The basement membrane of the insect and crustacean compound eye: Definition,fine structure,and comparative morphology

Summary The basement membrane of the compound eye of four insect species and three crustacean species was investigated employing electron microscopy. The basement membrane consists of an extracellular (basal lamina) and a cellular portion, the latter being composed of the flattened terminal extensions of cone cells and accessory pigment cells in insects and distal pigment cells in crustaceans. Other cells can also contribute to the basement membrane. It is thus a complex structure in all well-developed compound eyes. The cellular contributions vary in different species and were found to correlate to specific taxonomic units.     

Changes in cGMP concentration correlate with some, but not all, aspects of the light-regulated conductance of frog rod photoreceptors

Cyclic GMP has been implicated in controlling the light-regulated conductance of rod photoreceptors of the vertebrate retina. However, there is little direct evidence correlating changes in cGMP concentration with the light-regulated permeability mechanism in living cells. A preparation of intact frog rod outer segments suspended in a Ringer's medium containing low Ca2+ has been used to demonstrate that initial changes in total cellular cGMP concentration parallel changes in the light-regulated membrane current over a wide range of light intensities. At light intensities bleaching from 160 to 5.6 X 10(6) rhodopsin molecules/rod/s, decreases in the response latency for the cGMP kinetics parallel decreases in the latent period of the electrical response. Further, changes in the rate of the cGMP decrease parallel the rate of membrane current suppression as the light intensity is varied. Up to 10(5) cGMP molecules are hydrolyzed per photolyzed rhodopsin, consistent with in vitro studies showing that each bleached rhodopsin can activate over 100 phosphodiesterase molecules. Addition of the Ca2+ ionophore, A23187, does not affect the initial kinetics of the cGMP decrease or of the electrical response, excluding a direct role for Ca2+ in the initial events of phototransduction. These results are consistent with cGMP being the intracellular messenger that links rhodopsin isomerization with changes in membrane permeability upon illumination. It is unlikely, however, that light-induced changes in total cGMP concentration are the sole regulators of membrane current. This is suggested by several observations: at bright light intensities, the subsecond light-induced cGMP decrease is essentially complete prior to complete suppression of membrane current; maximal light-induced decreases in cGMP concentration occur at all light intensities tested, whereas the extent of membrane current suppression varies over the same range of light intensities; changing the external Ca2+ concentration from 1 mM to 10 nM in the dark causes an increase in membrane current that is significantly more rapid than corresponding changes in cGMP concentration. Thus, light-induced changes in total cellular cGMP concentration correlate with some, but not all, aspects of the visual excitation process in vertebrate photoreceptors.     

Rhabdom changes in the shrimp,Palaemonetes

The fine structure of the principal compound eye of the shrimp, Palaemonetes, was studied under conditions of light and dark adaptation. Ommatidium the situation in other decapod crustaceans. Light and dark adapted eyes differ in that the rhabdom changes its shape; morphological evidence suggests a possible sequence of events involving production, utilization, and degradation of photoreceptor membrane, a discontinuous process occurring only during changes from light to dark and dark to light. A hypothesis of membrane turnover is proposed.     

Photosensing in chemotrophic, non-phototrophic bacteria: let there be light sensing too

Putative light-sensing proteins are ubiquitously encoded in the genomes of chemotrophic, non-photosynthetic bacteria. Surprisingly, these are not limited to UV-receptors: the metagenome of the chemotrophic prokaryotes encodes representatives of all known major families of photoreceptors. Insight into the mechanism of light-mediated signaling is relatively advanced, but most light-induced physiological and behavioral responses in chemotrophic bacteria are not well understood. In the current era of 'omics' studies, this knowledge gap could be closed rapidly. Here we review the state of the art in this field. Because light signals can be manipulated accurately, these photoreceptors might help provide a systems-level understanding of the cytology of bacteria.     

Ultraviolet polarisation sensitivity in the stomatopod crustacean <Emphasis Type="Italic">Odontodactylus scyllarus</Emphasis>

The ommatidia of crustacean eyes typically contain two classes of photoreceptors with orthogonally oriented microvilli. These receptors provide the basis for two-channel polarisation vision in the blue–green spectrum. The retinae of gonodactyloid stomatopod crustaceans possess a great variety of structural specialisations for elaborate polarisation vision. One type of specialisation is found in the small, distally placed R8 cells within the two most ventral rows of the mid-band. These ultraviolet-sensitive photoreceptors produce parallel microvilli, a feature suggestive for polarisation-sensitive photoreceptors. Here, we show by means of intracellular recordings combined with dye-injections that in the gonodactyloid species Odontodactylus scyllarus, the R8 cells of mid-band rows 5 and 6 are sensitive to linear polarised ultraviolet light. We show that mid-band row 5 R8 cells respond maximally to light with an e-vector oriented parallel to the mid-band, whereas mid-band row 6 R8 cells respond maximally to light with an e-vector oriented perpendicular to the mid-band. This orthogonal arrangement of ultraviolet-sensitive receptor cells could support ultraviolet polarisation vision. R8 cells of rows 5 and 6 are known to act as quarter-wave retarders around 500 nm and thus are the first photoreceptor type described with a potential dual role in polarisation vision.     

Adaptation in the Ventral Eye of Limulus is Functionally Independent of the Photochemical Cycle, Membrane Potential, and Membrane Resistance

The early receptor potential (ERP), membrane potential, membrane resistance, and sensitivity were measured during light and/or dark adaptation in the ventral eye of Limulus. After a bright flash, the ERP amplitude recovered with a time constant of 100 ms, whereas the sensitivity recovered with an initial time constant of 20 s. When a strong adapting light was turned off, the recovery of membrane potential and of membrane resistance had time-courses similar to each other, and both recovered more rapidly than the sensitivity. The receptor depolarization was compared during dark adaptation after strong illumination and during light adaptation with weaker illumination; at equal sensitivities the cell was more depolarized during light adaptation than during dark adaptation. Finally, the waveforms of responses to flashes were compared during dark adaptation after strong illumination and during light adaptation with weaker illumination. At equal sensitivities (equal amplitude responses for identical flashes), the responses during light adaptation had faster time-courses than the responses during dark adaptation. Thus neither the photochemical cycle nor the membrane potential nor the membrane resistance is related to sensitivity changes during dark adaptation in the photoreceptors of the ventral eye. By elimination, these results imply that there are (unknown) intermediate process(es) responsible for adaptation interposed between the photochemical cycle and the electrical properties of the photoreceptor.     

The role of cytoplasmic calcium in photoreceptor light adaptation.

The process of light adaptation in vertebrate rod and cone photoreceptors is believed to involve a diffusible cytoplasmic messenger. Two lines of evidence indicate that photoreceptor light adaptation is mediated by a light-induced fall in cytoplasmic calcium concentration (Ca2+i). First, if changes in calcium concentration are slowed by the incorporation of calcium chelators into the photoreceptor cytoplasm then light adaptation is slowed also. Second, if the normal control of Ca2+i is prevented by simultaneously minimising calcium influx and efflux across the outer segment membrane by means of external solution changes, then all of the manifestations of light adaptation are abolished. Furthermore, recent results show that changes in Ca2+i imposed in the absence of light are sufficient to cause at least some of the manifestations of light adaptation. Together these results indicate that calcium acts as the messenger of light adaptation in the photoreceptors of both lower and higher vertebrates.     

Photosensitive neurons in mollusks

In addition to regular photoreceptors, some invertebrates possess simple extraocular photoreceptors. For example, the central ganglia of mollusks contain photosensitive neurons. These neurons are located on the dorsal surface of the ganglia and based on their electrophysiological properties, it has been postulated that they are the internal photoreceptors. However, besides the eye, transduction of the light also occurs in these extra-ocular photoreceptors. In the present work, we analyse the reactivity of these nerve cells to light and describe the underlying mechanism mediating the light-induced response.     

Membrane filtering properties of the bumblebee (Bombus terrestris) photoreceptors across three spectral classes

Filtering properties of the membrane form an integral part of the mechanisms producing the light-induced electrical signal in insect photoreceptors. Insect photoreceptors vary in response speed between different species, but recently it has also been shown that different spectral photoreceptor classes within a species possess diverse response characteristics. However, it has not been quantified what roles phototransduction and membrane properties play in such diversity. Here, we use electrophysiological methods in combination with system analysis to study whether the membrane properties could create the variation of the response speed found in the bumblebee (Bombus terrestris) photoreceptors. We recorded intracellular responses from each photoreceptor class to white noise-modulated current stimuli and defined their input resistance and linear filtering properties. We found that green sensitive cells exhibit smaller input resistance and membrane impedance than other cell classes. Since green sensitive cells are the fastest photoreceptor class in the bumblebee retina, our results suggest that the membrane filtering properties are correlated with the speed of light responses across the spectral classes. In general, our results provide a compelling example of filtering at the sensory cell level where the biophysical properties of the membrane are matched to the performance requirements set by visual ecology.     

Induction of reproductive diapause via perception of photoperiod through the compound eyes in the adult blow fly, Protophormia terraenovae

Covering and surgical removal of the compound eyes were performed to localize photoreceptors for photoperiodic responses in the blow fly Protophormia terraenovae (Diptera, Calliphoridae). Adult females showed a long-day photoperiodic response to control reproductive diapause. When the compound eyes were bilaterally covered with silver paint, diapause incidence increased under diapause-preventing conditions, i.e., a long-day photoperiod and constant light, as though flies were kept under constant darkness. Neither silver painting on a medial region of the head capsule nor control painting in which both compound eyes were painted in a clear solvent caused significant effects on diapause incidence. Unilateral painting of the compound eye caused an increment of diapause incidence under constant light but no effects under a long-day photoperiod. When the compound eyes were bilaterally removed, all the flies developed their ovaries both under a long-day and a short-day photoperiod. Unilateral removal of the compound eye also caused ovarian development under a short-day photoperiod, whereas removal of one antennal lobe or all ocelli caused no effects on diapause incidence. Since P. terraenovae completely lost responsiveness to photoperiod after blinding of the compound eyes, it is likely that this fly perceives photoperiod through its compound eyes. Accepted: 18 February 1997     

Lanthanum mimicks the trp photoreceptor mutant of Drosophila in the blowfly Calliphora

The effect of lanthanum on the light response of blowfly (Calliphora erythrocephala) photoreceptors was studied. The electrophysiological behaviour of the photoreceptors in the presence of La can be summarized as follows: 1. Upon long stimulation the photoreceptors responded with a 'transient receptor potential', i.e. the cells depolarized at the onset of the stimulus and then repolarized to (or below) the resting potential. This effect was dependent on stimulus intensity and occurred only at high intensities. During illumination membrane noise was reduced. 2. The light-induced changes in membrane potential were paralleled by changes in membrane resistance. 3. The time course of the receptor response was slowed down. 4. Light adaptation led to an increase in response latency. 5. The recovery of the receptor response after light adaptation was slowed down. 6. The sensitivity of the receptor cells measured by the response to short light stimuli was reduced. In summary, the electrophysiological behaviour of Calliphora photoreceptors in the presence of La was very similar to that of the photoreceptors of the trp (transient receptor potential) mutant of Drosophila melanogaster. This result suggests that La and trp mutation affect the same cellular processes in the photoreceptors.     

Fine structural correlates of sensitivity in the eyes of the ctenid spider, Cupiennius salei Keys

We studied fine structural correlates of sensitivity in the principal and secondary eyes of the nocturnal hunting spider Cupiennius salei. In night-adapted eyes the four rhabdomeres of the principal eye photoreceptors are 58 mum long and occupy together 234 mum(2) in cross-section (average), whereas the two rhabdomeres of the secondary eye photoreceptors are about 49 mum long and measure 135-183 mum(2) in cross-section (average). The rhabdoms (photosensitive structures) consist of tightly packed microvilli (diameter 0.1 mum, maximum length 3.5 mum) and occupy up to 63% of the cross-sectional area of the retina. When calculating the amount of light the eyes of Cupiennius are able to capture according to their morphological characteristics, the values for sensitivity S(see Land, 1981, 1985) are between 78 and 109 mum(2). Cupiennius is more sensitive than any other hunting spider examined except Dinopis whose posterior median eyes are the most sensitive ones of all terrestrial arthropod eyes studied. In day-adapted eyes the rhabdomeral microvilli are almost completely degraded. The remaining microvillar surface amounts to only about one-tenth compared with the night-adapted state. Efferent synaptoid terminals have been found to contact the photoreceptors in all eyes of C. salei. The present fine structural data are compared to previous electrophysiological research and underline the significance of vision in Cupiennius.     

Stomatopod eye structure and function: a review

Stomatopods (mantis shrimps) possess apposition compound eyes that contain more photoreceptor types than any other animal described. This has been achieved by sub-dividing the eye into three morphologically discrete regions, a mid-band and two laterally placed hemispheres, and within the mid-band, making simple modifications to a commonly encountered crustacean photoreceptor pattern of eight photoreceptors (rhabdomeres) per ommatidium. Optically the eyes are also unusual with the directions of view of the ommatidia of all three eye regions skewed such that over 70% of the eye views a narrow strip in space. In order to scan the world with this strip, the stalked eyes of stomatopods are in almost continual motion. Functionally, the end result is a trinocular eye with monocular range finding capability, a 12-channel colour vision system, a 2-channel linear polarisation vision system and a line scan sampling arrangement that more resembles video cameras and satellite sensors than animal eyes. Not surprisingly, we are still struggling to understand the biological significance of stomatopod vision and attempt few new explanations here. Instead we use this special edition as an opportunity to review and summarise the structural aspects of the stomatopod retina that allow it to be so functionally complex.     

Colour in the eyes of insects

Many insect species have darkly coloured eyes, but distinct colours or patterns are frequently featured. A number of exemplary cases of flies and butterflies are discussed to illustrate our present knowledge of the physical basis of eye colours, their functional background, and the implications for insect colour vision. The screening pigments in the pigment cells commonly determine the eye colour. The red screening pigments of fly eyes and the dorsal eye regions of dragonflies allow stray light to photochemically restore photoconverted visual pigments. A similar role is played by yellow pigment granules inside the photoreceptor cells which function as a light-controlling pupil. Most insect eyes contain black screening pigments which prevent stray light to produce background noise in the photoreceptors. The eyes of tabanid flies are marked by strong metallic colours, due to multilayers in the corneal facet lenses. The corneal multilayers in the gold-green eyes of the deer fly Chrysops relictus reduce the lens transmission in the orange-green, thus narrowing the sensitivity spectrum of photoreceptors having a green absorbing rhodopsin. The tapetum in the eyes of butterflies probably enhances the spectral sensitivity of proximal long-wavelength photoreceptors. Pigment granules lining the rhabdom fine-tune the sensitivity spectra.     

Ultrastructural study of the naupliar eye of the ostracodeVargula graminicola (Crustacea,Ostracoda)

Summary Ostracodes, like other crustaceans, have a simple naupliar eye that is built upon a theme of three eye cups surrounded by a layer of screening pigments. The single naupliar eye of the ostracodeVargula graminicola is situated medially on the dorsal-anterior side of the body and has three fused eye cups, two dorso-lateral and one ventral. Each eye cup has the following components: (1) pigment cells between the eye cups, (2) tapetal cells, (3) retinular cells with (4) microvillar rhabdomeres, and (5) axons extending into the protocerebrum. Typically two retinular cells contribute lateral microvilli to each rhabdom. The two dorso-lateral eye cups have about 40 retinular cells (20 rhabdoms) and the ventral eye cup has about 30 retinular cells (15 rhabdoms). Typical of myodocopid naupliar eyes (as reported from light microscopic studies), no lens cells or cuticular lenses were observed. The presence of tapetal cells identifies theVargula eye as a maxillopod-ostracode type crustacean naupliar eye. It is unlikely that the naupliar eye ofV. graminicola functions in image formation, rather it probably functions in the mediation of simple taxis towards and away from light.     

The frontal eyes of crustaceans

Frontal eyes of crustaceans (previously called nauplius eye and frontal organs) are usually simple eyes that send their axons to a medial brain centre in the anterior margin of the protocerebrum. Investigations of a large number of recent species within all major groups of the Crustacea have disclosed four kinds of frontal eyes correlated with taxonomic groups and named after them as the malacostracan, ostracod-maxillopodan, anostracan, and phyllopodan frontal eyes. The different kinds of eyes have been established using the homology concept coined by Owen [Owen, R., 1843. Lectures on the comparative anatomy and physiology of the invertebrate animals. Longman, Brown, Green, Longmans, London] and the criteria for homology recommended by Remane [Remane, A., 1956. Die Grundlagen des natürlichen Systems, der vergleichenden Anatomie und der Phylogenetik. 2nd ed. Akademische Verlagsgesellschaft, Geest und Portig, Leipzig]. Common descent is not used as a homology criterion. Frontal eyes bear no resemblance to compound eyes and in the absence of compound eyes, as in the ostracod-maxillopodan group, frontal eyes develop into complicated mirror, lens-mirror, and scanning eyes. Developmental studies demonstrate widely different ways to produce frontal eyes in phyllopods and malacostracans. As a result of the studies of recent frontal eyes in crustaceans, it is concluded by extrapolation that in crustacean ancestors four non-homologous frontal eye types evolved that have remained functional in spite of concurrent compound eyes.     

Evolution of Insect Eyes: Tales of Ancient Heritage, Deconstruction, Reconstruction, Remodeling, and Recycling

The visual organs of insects are known for their impressive evolutionary conservation. Compound eyes built from ommatidia with four cone cells are now accepted to date back to the last common ancestor of insects and crustaceans. In species as different as fruit flies and tadpole shrimps, the stepwise cellular patterning steps of the early compound eye exhibit detailed similarities implying 500 million years of developmental conservation. Strikingly, there is also a cryptic diversity of insect visual organs, which gives proof to evolution’s versatility in molding even the most tenacious structures into something new. We explore this fascinating aspect in regard to the structure and function of a variety of different insect eyes. This includes work on the unique compound–single-chamber combination eye of twisted-winged insects and the bizarre evolutionary trajectories of specialized larval eyes in endopterygote insects.     

Performance of blue- and green-sensitive photoreceptors of the cricket Gryllus bimaculatus

The compound eye of the cricket Gryllus bimaculatus contains a specialized dorsal rim area (DRA) populated by distinct blue-sensitive photoreceptors responsible for perception of polarized light. The rest of the eye is dominated by green-sensitive photoreceptors. Using patch clamp we studied dissociated ommatidia of nocturnal adults and diurnal eight-instar nymphs with the goals (1) of characterizing the biophysical properties of cricket photoreceptors in general and (2) describing the functionally dissimilar blue- and green-sensitive photoreceptors in terms of voltage-gated channel composition and signal coding. Despite different lifestyles, adult and nymph photoreceptors were indistinguishable. No significant circadian changes were observed in K⁺ currents. In contrast, prominent differences were seen between blue- and green-sensitive photoreceptors. The former were characterized by relatively low absolute sensitivity, high input resistance, slow quantum bumps with long latencies, small light-induced and K⁺ currents and low steady-state depolarization. Information rate, a measure of photoreceptor performance calculated from voltage responses to bandwidth-limited white noise-modulated light contrast, was 87 ± 8 bits s^?1 in green-sensitive photoreceptors vs. 59 ± 14 bits s^?1 in blue-sensitive photoreceptors, implying a limited role of DRA in the perception of visual contrasts. In addition, evidence of electrical coupling between photoreceptors is presented.     

The role of dermal photoreceptors during the sea lamprey (<Emphasis Type="Italic">Petromyzon marinus</Emphasis>) spawning migration

Light avoidance in larval lampreys is mediated by dermal photoreceptors located in the tail. These photoreceptors continue to function in adults, but they seem redundant because post-metamorphic lampreys possess well-developed eyes. This study examined the role of dermal photoreceptors in adult sea lampreys by testing whether temperature-induced changes in refuge-seeking behavior are mediated by a reduction in dermal photosensitivity. In a lighted arena containing a single shaded refuge platform, lampreys at 22°C displayed five times less search activity and were less likely to attach beneath the refuge platform than lampreys at either 7 or 15°C. A behavioral assay for tail photosensitivity (locomotor response to tail illumination) revealed a corresponding reduction in dermal photosensitivity at 22°C. Moreover, the responses to head illumination (eyes and pineal) did not correspond with the observed light avoidance behaviors. The head was less responsive to light than the tail and was not influenced by temperature. These results provide strong evidence that the dermal photoreceptors continue to mediate light avoidance in adult lampreys, even though adults possess fully functional eyes. The fact that the eyes apparently do not take on this role suggests that there is functional specialization between these two light sensing systems.     

Vanadate, tungstate and molybdate activate rod outer segment phosphodiesterase in the dark

Anionic activation of rod outer segment phosphodiesterase by vanadate, molybdate and tungstate is demonstrated. Comparisons are made to adenylate cyclase, which is known to be activated by vanadate and molybdate but not by tungstate. In view of the differences in anionic activation between these two important enzymatic regulators of intracellular cyclic nucleotide metabolism, it is possible that tungstate can be used as a selective probe for the effects of phosphodiesterase activity in photoreceptors and other cells. The known electrophysiological stimulation of Limulus photoreceptors by these anions is also interpreted in light of our results. If anionic production of quantum bumps in Limulus photoreceptors is mediated by changes in cyclic nucleotides, then the electrophysiological response of Limulus photoreceptors to tungstate may indicate a role for phosphodiesterase rather than adenylate cyclase in mediating light-induced cyclic nucleotide alterations in this cell.