[Paleopsych] SW: On the Optical Structure of Animal Eyes

Premise Checker checker at panix.com
Wed Aug 3 22:58:55 UTC 2005

Evolution: On the Optical Structure of Animal Eyes

     The following points are made by Michael F. Land (Current Biology 2005
     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
     Related Material:
     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.
     Related Material:
     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) 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,
     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

More information about the paleopsych mailing list