Nonvisual Photoreceptors in Arthropods with Emphasis on Their Putative Role as Receptors of Natural Zeitgeber Stimuli

In various insect and arachnid species, three different types of photoreceptors that do not serve image processing have been discovered and analyzed by means of neurobiological methods: They can be found for example: (1) as lamina and lobula organs (LaOs and LoOs) next to the optic neuropils in the optic lobes of holo‐ and hemimetabolous insects; (2) inside the last ganglia of the cord of the scorpion and a marine midge; and (3) as modified visual photoreceptors in metamorphosized larval stemmata and the lateral eyes of scorpions, which have been compound eyes in fossil scorpion relatives. Immunocytology with various antibodies against proteins of the phototransduction cascade, the rhabdom turnover cycle and neurotransmitters of afferent and efferent pathways, was combined with light‐ and ultrastructural investigations in well‐defined adaptational states, in order to study their photoreceptive function and neuronal wiring. Pilot chronobiological experiments with a newly developed twilight simulating lamp, behavioral studies, and model calculations provide evidence that these photoreceptors may well serve a role in the complex task of detecting time cues out of natural dawn and dusk.

“…Clearly more work will be necessary before truly informed judgements can be made about the functional significance of the diversity in photoreception for entrainment. A first step will be the precise identification of photoreceptors and investigations of the mechanisms of transduction, processing and transmission of temporal information provided by the daily light cycle.…” ()     

Repetitive spikes in photoreceptor axons of the scorpion eye. Invertebrate eye structure and tetrodotoxin

A graded depolarization accompanied by nerve impulses can be recorded from the scorpion lateral and median eyes in response to light. Electron microscopy shows that axons forming the optic nerve arise directly from the photoreceptors. Thus, photoreceptors must respond both by the generation of a slow receptor potential and the initiation of spikes. The latency of the first spike, and the maximal and mean discharge frequencies were a function of light intensity. Spikes were abolished by tetrodotoxin. Repetitive firing to light therefore appears to be a normal response of scorpion photoreceptors and is the result of regenerative Na influx in the cell membrane.     

Circadian organization in Aplysia californica.

Substantial progress has been made in unraveling the organization of the circadian system of Aplysia californica. There are at least three circadian pacemakers in Aplysia. One has been localized in each eye and a third lies outside the eyes. Removal of the eyes disrupts the free-running locomotor activity rhythm; however, an extraocular oscillator can mediate a free-running rhythm in some eyeless animals. Although photoreceptors sufficient for entrainment of the ocular oscillator have been localized in the retina, photoreceptors outside the eyes are capable of "driving" a diurnal rhythm of locomotor activity and may also influence entrainment of ocular pacemakers. Finally, attention has been focused on the optic nerve as a coupling pathway between various parts of the system. The evidence suggests that information transmitted in the optic nerves is involved in entrainment of the ocular pacemaker by light, and in ocular control of the locomotor activity rhythm.     

Spatial organization of lipids in the human retina and optic nerve by MALDI imaging mass spectrometry

MALDI imaging mass spectrometry (IMS) was used to characterize lipid species within sections of human eyes. Common phospholipids that are abundant in most tissues were not highly localized and observed throughout the accessory tissue, optic nerve, and retina. Triacylglycerols were highly localized in accessory tissue, whereas sulfatide and plasmalogen glycerophosphoethanolamine (PE) lipids with a monounsaturated fatty acid were found enriched in the optic nerve. Additionally, several lipids were associated solely with the inner retina, photoreceptors, or retinal pigment epithelium (RPE); a plasmalogen PE lipid containing DHA (22:6), PE(P-18:0/22:6), was present exclusively in the inner retina, and DHA-containing glycerophosphatidylcholine (PC) and PE lipids were found solely in photoreceptors. PC lipids containing very long chain (VLC)-PUFAs were detected in photoreceptors despite their low abundance in the retina. Ceramide lipids and the bis-retinoid, N-retinylidene-N-retinylethanolamine, was tentatively identified and found only in the RPE. This MALDI IMS study readily revealed the location of many lipids that have been associated with degenerative retinal diseases. Complex lipid localization within retinal tissue provides a global view of lipid organization and initial evidence for specific functions in localized regions, offering opportunities to assess their significance in retinal diseases, such as macular degeneration, where lipids have been implicated in the disease process.     

Nocturnal vision and landmark orientation in a tropical halictid bee

BACKGROUND: Some bees and wasps have evolved nocturnal behavior, presumably to exploit night-flowering plants or avoid predators. Like their day-active relatives, they have apposition compound eyes, a design usually found in diurnal insects. The insensitive optics of apposition eyes are not well suited for nocturnal vision. How well then do nocturnal bees and wasps see? What optical and neural adaptations have they evolved for nocturnal vision? RESULTS: We studied female tropical nocturnal sweat bees (Megalopta genalis) and discovered that they are able to learn landmarks around their nest entrance prior to nocturnal foraging trips and to use them to locate the nest upon return. The morphology and optics of the eye, and the physiological properties of the photoreceptors, have evolved to give Megalopta's eyes almost 30 times greater sensitivity to light than the eyes of diurnal worker honeybees, but this alone does not explain their nocturnal visual behavior. This implies that sensitivity is improved by a strategy of photon summation in time and in space, the latter of which requires the presence of specialized cells that laterally connect ommatidia into groups. First-order interneurons, with significantly wider lateral branching than those found in diurnal bees, have been identified in the first optic ganglion (the lamina ganglionaris) of Megalopta's optic lobe. We believe that these cells have the potential to mediate spatial summation. CONCLUSIONS: Despite the scarcity of photons, Megalopta is able to visually orient to landmarks at night in a dark forest understory, an ability permitted by unusually sensitive apposition eyes and neural photon summation.     

The fine structure of the visual system of Lycosa (Araneae: Lycosidae)

Summary Wolf spiders have four pairs of eyes distributed in three rows. The first row which lie in the frontal region of the caparace, just above the chelicera, contains four eyes: a medial pair known as the anterior medial eyes (AM eyes or principal eyes) and two smaller eyes known as the anterior lateral eyes (AL eyes). The second row which is located also in the frontal region of the prosoma consists of two big eyes. These are the posterior median eyes (PM eyes). The third row contains the posterior lateral eyes (PL eyes) which lie in the flanks of the prosomal caparace. The AL, PM and PL eyes are the so-called secondary eyes.The electron microscope shows that the AM eye photoreceptor cells have the rhabdomere in their distal segment, just behind the vitreous body. The rhabdomere consists of closely packed microvilli about 0.5 long exhibiting a uniform diameter of 500 Å. Each rhabdom consists of two rhabdomeres. The distal segment of the photoreceptor has a prismatic shape with four or five faces depending of their location within the retina.The distribution of the rhabdoms follows two different patterns or organization. In the peripheral portion of the retina they lie oriented either parallel or perpendicular to the retinal radii. In this zone most cells have four sides while in the central region five sided cells are predominant. These cells bear microvilli in three of their five faces and the rhabdoms show no preferential mode of orientation. Each retina contains approximately 450 photoreceptors. In the secondary eyes the rhabdoms lie far from the vitreous body behind the level of the cell nuclei. A light reflecting layer or tapetum is present in the three pairs of secondary eyes. The microvilli forming the rhabdomeres of the AL eyes are 0.5 long and 500 Å wide, while the microvilli of the rhabdomeres in the PM and PL eyes are longer and thicker (1.5 long and 550–660 Å wide). In these eyes the rhabdomeres are surrounded by abundant extracellular material. Like in the principal eyes each rhabdom consists of two rhabdomeres.In the AL eyes the photoreceptor cells send out collateral branches which end, without any specialization, in contact with other photoreceptors. Clear fibers running parallely to the tapetum have been found in the secondary eyes. These fibers show specialized regions corresponding to the zones of contact with the photoreceptor cells. These areas are characterized by an increased density of the membranes and groups of vesicles (the vesicles lie within the fibers).The optic nerves consist of photoreceptor axons, glial cells and a fibrous perineural sheath. The AM and AL eyes are connected to the CNS by a single compact optic nerve while in the PM and PL eyes the optic nerve consists of several individual bundles. The total number of optic fibers entering into the brain is about 12.000.A layer of glial cytoplasm covers each photoreceptor axon and the mesaxons appear as double lines which bifurcate frequently.Research sponsored by the Air Force Office of Scientific Research, Office of Aerospace Research, United States Air Force, under AFOSR Grant Nr. 618-64.     

Immunocytochemical demonstration of S-antigen (arrestin) in the brain of the blowfly Calliphora vicina

S-Antigen (arrestin)-immunoreaction can be considered as a marker for retinal and extraretinal photoreceptors in both vertebrate and invertebrate species. The present immunocytochemical study with the blowfly Calliphora vicina revealed S-antigen immunoreaction in retinal photoreceptors and various groups of neurons bilaterally distributed in the optic lobes and in the proto-, deuto- and tritocerebrum. S-Antigen-immunoreactive processes and terminal formations were found in the lower division of the central body complex and in the neuropil of the mushroom body. Also neuropil regions of the optic lobe, the lamina, medulla and lobula displayed S-antigen-immunoreactive fibers which were arranged in different patterns. These immunocytochemical data suggest that extraocular photoreceptors may be located in various parts of the blowfly brain. They provide a structural basis for further experiments which are needed to identify definitely these elements as extraretinal photoreceptors.     

Development of the eye in the turbot Psetta maxima (Teleosti) from hatching through metamorphosis

Development of the eyes during the larval and metamorphic stages of the turbot Psetta maxima (Teleosti) was studied using microscopy. Events during differentiation of both eyes occur simultaneously, and no differences between he migrating and no-migrating eye were observed during metamorphosis. At hatching, the eyes are rudimentary, consisting of a neuroepithelial optic cup and a small lens. During larval development, major changes occur in the lens and retina, in which cones are the only photoreceptors. The appearance of rods is delayed until metamorphosis. The outer ocular layers (sclera and choroid) arise during larval development as thin connective layers with little differentiation. These layers undergo important changes just before and during metamorphosis. These results indicate that development of the individual components of the eye occurs at different times. Those of ectodermal origin appear early, providing a simple visual organ during larval life. By metamorphosis, the eye shows adult characteristics, including two types of photoreceptors, a rich choroid vascular supply and ocular structures involved in protecting, shaping, and moving the eye. J Morphol 233:31–42, 1997. © 1997 Wiley-Liss, Inc.     

Ultrastructure of phaosomous photoreceptors in Stylaria lacustris (Naididae, ‘Oligochaeta’, Clitellata) and their importance for the position of the Clitellata in the phylogenetic system of the Annelida

Many species of Naididae possess a pair of pigmented eyes. Within Clitellata, eyes are generally present in Hirudinea, whereas Naididae are the only oligochaete taxon having these sense organs. The eyes of Naididae are epidermal structures and consist of a multicellular pigment cup in which a single row of five to six photoreceptor cells is embedded. The sensory cells are typical phaosomes: the photoreceptive structures (microvilli) project into a cavity formed by the sensory cell itself. In Stylaria lacustris this cavity opens to the exterior, clearly documenting that it represents an invagination of the apical cell membrane. The density of sensory microvilli is comparatively low and a central vitreous body is lacking. Similar phaosomous photoreceptors, not associated with either pigmented or unpigmented supporting cells, occur in the epidermis of the anterior end. These photoreceptors correspond to those found in other Clitellata, confirming that phaosomes are the only known type of photoreceptor cell occurring in this taxon. As a result of their simple structure they have been regarded as plesiomorphic for Annelida. However, an out‐group comparison with eyes and photoreceptors occurring in polychaetes and other spiralians reveals that they, in fact, are a rather specialized type of photoreceptor. Despite the simple structure, they most likely represent an autapomorphy of Clitellata. It follows that in all probability, these phaosomes are a secondarily evolved type of photoreceptor, which arose within the oligochaete clade after the primary photoreceptors present in the out‐groups had been lost. This loss might have occurred during evolution of a burrowing life style within the sediment and subsequent invasion of the terrestrial environment.     

Alterations of the eyes of Carinaria lamarcki (Gastropoda, Heteropoda) during the long pelagic cycle

 The eyes of different larval stages of Carinaria lamarcki were examined ultrastructurally. In all larval stages the eyes consist of a cornea, a lens and an everse retina. The photoreceptors in young larvae are exclusively of the ciliary type. In old larvae, however, two types of photoreceptors are present and the retina is composed of two segments: a posterior segment with altered ciliary photoreceptors (=type I sensory cells) and an anterior segment with what are presumably rhabdomeric photoreceptors (=type II sensory cells). The anterior retina is interpreted here as an accelerted character. Furthermore, the arrangement of the pigment granules changes during the long larval development being cup shaped in young larvae versus ribbon shaped in old larvae. The findings allow for the conclusions that: (a) the ciliary photoreceptors are correlated with the long larval period of Heteropoda and that (b) the eyes are altered continuously during the larval cycle. Accepted: 6 July 1998     

Neurosecretory cells in the circadian-clock system of the scorpion,Androctonus australis

Summary The somata of the efferent neurosecretory fibers that control the circadian sensitivity rhythm in the median eyes of the scorpion, Androctonus australis, were detected in the brain by retrograde labeling with Lucifer Yellow CH. A total of 20–40 neurons are arranged in two groups displaying a bilaterally symmetrical, marginal position near the circumesophageal connectives. Half the cells in each group send fibers into the ipsilateral optic nerve; the fibers from the other half enter the contralateral optic nerve.     

Motor excitation with reference to neural photoreception in scorpion

The effect of photic input from the neural photoreceptors in the metasoma of the scorpion $\text{Heterometrus}$ on the motor activity was examined. It was observed that the illumination of these photoreceptors results in the excitation of a large number of efferent fibers innervating various parts of the body. Furthermore, the input was also found to elicit a bending movement of the telson which constitutes an important part of the sting reflex of the animal.     

Foveate vision in deep-sea teleosts: a comparison of primary visual and olfactory inputs

The relative importance of vision in a foveate group of alepocephalid teleosts is examined in the context of a deep-sea habitat beyond the penetration limits of sunlight. The large eyes of Conocara spp. possess deep convexiclivate foveae lined with Müller cells comprising radial shafts of intermediate filaments and horizontal processes. Photoreceptor cell (171.8 x 10(3) rods mm(-2)) and retinal ganglion cell (11.9 x 10(3) cells mm(-2)) densities peak within the foveal clivus and the perifloveal slopes, respectively, with a centro-peripheral gradient between 3:1 (photoreceptors) and over 20:1 (ganglion cells). The marked increase in retinal sampling localized in temporal retina, coupled with a high summation ratio (13:1), suggest that foveal vision optimizes both spatial resolving power and sensitivity in the binocular frontal visual field. The elongated optic nerve head is comprised of over 500 optic papillae, which join at the embryonic fissure to form a thin nervous sheet behind the eye. The optic nerve is divided into two axonal bundles; one receiving input from the fovea (only unmyelinated axons) and the other from non-specialized retinal regions (25% of axons are myelinated), both of which appear to be separated as they reach the visual centres of the central nervous system. Comparison of the number of primary (first-order) axonal pathways for the visual (a total of 63.4 x 10(6) rod photoreceptors) and olfactory (a total of 15.24 x 10(3) olfactory nerve axons) inputs shows a marked visual bias (ratio of 41:1). Coupled with the relative size of the optic tecta (44.0 mm3) and olfactory bulbs (0.9 mm3), vision appears to play a major role in the survival of these deep-sea teleosts and emphasizes that ecological and behavioural strategies account for significant variation in sensory brain structure.     

BRAIN PHOTORECEPTOR PATHWAYS CONTRIBUTING TO CIRCADIAN RHYTHMICITY IN CRAYFISH

Freshwater crayfish have three known photoreceptive systems: the compound eyes, extraretinal brain photoreceptors, and caudal photoreceptors. The primary goal of the work described here was to explore the contribution of the brain photoreceptors to circadian locomotory activity and define some of the underlying neural pathways. Immunocytochemical studies of the brain photoreceptors in the parastacid (southern hemisphere) crayfish Cherax destructor reveal their expression of the blue light-sensitive photopigment cryptochrome and the neurotransmitter histamine. The brain photoreceptors project to two small protocerebral neuropils, the brain photoreceptor neuropils (BPNs), where they terminate among fibers expressing the neuropeptide pigment-dispersing hormone (PDH), a signaling molecule in arthropod circadian systems. Comparable pathways are also described in the astacid (northern hemisphere) crayfish Procambarus clarkii. Despite exhibiting markedly different diurnal locomotor activity rhythms, removal of the compound eyes and caudal photoreceptors in both C. destructor and P. clarkii (leaving the brain photoreceptors intact) does not abolish the normal light/dark activity cycle in either species, nor prevent the entrainment of their activity cycles to phase shifts of the light/dark period. These results suggest, therefore, that crayfish brain photoreceptors are sufficient for the entrainment of locomotor activity rhythms to photic stimuli, and that they can act in the absence of the compound eyes and caudal photoreceptors. We also demonstrate that the intensity of PDH expression in the BPNs varies in phase with the locomotor activity rhythm of both crayfish species. Together, these findings suggest that the brain photoreceptor cells can function as extraretinal circadian photoreceptors and that the BPN represents part of an entrainment pathway synchronizing locomotor activity to environmental light/dark cycles, and implicating the neuropeptide PDH in these functions. (Author correspondence: bbeltz@wellesley.edu)     

Both the anterior and posterior eyes function as photoreceptors for photoperiodic termination of diapause in the two-spotted spider mite

Photoreceptors involved in photoperiodism in insects and mites can be either the retinal photoreceptors in the visual system or nonvisual extraretinal photoreceptors. Mites with no eyes have a clear photoperiodic response, suggesting the involvement of extraretinal photoreceptors in mite photoperiodism. In mites equipped with eyes, however, it is not known whether the retinal or extraretinal photoreceptors are involved in photoperiodism. The two-spotted spider mite Tetranychus urticae possesses two pairs of eyes. Adult females of this species terminate diapause in response to long days. To investigate whether the eyes function as photoperiodic photoreceptors in T. urticae, their eyes were ablated using a laser ablation system. Mites with their eyes intact terminated diapause under long days after low temperature exposure, whereas they remained in diapause under short days. Under constant darkness, they did not terminate diapause. When all eyes were removed, the mites remained in diapause even when they were maintained under long days. In contrast, the mites showed clear photoperiodic response when only the anterior or posterior eyes were removed. These results indicate that both the anterior and posterior eyes function as photoreceptors in photoperiodic termination of diapause in T. urticae.     

Cerebral extraocular photoreceptors in ants

Clusters of dark pigmented cells, called putative cerebral extraocular photoreceptors (CEPs), are described in the optic lobes of four ant species: Atta sexdens, Camponotus rufipes, Camponotus crassus, and Pseudomyrmex adustus. Electron-micrographs of CEPs show a central rhabdom-like structure formed by tightly interleaved cells containing shielding pigments, with axons projecting toward the outer optic chiasm. The presence of a great number of mitochondria, nucleolus, and multivesciular bodies suggests that these clusters might be functional extraocular photoreceptors. Although some branches from GABA-like immunoreactive neurones occur near the CEP region, GABA-immunoreactivity was not detected in CEPs. The ant's cephalic cuticle blocks short wavelengths (< 500 nm) and the light transmittance is less than 20% for wavelengths between 500-700 nm. Ant species with both diurnal and nocturnal habits and heightened nocturnal visual sensitivity (A. sexdens and C. rufipes) contain more CEPs than those with diurnal habits and lower visual sensitivity (C. crassus and P. adustus). The reduction of light reaching this putative extra-ocular system could act as a signal for a circadian pacemaker and, as a possible consequence, lead to an increase of nocturnal visual sensitivity of the compound eyes and/or nocturnal locomotor activity, as already observed in the species studied.     

Comparative morphology of photoreceptors in free-living plathelminths — a survey

In free-living Plathelminthes, the best-known photoreceptors are pigment-cup ocelli, eyes formed of one or several pigmented supportive cells into whose cup-shaped cavity project the light-sensitive elements of one or several sensory cells. Besides these, so-called Sehkolben, photoreceptors lacking pigment granules, are found in some species. Sensory cells in plathelminth photoreceptors most commonly use microvilli as the light-sensitive organelles, but some use cilia and combinations of microvilli and cilia. Lamellate ciliary bodies with cilia whose membranes are strongly flattened and rolled and pericerebral ciliary aggregations with interwoven cilia protruding into an intracellular cavity are likely photoreceptors in that they show amplification of membrane likely to bear photoreceptive pigments. Cells with ballooned cilia and tubular vacuoles are other differentiations to which light-sensitivity has been attributed. A variety of structures serve as lenses, all usually formed from parts of the pigment cell.     

Anti-tumoral effect of scorpion peptides: Emerging new cellular targets and signaling pathways

Scorpion toxins have been the subject of many studies exploring their pharmacological potential. The high affinity and the overall selectivity to various types of ionic channels endowed scorpion toxins with a potential therapeutic effect against many channelopathies. These are diseases in which ionic channels play an important role in their development. Cancer is considered as a channelopathy since overexpression of some ionic channels was highlighted in many tumor cells and was linked to the pathology progression.Interestingly, an increasing number of studies have shown that scorpion venoms and toxins can decrease cancer growth in vitro and in vivo. Furthermore through their ability to penetrate the cell plasma membrane, certain scorpion toxins are able to enhance the efficiency of some clinical chemotherapies. These observations back-up the applicability of scorpion toxins as potential cancer therapeutics.In this review, we focused on the anti-cancer activity of scorpion toxins and their effect on the multiple hallmarks of cancer. We also shed light on effectors and receptors involved in signaling pathways in response to scorpion toxins effect. Until now, the anticancer mechanisms described for scorpion peptides consist on targeting ion channels to (i) inhibit cell proliferation and metastasis; and (ii) induce cell cycle arrest and/or apoptosis through membrane depolarization leading to hemostasis deregulation and caspase activation. Putative targets such as metalloproteinases, integrins and/or growth factor receptors, beside ion channels, have been unveiled to be affected by scorpion peptides.