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Vis 1--invertebrates-vision


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Vis 1--invertebrates-vision

  1. 1. Vision: Invertebrates E. Warrant, University of Lund, Lund, Sweden ã 2010 Elsevier Ltd. All rights reserved. Introduction Invertebrates – animals without backbones – constitute the vast majority of all known species of animal life on Earth. From a giant squid swimming in the dark cold depths of the sea to a tiny ant foraging in the leaf litter of a rainforest floor, invertebrates have conquered almost every imaginable habitat. This extraordinary adaptability is in no small part due to their sense organs, and particu- larly their eyes, which help them to find food, locate mates, escape predators, and migrate to new habitats. Even though most invertebrates do not see as sharply as we do, many see much better in dim light, can experience many more colors, can see polarized light, and can clearly distinguish extremely rapid movements. Moreover, they do all this with eyes and brains a fraction the size of our own. It is this small size – and comparative simplicity – that have allowed scientists to unravel many of vision’s most fundamental principles, as equally applicable to a dragonfly as they are to us. Due to their small size, invertebrates often rely on comparatively simple circuits of cells to efficiently decipher complex visual information. Manyof these circuits – and the computations they perform – seem ingenious to a human observer. Indeed, many have already been used with great success to create artificial visual systems for robots, aircraft, and autonomous vehicles. This short review explores the most important func- tional modalities of visual sensation in invertebrates and how vision is used in daily life, from the capture of light and its neural processing to the ways invertebrates use vision to orient, to navigate, to avoid predators, and to find food and mates. Invertebrate Visual Systems Light is a highly physical stimulus, with an intensity, a direction, a color, and sometimes a plane of polarization. All these properties of light are detectable, to a greater or lesser extent, by the eyes of all animals. This detection relies on the conversion of light energy into an electrical signal, a chemical process that involves rhodopsin, a light- absorbing protein found in the photoreceptor cells of the retina. These electrical signals are then processed by higher visual centers (in the optic lobes and brain) to allow inver- tebrates a visual impression of the world that is probably not unlike that experienced by vertebrates. Invertebrate Eye Designs Ten distinct types of visual organs have been identified in the animal kingdom (Figures 1 and 2). Vertebrates pos- sess only one of them, whereas invertebrates possess all ten, from simple assemblies of photoreceptors that under- lie phototaxis to advanced compound and camera eyes that support a sophisticated range of visual behaviors. Some invertebrates even possess several eyes of more than one type. Eye spots and pit eyes The simplest type of visual organ – found in many smaller invertebrates and larvae (notably of worms and insects) – is an aggregation of one or more photoreceptors on the body surface, shielded on one side by a pigment cell containing screening pigment granules. Such ‘eye spots’ are unable to detect the direction from which light is incident (i.e., they do not possess spatial vision) and are therefore little more than simple detectors of light inten- sity. Since spatial vision, no matter how crude, is consid- ered to be the hallmark of a ‘true eye,’ eye spots are not considered true eyes. But for those invertebrates that possess them, eye spots are able to detect the presence or absence of light and compare its intensity sequentially in different directions, thus allowing animals to avoid or to move toward it. Pit eyes, formed by a number of photoreceptors lining a pigmented invagination – or ‘pit’ – in the epidermis, are common in turbellarian worms. Since the photoreceptors each occupy different positions in the pigment-lined pit, they are each able to receive light from a different direc- tion in space. As a result, pit eyes are capable of crude spatial vision and are thus considered to be true eyes. Pinhole eyes One evolutionary route from a pit-eyed ancestor resulted in the eyes of the abalone Haliotis and the cephalopod mollusc Nautilus (Figure 2(a)). In these eyes, the pit has developed a spherical shape, with a small ‘pinhole’ pupil that admits light to the underlying retina. However, unlike the eyes of other cephalopods (squids and octopuses), the Nautilus eye has no lens. Its pinhole eye works like a pinhole camera: the small pupil creates a dim image on the retina. However, compared to camera eyes of the same size – like those found in other cephalopods – the pinhole 511
  2. 2. eye has rather poor sensitivity and resolution, which probably explains its rarity in nature. Nevertheless, the pinhole eye is a great improvement over a regular pit eye. Concave-mirror eyes Scallops, clams, and a few ostracods have another inter- esting eye type: the ‘concave-mirror eye’ (Figures 1 and 2(b)). In this design, light weakly focused by the cornea passes through the retina, and is then reflected from a hemi- spherical concave mirror (m in Figure 2(b)) lining the back of the eye. This reflected light is focused into the retina, but since the retina has already absorbed part of the weakly focused light on the way in, the image contrast is rather poor. With its large pupil, its potential for light capture, on the other hand, is excellent. Indeed, one of the most sensitive eyes in nature is of this design and found in the deep-sea ostracod Gigantocypris. Many scallops and clams have hundreds of concave-mirror eyes lining the edges of both shells, and these are optimized as ‘burglar alarms’ for the rapid detection of shadows cast by predators attempting to enter the shell. Compound eyes By far, the most widespread eye design in the animal kingdom is the ‘compound eye’ design, possessed by insects (75% of the world’s animal species), most crustaceans, myriapods, and even some clams and polychaetes. Compound eyes are composed of identical units called ‘ommatidia’ (Figure 3(a)), each consisting of a lens element – the ‘corneal lens’ and ‘crystalline cone’ – that focuses light incident from a narrow region of space onto the ‘rhabdom,’ a photoreceptive structure composed of membranous microvilli that house the rhodopsin molecules (Figure 3(b), 3(c), 3(e), and 3(f )). In all eyes, the rhodopsin molecules absorb photons of light and trigger the chain of biochemical events that leads to the generation of an electrical signal, a process known as ‘phototransduction.’ In most compound eyes, the rhabdom is built by fusing the photoreceptive segments (or ‘rhabdomeres’) of several photoreceptor cells (or ‘retinula cells’: rc in Figure 3(a)). A compound eye may contain as many as 30 000 ommatidia, as in large dragonflies, or as fewas 1, as in some ants. Each ommatidium is responsible for reading the average intensity, color, and (in some cases) plane of polarization within the small region of space that they each view. Two neighboring ommatidia view two neighboring regions of space. Thus, each ommatidium supplies a ‘pixel’ of information to a larger image of pixels that the entire compound eye con- structs. Larger compound eyes with more ommatidia thus have the potential for greater spatial resolution. Compound eyes come in two main forms: ‘apposition eyes’ and ‘super- position eyes.’ Apposition eyes (Figure 2(d)) are typical of (but not restricted to) animals living in bright habitats. Each ommatidium in an apposition eye is isolated from its neighbors by a sleeve of light-absorbing screening pig- ment, thus preventing light reaching the photoreceptors from all but its own small corneal lens. This tiny lens – typically about 30 mm across – represents the pupil of the apposition eye. Such a tiny pupil only allows very little light to be captured. Not surprisingly, apposition eyes are best suited to bright habitats. Day-active insects with apposition eyes include butterflies, bees, wasps, ants, dra- gonflies, and grasshoppers. Many crabs also have apposi- tion eyes. There are two types of apposition eye known: the widespread ‘focal’ type (Figure 2(d)) and the less com- mon ‘afocal’ type. In focal apposition eyes, the crystalline cone has a homogeneous refractive index, and light is focused by the curved exterior surface of the corneal Figure 1 Invertebrate eyes. Row 1, left to right: the camera (two larger eyes) and pigment cups eyes (two smaller eyes) that equip a single rhopalium of the box jellyfish Tripedalia cystophora (courtesy of D.E. Nilsson); three of the many compound eyes that line the mantle edge of the ark clam Barbatia cancellaria (courtesy of D.E. Nilsson); two of the many concave-mirror eyes that line the mantle edge of the scallop Pecten (courtesy of D.E. Nilsson); the pinhole eye of the cephalopod mollusc Nautilus. Row 2, left to right: the camera eyes of an unknown species of conch; the camera eyes of an unknown species of cuttlefish; the apposition compound eyes of a crab zoea (larva) (courtesy of D.E. Nilsson); the apposition compound eyes of an unknown species of fiddler crab. Row 3, left to right: the apposition compound eyes of an unknown species of mantis shrimp; the apposition compound eyes of the nocturnal bee Megalopta genalis; the refracting superposition compound eyes of the mayfly Baetis (courtesy of D.E. Nilsson); the apposition compound eyes of an unknown species of katydid. Row 4, left to right: the apposition compound eyes of an unknown species of robber fly; the apposition compound eyes of an unknown species of dragonfly; the camera eyes of an unknown species of jumping spider; the camera eyes of the net-casting spider Dinopis subrufus. 512 Vision: Invertebrates
  3. 3. facet lens onto the distal tip of the rhabdom. In flies, the rhabdom is ‘open,’ meaning that its eight rhabdomeres are separated rather than fused. In fly eyes – called ‘neural superposition eyes’ – each point in space is imaged by seven rhabdomeres in each of seven neighboring omma- tidia. The axons of six of these rhabdomeres superimpose on a neural cartridge under the central ommatidium, in the lamina, the first optic neuropil of the brain. Thus, compared with a conventional focal apposition eye, this rewiring arrangement allows a sixfold increase in sensi- tivity for no loss in spatial resolution. Afocal apposition eyes are only known in papilionoid butterflies and differ from the focal type by having a strong gradient of refractive index in the extreme proxi- mal end (or ‘cone stalk’) of the crystalline cone. Rays are brought to an intermediate focus at the entrance of the cone stalk and are then recollimated by the refractive- index gradient, which acts like a powerful second lens, an adaptation that improves both spatial resolution and sensitivity. Superposition eyes (Figure 2(e)) – of which there are three different types – are typical for (but not restricted to) animals living in dimmer habitats. In superposition eyes the pigment sleeve is withdrawn, and a wide optically transparent area, the clear zone, is interposed between the lenses and the retina. This clear zone (cz in Figure 2(e)) – and specially modified crystalline cones – allow light from a narrow region of space to be collected by a large number of ommatidia (comprising the superposition aperture) and focused onto a single rhabdom. Unlike the crystalline cones of apposition eyes, those of superposition eyes have evolved refractive index gradients or reflecting sur- faces, that allow as many as 2000 lenses to collect the light for a single photoreceptor (as in some nocturnal moths). This represents a massive improvement in sensitivity while still producing a reasonably sharp image. (a) (b) (d) (e) (c) cz m Figure 2 The main optical designs of invertebrate eyes. (a) The pinhole eye, possessed by the cephalopod mollusc Nautilus, lacks a lens: the small pupil creates a dim and blurred image on the retina in much the same way that a pinhole camera does. (b) The concave-mirror eye, possessed by many scallops, clams, and ostracods, relies on a hemispheric reflective mirror m (or ‘tapetum’) that lines the back of the eye. Light first passes unfocused through the retina, and is then focused into the retina upon reflection. (c) The camera eye, possessed by all vertebrates, cephalopod and gastropod molluscs, and most arachnids. Light is focused by the cornea (air only) and lens to form an image on the retina. (d) The focal apposition compound eye. Light reaches the photoreceptors exclusively from the small corneal lens located directly above. This eye design is thus rather insensitive to light, and is typical of day-active insects and many crustaceans. (e) The refracting superposition compound eye. A large number of corneal facets and bullet-shaped crystalline cones collect and focus light – across the clear zone of the eye (cz) – toward single rhabdoms in the retina. Several hundred, or even thousands, of facets service a single rhabdom. Not surprisingly, many nocturnal and deep-sea animals – for example, nocturnal insects and krill – have refracting superposition eyes, and benefit from the significant improvement in sensitivity. Diagrams courtesy of Dan-Eric Nilsson. Vision: Invertebrates 513
  4. 4. In the ‘refracting superposition eye’ (Figure 2(e)) – found in many beetles, moths, and some crustaceans such as krill – there is a powerful gradient of refractive index from the axis to the edge of each crystalline cone (which is circular in cross-section). There is also a weak gradient present in the corneal lens. These gradients turn the corneal and crystalline cone lenses into an afocal tele- scope: light rays focused by the corneal facet to an inter- mediate focus in the cone are then recollimated into a parallel bundle before exiting proximally toward the tar- get rhabdom. The superposition image is formed from the incidence of all such bundles on the retina. In the ‘reflect- ing superposition eye’ – found in aquatic and marine Macruran crustaceans – the crystalline cone is square in cross-section, has a homogeneous refractive index, and is coated in reflective pigment. Parallel light rays are focused across the clear zone by reflection within the crystalline cones, each of which acts as a mirror box. The clear zone, however, is not optically homogeneous (as in the refracting design) but is instead crossed by tapering cone tracts that connect the crystalline cones to the retina. These tracts have a shallow gradient of refrac- tive index along their length. For rays well away from the ommatidial axis, reflection takes place in the crystalline cones, whereas for those nearer the axis, reflection occurs within the cone tract. This unique arrangement allows for a superposition image on the retina. A third type – the ‘parabolic superposition eye’ – is so far only known in some swimming and hermit crabs, and works using a combination of refraction and reflection. Camera eyes In camera-type simple eyes (Figure 2(c)), light is focused onto the retina by a single optical system comprising a lens and in some cases an overlying cornea. All vertebrates have camera eyes, including ourselves. So do many c cc pc sc rh rc bp bm (a) Δφ(d) (b) (c) 1 2 3 45 c.c. co. 6 7 8 7 1 2 34 5 6 (f) (e) Figure 3 Compound eyes. (a) A schematic longitudinal section (and an inset of a transverse section) through a generalized Hymenopteran ommatidium, showing the corneal lens (c), the crystalline cone (cc), the primary pigment cells (pc), the secondary pigment cells (sc), the rhabdom (rh), the retinula cells (rc), the basal pigment cells (bp), and the basement membrane (bm). The left half of the ommatidium shows screening pigment granules in the dark-adapted state, while the right half shows them in the light-adapted state. (b) A schematic transverse section through the open rhabdom of a higher fly, showing the seven distal retinula cells with their separated rhabdomeres. (c) A schematic transverse section through the fused rhabdom of the Collembolan Orchesella, showing the eight retinula cells with their apposed rhabdomeres. (d) A schematic longitudinal section through nine neighboring ommatidia in a focal apposition eye. The interommatidial angle △f is the divergence angle between two adjacent ommatidia. co: corneal lens; c.c.: crystalline cone. (e, f) Transverse sections of rhabdoms in the dorsal rim area (DRA, (e)), and remainder of the eye (f), in the dung beetle Scarabaeus zambesianus. In the dorsal rim, the rhabdomeres each have one of two possible perpendicular microvillar directions (white perpendicular bars), whereas in the remainder of the eye the rhabdoms are flower-shaped and the rhabdomeres have microvilli oriented in one of several possible directions. Scale bar for both parts: 5 mm. Adapted from Warrant EJ, Kelber A, and Frederiksen R (2007) Ommatidial adaptations for spatial, spectral and polarisation vision in arthropods. In: North G and Greenspan R (eds.) Invertebrate Neurobiology, pp. 123–154. Woodbury, NY: Cold Spring Harbor Laboratory Press. 514 Vision: Invertebrates
  5. 5. invertebrates, including many molluscs (including squids and octopuses), some annelid worms and various arthro- pods including spiders, and many insect larvae and cope- pods. Despite their functional similarity, the camera eyes of vertebrates and invertebrates have very different devel- opmental origins. The vertebrate retina derives from the frontal part of the brain, whereas the lens derives from the skin. In invertebrates, both the retina and the lens derive from the skin. In nonarthropod invertebrates – such as cephalopod and gastropod molluscs – the lens is inside the eye, beneath an external cornea. In arthropods, the lens is formed by a thickening of the corneal cuticle. The camera eyes of deep-sea animals – particularly those of squids – can reach enormous size. The largest eyes known in the animal kingdom are the camera eyes of the giant deep-sea squid (Architeuthis dux) that can reach a diameter of over 30 cm! Camera eyes have better resolution and sensitivity than any other eye type of comparable size. Higher Visual Centers Just as in vertebrates, which have a visual cortex and several other brain areas for the higher processing of visual infor- mation, visual signals leaving the retina of invertebrates are processed sequentially, and along several parallel informa- tion pathways, in a number of higher visual centers located in the cephalic ganglion (the brain: Figure 4). In the well- studied insects, visual information is first processed by the retinotopically organized neuropils of the optic lobe: the lamina, medulla, lobula, and in some species (notably flies, butterflies, and beetles), a subdivision of the lobula known as ‘the lobula plate.’ The lamina optimizes the signals coming from the retina, and after receiving these signals, the medulla – which remains little understood – makes elementary analyses of the fundamental modalities of the visual signal (space, time, color, and polarization). The lobula, which receives retinotopic input from the medulla, plays an important role in the analysis of color, the discrim- ination of line orientation, and the detection of moving small-field targets. The lobula plate, which receives retino- topic input from both the medulla and the lobula, houses large wide-field motion-sensitive cells that are responsible for analyzing optic flow induced during locomotion. The optic lobes of other invertebrates are less well understood, but they contain similar neuropils. The optic lobes of cephalopods are particularly well developed. In Octopus vulgaris, it has been estimated that the optic lobes alone contain about 75% of the total number of neurons found in the central nervous system. An identical optic lobe connects each eye to the supra- and subesophageal ganglia, and permits tracts of visual information leaving the lobula and lobula plate to be processed further in the brain. The tract (or pathway) for polarization vision in a locust is shown in Figure 4(b). This visual information is integrated with information derived from other senses, after which it is relayed by giant descending fibers that carry highly specific sensory information to the motor circuitry of the thoracic ganglia that control the wings and legs (and thus locomotion). In some species, some visual information is also carried to the abdominal ganglia. Several important areas of visual processing have now been identified in the insect brain. The mushroom bodies – paired structures located in both halves of the central brain region – are important in integrating information from several sensory modalities, and for their role in learning and memory. The central complex – a highly columnar neuropil in the center of the brain – seems to be involved in the spatial organization of locomotion (and possibly spatial organization in general). The Modalities of Vision Like vertebrates, invertebrates have the ability to detect and analyze the main properties of light, namely its inten- sity, its direction, its color, and its polarization. These properties define the modalities of vision, and together these provide the information necessary for invertebrates to interpret the visual world. Sensitivity to Light The greatest challenge for an eye that views a dimly illuminated scene is to absorb sufficient photons of light to reliably discriminate it. Certainly, ever since the pio- neering studies of Yeandle in the horseshoe crab Limulus in the late 1950s, we have known that photoreceptors can respond to single photons with small but distinct electri- cal responses known as ‘bumps.’ Such responses are found in both vertebrates and invertebrates, and seem to indi- cate that animal eyes are exquisitely sensitive to light. While this is certainly true, the visual response is also inherently noisy, due to the unpredictable and random nature of photon arrivals as well as to sources of neural noise in the photoreceptors themselves. The effects of these sources of noise are minimized by capturing more light: the greater the number of photons captured, the greater the signal relative to the noise and the more reliable is visual discrimination. In regard to light capture, the eyes of invertebrates living in dim light are among the most sensitive found in the animal kingdom. Indeed, the huge eyes of giant deep-sea squids (with a diameter of up to 30–40 cm) are likely to be the most sensitive eyes that have ever existed. Eyes of high absolute sensitivity to extended scenes tend to have (relative to eye size) large pupils, short focal lengths, and large photoreceptors. A frequently used parameter to describe the light-gathering capacity of an imaging system is its ‘F-number,’ the ratio of its focal length f to the diameter of its entrance pupil A (i.e., f/A). Vision: Invertebrates 515
  6. 6. This is a useful and easy metric for comparing the light- gathering capacities of different eyes, with a lower F-number indicating a brighter image. The huge camera eyes of the nocturnal net-casting spider Dinopis subrufus have an F-number of < 0.6, a much lower value than in the anterior-median (AM) eyes of the diurnal jumping spider Phidippus johnsoni (F-number ¼ 2.0). The dark- adapted human eye has an F-number of around 2.1. Thus, the eyes of Dinopis are clearly constructed for high sensitivity. Among compound eyes, the superposition eyes of the nocturnal hawkmoth Deilephila elpenor have an F-number of around 0.7. This high sensitivity to light has permitted many invertebrates to have remarkably good vision in dim light. Nocturnal hawkmoths and bees can see the colors of flowers and negotiate dimly illuminated obstacles dur- ing flight. Nocturnal bees can also home using learned terrestrial landmarks, while moths and dung beetles can navigate using constellations of stars or the dim pattern of polarized light formed around the moon. ca pe β al lo me la r (a) (b) 500 μm DRMe ALo2 Ca P PB CB MO LAL IL LU OLo OL ∗ ∗ LT ALo1 OLoMe Figure 4 Visual neuropils and pathways in the insect brain. (a) A frontal section of the entire bee brain. The retina r and various neuropils of the optic lobe (lamina, la; medulla, me; and lobula, lo) are shown with neuropils of the brain: the mushroom body (comprising the calyx, ca; the peduncle, pe; and the b-lobe of the peduncle, b), and the antennal lobe al. Section courtesy of Wulfila Gronenberg. Reproduced from Ehmer B and Gronenburg W (2002) Segregation of visual input to the mushroom bodies in the honeybee (Apis mellifera). The Journal of Comparative Neurology 451: 362–373. (b) A schematic drawing of the optic lobes and brain of the locust Schistocerca gregaria, with the polarization pathways shown in dark gray. Me: medulla; DRMe: dorsal rim area in the medulla; ALo1–2: layers 1 and 2 of the anterior lobe of the lobula; OLo: outer lobe of the lobula; Ca and P: calyces and penduncles of the mushroom bodies; CB: central body; LAL: lateral accessory lobe; PB: protocerebral bridge; OL and IL: outer and inner lobes of the upper unit of the anterior optic tubercle; LU: lower unit of the anterior optic tubercle; LT and MO: lateral triangle and median olive of the lateral accessory lobe. Scale bar ¼ 200 mm. Diagram courtesy of Uwe Homberg. Reproduced from Homberg U, Hofer S, Pfeiffer K, and Gebhardt S (2003) Organization and neural connections of the anterior optic tubercle in the brain of the locust, Schistocerca gregaria. The Journal of Comparative Neurology 462: 415–430. 516 Vision: Invertebrates
  7. 7. Temporal Vision The ability of animals to see things that move at different speeds is a reflection of their temporal vision, that is, how ‘fast’ they are able to see. A human observer is unable to discriminate a bullet fired from a rifle simply because it moves too rapidly to be seen. The fastest objects that can be seen by an animal depend on many factors, including the physiological properties of the photoreceptors and the ambient light intensity. Moreover, the speed of vision varies from species to species, with some species having very fast vision (like the fast-flying aerobatic diurnal insects) and others having very slow vision (like sedentary nocturnal toads). This indicates that the speed of vision, like every other aspect of vision, is matched to the ecol- ogies of animals: those that move rapidly, or need to detect fast-moving objects (e.g., mates or prey in full flight), tend to have fast vision, while those that are sedentary or slowly moving tend to have slow vision. The speed of vision varies widely between animals because the dynamics of phototransduction, and the iden- tities and proportions of ion channels present in the photo- receptors (and the membrane kinetics they thus establish), differ substantially from species to species, and these dif- ferences have evolved in response to the various ecological needs of animals. In fact, the cell membrane, via its electri- cal properties, acts as a ‘matched filter’ that is able to match the response properties of the eye to the lifestyle that the animal possesses, such as its locomotion speed or its pre- ferred light intensity niche. In addition to these ecological influences, the filtering properties of the photoreceptor membrane and the transduction cascade are influenced by the state of adaptation and the temperature. The fastest visual systems found in the animal king- dom are possessed by invertebrates, and the fastest are likely to be those of calliphorid flies, which in a light- adapted state are able distinguish light stimuli that flicker at rates of up to around 300 Hz (for humans, in compari- son, the limit is around 50 Hz). These flies engage in high- speed pursuit and interception of mates, a behavior that involves rapid and unpredictable changes in flight trajec- tory and which requires a rapid visual response. For all species, vision slows down as light levels fall (due to adaptive changes in the physiological properties of the photoreceptors), and nocturnal and deep-sea species tend to have intrinsically slower vision than species active in bright sunshine. Slower vision in dim light significantly improves the reliability of vision because it filters out faster visual details that tend to be inherently noisy and degrade visual performance. Spatial Vision Most visual scenes viewed by animals on land or in the upper depths of the ocean are extended in nature, meaning that light reaches the eye from many different directions at once. The spatial details of such a scene – defined by local contrast differences between areas of light and dark – are imaged by the eye onto the underlying retina. The finest spatial details that can be seen by an eye are deter- mined by two main factors: (1) the quality of the optical system that images the scene (i.e., the cornea and lens(es)) and (2) the density and visual fields of the photoreceptors that receive the image. Both these factors are in turn subservient to the amount of light that the eye can collect from the scene. As observed earlier, as light levels fall, visual reliability declines because of a decreasing signal- to-noise ratio. This is particularly true for the smaller contrast differences typical of finer spatial details, which tend to be lost in the noise as intensity falls, a limitation that is equally problematic for all eyes, irrespective of their optical quality or photoreceptor density. Thus, in general, spatial resolution declines with light intensity. The optical quality of an imaging system depends on the extent it suffers from various aberrations, particularly spherical and chromatic aberrations. Moreover, in very small lenses such as those found in compound eyes, it also depends on diffraction of light waves entering the aper- ture. The effect of all these optical imperfections is to blur the image formed on the retina, that is, to reduce its contrast. Even though there are many invertebrate species whose eyes lack an imaging system altogether (e.g., the cephalopod Nautilus), those that do possess one very fre- quently have surprisingly crisp optics and good optical image resolution. For example, among the single lenses of camera eyes, those of tiny cubozoan jellyfish eyes are remarkably sharp, as are those of most gastropod and cephalopod molluscs and most arachnids. What is typical for most of these lenses is the presence of a powerful radial (and often parabolic) gradient of refractive index from the center to the edge of the lens, which tends to almost exactly cancel spherical aberration. The lenses of jumping spiders are an excellent example, which together with a densely packed retina, allow jumping spider eyes to have among the best spatial vision for their size in the animal kingdom. In compound eyes, the small ommatidial lenses are typically only 20–100 times wider than the wavelength of visible light, a fact that invariably leads to image degradation due to diffraction. In superposition eyes, optical image quality is additionally limited by the accuracy of superposition of light rays on the target rhab- dom, and in species where the rhabdoms are not shielded by screening pigments or a tapetal sheath, by the spread of more steeply incident rays through neighboring rhab- doms (which blurs the image neurally). Once the image is focused on the retina, the underly- ing matrix of photoreceptors must reconstruct it. Like the pixels of a digital camera, the density of photorecep- tors in an eye sets the finest spatial detail that can be reconstructed: more densely packed photoreceptors can Vision: Invertebrates 517
  8. 8. reconstruct finer details. Ideally, the density of photore- ceptors should be matched to the finest spatial detail that can be passed by the optics, but often this is not the case. For example, in many gastropod mollusc camera eyes – such as those in the giant queen conch – the lens supplies much sharper images than the retina can resolve, and in the tiny camera eyes of cubozoan jellyfishes, the retina is located distal to the focal plane of the lens, which means that the photoreceptors do not receive the sharply focused image that the lens supplies. It would seem that even though the eyes are capable of providing a sharp image, these animals do not require the spatial acuity their lenses afford. To exploit this acuity, a larger number of visual cells would undoubtedly be needed to process the addi- tional spatial information, bringing with it an energy cost that the animal might not be able to afford. Ultimately, the eye that evolves in a particular animal is the result of natural selection, whereby an optimal balance is found between the costs of maintaining the eye and the ecologi- cal benefits it bestows upon the animal. This reasoning is equally true for the evolution of all sensory organs. In other camera eyes – particularly those of spiders and cephalopods – the matrix of photoreceptors is usually well matched to the optical quality of the image focused by the lens. As an example, we can consider the AM eyes of diurnal jumping spiders. In the jumping spider Portia fimbriata, the AM eyes are among the sharpest known in invertebrates, with the potential to discriminate spatial details subtending as little as 2.4 min of arc, a performance approaching that of our own eyes. Just as amazing is that muscles connected to the internal structure of the eye allow the sharpest region of the retina to be scanned across the visual field. This outstanding spatial resolution can be explained by both optical and neural adaptations. In Portia, the AM eyes are almost 1 mm wide and almost 2 mm deep, with a retina divided into four distinct layers of receptors (I–IV) arranged proximally to distally. Distal to the receptors, the retina forms a pit aligned with the ocular axis, the curved surface of which forms an interface with the lower refractive index internal vitreous of the eye. This interface acts as a diverging lens, increasing the focal length of the system and magnifying the image by about one-and-a-half times. This is analogous to the telephoto system employed in falconiform birds of prey and almost doubles visual acuity. Spatial resolution is further improved by the presence of a gradient of refrac- tive index in the lens that corrects for spherical aberration in the image. However, the lens also suffers from chro- matic aberration: light of shorter wavelength is focused to a position closer to the lens than light of longer wave- length, thus blurring the image. This has also been cor- rected in a most remarkable manner: receptors with maximum sensitivity to the shorter wavelengths are placed more distally in layer IV (found to be ultraviolet-sensitive cells), whereas those with maximum sensitivity to the longer wavelengths are placed more proximally in layers I and II (found to be green-sensitive cells). In compound eyes, spatial vision is highly dependent on the number of ommatidia present in each eye and on their packing density. The number of ommatidia in a single eye can vary from as few as one, as found in some primitive ants, to as many as 30 000, as found in some species of large dragonfly. Since each ommatidium essentially accounts for a single ‘pixel’ of the image, eyes with more ommatidia have the potential for higher spatial resolution. The density of ommatidia – specified by their interom- matidial angle △f (Figure 3(d)) – is also important. The interommatidial angle is a measure of how tightly packed the ommatidia are within an eye or a specific eye region: the smaller this angle, the more tightly packed the omma- tidia and the more finely sampled the visual scene. The interommatidial angle (in radians) is also related to the corneal facet diameter (D) and the local radius of curvature of the eye (R) by △f ¼ D/R, showing that a larger local eye radius, or a smaller facet, produces a smaller inter- ommatidial angle and greater spatial resolution. A smaller facet, however, collects less light and invariably suffers from the image-degrading effects of diffraction. A larger eye radius means a larger eye, and this has limits too: animals with compound eyes are generally rather small and there is a limit to how big an eye they can carry. Apart from anything else, the metabolic cost of having a larger eye is quite enormous and sets a serious limit to how big a particular eye can be. Instead, a wonderful compromise has evolved that maintains eye size. Rather than enlarging the whole eye, some animals have ‘enlarged’ a small part of their eye, and thus a small part of their visual field. A local increase in eye radius may not only allow an increase in lens size (which reduces diffraction and improves light capture) but if eye radius is increased sufficiently, it might even allowa simultaneous reduction in △f (thus sharpening spatial resolution). Unfortunately, any benefits gained in one eye region necessarily come at the cost of other regions. Despite this, it turns out that these specialized eye regions – known as ‘acute zones’ – are quite common, especially in apposition eyes. The presence of an acute zone implies that one region of the visual world is more important to an animal than others. Exactly which region depends on several factors, many reflecting transient needs, such as the need to find a mate or prey, or the need to detect the advance of a predator. Others reflect more permanent needs, not the least of which is the structure of the habitats where animals live. As an example of the latter, consider the apposition eyes of animals adapted for life in a flat habitat: a desert ant that runs across a salt pan or a fiddler crab that scans a flat intertidal beach for mates. All experience a bright world dominated by the horizon, and all possess eyes having an elongated horizontal acute zone of enhanced resolution known as a ‘visual streak.’ Because most objects 518 Vision: Invertebrates
  9. 9. of interest for these animals occur either at or very near the horizon, visual streaks concentrate the majority of the eye’s sampling stations – and thereby visual capacity – at the same locations. In fiddler crabs, the apposition eyes are vertically elongated, almost cylindrical, and located on long stalks above the carapace. The shape of the eye means that the radius of curvature in the vertical eye plane is much greater than in the horizontal eye plane, resulting in the vertical interommatidial angles (△fv) being much smaller (by up to a factor of 4) than the horizontal ones. △fv steeply narrows toward the horizon (from both above and below) becoming smallest (0.3 ) just along the eye’s equator. Acute zones have also evolved in the context of mate detection. Female brachyceran flies, like blowflies and hoverflies, have their eyes spaced well apart, but in males the eyes are joined at the top of the head. This extra area of eye constitutes a frontal-dorsal acute zone used by the males to keep sight of females during high- speed pursuits. Amusingly, these acute zones are often referred to as ‘love spots.’ They are clearly seen in the male hoverfly Volucella pellucens, which has large love spots located frontally, 20 above the equator (Figure 5). The interommatidial angle here falls to just 0.7 . The size of the acute zone (the eye region where, say, △f 1.1 ) occupies 2230 deg2 of the visual field (shaded area in Figure 5). In females there is also an acute zone, directed exactly frontally and probably used for controlling flight. In females, △f only falls to 0.9 , and the area of the acute zone (△f 1.1 ) is a mere 23% as large as that of males (510 deg2 : shaded area in Figure 5). The acute zones of male flies are not restricted to the eye surface. Below the eye, there is an intricate neural pathway that is specific to males. First, the connections of photoreceptor axons to the lamina are quite different in the acute zone compared to both the female’s eye and the rest of the male’s eye. Higher up the brain, in the lobula, large male-specific visual cells respond maximally to small dark objects that move across a bright background in the frontal-dorsal visual field, an ideal physiology for detecting silhouetted females flying against the sky! Color Vision Many invertebrates experience a richly colored world, some much more richly than we ourselves experience it. The reason for this is that color is important in a variety of behavioral contexts including phototaxis and orientation, camouflage, object detection and recognition, the detec- tion of host plants for oviposition, the recognition of flowers and other food sources, the detection and inter- pretation of colored signals during sexual and social inter- actions, and the location of new shelters and recognizing learned landmarks. The sensation of color requires the presence of at least two ‘spectral types’ of photoreceptor that view the same region of space, followed by a neural comparison of the signals generated in these photoreceptors (usually via a neural opponency mechanism) at a subsequent (higher) level of the visual system. The spectral type of a photore- ceptor is defined by its spectral sensitivity, that is, its sensitivity to different wavelengths (or colors) of light. For example, a UV spectral type absorbs primarily in the ultraviolet part of the spectrum, whereas a green L D D V Male A L Female V A 1.3Њ 1.3Њ 1.2Њ 1.2Њ 1.1Њ 1.3Њ 1.4Њ 1.0Њ 0.9Њ 0.8Њ 0.7Њ 0.9Њ 1.1Њ 1.0Њ 1.4Њ 1.4Њ 1.5Њ 1.5Њ 1.6Њ 1.6Њ 1.3Њ 1.4Њ 1.5Њ 1.6Њ Figure 5 Sexual dimorphism in the apposition eyes of the hoverfly Volucella pellucens. (a) Female and (b) male. The visual fields of the left eyes of the two sexes, and interommatidial angles shown by isolines, are projected onto spheres, where A: anterior; M: medial; L: lateral; V: ventral; and D: dorsal. Both sexes possess acute zones directed frontally, an adaptation for processing optic flow during forward flight. Compared to the female, however, the male has a much larger acute zone directed 20 –30 dorsally (shaded regions, where △f 1.1 ). The male’s acute zone is used for fixating females during sexual pursuit. Reproduced from Warrant EJ (2001) The design of compound eyes and the illumination of natural habitats. In: Barth FG and Schmid A (eds.) Ecology of Sensing, pp. 187–213. Berlin: Springer Verlag. Vision: Invertebrates 519
  10. 10. spectral type absorbs primarily in the green part of the spectrum. Exactly which band of wavelengths a receptor absorbs, and how sensitive it is to individual wavelengths within that band, depends mainly on the nature of its ‘visual pigment’ rhodopsin. Rhodopsin molecules – which absorb photons of light and trigger the generation of an electrical signal – are composed of two parts: a large ‘opsin’ molecule, a protein consisting of a chain of around 350 amino acids embedded in the photoreceptor mem- brane, and a small ‘chromophore,’ a molecule (typically retinal, hydroxyretinal or dehydroretinal) that is coupled to the opsin. The band of wavelengths absorbed by the rhodopsin molecule depends on the exact sequence of amino acids present in the opsin molecule and the iden- tity of the chromophore. Even though the absorption spectrum of the resident rhodopsin molecule is the main determinant of the photo- receptor’s spectral sensitivity (and thus its spectral type), it is also affected by the concentration of rhodopsin, the presence or absence of sensitizing or filtering pigments, the photoreceptor’s length and placement, and the absor- bance and reflectance of structures within the eye. For instance, if the rhabdom of a UV spectral type lies distal to that of a green spectral type (i.e., if the rhabdoms are ‘tiered’), the spectrum of light received by the green- sensitive photoreceptor will be filtered because of its partial absorption by the overlying UV-sensitive photore- ceptor. This filtering will tend to narrow the spectral sensitivity of the underlying green-sensitive photorecep- tor and often shift its peak. Filtering resulting in spectral sensitivity changes also occurs if a colored filter (e.g., a membrane-bound vesicle of colored pigment) is located at the distal entrance to the rhabdom, or between two tiered rhabdoms (a common arrangement in the apposition eyes of mantis shrimps), or if colored pigment granules are located within or around the photoreceptor cells (as found in a variety of insect and crustacean species). The effect of all filtering mechanisms is to sharpen and tune the spectral sensitivities of the resident spectral types of photoreceptors, to maximize and optimize the range and/ or numbers of colors seen. Of course, the colors that animals need to see in order to survive and reproduce vary dramatically from species to species according to their ecology. In fact, the number of photoreceptor spec- tral types and the nature of any filtering that evolves in an eye are ultimately driven by the ecological needs of its owner (Figure 6). Most invertebrate rhabdoms contain at least two pho- toreceptor spectral types that share the same receptive field, thus fulfilling the first precondition of color vision. However, in the deep sea, where the spectrum of down- welling daylight is almost monochromatically blue (around 480 nm), there is almost no need for color vision, and with few exceptions, deep-sea animals are mono- chromats, possessing only one photoreceptor spectral type (e.g., deep-sea crustaceans and cephalopods). More- over, in the same eye, there can be regions of the retina where only one photoreceptor spectral type is present, whereas in other retinal areas, two or more types can be present. This allows monochromatic vision in one part of the visual field and the potential for color vision in another part. A good example of this is the camera eye of the firefly squid Watasenia scintillans (Figure 6(g)). Most of the retina contains only one photoreceptor spectral type with peak absorption at 484 nm (and allowing mono- chromatic vision), whereas a small region of the ventral retina (which views the dorsal visual field) contains two further photoreceptor spectral types (peaking at 470 and 500 nm) and the possibility of dichromatic color vision (which may be useful for detecting and analyzing the two colors of bioluminescence produced by the squid during courtship). Many invertebrates have evolved two photoreceptor spectral types throughout the retina (e.g., many spiders, crustaceans, cockroaches, and ants), with the potential for dichromatic color vision. Trichromacy, based on three photoreceptor spectral types with peak absorptions in the UV (350 nm), blue (450–480nm), and green (500–550 nm), is also common and found in many clams (Figure 6(h)), spiders (Figure 6(e)), crustaceans (e.g., isopods), and insects (e.g., grasshoppers, bugs, bees, wasps, moths: Figure 6(a)). As a comparison, our own trichromacy is based on three photoreceptor spectral types (blue, green, and yellow-red) with peak absorptions at around 420, 530, and 560 nm. Some invertebrates – notably some jumping spiders, water fleas, and butterflies – have extended their spectral range from the UV to the red by adding a fourth photore- ceptor spectral type. Others have five photoreceptor spec- tral types (e.g., some dragonflies (Figure 6(b)) and flies), while yet others have six (some butterflies of the genus Papilio : Figure 6(c)). Remarkably, the eyes of mantis shrimps (Stomatopoda) have 12 photoreceptor spectral types (Figure 6(f )) – the largest number known in the animal kingdom – each narrowly tuned as the result of spectral filtering. These 12 types evenly sample the spec- trum from the deep UV to the far red but are only found in a narrow band of ommatidia stretched across the center of each eye (which is scanned across objects of interest). Whether or not these colorful reef-dwelling crustaceans have 12-dimensional color vision remains unknown, but even if an animal possesses a certain number of photore- ceptor spectral types, this does not necessarily imply that all interact to create the maximal dimension of color vision possible. Polarization Vision In addition to its particulate (photon) nature, light can also be physically described as an electromagnetic wave, an electric field and a magnetic field that oscillate in 520 Vision: Invertebrates
  11. 11. unison at the same frequency, but are perpendicular to each other. The polarization properties of the wave can be described by its electric field component, and particularly by the electric field’s phase relationships, which deter- mine whether the light wave is linearly (or plane) polar- ized or whether it is elliptically or circularly polarized. Remarkably, invertebrates are able to see both plane and circularly polarized light, and to use it in several impor- tant behavioral contexts, notably navigation, orientation, prey detection, and for interactions between individuals of the same species. Except for a few controversial cases (notably among the birds and fishes), polarization vision is unknown in vertebrates. The most common polarization vision in invertebrates involves the detection and analysis of linearly (plane) polarized light, since this is the most common form of polarized light found in Nature. The plane of polarization is defined as the plane in which the electric field wave (or e-vector) oscillates. Most sources of light (both natural and artificial) emit an immense number of such electro- magnetic waves, and commonly these waves are collectively plane unpolarized: the planes of polarization of individual waves are randomly distributed in the light beam. How- ever, natural sources of light are quite often plane polar- ized, meaning that all individual light waves more or less share the same plane of polarization. Watasenia Deilephila Papilio 1.0 0.5 0.0 Wavelength (nm) Torrea Primary retina Secondary retina Tridacna Cupiennius RelativesensitivityRelativesensitivity 1.0 0.5 0.0 1.0 0.5 0.0 1.0 0.5 0.0 1.0 0.5 0.0 1.0 0.5 0.0 1.0 0.5 0.0 1.0 0.5 0.0 Hemi- cordelia (a) (b) (c) (d) (e) (f) (g) (h) G G G G R R B B B B V V UV UV GBUV UV UV RelativesensitivityRelativesensitivity 300 300 Wavelength (nm) 700600500400700600500400 Figure 6 Photoreceptor spectral sensitivities in selected invertebrates. UV: ultraviolet; V: violet; B: blue; G: green; R: red. (a) The trichromatic visual system of the nocturnal hawkmoth Deilephila elpenor (based on opsin templates). (b) The spectral sensitivities of five spectral receptor classes of photoreceptors in the dragonfly Hemicordulia tau (based on intracellular recordings). (c) Six spectral classes of photoreceptors in the butterfly Papilio xuthus. Dashed line: receptor with broad sensitivity caused by expression of two opsins within one cell. (d) Photoreceptors in the primary and secondary retinae of the annelid worm Torrea candida. (e) The three spectral classes of photoreceptors found in the nocturnal spider Cupiennius salei (based on intracellular recordings). (f) The multiple spectral classes of photoreceptors found in midband ommatidial rows of the stomatopod apposition eye (based on MSP and intracellular recordings). Dashed line: a receptor with broad sensitivity outside the midband rows. (g) The firefly squid Watasenia scintillans. Solid lines: photoreceptors in the ventral part of the retina (the 550-nm receptor results from a 500-nm pigment filtered by a distal 470-nm pigment). Dashed line: a photoreceptor in the larger dorsal retina. (h) Three spectral classes of photoreceptors in the giant clam Tridacna maxima. Adapted with permission from Kelber A (2006) Invertebrate color vision. In: Warrant EJ and Nilsson D-E (eds.) Invertebrate Vision, pp. 83–126. Cambridge: Cambridge University Press. Vision: Invertebrates 521
  12. 12. Time (s) 360Њ 20mV 20mV 250 μm 0Њ 360Њ 0Њ 90Њ 0Њ 2 4 6 8 10 12 14 16 4 6 AM AM S OTOT −1 1 1 0 0 11 (a) (b) (d) (e) (c) (f) Retinula POL neuron Relativeresponse Leptograpsus (crustacea) Gryllus (orthoptera) Melolontha (coleoptera) Cataglyphis (hymenoptera) Apis (hymenoptera) Danaus (lepidoptera) Notonecta (hemiptera) 2–1 22 MM LL 8 10 12 14 Time (s) φ Figure 7 Polarization vision in arthropods. (a–c) Schematic cross-sections through rhabdoms in the ommatidia of arthropod compound eyes (not to scale). (a) Dorsal rim areas (DRAs) of various groups of insects. (b) Typical ommatidium in the retina of decapod crustaceans; the two mutually perpendicular microvillar arrangements alternate in regular intervals along the rhabdom. (c) Ventral POL area of the backswimmer. Color indicates the spectral type of receptors mediating polarization vision (pink, UV); receptors not contributing to polarization vision are given in white; rhabdoms in gray indicate that the spectral range of polarization vision is unknown. (d) Principle of polarization opponency. Left, two analyzer channels (represented by the two receptors 1 and 2) act antagonistically on a POL neuron. Right, e-vector response functions of photoreceptors and POL neuron. (e, f) POL1 neuron in the optic lobe of the cricket, Gryllus campestris. (e) Morphology reconstructed by neurobiotin staining. Input region (ipsilateral) receiving inputs from the POL area is 522 Vision: Invertebrates
  13. 13. The dome of the sky is an excellent example of such a source. Light from the sun (or the moon) is scattered by air molecules in the Earth’s atmosphere to produce a circularly symmetric pattern of linearly polarized light centered on the disk of the sun (or moon). Each point in the sky emits light polarized in only one direction, and the direction of polarization shifts systematically from one point in the sky to the next (which produces the pattern). The degree of polarization is greatest along a circular locus that is 90 from the sun or moon (and centered on it). If an invertebrate has the possibility to unravel the 180 directional ambiguity inherent in the circularly sym- metric pattern (which they do, by analyzing spectral gra- dients in the sky), then they can use the pattern as a gigantic compass cue for extracting directional informa- tion while navigating, either to simply keep a straight-line course (e.g., ball-rolling dung beetles) or to use as a component of an advanced path integration system used for homing (e.g., the well-studied desert ant Cataglyphis bicolor). Polarized skylight is even seen underwater, partic- ularly at shallower depths (down to about 200 m). The fact that water has a higher refractive index than air means that the entire 180 dome of the sky is compressed to a 97 cone of light underwater. This circular window of light – called ‘Snell’s window’ – allows the polarized skylight pattern to remain visible underwater, but turbid water and the presence of waves can degrade it significantly. Nevertheless, some species (e.g., grass shrimps and juve- nile trout) can apparently use the underwater skylight pattern to maintain a straight swimming course. Outside Snell’s window, the space light is strongly polarized in the horizontal direction because of scattering from suspended particles. Near the shore, the degree of horizontal polari- zation is greater toward the open water, and some inverte- brates (notably the branchiopod Daphnia) use this fact to orient away from the shore (and danger). Some inverte- brates also use the aquatic backdrop of horizontally polar- ized light to detect transparent prey. Many transparent planktonic organisms are highly birefringent, which means that they are opaque (and highly visible) when seen against a polarized background by a polarization- sensitive visual system (as found in squids). In terrestrial habitats, horizontally plane-polarized light is formed by reflection from horizontal surfaces, notably water surfaces and shiny waxy leaves. Many flying insects – such as the backswimmer Notonecta – search for new bodies of water by looking for bright areas of horizontally polarized light in the ventral visual field. In combination with appropri- ate color cues, some papilionid butterflies also detect suitable oviposition sites on the basis of horizontally polarized light reflected from the leaves of their host plants. Finally, some heliconid butterflies, squids, and mantis shrimps use polarized light signals reflected from their integuments in intraspecific communication. The reason why most invertebrates can see plane- polarized light is due to the structure of their rhabdoms, which are formed from tube-like membranous microvilli. These microvilli – which are all highly aligned – each constrain the orientation of their resident rhodopsin molecules, so that they are aligned along the microvillar axis. Since each rhodopsin molecule is a linear absorption dipole, and the dipole orientation is constrained by the microvillus (and is identical to that for every other rho- dopsin molecule), the rhabdom as a whole becomes highly polarization sensitive. To actively remove polarization sensitivity requires that the microvilli become disoriented (e.g., by the rhabdom being twisted along its length, as found in certain eye regions of many insects). In contrast, the photoreceptors of vertebrates have a structure unsuit- able to the detection of polarized light. The flat disk-like membranes of their photoreceptor outer segments allow rhodopsin molecules to diffuse in any random direction: the crystalline alignment of rhodopsin molecules neces- sary to detect polarized light is thus impossible. Just as with color vision, the analysis of plane-polarized light requires two ‘polarization classes’ of photoreceptor that view the same region of space, followed by a neural comparison of the signals generated in each (usually via a neural opponency mechanism) at a subsequent (higher) level of the visual system. Our understanding of this process is almost entirely due to decades of research in desert ants (Catalglyphis bicolor), crickets (Gryllus campes- tris), and locusts (Schistocerca gregaria), all of which have a specialized ‘dorsal rim area’ (or DRA), a narrow strip of ommatidia along the dorsal-most margin of the compound eye. The ommatidia of the DRA house the polarization- sensitive photoreceptors, all of which have a dorsal field of view. Outside the DRA, the rhabdoms are deliberately twisted to eliminate their polarization sensitivity. The two polarization classes of photoreceptor found in the DRA have microvilli oriented in only one of two possible per- pendicular directions (Figure 7(a)–7(c)). Within a rhabdom of (say) eight rhabdomeres, at least one rhabdomere has microvilli oriented in one direction, while all others have shown to the right. L, lamina; M, medulla; AM, accessory medulla; OT, optic tract; S, cell soma. (f) Intracellular recordings from the ipsilateral (right) and the contralateral part (left) of POL1 neurons while the e-vector orientation of a strongly polarized stimulus was rotated by 360 . In the ipsilateral recording, the baseline undulates as a result of EPSP summation. The contralateral recording starts in the dark, demonstrating spontaneous spiking activity; the white triangle marks the onset of the stimulus. In both recordings, the spike frequency modulates as a function of e-vector orientation. Ipsilateral and contralateral recordings are from two POL1 neurons with different e-vector tuning axes. Adapted with permission from Wehner R and Labhart T (2006) Polarisation vision. In: Warrant EJ and Nilsson D-E (eds.) Invertebrate Vision, pp. 83–126. Cambridge: Cambridge University Press. Vision: Invertebrates 523
  14. 14. microvilli oriented in the perpendicular direction (thus forming two orthogonal analysis components for any direc- tion of plane-polarized light). The signals generated in these two classes form two analyzer channels, each of which can act antagonistically (Figure 7(d)) on a polarization-sensitive interneuron (known as ‘a POL neuron’) that arises in the medulla (Figure 7(d)–7(f)). A well-studied POL neuron is POL1 (found in crickets), a cell that sends its outputs to both the central brain and to the contralateral medulla in the optic lobe of the other eye (Figure 7(e)). In crickets, three types of POL1 neurons have been found, each highly sensitive and each having a very large receptive field (60 across). The three types differ only in their preferred orientation of polarized light relative to the long axis of the head – 10 , 60 , and 130 – directions that roughly correspond to the combined directional prefer- ence of the pool of 200 DRA ommatidia that feed each receptive field of each of the three POL1 neurons (there are approximately 600 ommatidia in the cricket DRA). These three classes of POL1 neurons are believed to indirectly feed an array of ‘compass neurons’ (probably located in the central brain), each of which represents a certain body orientation relative to the symmetry plane of the celestial polarization pattern. The pattern of responses in the array of compass neurons, due to the inputs of the three-axis system of POL1 neurons (10 , 60 , and 130 ), is then thought to code body orientation exactly. Evidence for the existence of compass-like neurons is beginning to emerge in the central complex of the locust brain (see Figure 4(b) for the visual pathways of the brain involved in polarization vision). While much less common than linearly polarized light, circularly polarized light can be produced by reflection from certain natural surfaces, notably the cuticle of some arthropods. Many scarab beetles – particularly those that are brilliantly iridescent – have exactly the type of cuticle necessary. To become circularly polarized, the two per- pendicular components of the electric field wave of light must become 90 out of phase (i.e., by a quarter of a wavelength). Certain materials – such as the cuticle of some beetles – induce this phase shift upon reflection. Even though circularly polarized cuticular reflections have been known for some time, their visual and behavioral functions (if any) were unknown. Very recently, however, certain species of mantis shrimps (stomatopods) have been shown to not only reflect circularly polarized light, but also to visually detect it and to react to it behaviorally. The physiological basis for this ability lies within the rhabdoms of a specialized band of ommatidia in the com- pound eye: the eighth rhabdomere, which sits on top of the other seven, has a thickness and microvillar orientation that removes the 90 phase difference between the two perpen- dicular components of the electric field of the incoming circularly polarized light (i.e., it acts as a ‘quarter-wave retarder’), thereby converting it to linearly polarized light. This linearly polarized light is then detected and analyzed in the conventional manner by the seven underlying rhab- domeres, but in this case, as a code for the presence of circularly polarized light. Conclusions The invertebrates – constituting nearly all species of animal life on Earth – have conquered almost all known habitats. Not surprisingly, their sensory organs, and par- ticularly their eyes, have adapted to a remarkable range of sensory environments and sensory stimuli. Among the invertebrates are found all known optical designs of eyes, endowing these animals with visual abilities that in many cases rival, and occasionally even exceed, those of humans. Compared with our own visual impression, many species see much better in dim light, experience a faster and more colorful world, and are able to distinguish the subtleties of polarized light, a visual modality forever beyond our perceptual limits. See also: Crabs and Their Visual World; Insect Naviga- tion; Nervous System: Evolution in Relation to Behavior; Vision: Vertebrates; Visual Signals. Further Reading Chiou TH, Kleinlogel S, Cronin T, et al. (2008) Circular polarization vision in a stomatopod crustacean. Current Biology 18: 429–434. Krapp HG and Wiklein M (2008) Central processing of visual information in insects. In: Albright T and Masland RH (eds.) The Senses: A Comprehensive Reference, vol. 1, Basbaum AI, Kaneko A, Shepherd GM, and Westheimer G (series eds.) Vision I, pp. 131–203. Oxford: Academic Press. Land MF and Nilsson DE (2002) Animal Eyes. Oxford: Oxford University Press. Warrant EJ and Nilsson DE (2006) Invertebrate Vision. Cambridge: Cambridge University Press. 524 Vision: Invertebrates