Apposition Eyes Research Articles

Refractive index gradients subserve optical isolation in a light‐adapted reflecting superposition eye

AbstractThe freshwater shrimp Macrobrachium rosenbergii (de Man) has reflecting superposition compound eyes. Upon adaptation from dark to light conditions, the eye converts from superposition to apposition optics by screening pigment migration. The clear zone, typical of dark‐adapted superposition eyes, persisted after adaptation to 500 lux, when the eye optically behaved like an apposition eye. In this state, optical isolation is maintained by a proximal refractive‐index gradient in the crystalline cone, which only requires the proximal pigment to be in the light‐adapted position around the junction between the cone and rhabdom. Thus, the distal pigment need not invade the clear zone for the eye to convert to apposition optics. This mechanism probably decreases the time required for light adaptation. Furthermore, as a result of total internal reflections in the cone tip, the proximal gradient increases the acceptance angle.

Light guides in the dorsal eye of the male mayfly

(i) The dorsal eyes are sensitive to ultraviolet light, which is focused by the corneal lens into crystalline cones in the region where these taper progressively to columns across the clear zone. The action of these columns as light guides can be observed in fixed eyes embedded in polymerized resin. In life the light guide part of the column is surrounded by watery non-cellular haemolymph. (ii) Shadowing the eye surface with a thin wire (three facets wide) while recording from individual receptor units shows that ultraviolet light reaches each receptor by its own facet as in an apposition eye, and not, as in a superposition eye, by a group of many facets. (iii) As shown by the dye Lucifer Yellow injected from a microelectrode, the electrophysiological unit consists of all seven retinula cells in the rhabdom region. Consistent with this tight coupling of retinula cells there is no polarization sensitivity. The peak spectral sensitivity of all single units is at 345-365 nm in the ultraviolet. The acceptance angle is 2.0–2.5°. The sensitivity at the spectral peak to a point source on the optical axis of the unit is poor compared to that in other insects tested with the same equipment. (iv) The acceptance angles (∆ ρ ) in the dorsal eye are at the theoretical minimum for the facet diameter and wavelength from diffraction theory. Ultraviolet vision, therefore, has made possible a reduction in facet size but the interommatidial angle ∆ ϕ is greater than expected from the optimum sampling theory of the diffraction limited compound eye. In fact ∆ ρ ≈ ∆ ϕ ≈ 2°. (v) The dorsal eye is effectively a foveal region with greater sampling density and narrower receptive fields but less overlap of fields than the lateral eye. (vi) The square cones and yellow screening pigment strongly suggest that there is superposition by reflexion of yellow light that spreads between ommatidia across the clear zone. This yellow light might photoreisomerize the visual pigment. Attempts to prove this theory during the recording from single units have so far failed but no better function for the clear zone has been suggested.

The structure of the double-eyes of Baetis and the uniform eyes of Ecdyonurus (Ephemeroptera)

The lateral eyes of Baetis vernus are structured similarly in both sexes. They are eucone apposition eyes with a closed rhabdom formed by eight retinula cells. The accessory pigment cells surround the ommatidia over their entire length. The morphological adaptation to different illuminations consists of a radial displacement of mitochondria and endoplasmic vacuoles. The dorsal eyes of the male Baetis, often called turban eyes, differ remarkably in structure and size from the lateral organs by a large clear zone which is only crossed by thread-like elongations of the retinula cells; the rhabdom is divided in a distal part next to the cone and a large basal part. Each of the seven retinula cells contributes microvilli to both parts of the rhabdom. The pigment cells only surround the cone and the distal part of the rhabdom, whereas the basal rhabdoms are optically isolated from each other by a ring of trachea. No morphological adaptation to different illumination is detectable in the dorsal eyes. The relation of the two different eyes of the male, being optically isolated but forming a morphologically connected complex, are discussed. With the description of the dorsal eyes of the subimago the formation of the dorsal eyes is investigated. A possible mode of function is considered. The male of Ecdyonurus venosus has larger eyes than the female, but they are structured after the same scheme. The eyes are similar to the lateral eyes of Baetis.

Focusing of Light by Corneal Lenses in a Reflecting Superposition Eye

Focusing of Light by Corneal Lenses in a Reflecting Superposition Eye

Diurnal changes in angular sensitivity of crab photoreceptors

The electrophysiological and anatomical consequences of diurnal changes in screening pigment position were investigated in the apposition eye of the portunid crabScylla serrata. Intracellular recordings revealed that the acceptance angles of dark-adapted photoreceptors enlarged up to four-fold at night compared with photoreceptors dark-adapted in the day. Furthermore, while light adaptation at night caused acceptance angles to narrow, dark adaptation in the day caused no significant broadening of angles. These electrophysiological changes correlated with pigment movements in the eye observed both histologically and in the deep pseudopupil. It is found that the distal pigment cells change diurnally so that the field-stop which these cells form in front of the photoreceptors is opened in the night and closed in the day time. One feature of the diurnal rhythm is that it prevents photoreceptor fields of view enlarging when eyes are dark adapted in the day. InScylla, photoreceptor fields of view take tens of minutes to narrow upon exposure of crabs to light at night. By preventing a similar broadening in the day, the diurnal rhythm may enable animals suddenly leaving dark refuges to be pre-adapted to daylight. To a range of species which utilise refuges such a mechanism would be of significant advantage, especially after disturbance by predators.

Spectral sensitivity and retinal pigment movement in the crab Leptograpsus variegatus (fabricius).

1. The retina of Leptograpsus contains five types of movable screening pigment. The positions of these were found under various conditions of illumination in the day and at night. 2. Intracellular recordings were made of the spectral responses of retinula cells R1-7 under the same conditions, with the eye in situ. 3. The spectral absorptions of the individual screening pigments were measured by ultramicrospectrophotometry. 4. Calculations based on a simple model of screening pigment action suggest that the observed variation in spectral sensitivity with light and dark adaptaton may be largely explicable in terms of the effects of these screening pigments on a rhodopsin of peak absorbance at 485 nm. 5. Light-adapted angular sensitivities are comparable to those of insects with high acuity apposition eyes.

Crustacean Eye Fine Structure Seen with Scanning Electron Microscopy

The internal fine structure of crustacean compound eyes has been reexamined with scanning electron microscopy. Several different preparative techniques were used in a comparative study of crab, crayfish, shrimp, and stomatopod eyes. The three-dimensional pattern of photoreceptive, dioptric, and screening components of these eyes has been directly demonstrated, and new insight has been gained into their functional organization. Particularly interesting in apposition eyes is the elaborate array of boundary membranes and protoplasmic strands linking the photoreceptive microvilli to their parent cell cytoplasm across the large intracellular vacuoles surrounding the axial rhabdom. Quantitative application of scanning electron microscopy to this system promises to advance our understanding of its proven high rate of receptor membrane turnover.

Review lecture: Apposition eyes of large diurnal insects as organs adapted to seeing

(1) The fields of view of the photoreceptor cells are determined by the dimensions and anatomical arrangement of the optical part of the ommatidium. The dimensions, and therefore the fields of view of the ommatidia are also related across the eye. In the relation between structure and function there are many points that invite discussion, but the intention is to order our knowledge so that the gaps become obvious. (2) The first step has been to make maps of the eyes showing the maximum theoretical resolving power of the facets and also the interommatidial angle, the reciprocal of which is the maximum spatial resolution of combinations of facets. The ratio of these two resolutions at each point shows the minimum overlap of the visual fields. These maps can be made from the outside of the eye; they show the main types of eye. (3) The next step is to work out the optics of individual ommatidia so that the focal lengths and receptor widths can be measured. The field width can then be predicted from the facet size and the subtense of the receptor at the posterior nodal point. The final step is to measure the field widths of individual ommatidia experimentally as a test of the optical theory, and to make maps of the actual fields in their correct position on the eye in angular coordinates. (4) Three examples of maps of actual fields are given, and their anato­mical and diffraction components are separated. The maps are an essential step towards the electrophysiological analysis of the ganglia behind the eye. A theory of the origin of the fields in terms of anatomy and optics also opens the way to an analysis of mechanisms that change the field size upon adaptation to light. A comparative study of the fields in different eye regions and in different species can also be related to visual habits and behaviour.

The optical mechanism of the eye of Limulus

THE compound eyes of many marine and some terrestrial arthropods have smooth surfaces with no convex curvature to the facets. This means that image formation by ordinary spherical refraction is impossible. Nevertheless, apposition eyes of this kind form images behind each surface facet1,2 (Fig. 1b) and the question has repeatedly arisen as to how these images are produced. Exner chose the king crab, Limulus, as providing the definitive example of such an eye, and from a mixture of observation and theory came up with the idea of a lens-cylinder, a flat-ended optical device in which the refractive index decreases from the central axis to the periphery in a roughly parabolic manner1. This arrangement will form an image (Fig. 2a), and devices of this kind have actually been manufactured3,4. Exner's theory has long been considered to be the correct account of image formation in this type of eye5. However, Levi-Setti, Park and Winston2 have recently produced a fundamentally different explanation of image formation in Limulus eyes (Fig. 2b). This was based on the idea that each optical element, or crystalline cone, concentrated light by reflection, not refraction, and that it was the shape of the crystalline cone's reflective surface, and not its internal refractive index gradient, that led to the image-forming properties of the structure. This principle had already been used in another optical device, the ‘ideal light collector’ (ref. 6) which was invented as a tool for concentrating faint radiation. In this report I discuss the two suggested optical mechanisms for the eye of Limulus, and present evidence from interference microscopy that Exner's theory is probably the correct one.

The separation of visual axes in apposition compound eyes.

The separation of visual axes in apposition compound eyes.

The structures of dorsal and ventral regions of a dragonfly retina.

The apposition eyes of the corduliid dragonfly Hemicordulia tau are each divided by pigment colour, facet size and facet arrangement into three regions: dorsal, ventral, and a posterior larval strip. Each ommatidium has two primary pigment cells, twenty-five secondary pigment cells, and eight receptor cells, all surrounded by tracheae which probably prevent light passing between ommatidia, and reduce the weight of the eye. Electron microscopy reveals that the receptor cells are of two types: small vestigial cells making virtually no contribution to the rhabdom, and full-size typical cells. The ventral ommatidia have a distal typical cell (oriented either horizontally or vertically), four medial typical cells, two proximal typical cells and one full-length vestigial cell. The dorsal ommatidia have only four full-length typical cells, and one distal and three vestigial full-length cells. The cross-section of dorsal rhabdoms is small and circular distally, but expands to a large three-pointed star medially and proximally. The tiered receptor arrangement in the ventral ommatidia is typical of other Odonata but the dorsal structure has not been fully described in other species. Specialised dorsal eye regions are typical of insects that detect others against the sky.

The Fine Structure of the Compound Eye ofTanais cavoliniiMilne-Edwards (Crustacea: Tanaidacea)

The compound (apposition) eyes of Tanais cavolinii are not well developed: the number of ommatidia is small and there are certain irregularities in structure. The refractive components are formed by the cornea and the cone. The latter is built up by two cone cells. In addition, there are two accessory cone cells confined to the distal part of the cone. The eight pigmented retinular cells extend from the cornea to the basement membrane. Proximal to the cone, they form a fused continuous rhabdom, which in cross section has a rectangular outline. In the middle part of the rhabdom, the microvilli are arranged perpendicular to the long axis of the rhabdom when seen in cross section. The microvilli outside of this area can be arranged either parallel or perpendicular to the microvilli of the middle part. Other irregularities occur in the ommatidium, e.g. the position of the retinular cell nuclei, which are found at different levels. Extensions from the cone cells fuse and form a mesh proximal to the rhabdom. Between the mesh and basal lamina is a basal cell type enveloping the proximal parts of the retinular cells and their axons. These cells also form the basal lamina, which delimits the compound eye from the haemocoel. No special pigment cells are present in the compound eye of Tanais cavolinii.

The superposition eye of Cloeon dipterum: the organization of the lamina ganglionaris.

The lamina ganglionaris of the superposition eye of Cloeon dipterum is composed of separate optic cartridges arranged in a hexagonal pattern. Each optic cartridge consists of one central, radially branched monopolar cell (Li) surrounded by a crown of seven retinula cell terminals and two more unilaterally branched monopolar cells (La1/La2) situated close together outside the cartridge. Projections to neighbouring cartridges have not been observed. In most cases, synaptic contacts could be seen between a presynaptic retinula cell and more than two other postsynaptic profiles, which belong to monopolar cells or sometimes to glial cells. Seven retinula cell fibers of one ommatidium pass in a bundle through the basement membrane, run into their respective cartridges without changing orientation and terminate at approximately equal levels in the lamina. Long visual fibers with endings in the medulla are not visible in the superposition eye lamina, but are present in the lateral apposition eye. The relationship between the behaviour of the animal, optic mechanisms of the superposition eye and the structure of the lamina is discussed.

The relevance of the brightness to visual acuity, predation, and activity of visually hunting ground-beetles (Coleoptera, Carabidae).

Carabid species of the visually hunting type living in dim habitats have larger frontal ommatidia and gain their optimal visual performance with lower light intensity than species inhabiting bright places.The latter phenomenon is based upon the mechanisms of light adaptation, which reduce the acceptance angles of the ommatidia thus increasing their visual acuity. In more sensitive ommatidia adaptation occurs with lower light intensity.The differences between the species concerning the intensity dependence of their visual performance are regarded as an effect of natural selection. Thereafter an apposition eye more sensitive to light should be advantageous in a dim environment.This hypothesis has been investigated and verified by observation of the predation behaviour of Notiophilus biguttatus confronted with Collembola: From 1 to 500 lux the hunting success of the beetles increased proportionally to the light intensity.Measurements of the activity at dawn and at dusk under natural conditions showed that the beginning and the conclusion of activity are correlated with a critical level of illumination. Notiophilus biguttatus starts being active if the illumination is sufficient for successful hunting.

The structure of the eye ofPieris brassicae L. (Lepidoptera)

The apposition eye of the large Cabbage Butterfly,Pieris brassicae L., was investigated electronmicroscopically (TEM). Diagrams based on micrographs show details of the structure of an ommatidium. The dioptric apparatus is made up of cornea, corneal process, and crystalline cone. The sensory part consists of nine visual cells. The retina is tiered. Four distal visual cells (type I) participate in forming the distal rhabdome, the proximal part being formed by four proximal visual cells (type II) with proximal main sections. There are ultrastructural differences between these two types of receptors. The basal ninth visual cell forms, if any, only stubby microvilli that have no part in the formation of the ‘banded rhabdome’. There is no gap between the distal and proximal parts of the rhabdome, but the two parts differ morphologically. In the distal part the rhabdomeres do not interlock at right angles and are, for the most part, not exactly perpendicular to the optical axis of the ommatidium; their microvilli may be bent and sometimes extend more than halfway across the rhabdome. In the proximal rhabdome the microvilli are straight and parallel, though they too vary in extent across the rhabdome. The microvilli plates of neighbouring rhabdomeres interlock here at right angles. Basally the rhabdome ends at a large tracheal fork that acts as a tapetum. There are five different types of pigment granules in the ommatidium each belonging to a particular cell type. Distal and proximal visual cells each have one type of pigment; the other three types of pigment granules belong to two principal, six secondary, and six basal pigment cells, respectively. Each distal process of the secondary pigment cells contains microtubule bundles and is joined horizontally to the processes of neighbouring secondary pigment cells. Bundles of microtubules running parallel to the optical axis are found in the primary pigment cells, too. The ultrastructure is described, and its relevance for the eyes function, especially in the ultraviolet wavelength-range, is discussed.

Analysis of the organization and overlap of the visual fields in the compound eye of the honeybee (Apis mellifera).

Using the results of an optical analysis, a digital computer technique was developed to analyze the relative excitation produced by arbitrary figures at the rhabdom of the receptors of a compound eye. This technique was applied to several sets of figures for the honeybee (Apis mellifera) and a reasonable agreement was found with behavioral data. Similarly, the significance of a fixed cutoff angle for a visual field was investigated. It is concluded that overlap between neighboring ommatidia is highly significant for visual processing in the apposition eye, contrary to the assumptions of the mosaic theory.

The exact neural projection of the visual fields upon the first and second ganglia of the insect eye

In apposition eyes with fused rhabdomeres, six retinula cells of one ommatidium have short axons which terminate in a single cartridge. Each ommatidium corresponds to one lamina cartridge, the two ganglion cell axons of which, together with the long axons from that ommatidium and a fifth axon, proceed as a bundle through the lamina-medulla chiasma to form a cartridge of the medulla. The projection of the lamina cartridges upon those of the medulla forms a series exactly in order but reversed about the vertical plane. In the fly Calliphora, in which the optical axes of the rhabdomeres of a single ommatidium diverge, the existing description of the projection to the lamina is confirmed and extended to the medulla. As in fused rhabdomere eyes, the lamina cartridges project by bundles, each of which contains five axons, in an exact series but in reverse order, to the cartridges of the medulla.

The projection of the optical environment on the screen of the rhabdomere in the compound eye of the Musca

The dioptrics of the Musca ommatidium acts as an inverting lens system. The distal endings of the rhabdomeres at the basis of the dioptric apparatus are separated and arranged in a typical asymmetric pattern. The optical axes of the individual rhabdomeres of one ommatidium are the geometric projections of the distal rhabdomere endings into the environment, inverted by 180° by the dioptric apparatus. The divergence angles between the optical axes of the rhabdomeres of one ommatidium correspond to divergence angles between the appropriate set of ommatidia in such a way, that seven rhabdomeres of seven ommatidia are looking at one point in the environment (in the intermediate region between dorsal and ventral part of the eye: eight to nine rhabdomeres of a set of eight to nine ommatidia). These facts were established from sections of living eyes and confirmed by using special optical methods in the intact animal. The pattern of the decussation of individual retinulacell axons between retina and lamina was predicted adopting the hypothesis that the fibres of retinulacells number one to six, whose rhabdomers are looking at one point in the environment, project into a single “cartridge” in the lamina. These predicted connections were confirmed by other investigators. We have therefore a one to one correspondence between a lattice of points in the environment and the lattice of “cartridges” in the lamina. It is shown that the unfused rhabdomeric structure of the Musca ommatidium increases the effective entrance pupil of the eye by a factor of seven (resp. eight to nine in the intermediate region between dorsal and ventral part of the eye) compared to the classical apposition eye. —The Musca compound eye can be regarded as a “neural superposition eye”.

PIGMENT MIGRATION AND LIGHT-ADAPTATION IN THE EYE OF THE MOTH, GALLERIA MELLONELLA

1. An energy flux at the cornea of 5 x 103 ergs sec.-1 cm.-2 at 500 mµ causes almost complete migration of the accessory shielding pigment in the eye of the wax moth, Galleria mellonella. Movement requires approximately 30 minutes. Lower energies bring the pigment to steady-state positions intermediate between the fully light- and dark-adapted positions. 2. Light-adaptation, unlike dark-adaptation, runs a faster time course than pigment migration and is frequently complete in several seconds. This confirms an earlier report of Höglund. The theoretical reasons for a rapid rate of light-adaptation in the face of slow pigment migration are discussed and are shown to be a consequence of (a) equal absorption of the test and adapting lights by the sleeves of accessory pigment, and (b) a linear relation between ΔI and I. 3. It is suggested that the terms, superposition and apposition eye, be replaced by scotopic and photopic eye, as the latter indicate more accurately the physiological properties of these photoreceptors.

On optical resolving ability of the facet eye of Limulus

The resolving power of the human eye and the apposition eye in insects is discussed on the basis of Fraunhofer's diffraction theory. It is then shown that diffraction does not play an important role in the Limulus facet eye. In spite of this the visual fields of neighboured ommatidia overlap strongly as Waterman has shown. A mathematical relation which describes the process of imaging the optical surroundings onto the generator potentials of the excentric cells of the receptors is presented. This relation takes into account the overlap of the visual fields and the logarithmic relation between light intensity and generator potential (MacNichol, Fuortes). On the basis of Hartline and Ratliff's reports on lateral inhibition in the Limulus eye it is shown that this process corrects the overlap and therefore increases the resolving power of the eye. The functional mechanism of lateral inhibition is in principle able to create an image of the optical surroundings in the optic nerve. It therefore can compensate for the dioptric apparatus in front of the receptor mosaic. The correction process in the Limulus eye is studied quantitatively and other cases of principle interest are investigated by means of an analog computer. The results are discussed and other inhibitory processes in the visual and auditory system etc. are mentioned.