Retina mediators in fresh-water mollusc Lymnaeae stagnalis

Retrograde staining of the Lymnaeae stagnalis retina with neurobiotin has shown that most photoreceptor cells send axons to optic nerve without intermediate contacts. A part of these photoreceptors have immunireactivity to glutamate that possibly provides synaptic transmission of visual signal to central neurons. Other photoreceptors stained through optic nerve seem to have different transmitter systems. In some retina cell, but not in optic nerve fibers, immunoreactivity to pigment-dispersing hormone has been revealed. In tissues surrounding the eye cup numerous serotonin-containing fibers are present, a part of them penetrating the retina basal layer. Some of them belong to central neurons responsible for efferent innervation of the pond snail eye. It is suggested that the serotoninergic innervation as well as the cell containing the pigment-dispersing hormone are included in the mechanism of regulation of light sensitivity of the mollusc eye.     

Spatial modulation of primate inferotemporal responses by eye position

Background

A key aspect of representations for object recognition and scene analysis in the ventral visual stream is the spatial frame of reference, be it a viewer-centered, object-centered, or scene-based coordinate system. Coordinate transforms from retinocentric space to other reference frames involve combining neural visual responses with extraretinal postural information.

Methodology/Principal Findings

We examined whether such spatial information is available to anterior inferotemporal (AIT) neurons in the macaque monkey by measuring the effect of eye position on responses to a set of simple 2D shapes. We report, for the first time, a significant eye position effect in over 40% of recorded neurons with small gaze angle shifts from central fixation. Although eye position modulates responses, it does not change shape selectivity.

Conclusions/Significance

These data demonstrate that spatial information is available in AIT for the representation of objects and scenes within a non-retinocentric frame of reference. More generally, the availability of spatial information in AIT calls into questions the classic dichotomy in visual processing that associates object shape processing with ventral structures such as AIT but places spatial processing in a separate anatomical stream projecting to dorsal structures.     

Cellular and ultrastructural features of the adult and the embryonic eye in the marine gastropod,Ilyanassa obsoleta

Light and electron microscopic techniques show that the eye of the marine prosobranch gastropod, Ilyanassa obsoleta, is composed of an optic cavity, lens, cornea, retina, and neuropile, and is surrounded by a connective tissue capsule. The adult retina is a columnar epithelium containing three morphologically distinct cell types: photoreceptor, pigmented, and ciliated cells. The retina is continuous anteriorly with a cuboidal corneal epithelium. The neuropile, located immediately behind the retina, is composed of photoreceptor cell axons, accessory neurons, and their neurites. The embryonic eye is formed from surface ectoderm, which sinks inward as a pigmented cellular mass. At this time, the eye primordium already contains presumptive photoreceptor cells, pigmented retinal cells, and corneal cells. Several days later, just before hatching, the embryonic eye remains in intimate contact with the cerebral ganglion. It has no ciliated retinal cells, neuropile, optic nerve, or connective tissue capsule and its photoreceptor cells lack the electron-lucent vesicles and multivesicular bodies of adult photoreceptor cells. As the eye and the cerebral ganglion grow apart, the optic nerve, neuropile, and connective tissue capsule develop.     

Fixational Eye Movements in the Earliest Stage of Metazoan Evolution

All known photoreceptor cells adapt to constant light stimuli, fading the retinal image when exposed to an immobile visual scene. Counter strategies are therefore necessary to prevent blindness, and in mammals this is accomplished by fixational eye movements. Cubomedusae occupy a key position for understanding the evolution of complex visual systems and their eyes are assumedly subject to the same adaptive problems as the vertebrate eye, but lack motor control of their visual system. The morphology of the visual system of cubomedusae ensures a constant orientation of the eyes and a clear division of the visual field, but thereby also a constant retinal image when exposed to stationary visual scenes. Here we show that bell contractions used for swimming in the medusae refresh the retinal image in the upper lens eye of Tripedalia cystophora. This strongly suggests that strategies comparable to fixational eye movements have evolved at the earliest metazoan stage to compensate for the intrinsic property of the photoreceptors. Since the timing and amplitude of the rhopalial movements concur with the spatial and temporal resolution of the eye it circumvents the need for post processing in the central nervous system to remove image blur.     

Avian Cone Photoreceptors Tile the Retina as Five Independent,Self-Organizing Mosaics

The avian retina possesses one of the most sophisticated cone photoreceptor systems among vertebrates. Birds have five types of cones including four single cones, which support tetrachromatic color vision and a double cone, which is thought to mediate achromatic motion perception. Despite this richness, very little is known about the spatial organization of avian cones and its adaptive significance. Here we show that the five cone types of the chicken independently tile the retina as highly ordered mosaics with a characteristic spacing between cones of the same type. Measures of topological order indicate that double cones are more highly ordered than single cones, possibly reflecting their posited role in motion detection. Although cones show spacing interactions that are cell type-specific, all cone types use the same density-dependent yardstick to measure intercone distance. We propose a simple developmental model that can account for these observations. We also show that a single parameter, the global regularity index, defines the regularity of all five cone mosaics. Lastly, we demonstrate similar cone distributions in three additional avian species, suggesting that these patterning principles are universal among birds. Since regular photoreceptor spacing is critical for uniform sampling of visual space, the cone mosaics of the avian retina represent an elegant example of the emergence of adaptive global patterning secondary to simple local interactions between individual photoreceptors. Our results indicate that the evolutionary pressures that gave rise to the avian retina''s various adaptations for enhanced color discrimination also acted to fine-tune its spatial sampling of color and luminance.     

On the problem of retinal transmitters of the freshwater mollusc <Emphasis Type="Italic">Lymnaea stagnalis</Emphasis>

Retrograde staining of retina of Lymnaea stagnalis with neurobiotin demonstrated that most photoreceptor cells send axons to the optic nerve directly, without intermediate contacts. Some of the photoreceptors are glutamate-immunoreactive suggesting that glutamate can provide the synaptic transmission of visual signal to the central neurons. Other photoreceptors stained via optic nerve seem to have other transmitter systems. Some of the retinal cells, but not the optic nerve fibers are pigment-dispersing hormone-immunoreactive. There are many serotonin-containing fibers in the tissue surrounding the optic cup with some of them penetrating the basal lamina of retina. Some of them belong to central neurons providing efferent innervation of the pond snail eye. Serotonergic innervation as well as pigment-dispersing hormone-containing cells are supposed to be involved in mechanism of the photosensitivity regulation of the molluscan eye.     

Eye Structure and Vision in the Freshwater Pulmonate Mollusc Planorbarius corneus

The structure of the mollusc Planorbarius corneus eye was studied using light and electron microscopy. The eye consists of the cornea, eye lens of non-spherical shape, and the vitreous body tightly bound to it, as well as of a monolayer non-inverted retina composed of photoreceptor and supporting (pigmented) cells. Its inner surface has two invaginations. The apices of several hundreds of photoreceptors directed to the vitreous body have groups of microvilli with a parallel orientation to each other. The eye optic system places the image into the base of the retinal microvillar layer. Its angle resolution provided by density of distribution of photoreceptor cells and the value of the index F = 1.71 is to be about 2.06° with a correction for the light spreading between microvilli of neighbor cells. Under conditions of a V-shaped labyrinth, the P. corneus molluscs show positive phototaxis by moving to the light source. The angular acuity of vision was assessed from differences in the choice by the molluscs of direction of movement to the pattern of vertical black bands with different periods of alternation. The differential threshold obtained is within an interval of 1.43–1.91°, which is close to the calculated value of angular resolution of the retina.     

Interstitial cells of Cajal in the striated musculature of the mouse esophagus

A key feature of signal processing in the mammalian retina is parallel processing, where the segregation of visual information, e.g., brightness, darkness, and color, starts at the first synapse in the retina, the photoreceptor synapse. These various aspects are transmitted in parallel from the input neurons of the retina, the photoreceptor cells, through the interconnecting bipolar cells, to the output neurons, the ganglion cells. The photoreceptors and bipolar cells release a single excitatory neurotransmitter, glutamate, at their synapses. This parsimony is contrasted by the expression of a plethora of glutamate receptors, receptor subunits, and isoforms. The detailed knowledge of the synaptic distribution of glutamate receptors thus is of major importance in understanding the mechanisms of retinal signal processing. This review intends to highlight recent studies on the distribution of glutamate receptors at the photoreceptor synapses of the mammalian retina.     

Color image detection by biomolecular photoreceptor using bacteriorhodopsin-based complex LB films

A biomolecular photoreceptor consisting of bacteriorhodopsin (bR)-based complex Langmuir–Blodgett (LB) films was developed for color image detection. By mimicking the functions of the pigments in retina of human visual system, biomolecules with photoelectric conversion function were chosen and used as constituents for an artificial photoreceptor. bR and flavin were deposited onto the patterned (9-pixelized) ITO glass by LB technique. A 9-pixel biomolecular photoreceptor was fabricated with a sandwich-type structure of ITO/LB films/electrolyte gel/Pt. Since each functional molecule shows its own response characteristic according to the light illumination in the visible region, the simplified knowledge-based algorithm for interpretation of the incident light wavelength (color) was proposed based on the basic rule describing the relationship between the photoelectric response characteristics and the incident light wavelength. When simple color images were projected onto the photoreceptor, the primary colors in visible light region, red, green, and blue were clearly recognized, and the projected color images were fairly well reproduced onto the color monitor by the proposed photoreceptor with the knowledge-based algorithm. It is concluded that the proposed device has a capability of recognizing the color images and can be used as a model system to simulate the information processing function of the human visual system.     

Modelling the visual world of a velvet worm

In many animal phyla, eyes are small and provide only low-resolution vision for general orientation in the environment. Because these primitive eyes rarely have a defined image plane, traditional visual-optics principles cannot be applied. To assess the functional capacity of such eyes we have developed modelling principles based on ray tracing in 3D reconstructions of eye morphology, where refraction on the way to the photoreceptors and absorption in the photopigment are calculated incrementally for ray bundles from all angles within the visual field. From the ray tracing, we calculate the complete angular acceptance function of each photoreceptor in the eye, revealing the visual acuity for all parts of the visual field. We then use this information to generate visual filters that can be applied to high resolution images or videos to convert them to accurate representations of the spatial information seen by the animal. The method is here applied to the 0.1 mm eyes of the velvet worm Euperipatoides rowelli (Onychophora). These eyes of these terrestrial invertebrates consist of a curved cornea covering an irregular but optically homogeneous lens directly joining a retina packed with photoreceptive rhabdoms. 3D reconstruction from histological sections revealed an asymmetric eye, where the retina is deeper in the forward-pointing direction. The calculated visual acuity also reveals performance differences across the visual field, with a maximum acuity of about 0.11 cycles/deg in the forward direction despite laterally pointing eyes. The results agree with previous behavioural measurements of visual acuity, and suggest that velvet worm vision is adequate for orientation and positioning within the habitat.     

Divergent decapentaplegic expression patterns in compound eye development and the evolution of insect metamorphosis

In the fruit fly Drosophila, the patterning genes decapentaplegic and wingless contribute to the spatial control of retina development in an antagonistic manner. We examined the expression patterns of these genes in the developing visual system of the hemimetabolous grasshopper Schistocerca americana and the primitive holometabolous beetle species Tribolium castaneum. The pattern of wingless expression was strongly conserved as a pair of lateral domains at the anterior margins of both the developing retina and the developing optic lobes. The expression of decapentaplegic, on the other hand, is different. Unlike in Drosophila, no decapentaplegic expression was detected before the onset of photoreceptor differentiation in the retinal precursor tissue of either grasshopper or beetle. Moreover, the subsequent expression of decapentaplegic in the latter species was not concentrated in the moving front of retina differentiation, as in Drosophila, but observed in anterior and posterior regions. Our results indicate that Drosophila eye development contains elements of both ancestral and derived regulatory gene functions. The requirement for decapentaplegic as an antagonist of wingless during the early development of the Drosophila retina might have originated during the evolution of insect metamorphosis.     

Parallel processing and image analysis in the eyes of mantis shrimps

The compound eyes of mantis shrimps, a group of tropical marine crustaceans, incorporate principles of serial and parallel processing of visual information that may be applicable to artificial imaging systems. Their eyes include numerous specializations for analysis of the spectral and polarizational properties of light, and include more photoreceptor classes for analysis of ultraviolet light, color, and polarization than occur in any other known visual system. This is possible because receptors in different regions of the eye are anatomically diverse and incorporate unusual structural features, such as spectral filters, not seen in other compound eyes. Unlike eyes of most other animals, eyes of mantis shrimps must move to acquire some types of visual information and to integrate color and polarization with spatial vision. Information leaving the retina appears to be processed into numerous parallel data streams leading into the central nervous system, greatly reducing the analytical requirements at higher levels. Many of these unusual features of mantis shrimp vision may inspire new sensor designs for machine vision.     

Embryonic appearance of rod opsin in the urodele amphibian eye

Notophthalmus (Triturus) viridescens, a urodele amphibian (newt) common to the Eastern United States, is a promising subject for developmental and regeneration studies. We have available a monoclonal antibody shown to be specific in many vertebrates for rod opsin, the membrane apoprotein of the visual pigment rhodopsin. This antibody to an N-terminal epitope, by rigorous biochemical and immunological criteria, recognizes only rod photoreceptor cells of the retina in light-and electron-microscopic immunocytochemistry. To determine the ontogeny and localization of rhodopsin in developing rods as an indicator of function in the embryonic urodele retina, we have utilized this antibody in the immunofluorescence technique on sections of developing N. viridescens. It was applied to serial sections of the eye region of Harrison stage 28 (optic vesicle) through stage 43 (most adult retina histology complete) embryos, and subsequently visualized with biotinylated species antibody followed by extravidin fluorescein isothiocyanate. The first positive reaction to rhodopsin could be detected in two to four cells (total) of the stage 37 embryonic eye, in the region of the central retinal primordium where the photoreceptors will be found. Some indications of retinal outer nuclear and inner plexiform layers could be seen at this time. Later embryonic stages demonstrated increasing numbers of positive cells in the future photoreceptor outer nuclear layer and outer and inner segments, spreading even to the peripheral retina. Nevertheless, by stale 43, no positive cells could be found at the dorsal or ventral retinal margins. Thus, biochemical differentiation of a photoreceptor population in the urodele retina occurs at a stage before retinal histogenesis is complete. The total maturation of retinal rods occurs topographically over a long period until the adult distribution is achieved. Correspondence to: D.S. McDevitt     

Photoreceptor number and outer segment disk membrane surface area in the retina of the rat: stereological data for whole organ and average photoreceptor cell

A random sampling scheme is employed to obtain stereological estimates of disk membrane surface area in the entire retina and in the average photoreceptor cell. The scheme involves the use of vertical sections with combined light and electron microscopy at several magnification levels. Left and right retinas from six albino animals were analysed. There were no significant lateral differences. On average, the retina had a volume of 16 mm3, thickness of 200 μm and surface area of 80 mm2 (representing about 56% of the external surface of the eyeball). Photoreceptor disk membranes within outer segments amplified total retinal surface by almost 1000-fold (final surface 770 cm2 per retina). The retina contained 3×107 photoreceptors (packing density 374 000 mm-2) with an average disk membrane surface area of 2600 μm2. Mean nuclear volume in photoreceptor cells was 59 μm3 and the coefficient of variation for the distribution of nuclear volumes was 57%. The data are consistent with an average of 700 disks per photoreceptor cell, a membrane area of 4 μm2 per disk and a convergence ratio of ～260 photoreceptors per optic nerve fibre. The basic scheme could be modified for other species and for direct cell counts conducted on rods and cones separately.     

Opsin-immunoreactive outer segments of photoreceptors in the eye and in the lumen of the optic nerve of the hagfish,Myxine glutinosa

Summary Opsin-immunoreactive sites in the eye and optic nerve of the hagfish, Myxine glutinosa, were studied by use of light-microscopic pre- and postembedding peroxidase-antiperoxidase or avidin-biotin-peroxidase techniques, and the immuno-electron-microscopic protein A-gold method. At the light-microscopic level, a strong opsin immuno-reaction was obtained on the outer segments of the photoreceptor cells with sheep and rat antibodies against bovine (rhod)opsin. These outer segments were located in the marginal photoreceptor space and in follicles of the retina, as well as in the tubular lumen of the optic nerve. Ultrastructurally, two classes of outer segments can be distinguished; most of them exhibited a strong antiopsin reaction, while certain elements lacked immunoreactivity with the antisera employed. The protein A-gold particles marked opsin-immunoreactive sites on the photoreceptor membranes. The presence of opsin-immunoreactive material in the retina and optic nerve of the hagfish strengthens the view that this primitive eye lacking a cornea, lens and vitreous body is engaged in light perception. The morphological similarity between the eye and pineal tissue is discussed in connection with the absence of a pineal organ in this species.This investigation was supported by grants from the Swedish Natural Sciences Research Council to R.O. (No. B-BU 2124), and the Royal Physiographic Society of Lund and the Swedish Natural Sciences Research Council to Th. v.V. (No. 4644-105)On leave of absence from the 2nd Department of Anatomy, Semmelweis OTE, Budapest, Hungary     

Retinal adaptation to object motion

Due to fixational eye movements, the image on the retina is always in motion, even when one views a stationary scene. When an object moves within the scene, the corresponding patch of retina experiences a different motion trajectory than the surrounding region. Certain retinal ganglion cells respond selectively to this condition, when the motion in the cell's receptive field center is different from that in the surround. Here we show that this response is strongest at the very onset of differential motion, followed by gradual adaptation with a time course of several seconds. Different subregions of a ganglion cell's receptive field can adapt independently. The circuitry responsible for differential motion adaptation lies in the inner retina. Several candidate mechanisms were tested, and the adaptation most likely results from synaptic depression at the synapse from bipolar to ganglion cell. Similar circuit mechanisms may act more generally to emphasize novel features of a visual stimulus.     

Modelling place memory in crickets

Insects can remember and return to a place of interest using the surrounding visual cues. In previous experiments, we showed that crickets could home to an invisible cool spot in a hot environment. They did so most effectively with a natural scene surround, though they were also able to home with distinct landmarks or blank walls. Homing was not successful, however, when visual cues were removed through a dark control. Here, we compare six different models of visual homing using the same visual environments. Only models deemed biologically plausible for use by insects were implemented. The average landmark vector model and first order differential optic flow are unable to home better than chance in at least one of the visual environments. Second order differential optic flow and GradDescent on image differences can home better than chance in all visual environments, and best in the natural scene environment, but do not quantitatively match the distributions of the cricket data. Two models—centre of mass average landmark vector and RunDown on image differences—could produce the same pattern of results as observed for crickets. Both the models performed best using simple binary images and were robust to changes in resolution and image smoothing.     

The stepwise development of the lamprey visual system and its evolutionary implications

Lampreys, which represent the oldest group of living vertebrates (cyclostomes), show unique eye development. The lamprey larva has only eyespot‐like immature eyes beneath a non‐transparent skin, whereas after metamorphosis, the adult has well‐developed image‐forming camera eyes. To establish a functional visual system, well‐organised visual centres as well as motor components (e.g. trunk muscles for locomotion) and interactions between them are needed. Here we review the available knowledge concerning the structure, function and development of the different parts of the lamprey visual system. The lamprey exhibits stepwise development of the visual system during its life cycle. In prolarvae and early larvae, the ‘primary’ retina does not have horizontal and amacrine cells, but does have photoreceptors, bipolar cells and ganglion cells. At this stage, the optic nerve projects mostly to the pretectum, where the dendrites of neurons in the nucleus of the medial longitudinal fasciculus (nMLF) appear to receive direct visual information and send motor outputs to the neck and trunk muscles. This simple neural circuit may generate negative phototaxis. Through the larval period, the lateral region of the retina grows again to form the ‘secondary’ retina and the topographic retinotectal projection of the optic nerve is formed, and at the same time, the extra‐ocular muscles progressively develop. During metamorphosis, horizontal and amacrine cells differentiate for the first time, and the optic tectum expands and becomes laminated. The adult lamprey then has a sophisticated visual system for image‐forming and visual decision‐making. In the adult lamprey, the thalamic pathway (retina–thalamus–cortex/pallium) also transmits visual stimuli. Because the primary, simple light‐detecting circuit in larval lamprey shares functional and developmental similarities with that of protochordates (amphioxus and tunicates), the visual development of the lamprey provides information regarding the evolutionary transition of the vertebrate visual system from the protochordate‐type to the vertebrate‐type.     

Ocular dimensions and cone photoreceptor topography in adult Nile Tilapia <Emphasis Type="Italic">Oreochromis niloticus</Emphasis>

Information on the anatomy of the eye and the topography of cone photoreceptor cells in the retina is presented for the Nile Tilapia (Oreochromis niloticus). In adults, the shape and proportions of the ocular components of the prominent eye conform to the general form of fish eyes, as determined using cryo-sectioned eyes. The lens is approximately spherical and there is little variation in the distance from the centre of the lens to the border between the choroid and retina at a range of angles about the optical axis. The average ratio of the distance from the centre of the lens to the retina: lens radius (Matthiessen’s ratio) is 2.44:1. In retinal wholemounts, single and double (twin) cone photoreceptors, forming a square mosaic, are present. Peak photoreceptor densities for both morphological cone types are found in the temporal retina. Using peak cone densities and estimates of focal length from cryo-sectioned eyes, visual acuity is calculated to be 5.44 cycles per deg. The lack of apparent specific ocular or retinal specializations and the relatively low visual acuity reflect the lifestyle of the Nile Tilapia and may allow it to adapt to changes in visual environment in its highly variable natural habitat as well as contributing to the ‘ecological flexibility’ of this species.