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ScienceWeek
EVOLUTION: ON THE OPTICAL STRUCTURE OF ANIMAL EYES
The following points are made by Michael F. Land (Current Biology 2005 15:R319):
1) The ability to respond to light is common to many forms of life, but eyes themselves -- structures that break up environmental light according to its direction of origin -- are only found in animals. At its simplest, an eye might consist of a small number of light-responsive receptors in a pigmented pit, which shadows some receptors from light in one direction, and others from a different direction. This definition distinguishes an eye from an organ with a single photoreceptor cell, which may indeed be directional because of screening pigment, but which does not allow for spatial vision -- the simultaneous comparison of light intensities in different directions [1]. An alternative starting point for an eye would be for each receptor to have its own pigmented tube, the assemblage forming a convex cushion. In these two proto-eye structures we have the beginnings of the two mutually exclusive ways of building an eye: the single-chambered range of eyes, often misleadingly called "simple", and the compound eyes.
2) Although no eyes survive in fossils from the Precambrian (more than 550 million years ago) it seems certain that eyes like these were present from early in the evolution of the Bilateria [2], long before the Cambrian explosion. Simple pit eyes are still present in flatworms, annelid worms, and molluscs, and in many larval eyes. Proto-compound eyes occur in ark clams and some tube-dwelling polychaetes, where they act as detectors of moving predators. Genetic, developmental, and morphological evidence indicates that from the earliest times eyes had access to two different photoreceptor types: ciliary receptors, in which the photosensitive pigment is displayed on outgrowths of cilia, and rhabdomeric receptors, in which the expanded pigment-containing membrane consists of microvilli. The two receptor types use different transducer cascades, and their opsins -- the protein component of the photopigments -- are also different. Ciliary receptors are typical of deuterostomes (echinoderms and chordates) and rhabdomeric receptors of the protostomes (annelids, molluscs and arthropods), but both types can be found in both lineages. The development of cerebral eyes in both of these lineages has been associated with the Pax-6 control gene, evidently from early in bilaterian evolution.
3) In the Cambrian period, carnivory became important as a way of life and both predators and prey needed better vision. During the hundred million years from about 550 millions years ago, compound and then single-chambered eyes increased greatly in size, in their ability to resolve, and in optical sophistication. One way to improve the performance of a single-chambered proto-eye is to make the eye bigger and the aperture smaller, so that it becomes a genuine pinhole eye. This is a far from ideal solution, because the small aperture lets in little light, and so makes for a very insensitive eye, and increasing the aperture diameter drastically reduces the ability of the eye to resolve. For reasons that remain obscure, this design has been retained in the quite large (1 cm) eyes of the cephalopod Nautilus, even though its relatives (octopus and squid) have eyes with excellent lenses. Giant clams also have small pinhole eyes around their mantles, which do allow them to detect the presence of browsing fish.
4) A much better solution is to provide the eye with a lens, usually spherical in marine animals as a sphere provides the shortest focal length for a structure of a given diameter, and hence the most compact design. Such a structure might be made of protein, or some other substance with a refractive index higher than that of water. Refraction at each surface would bend rays and produce an image behind the lens. There is, however, a serious problem with a lens of this kind. Rays striking the outer regions of the lens are bent too much, so that they are focussed much closer to the lens than rays nearer to the lens center. This defect is known as spherical aberration, and in a spherical lens this is so severe that the image would be effectively unusable. The solution (attributed to James Clerk Maxwell) is for the lens to have a gradient of refractive index, highest in the center and falling to close to that of water in the periphery [3]. Peripheral rays are then bent much less, and overall the focal length of the eye becomes much shorter -- about 2.5 lens radii as opposed to 4 radii for a homogeneous lens. This makes for a lens that resolves well, and has a very high light-gathering power --an F-number of 1.25.[4,5]
References (abridged):
1. Land, M.F. and Nilsson, D.-E. (2002). Animal Eyes. Oxford University Press
2. Arendt, D. and Wittbrodt, J. (2001). Reconstructing the eyes of Urbilateria. Philos. Trans. R. Soc. Lond. B Biol. Sci. 356, 1545-1563
3. Jagger, W.S. (1992). The optics of the spherical fish lens. Vision Res. 32, 1271-1284
4. Land, M.F. (1984). Crustacea. In: Ali, M.A. (Ed.), Photoreception and Vision in Invertebrates.. (1984). Plenum, New York
5. Kröger, R.H.H., Campbell, M.C.W., Fernald, R.D., and Wagner, H.-J. (1999). Multifocal lenses compensate for chromatic defocus in vertebrate eyes. J. Comp. Physiol. [A] 184, 361-369
Current Biology http://www.current-biology.com
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ON THE EVOLUTION OF THE EYE
The following points are made by E.J.W. Barrington (citation below):
1) Two main types of highly differentiated photoreceptor system have appeared in the invertebrates: the compound eyes of arthropods and the camera-type eyes of cephalopods. Enough is known of the mode of functioning of these, and of their probable past history, to show that they represent the evolution, along two very different lines, of organs that have some striking points of similarity with the vertebrate eye, not only in their pigments but also in certain details of their structural organization. Indeed, this is an aspect of animal organization which is of considerable significance -- a convergence resulting from the widespread distribution of a common biochemical ground plan. In this instance the common feature is, of course, the nature of the photosensitive pigments.
2) Simple types of eyes are seen in the free-living Platyhelminthes and in the Annelida, where they are often composed of sensory cells associated with screening pigment cells. In their simplest form they may be no more than pigment spots, forming part of the general epithelium, but more usually they sink inwards to form cups. In the Turbellaria the pigment cells are often arranged to form the wall of an open bowl, the bipolar receptor cells projecting into this through its aperture. In such an eye there can be no possibility of forming an image, for there is no refractive structure. These organs are doubtless restricted to the differentiation of light and darkness, and in this way they make it possible for the animal to orientate itself with respect both to the intensity and to the source of the illumination. The distal ends of the receptor cells are differentiated to form a rod border, in which longitudinal striations can be seen with the light microscope...
3) Cup-like arrangements of pigment cells are common in the eyes of polychaetes, but a higher level of differentiation is reached in this group. Not only do the receptor cells themselves have a rod like tip, but the epithelium of the cup may produce secretions that fuse to form one or more lenses. Moreover, groups of sensory cells may be closely collected together to form ommatidia, recalling the unit structures of the compound eye of arthropods. Indeed, in sabellids (Branchiomma, for example) the ommatidia themselves may be grouped together to form a rudimentary type of compound eye. No doubt a similar tendency played an important part in the ancestors of arthropods, contributing to the establishment of their characteristic compound eyes. Convergence was probably involved in the process of arthropodization, so much so that it is necessary to envisage the possibility of an independent evolution of compound eyes in more than one line. The situation in annelids goes some way to make the possibility of the independent evolution of compound eyes acceptable, although it does not reveal the actual ancestry of these organs.
Adapted from: E.J.W. Barrington: Invertebrate Structure and Function. Nelson 1967, p.282.
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ON THE MAMMALIAN CLOCK-EYE
T. Roenneberg and M. Merrow (University of Munich, DE) discuss mammalian clocks, the authors making the following points:
1) Even without time cues from the environment, physiological events, from gene expression to behavior, recur with a high regularity but not necessarily in a precise 24 hour rhythm --hence the term "circadian" ("about one day"). Circadian rhythms are controlled by endogenous "clocks" which are synchronized, or "entrained", to the 24-hour day predominantly by light [1]. The central circadian pacemaker in mammals resides above the optic chiasm in the suprachiasmatic nuclei (SCN). It has long been known that light entrainment in mammals requires the eyes, but it was unclear through which photoreceptor the signal was processed. It came as a surprise that the circadian clock remains perfectly entrainable by light in mutant mice devoid of rods and cones [2].
2) Researchers are racing to identify the novel receptor in the mammalian retina. Its spectral characteristics have been defined in mice and, more recently, in humans [3,4]. In addition to its role in entrainment, the novel photoreceptor is responsible for several other non-visual light responses, such as melatonin suppression, pupillary constriction and direct effects of light on motor-activity ("masking"), or for many other "vegetative" light effects, for example on cortisol levels or heart rate. Hankins and Lucas (5) have taken our understanding of this novel light input pathway a step further, showing that its influence is already apparent in the primary steps of intra-retinal signal processing.
3) The authors discuss vision vs. irradiation detection. Vision capitalizes on photons, using rods or cones as "pixels" to create a retinal image that is processed in the thalamus and the cortex. While a memory of these "pictures" may be stored in the brain, the retinal picture itself has to be renewable within milliseconds for instant detection of any changes. Visual processing thus requires both fast kinetics and high spatial resolution. In contrast, a detector for the assessment of day and night should not care about a flash of lightning or the shadow of a flying object. Its task is to integrate photons over a long time. This integration mechanism is partially responsible for the difficulties that shift workers have in adjusting their biological clocks to socially enforced schedules -- the competition between indoor and outdoor light cannot be won. A worker who is exposed to 500 lux over an eight-hour night shift collects a similar quantity of photons waiting 15 minutes for the bus, even on a cloudy day. As a result, the circadian system remains entrained to the "real" day -- it cannot adjust to the implemented night shift, so workers try to be active and alert when their physiology is tuned to sleep. In fact, workers on night shifts, with most of the rest of the day free to spend outdoors, may collect more day light than their non-shifting colleagues. The invention of artificial light has ironically created a biological shadow world because we spend more time indoors.
4) In summary: Light is the most reliable environmental signal for adjusting biological clocks to the 24-hour day. Mammals receive this signal exclusively through the eyes, but not just via rods and cones. New evidence has been uncovered for a novel photoreceptor that may be responsible for more than just adjusting the clock.
References (abridged):
1. Roenneberg T. and Foster R.G. (1997) Twilight Times-light and the circadian system. Photochem. Photobiol., 66:549-561
2. Freedman M.S., Lucas R.J., Soni B., von Schantz M., Munoz M., David-Gray Z.K. and Foster R. (1999) Non-rod, non-cone ocular photoreceptors regulate the mammalian circadian behavior. Science, 284:502-504
3. Brainard G.C., Hanifin J.P., Greeson J.M., Byrne B., Glickman G., Gerner E. and Rolag M.D. (2001) Action spectrum for melatonin regulation in humans: evidence for a novel circadian photoreceptor. J. Neurosci., 21:6405-6412
4. Thapan K., Arendt J. and Skene D.J. (2001) An action spectrum for melatonin suppression: evidence for a novel non-rod, non-cone photoreceptor system in humans. J. Physiol., 535:261-267
5. Hankins, M.W. and Lucas, R.J. (2002). A novel photopigment in the human retina regulates the activity of primary visual pathways according to long-term light exposure. (in press)
Current Biology 2002 12:R163
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