Benjamin Franklin is alleged to have written: ‘But in this world nothing can be said to be certain, except death and taxes’. And one is sorely tempted to add ‘the colour problem’. As black people have discovered during this and previous centuries, skin colour is the most decisive and the most abused of all the physical characteristics of humankind. It determines social perceptions, value judgments and interpersonal relationships, and it can wreak havoc on an individual's sense of dignity and selfesteem.

In this book I have endeavoured to analyse the essential nature and functions of human skin colour. I have done this predominantly from a biological standpoint, although I have included a chapter on the psychosocial dimensions of the subject and also one on the possible evolutionary forces which have determined skin colour variations among populations in different geographical regions. Disorders of pigmentation receive special attention, and I have given fairly detailed consideration to the pigmentation that occurs in sites other than the skin and hair.

The field of melanin pigmentation in all its guises is awash with journal articles, monographs and books. I have generally restricted references either to the original authors or to updated reviews, as it would have been unnecessarily cumbersome to cite the multiplicity of contributors to a particular topic. An exception is where the matter under discussion is controversial, or where I expose a personal viewpoint (as I do in assessing the vitamin D hypothesis of skin depigmentation). Here I have felt obliged to furnish fuller documentation for the arguments advanced.

The problem of race and racial labelling has been one of the most taxing for me.

The previous chapter discussed the variable influences of hormones on the epidermal melanin unit. The secretion of the pineal hormone, melatonin, is governed by the amount of light reaching the eye and this mechanism enables animals like the weasel and arctic fox to alter their coat colour according to the seasons. In humans light also plays a dominant role in pigmentation; not indirectly through hormones, but by the direct effect of solar ultraviolet radiation (UV) on the epidermal melanin unit. This effect induces the so-called tanning reaction, which can increase the pigmentation of sun-exposed areas markedly above the level of natural pigmentation. The contrast can be striking and, as Noel Coward observed, ‘Sunburn is very becoming – but only when it is even – one must be careful not to look like a mixed grill’!

In this century, and particularly in the Western world, the pursuit of a tan has become a passion, and there are people who will spend hours sunbathing (Fig. 3.1) or in sunbeds and suntan parlours. The achievement of a bronzed appearance is believed to signify health and beauty whereas, in fact, exposure to the sun (particularly in vulnerable, light-skinned Caucasoids) can have the very harmful effects which are discussed below.

Types of ultraviolet radiation (UV)

UV is part of the electromagnetic spectrum and it lies between the visible and X-ray regions (Fig. 3.2). Of the total radiant energy received by the earth from the sun, only 5–10 per cent is in the ultraviolet, the remainder being divided between the visible (about 40 per cent) and the infrared (about 50 per cent). Different wavebands in the UV spectrum show different capacities to cause biological injury.

This chapter deals with the occurrence of melanin in sites other than skin and hair, and it will explore the putative role of the pigment in these situations. With the exception of melanin in the eye all the other melaninbearing tissues are internal and are totally shielded from light. Hence arises the problem of what likely use melanin would have in locations where it is deprived of its primary functions of photoprotection, thermoregulation and ecological adaptation (e.g. camouflage). Indeed, unlike beauty, melanin is not skin deep!

Eye

Iris

This is the visible pigmented region of the eye, and in describing an individual's eye colour one is referring to the pigmentation of the iris. The iris consists of several layers but, from the standpoint of colour, the two most important portions are the anterior layer together with its underlying stroma (both containing melanocytes) and the posterior pigmented epithelium.

Eye colour depends partly on the amount of melanin pigment in the anterior layer and stroma and partly on optical phenomena. In brown and dark brown irises there is an abundance of melanocytes and melanosomes in the anterior layer and stroma. Blue eyes are not the effect of a blue pigment, but represent Tyndall scattering (see p. 72). In blue-eyed individuals the anterior layer and stroma contain very little (if any) melanin. As light traverses these relatively melanin-free layers, the minute protein particles of the iris scatter the short blue wavelengths to the surface. The blue colour is heightened because the longer wavelengths (yellow and red) are absorbed by the dark background of the posterior pigmented epithelium, which also obscures the reddish hue of the adjacent blood vessels.

W. E. B. DuBois once remarked that the problem of the twentieth century was the problem of the colour line; and even in the closing years of this century there is little doubt that the impact of skin colour continues to be profound, whether at the macro-level of global politics or the microlevel of a person-to-person transaction. Like three other exceedingly small entities – the atom, the ovum and the AIDS virus – the melanosome still has a place on the agenda of human catastrophe. It would therefore be a glaring omission in a book such as this to overlook the immense interaction between skin pigmentation and the psychosocial dimensions of human behaviour.

Legends, symbolism and culture

The colour of the skin, hair and eyes has intrigued people from time immemorial, as it has also engendered curiosity about the reasons for colour differences between human populations. In prescientific eras much of the thinking on the subject was based on mythology or primitive religious concepts. The well-known scriptural interpretation from Genesis blamed blackness on a curse delivered by Noah to his son Ham as a punishment for having gazed on him when he lay naked and drunk in his tent. The Ancient Greeks narrated that Phaeton, the son of Helios (god of the Sun), successfully coaxed his father to allow him to drive the fiery chariot of the Sun for one day. His maladroitness caused him to lose control of the reins so that the chariot came too close to the earth in one region (Ethiopia), burning the people there black, and was too far from the earth in other regions, turning the inhabitants there pale from cold.

Photoprotection

The two major defences of the skin against radiation injury are the presence of melanin pigment and the thickness of the stratum corneum. There was a time when the role of melanin in photoprotection was subordinated to that of the stratum corneum but, in the recent past, the burden of evidence has declared melanin to be the natural sunscreen par excellence. The arguments in favour of the superior photoprotective properties of melanin have been convincingly set out by Pathak & Fitzpatrick (1974) and they are based on clinical, epidemiological and experimental findings.

Skin cancer

The most obvious clue to the photoprotective role of melanin resides in the prevalence of skin cancer, which is by far the commonest of the cancers. As already noted, it is associated with intense and long-term exposure to UV-B and it therefore occurs more frequently on the chronically exposed body areas, such as the head and neck (see Fig. 9.4). There is a relative infrequency of skin cancer in Negroids and other pigmented peoples (Amerindians, Asians), even at the equator where UV is strongest. Susceptibility to skin cancer (including malignant melanoma) is enhanced in fair-skinned, light-haired Caucasoids who sunburn easily and tan poorly.

Persons of Celtic background appear to be significantly over-represented in the skin cancer statistics (Urbach, 1969). The Republic of Ireland has the third-highest death rate from skin cancer (next to Australia and South Africa), even though it is located between 52° N and 54° N and receives a relatively low annual influx of UV-B. It may be that the individual with Celtic skin and red hair has a genetic inability to resist the deleterious effects of UV.

Measurement techniques

The scientific study of human skin colour requires accurate measuring instruments. Before the latter became available verbal descriptions of skin colour had to suffice. It is true that terms such as ‘black’, ‘brown’ and ‘white’ (or ‘blond’ and ‘brunet’) are universally understood and each can be further qualified as light, medium or dark, but verbal descriptions such as these are only really applicable to broad categories and they are not discriminating enough to identify gradations of skin colour within and between populations. In the same way, a verbal description of a green paint would be totally inadequate for the selection of an accurate colour match. Furthermore, verbal reporting relies on subjectivity and this often introduces bias and distortion. Any form of measurement which seeks scientific acceptability must use standardized methods that are not only reliable and objective but easily reproducible.

In order to meet these needs various colour-matching techniques have been devised (e.g. Gates's tinted papers). The most widely used of these has been von Luschan's skin colour tablets. These consist of a set of small ceramic tiles consecutively numbered from 1 to 36 and ranging from pure white to black. There have also been colour atlases (e.g. the Munsell system and the Medical Colour Standard for Skin) which have provided sets of standard colour chips for skin matching. However, these methods have the disadvantages not only of subjectivity but that the surface texture of the chip or tile may not resemble that of the skin (or may have deteriorated with time) so that matching becomes imperfect.

Another colour-matching method was the Bradley colour top.

Architecture of the skin

An understanding of the biology of skin pigmentation requires some knowledge of the structure of the skin. There is a tendency to regard skin merely as the integument for the otherwise intricate and intriguing machinery of the human body. Yet, in terms of its multiplicity of cellular and fibrous constituents, the skin is not only the largest and most versatile organ of the body but also, with the possible exception of the brain, the most complex.

Dermis

The skin (Fig. l.l(a)) has two major components, the dermis and the epidermis. The dermis is basically a connective tissue layer comprising collagen, elastic and reticular fibres. It is traversed by a rich network of blood and lymphatic vessels. It also contains structures originally derived from the epidermis – the sweat and sebaceous glands, the hair follicles, and the hairs themselves. Attached to the hair follicles are minute bundles of smooth muscle (arrector pili), the contraction of which during cold or fear produces the phenomenon of ‘goose-flesh’. The dermis is supplied with sensory nerve endings (mediating the sensations of touch, heat, cold and pain) and with sympathetic nerves which regulate the activity of the sweat gland, arteriole and arrector pili.

Epidermis

The epidermis is a thin layer (about 0.10–0.15 millimetres in thickness) devoid of either blood or nerve supplies. It is composed of two distinct cell populations – epithelial cells or keratinocytes (also known as Malpighian cells) and pigment cells or melanocytes.

The circulation of melanin

The melanosomes in epidermal melanocytes are transferred to keratino cytes, thereafter conveyed upwards to the stratum corneum, and eventually disposed of by desquamation. There is also a less well-known transaction that proceeds in the opposite direction: a circulation of melanin from the skin to the internal organs of the body.

The knowledge that melanin is manufactured in the skin by in situ pigment cells dates from relatively recent times. The early nineteenthcentury notion was that black pigment originated in the bile, and ingenious theories were devised of how bile turned itself into the colouring material of the skin. In an informative review of the literature, Wassermann (1965a) showed that the circulation of pigment was actually the first aspect to be described. A hundred years ago it was thought that wandering cells, probably leucocytes (white blood corpuscles), scavenged red blood cells and carried them and their pigment (haemoglobin) to the epidermis for its nutrition, the haemoglobin then being transformed into melanin. Even though these ideas may now seem preposterous, the concept of a circulation of melanin has recently been revived and revised.

The dermis contains an extensive network of lymphatic ducts which drain into lymph nodes. There is a much higher incidence of melanin deposition in the skin-draining lymph nodes of Negroids than of Caucasoids (Wassermann, 1965a). This suggests that melanin is transported by lymphatic drainage into the circulation from which it can then be distributed throughout the body.

The modern approach to the circulation of melanin stems chiefly from the work of Wassermann (1974). He used the skin-window technique to show the inflammatory response in the skin of South African Negroid and ‘Cape Coloured’ subjects.

Character of melanin

Melanins are among the most widespread natural pigments, being present in all living organisms including plants, fungi and bacteria. Plant melanins have a different biochemical derivation from animal melanins. The latter originate from the amino acid tyrosine, and they are characterized by a brown-black colour, a high molecular weight and a polymeric structure. One of the most problematic features of melanin to the scientist is its insolubility in almost all solvents. Because it is stubbornly resistant to chemical treatment melanin is difficult to purify and analyse. Both Littre and Albinus, in the eighteenth century, were amazed at their failure to extract pigment from black skin after subjecting it to prolonged immersion in water and alcohol. Even after two and a half centuries of technology there are still no general methods to solubilize natural melanin under physiological conditions. Hence the Harvard biologist Carroll Williams was moved to describe melanin as ‘a pigment of the imagination’!

The intractability of melanin, on the other hand, may prove of value to palaeontologists (Daniels, Post & Johnson, 1972). Melanin has been found in a 150-million-year-old ichthyosaur, in extinct mammoth skin and in mummy skin. The cephalopod molluscs possess an ‘ink gland’, the secretion of which (i.e. melanin) was used by the ancients as a dye (sepia). The squid stores its melanin in a reservoir and, in time of danger, squirts the pigment from a siphon so as to create a smokescreen to divert its enemy. Cephalopod melanin is invulnerable to decay and early in the nineteenth century, in the south of England, a 150-million-year-old squid was discovered whose own ink was used to make drawings of its remains (Fox & Vevers, 1960).

Introduction

One of the most remarkable achievements of the human visual system is the capacity to resolve fine detail in the retinal image and efficiently to detect contrast between neighbouring regions of the image. In the central visual field these perceptual abilities appear to be limited by the physical properties of the photoreceptors themselves. The development of spatial vision provides a fine example of the way in which the efficiency of coding in the visual system emerges through an interplay between innate (presumably genetically determined) organization and plasticity of synaptic organization at the level of the visual cortex. As Barlow (1972) pointed out, developmental plasticity might allow the visual cortex to discover, in the pattern of stimulation it receives, important associations and coincidences in the retinal image that relate to the nature of the visual world.

Efficiency of spatial vision in the adult

Factors that might limit spatial vision

The resolution of spatial detail and the detection of contrast in the retinal image might, in principle, be limited by one of a number of factors. Obviously, the optical quality of the image could determine spatial performance and certainly does so in states of refractive error. Even when the eye is accurately focused, chromatic and spherical aberration degrade the image, as does the effect of diffraction, which is dependent on the size of the pupil. Interestingly, under photopic conditions, the pupil of the human eye tends to adopt a diameter that optimizes visual acuity: a larger pupil size would augment the effects of aberrations and a smaller one would increase diffraction, as well as decreasing retinal illumination (Campbell & Gregory, 1960).

Photoreceptors perform the first step in the analysis of a visual image, namely the conversion of light into an electrical signal. The cellular mechanism of this process of energy transformation or transduction has become much clearer in recent years as a result of advances in the study of the biochemistry and physiology of single photoreceptors, and it is on this aspect that this brief review mainly focuses. It should not be forgotten, though, that photoreceptors perform a more complex task than mere energy conversion and amplification. Photoreceptors adapt by altering the gain of transduction to accord with the prevailing level of illumination, and they thereby widen the range of light intensities over which they can respond. The first stage of temporal analysis occurs in the photoreceptors: time-dependent conductance mechanisms in the inner segment membrane ensure that the voltage signal which drives the transfer of information to second-order cells reaches a peak earlier than the current change across the outer membrane. Finally, the synaptic transfer itself seems to be highly nonlinear, so that even a small hyperpolarization caused by steady illumination greatly reduces the gain of signal transfer. All of these features must be considered by those studying higher levels of information processing in the visual system, and it should be borne in mind that the photoreceptors do not present a faithful spatial and temporal map of the external world to second-order neurons in the visual pathway any more than the visual system as a whole presents an unprocessed image to an imaginary homunculus sitting at the seat of consciousness deep within the brain.

Introduction

Over the last few years we have developed machine algorithms for detection and discrimination of liver disease from diagnostic ultrasound scans of the liver (Wagner, Insana & Brown, 1986; Insana et al., 1986a; Insana et al, 1986b; Wagner, Insana & Brown, 1987). Several diffuse disease conditions are manifested through very subtle changes in the texture of the image. In these cases the machine algorithms significantly outperform expert clinical readers of the images (Garra et al., 1989). The discrimination of textures by the machine depends principally on an analysis and partitioning of second-order statistical features such as the autocorrelation and power spectral estimators. This finding has prompted us to investigate whether the human visual system might be more limited in its performance of such second-order tasks than it is for the wide range of first-order tasks where it scores so well.

At the beginning of this decade we learned how to use the words ‘well or good’ and ‘poorly or bad’ in the context of visual performance. We enjoyed a very fruitful collaboration with Horace Barlow through Arthur Burgess who split his sabbatical at that time between Horace Barlow's lab and ours (Burgess, Wagner, Jennings & Barlow, 1981; Burgess, Jennings & Wagner, 1982). From this collaboration we learned how instructive it is to compare the performance of the human visual system with that of the ideal observer from statistical decision theory. The latter introduces no fluctuations or sources of error beyond those inherent to the data that conveys the scene or image.

Many striking visual illusions are caused by disturbances to the equilibrium of the visual system resulting from relatively short periods of intense activation; after-images fall into this category, as do motion and tilt after-effects. I am going to suggest a goal, or computational theory, for the equilibration mechanisms that are revealed by some of these illusions: I think they take account of the correlational structure of sensory messages, thereby making the system specially sensitive to new associations. The suspicious coincidences thus discovered are likely to signal new causal factors in the environment, so adaptation mechanisms of the kind suggested could provide the major advantageous feature of the sensory representations formed in the cortex.

Visual adaptation

The visual system changes its characteristics when the image it is handling alters. The simplest and best understood example is the change in sensitivity that occurs when the mean luminance increases or decreases, and it is now well recognised that this parallels the electronic engineer's automatic gain control. The idea was formulated by Craik (1938) and recordings from photoreceptors and bipolars in the retina show the system in operation (e.g. Werblin, 1973), though the exact parts played by the different elements are not yet clear. What is obvious, however, is that the retinal ganglion cells could not possibly be so sensitive to small increments and decrements of light if they had to signal the whole range of luminances the eye is exposed to without changing their response characteristics.

Introduction

Perhaps the most fascinating and yet provocative aspect of vision is the manner in which eyes adapt to their environment. There is no single optimum eye design as physicists might like, but rather a variety of different solutions each dictated by the animals lifestyle, e.g. the ‘Four-eyed fish’, Anableps anableps, with one pair of aerial pupils and a second pair of aquatic pupils (Walls, 1942). This unique fish, which patrols the water surface, dramatizes the extreme plasticity of optics in adapting to a particular subset of the environment. The animal's life style within an environment obviously shapes many properties of the retina such as the distribution and types of rods, cones and ganglion cells (Walls, 1942; Hughes, 1977; Lythgoe, 1979). Furthermore, it is probable that the grand strategy of early visual information processing is also an adaptation to the particular world in which we live, i.e. a world of objects rather than the infinitely unexpected. We develop this perspective after considering the optical design of eyes.

Our first objective here is to show that elementary ideas of physics and information sciences can give insight into eye design. In doing so we stress the comparative approach. Only by studying diverse eyes, of both the simple and compound variety can we appreciate the common design principles necessary to apply meaningfully concepts from physics to biology. Accordingly, we try to explain observations such as: (a) the optical image quality is often superior to the photoreceptor grain; (b) the resolving power of falconiforms and dragonflies is proportional to their head size; (c) the cone outer segment diameter of diverse hawks that differ enormously in head size is fixed at about 2μm;

We have recently been doing some experiments inspired by Horace Barlow's ideas about adaptation and spatial integration. But instead of looking for support for Horace's point of view, we have been hoping to displace one of his ideas by one of our own. This revisionist attitude can be justified by an argument from information theory. Barlow is almost always right, so further demonstrations of his correctness are largely redundant; to catch him out is more difficult but also in a quite objective and technical sense more informative.

It is obvious that at high levels we see textures and details that we miss when the illumination is dim: more light means better sight. This improvement could be due to any of a number of factors, but here we wish to examine one suggestion in particular: that the improvement in vision occurs because light adaptation changes the spatial organization of the retina. That some such change occurs is well documented physiologically. Neurons in the vertebrate visual system typically receive antagonistic influences from the centre and surrounding regions of their receptive fields (Barlow, 1953). Barlow, Fitzhugh & Kuffler (1957) found in cat retinal ganglion cells that light adaptation increases the prominence of the antagonistic surround relative to the centre, thereby reducing the effective size of the central summing area (or, roughly speaking, of the spatial integration region) of each cell. As Barlow (1972) has noted, the effect is rather like reducing the grain size in a photographic film. Like the photographic analog, it could provide an efficient way of regulating sensitivity, because the system would gain a useful improvement in resolution by sacrificing sensitivity that is no longer needed or even desirable.