplaneta, ommatidia in Panchlora were characterized by two-tiered rhabdom, which might facilitate detection of polarized light while flying in the dark. In patch-clamp experiments, we assessed the absolute sensitivity to light, elementary and macroscopic light-activated current and voltage responses, voltage-activated potassium (Kv) conductances, and information transfer. Both species are nocturnal, and their photoreceptors were similarly sensitive to light. However, a number of important differences were found, including the presence in Panchlora of a prominent transient Kv current and a generally low variability in photoreceptor properties. The maximal information rate in Panchlora was one-third higher than in Periplaneta, owing to a substantially higher gain and membrane corner frequency. The differences in performance could not be completely explained by dissimilarities in the light-activated or Kv conductances; instead, we suggest that the superior performance of Panchlora photoreceptors mainly originates from better synchronization of elementary responses. These findings raise the issue of whether the evolutionary tuning of photoreceptor properties to visual demands proceeded differently in Blattodea than in Diptera.

EAG channels expressed in microvillar photoreceptors are unsuited to diurnal vision.

KEY POINTS: The principles underlying the evolutionary selection of ion channels for expression in sensory neurons are unclear. Photoreceptor depolarization in the diurnal Drosophila melanogaster is predominantly provided by light-activated transient receptor potential (TRP) channels, whereas repolarization is mediated by sustained voltage-gated K+ channels of the Shab family. In the present study, we show that phototransduction in the nocturnal cockroach Periplaneta americana is predominantly mediated by TRP-like channels, whereas membrane repolarization is based on EAG channels. Although bright light stimulates Shab channels in Drosophila, further restricting depolarization and improving membrane bandwidth, it strongly suppresses EAG conductance in Periplaneta. This light-dependent inhibition (LDI) is caused by calcium and is abolished by chelating intracellular calcium or suppressing eag gene expression. LDI increases membrane resistance, augments gain and reduces the signalling bandwidth. This makes EAG unsuitable for light response conditioning during the day and might have resulted in the evolutionary replacement of EAG by other delayed rectifiers in diurnal insects. ABSTRACT: The principles underlying evolutionary selection of ion channels for expression in sensory neurons are unclear. Among species possessing microvillar photoreceptors, the major ionic conductances have only been identified in Drosophila melanogaster. In Drosophila, depolarization is provided by light-activated transient receptor potential (TRP) channels with a minor contribution from TRP-like (TRPL) channels, whereas repolarization is mediated by sustained voltage-gated K+ (Kv) channels of the Shab family. Bright light stimulates Shab channels, further restricting depolarization and improving membrane bandwidth. In the present study, data obtained using a combination of electrophysiological, pharmacological and molecular knockdown techniques strongly suggest that in photoreceptors of the nocturnal cockroach Periplaneta americana the major excitatory channel is TRPL, whereas the predominant delayed rectifier is EAG, a ubiquitous but enigmatic Kv channel. By contrast to the diurnal Drosophila, bright light strongly suppresses EAG conductance in Periplaneta. This light-dependent inhibition (LDI) is caused by calcium entering the cytosol and is amplified following inhibition of calcium extrusion, and it can also be abolished by chelating intracellular calcium or suppressing eag gene expression by RNA interference. LDI increases membrane resistance, augments gain and reduces the signalling bandwidth, impairing information transfer. LDI is also observed in the nocturnal cricket Gryllus integer, whereas, in the diurnal water strider Gerris lacustris, the delayed rectifier is up-regulated by light. Although LDI is not expected to reduce delayed rectifier current in the normal illumination environment of nocturnal cockroaches and crickets, it makes EAG unsuitable for light response conditioning during the day, and might have resulted in the evolutionary replacement of EAG by other delayed rectifiers in diurnal insects.

Fine structure of the anterior median eyes of the funnel-web spider Agelena labyrinthica (Araneae: Agelenidae).

Only few electron microscopic studies exist on the structure of the main eyes (anterior median eyes, AME) of web spiders. The present paper provides details on the anatomy of the AME in the funnel-web spider Agelena labyrinthica. The retina consists of two separate regions with differently arranged photoreceptor cells. Its central part has sensory cells with rhabdomeres on 2, 3, or 4 sides, whereas those of the ventral retina have only two rhabdomeres on opposite sides. In addition, the rhabdomeres of the ventral retina are arranged in a specific way: Whereas in the most ventral part they form long tangential rows, those towards the center are detached and are arranged radially. All sensory cells are wrapped by unpigmented pigment cell processes. In agelenid spiders the axons of the sensory cells exit from the middle of the cell body; their fine structure and course through the eye cup is described in detail. In the central part of the retina efferent nerve fibres were found forming synapses along the distal region of the receptor cells. A muscle is attached laterally to each eye cup that allows mainly rotational movements of the eyes. The optical performance (image resolution) of these main eyes with relatively few visual cells is discussed.