eye

Overview

Complex eyes distinguish shapes and colours. The visual fields of many organisms, especially predators, involve large areas of binocular vision for depth perception. In other organisms, particularly prey animals, eyes are located to maximise the field of view, such as in rabbits and horses, which have monocular vision.

The first proto-eyes evolved among animals 600 million years ago about the time of the Cambrian explosion. The last common ancestor of animals possessed the biochemical toolkit necessary for vision, and more advanced eyes have evolved in 96% of animal species in six of the ~35 main phyla. In most vertebrates and some molluscs, the eye allows light to enter and project onto a light-sensitive layer of cells known as the retina. The cone cells (for colour) and the rod cells (for low-light contrasts) in the retina detect and convert light into neural signals which are transmitted to the brain via the optic nerve to produce vision. Such eyes are typically spheroid, filled with the transparent gel-like vitreous humour, possess a focusing lens, and often an iris. Muscles around the iris change the size of the pupil, regulating the amount of light that enters the eye and reducing aberrations when there is enough light. The eyes of most cephalopods, fish, amphibians and snakes have fixed lens shapes, and focusing is achieved by telescoping the lens in a similar manner to that of a camera.

The compound eyes of the arthropods are composed of many simple facets which, depending on anatomical detail, may give either a single pixelated image or multiple images per eye. Each sensor has its own lens and photosensitive cell(s). Some eyes have up to 28,000 such sensors arranged hexagonally, which can give a full 360° field of vision. Compound eyes are very sensitive to motion. Some arthropods, including many Strepsiptera, have compound eyes of only a few facets, each with a retina capable of creating an image. With each eye producing a different image, a fused, high-resolution image is produced in the brain.

The mantis shrimp has the world's most complex colour vision system. It has detailed hyperspectral colour vision.

Trilobites, now extinct, had unique compound eyes. Clear calcite crystals formed the lenses of their eyes. They differ in this from most other arthropods, which have soft eyes. The number of lenses in such an eye varied widely; some trilobites had only one while others had thousands of lenses per eye.

Types

There are ten different eye layouts. Eye types can be categorised into "simple eyes", with one concave photoreceptive surface, and "compound eyes", which comprise a number of individual lenses laid out on a convex surface. "Simple" does not imply a reduced level of complexity or acuity. Indeed, any eye type can be adapted for almost any behaviour or environment. The only limitations specific to eye types are that of resolution—the physics of compound eyes prevents them from achieving a resolution better than 1°. Also, superposition eyes can achieve greater sensitivity than apposition eyes, so are better suited to dark-dwelling creatures.

Eyes also fall into two groups on the basis of their photoreceptor's cellular construction, with the photoreceptor cells either being ciliated (as in the vertebrates) or rhabdomeric. These two groups are not monophyletic; the Cnidaria also possess ciliated cells, and some gastropods and annelids possess both.

Some organisms have photosensitive cells that do nothing but detect whether the surroundings are light or dark, which is sufficient for the entrainment of circadian rhythms. These are not considered eyes because they lack enough structure to be considered an organ, and do not produce an image.

Every technological method of capturing an optical image that humans commonly use occurs in nature, with the exception of zoom and Fresnel lenses.

Non-compound eyes

Simple eyes are rather ubiquitous, and lens-bearing eyes have evolved at least seven times in vertebrates, cephalopods, annelids, crustaceans and Cubozoa.

Pit eyes, also known as stemmata, are eye-spots which may be set into a pit to reduce the angles of light that enters and affects the eye-spot, to allow the organism to deduce the angle of incoming light. Found in about 85% of phyla, these basic forms were probably the precursors to more advanced types of "simple eyes". They are small, comprising up to about 100 cells covering about 100 μm. The directionality can be improved by reducing the size of the aperture, by incorporating a reflective layer behind the receptor cells, or by filling the pit with a refractile material.

Pit vipers have developed pits that function as eyes by sensing thermal infra-red radiation, in addition to their optical wavelength eyes like those of other vertebrates (see infrared sensing in snakes). However, pit organs are fitted with receptors rather different from photoreceptors, namely a specific transient receptor potential channel (TRP channels) called TRPV1. The main difference is that photoreceptors are G-protein coupled receptors but TRP are ion channels.

The resolution of pit eyes can be greatly improved by incorporating a material with a higher refractive index to form a lens, which may greatly reduce the blur radius encountered—hence increasing the resolution obtainable. The most basic form, seen in some gastropods and annelids, consists of a lens of one refractive index. A far sharper image can be obtained using materials with a high refractive index, decreasing to the edges; this decreases the focal length and thus allows a sharp image to form on the retina. This also allows a larger aperture for a given sharpness of image, allowing more light to enter the lens; and a flatter lens, reducing spherical aberration. Such a non-homogeneous lens is necessary for the focal length to drop from about 4 times the lens radius, to 2.5 radii.

So-called under-focused lens eyes, found in gastropods and polychaete worms, have eyes that are intermediate between lens-less cup eyes and real camera eyes. Also box jellyfish have eyes with a spherical lens, cornea and retina, but the vision is blurry.

Heterogeneous eyes have evolved at least nine times: four or more times in gastropods, once in the copepods, once in the annelids, once in the cephalopods, and once in the chitons, which have aragonite lenses. No extant aquatic organisms possess homogeneous lenses; presumably the evolutionary pressure for a heterogeneous lens is great enough for this stage to be quickly "outgrown".

Compound eyes

A compound eye may consist of thousands of individual photoreceptor units or ommatidia (ommatidium, singular). The image perceived is a combination of inputs from the numerous ommatidia (individual "eye units"), which are located on a convex surface, thus pointing in slightly different directions. Compared with simple eyes, compound eyes possess a very large view angle, and can detect fast movement and, in some cases, the polarisation of light. Because the individual lenses are so small, the effects of diffraction impose a limit on the possible resolution that can be obtained (assuming that they do not function as phased arrays). This can only be countered by increasing lens size and number. To see with a resolution comparable to our simple eyes, humans would require very large compound eyes, around 11 metres (36 ft) in radius.

Compound eyes fall into two groups: apposition eyes, which form multiple inverted images, and superposition eyes, which form a single erect image. Compound eyes are common in arthropods, annelids and some bivalved molluscs. Compound eyes in arthropods grow at their margins by the addition of new ommatidia.

Apposition eyes are the most common form of eyes and are presumably the ancestral form of compound eyes. They are found in all arthropod groups, although they may have evolved more than once within this phylum. Some annelids and bivalves also have apposition eyes. They are also possessed by Limulus, the horseshoe crab, and there are suggestions that other chelicerates developed their simple eyes by reduction from a compound starting point. (Some caterpillars appear to have evolved compound eyes from simple eyes in the opposite fashion.)

Apposition eyes work by gathering a number of images, one from each eye, and combining them in the brain, with each eye typically contributing a single point of information. The typical apposition eye has a lens focusing light from one direction on the rhabdom, while light from other directions is absorbed by the dark wall of the ommatidium.

The second type is named the superposition eye. The superposition eye is divided into three types:

refracting,

reflecting and

Evolution

Photoreception is phylogenetically very old, with various theories of phylogenesis. The common origin (monophyly) of all animal eyes is now widely accepted as fact. This is based upon the shared genetic features of all eyes; that is, all modern eyes, varied as they are, have their origins in a proto-eye believed to have evolved some 650-600 million years ago, and the PAX6 gene is considered a key factor in this. The majority of the advancements in early eyes are believed to have taken only a few million years to develop, since the first predator to gain true imaging would have touched off an "arms race" among all species that did not flee the photopic environment. Prey animals and competing predators alike would be at a distinct disadvantage without such capabilities and would be less likely to survive and reproduce. Hence multiple eye types and subtypes developed in parallel (except those of groups, such as the vertebrates, that were only forced into the photopic environment at a late stage).

Eyes in various animals show adaptation to their requirements. For example, the eye of a bird of prey has much greater visual acuity than a human eye, and in some cases can detect ultraviolet radiation. The different forms of eye in, for example, vertebrates and molluscs are examples of parallel evolution, despite their distant common ancestry. Phenotypic convergence of the geometry of cephalopod and most vertebrate eyes creates the impression that the vertebrate eye evolved from an imaging cephalopod eye, but this is not the case, as the reversed roles of their respective ciliary and rhabdomeric opsin classes and different lens crystallins show.

The very earliest "eyes", called eye-spots, were simple patches of photoreceptor protein in unicellular animals. In multicellular beings, multicellular eyespots evolved, physically similar to the receptor patches for taste and smell. These eyespots could only sense ambient brightness: they could distinguish light and dark, but not the direction of the light source.

Through gradual change, the eye-spots of species living in well-lit environments depressed into a shallow "cup" shape. The ability to slightly discriminate directional brightness was achieved by using the angle at which the light hit certain cells to identify the source. The pit deepened over time, the opening diminished in size, and the number of photoreceptor cells increased, forming an effective pinhole camera that was capable of dimly distinguishing shapes. However, the ancestors of modern hagfish, thought to be the protovertebrate, were evidently pushed to very deep, dark waters, where they were less vulnerable to sighted predators, and where it is advantageous to have a convex eye-spot, which gathers more light than a flat or concave one. This would have led to a somewhat different evolutionary trajectory for the vertebrate eye than for other animal eyes.

Relationship to life requirements

Eyes are generally adapted to the environment and life requirements of the organism which bears them. For instance, the distribution of photoreceptors tends to match the area in which the highest acuity is required, with horizon-scanning organisms, such as those that live on the African plains, having a horizontal line of high-density ganglia, while tree-dwelling creatures which require good all-round vision tend to have a symmetrical distribution of ganglia, with acuity decreasing outwards from the centre.

Of course, for most eye types, it is impossible to diverge from a spherical form, so only the density of optical receptors can be altered. In organisms with compound eyes, it is the number of ommatidia rather than ganglia that reflects the region of highest data acquisition. Optical superposition eyes are constrained to a spherical shape, but other forms of compound eyes may deform to a shape where more ommatidia are aligned to, say, the horizon, without altering the size or density of individual ommatidia. Eyes of horizon-scanning organisms have stalks so they can be easily aligned to the horizon when this is inclined, for example, if the animal is on a slope.

An extension of this concept is that the eyes of predators typically have a zone of very acute vision at their centre, to assist in the identification of prey. In deep water organisms, it may not be the centre of the eye that is enlarged. The hyperiid amphipods are deep water animals that feed on organisms above them. Their eyes are almost divided into two, with the upper region thought to be involved in detecting the silhouettes of potential prey—or predators—against the faint light of the sky above. Accordingly, deeper water hyperiids, where the light against which the silhouettes must be compared is dimmer, have larger "upper-eyes", and may lose the lower portion of their eyes altogether. In the giant Antarctic isopod Glyptonotus a small ventral compound eye is physically completely separated from the much larger dorsal compound eye. Depth perception can be enhanced by having eyes which are enlarged in one direction; distorting the eye slightly allows the distance to the object to be estimated with a high degree of accuracy.

Acuity is higher among male organisms that mate in mid-air, as they need to be able to spot and assess potential mates against a very large backdrop. On the other hand, the eyes of organisms which operate in low light levels, such as around dawn and dusk or in deep water, tend to be larger to increase the amount of light that can be captured.

Physiology

Visual acuity

Visual acuity, or resolving power, is "the ability to distinguish fine detail" and is the property of cone cells. It is often measured in cycles per degree (CPD), which measures an angular resolution, or how much an eye can differentiate one object from another in terms of visual angles. Resolution in CPD can be measured by bar charts of different numbers of white/black stripe cycles. For example, if each pattern is 1.75 cm wide and is placed at 1 m distance from the eye, it will subtend an angle of 1 degree, so the number of white/black bar pairs on the pattern will be a measure of the cycles per degree of that pattern. The highest such number that the eye can resolve as stripes, or distinguish from a grey block, is then the measurement of visual acuity of the eye.

For a human eye with excellent acuity, the maximum theoretical resolution is 50 CPD (1.2 arcminute per line pair, or a 0.35 mm line pair, at 1 m). A rat can resolve only about 1 to 2 CPD. A horse has higher acuity through most of the visual field of its eyes than a human has, but does not match the high acuity of the human eye's central fovea region.

Spherical aberration limits the resolution of a 7 mm pupil to about 3 arcminutes per line pair. At a pupil diameter of 3 mm, the spherical aberration is greatly reduced, resulting in an improved resolution of approximately 1.7 arcminutes per line pair. A resolution of 2 arcminutes per line pair, equivalent to a 1 arcminute gap in an optotype, corresponds to 20/20 (normal vision) in humans.

However, in the compound eye, the resolution is related to the size of individual ommatidia and the distance between neighbouring ommatidia. Physically these cannot be reduced in size to achieve the acuity seen with single lensed eyes as in mammals. Compound eyes have a much lower acuity than vertebrate eyes.

Colour perception

"Colour vision is the faculty of the organism to distinguish lights of different spectral qualities." All organisms are restricted to a small range of electromagnetic spectrum; this varies from creature to creature, but is mainly between wavelengths of 400 and 700 nm. This is a rather small section of the electromagnetic spectrum, probably reflecting the submarine evolution of the organ: water blocks out all but two small windows of the EM spectrum, and there has been no evolutionary pressure among land animals to broaden this range.

The most sensitive pigment, rhodopsin, has a peak response at 500 nm. Small changes to the genes coding for this protein can tweak the peak response by a few nm; pigments in the lens can also filter incoming light, changing the peak response. Many organisms are unable to discriminate between colours, seeing instead in shades of grey; colour vision necessitates a range of pigment cells which are primarily sensitive to smaller ranges of the spectrum. In primates, geckos, and other organisms, these take the form of cone cells, from which the more sensitive rod cells evolved. Even if organisms are physically capable of discriminating different colours, this does not necessarily mean that they can perceive the different colours; only with behavioural tests can this be deduced.

Most organisms with colour vision can detect ultraviolet light. This high energy light can be damaging to receptor cells. With a few exceptions (snakes, placental mammals), most organisms avoid these effects by having absorbent oil droplets around their cone cells. The alternative, developed by organisms that had lost these oil droplets in the course of evolution, is to make the lens impervious to UV light—this precludes the possibility of any UV light being detected, as it does not even reach the retina.

Rods and cones

The retina contains two major types of light-sensitive photoreceptor cells used for vision: the rods and the cones.

Rods cannot distinguish colours, but are responsible for low-light (scotopic) monochrome (black-and-white) vision; they work well in dim light as they contain a pigment, rhodopsin (visual purple), which is sensitive at low light intensity, but saturates at higher (photopic) intensities. Rods are distributed throughout the retina but there are none at the fovea and none at the blind spot. Rod density is greater in the peripheral retina than in the central retina.

Cones are responsible for colour vision. They require brighter light to function than rods require. In humans, there are three types of cones, maximally sensitive to long-wavelength, medium-wavelength, and short-wavelength light (often referred to as red, green, and blue, respectively, though the sensitivity peaks are not actually at these colours). The colour seen is the combined effect of stimuli to, and responses from, these three types of cone cells. Cones are mostly concentrated in and near the fovea. Only a few are present at the sides of the retina. Objects are seen most sharply in focus when their images fall on the fovea, as when one looks at an object directly. Cone cells and rods are connected through intermediate cells in the retina to nerve fibres of the optic nerve. When rods and cones are stimulated by light, they connect through adjoining cells within the retina to send an electrical signal to the optic nerve fibres. The optic nerves send off impulses through these fibres to the brain.

Pigmentation

The pigment molecules used in the eye are various, but can be used to define the evolutionary distance between different groups, and can also be an aid in determining which are closely related—although problems of convergence do exist.

Opsins are the pigments involved in photoreception. Other pigments, such as melanin, are used to shield the photoreceptor cells from light leaking in from the sides. The opsin protein group evolved long before the last common ancestor of animals, and has continued to diversify since.

There are two types of opsin involved in vision; c-opsins, which are associated with ciliary-type photoreceptor cells, and r-opsins, associated with rhabdomeric photoreceptor cells. The eyes of vertebrates usually contain ciliary cells with c-opsins, and (bilaterian) invertebrates have rhabdomeric cells in the eye with r-opsins. However, some ganglion cells of vertebrates express r-opsins, suggesting that their ancestors used this pigment in vision, and that remnants survive in the eyes. Likewise, c-opsins have been found to be expressed in the brain of some invertebrates. They may have been expressed in ciliary cells of larval eyes, which were subsequently resorbed into the brain on metamorphosis to the adult form. C-opsins are also found in some derived bilaterian-invertebrate eyes, such as the pallial eyes of the bivalve molluscs; however, the lateral eyes (which were presumably the ancestral type for this group, if eyes evolved once there) always use r-opsins. Cnidaria, which are an outgroup to the taxa mentioned above, express c-opsins—but r-opsins are yet to be found in this group. Incidentally, the melanin produced in the cnidaria is produced in the same fashion as that in vertebrates, suggesting the common descent of this pigment.

Human use

Animal eyes, particularly non-compound spherical eyes, are eaten by humans in multiple culinary cultures.