Retinal Pigmentation, Visual Acuity and Brightness Levels J M I C H A E L HOFFMAN D e p a r t m e n t of A n t h r o p o l o g y , Uniuerazty of Culifornm, Berkeley, Calzforniu 94720
K E Y WORDS Brightness.
Eye . Melanin . Retina
. Vision
. Visual acuity
ABSTRACT This study investigates the hypothesis that the degree of retinal pigmentation i n the human eye is adaptive as it relates to the maintenance of visual acuity i n optically stressful environments, deserts and snowfields. Eightyfour subjects were examined, an estimation of their degree of retinal pigmentation made by ophthalmoscopic examination, and their binocular visual acuity tested over ten levels of brightness. The general level of retinal pigmentation did not influence mean visual acuity within the levels of brightness used in this study. The hypothesis was, therefore, rejected, but with the proviso that this study should be extended to even higher levels of brightness than were obtained here. There was no difference in mean pupil size at various levels of illumination between individuals grouped by degree of retinal pigmentation.
Primates are visual animals and, in this respect, man is no exception. In his work on the vertebrate visual system, Polyak ('57) lists that combination of characteristics specific to primate and human vision and then discusses the role of visual acuity in the phylogeny of primate vision. He sees primate vision as unique in its combination of diurnalism associated with a high visual acuity, well-differentiated sense of color and strictly binocular stereopsis, all coupled with richly developed mental attributes. As diurnal animals, most primates are faced with a great range of environments in terms of their overall illumination or brightness, from heavily canopied tropical forests which effectively screen nearly all direct sunlight, through various degrees of open woodland, to the extreme of highly illuminated deserts or near-deserts and snowfields. The ability of a primate to maintain its visual acuity when faced with such a range of potentially optically stressful environments, as well as with the variation in sunlight occurring between dawn and nightfall, is a problem to be mastered because optimal visual acuity will be maintained within a certain threshold and maximum intensity of illumination. On either side of this range of light intensities visual acuity drops dramatically. What mechaA M . J. P K Y S . ANTHROP.,4 3 ; 417-424.
nisms, then, are available to the primate faced with this problem? Obviously, adjustment of pupil size serves as an efficient regulatory mechanism over a wide range of light intensities, but is this the only method available for regulating the amount of light which eventually strikes the photoreceptors deep in the retina? An established biological phenomenon in some lower vertebrates and invertebrates is the migration of melanin from the basal aspect of the retinal pigment epithelium into processes surrounding the outer segments of the photoreceptors as the amount of light entering the eye increases. This phenomenon is assumed to increase visual acuity in these animals by reducing the scattering of light rays in the interior of the eye before the light reaches the photoreceptor cells' outer segments (Polyak, '57; Wolff, '68). Numerous authors state, although not without controversy, that this phenomenon either does not occur or has not been observed in higher vertebrates, especially the primates and man, arguing that this function has been superceded and replaced by a highly reactive and contractile pupil which serves to reduce the amount of incoming light as intensity increases (Walls, '67). However, the retina in all higher vertebrates, man not ex417
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cluded, still contains melanin in a discrete layer abutting the outer segments of the photoreceptor cells. The amount of melanin varies greatly therein when viewed ophthalmoscopically and microscopically. Why does the retinal pigment epithelium continue to possess melanin when no obvious function for i t remains and why does such variation remain in the amount of melanin in human retinae? Although numerous studies of the retinal pigment epithelium have been conducted, nowhere has anyone systematically examined the questions posed. Some biological studies do mention variability in the amount of melanin in the retinal pigment epithelium, but only to alert the physician to this normal variation, thereby begging the question why. Coon, Garn and Birdsell, collectively and individually, have addressed themselves to these questions but have not made the necessary tests of their hypotheses. As physical anthropologists they confront the question of variation in human retinal pigmentation, left begging by the biologists, and hypothesize that the amount of melanin in the retina is adaptive in maintaining visual acuity in optically stressful environments. Their basic argument is that an increase in the amount of melanin in the retina helps shield the photoreceptors’ outer segments thereby maintaining visual acuity in brightly lit environments, i.e., those with a great deal of sunlight and glare, by reducing the scattering of light within the eye and reducing the absolute amount of light which impinges on the photoreceptors. In their jointly-authored work Races (‘50), they implied by a diagram that pigment migration occurs in humans as in some invertebrates and lower vertebrates. However, Coon (’65) and Birdsell (‘71) do not mention this process in their individual works, nor do modern workers in vision research feel that i t is operative in man. Their basic argument, though, remains the same even in light of a change in mechanism, now implied to be the constant anatomical juxtaposition of the retinal pigment epithelial cells’ pigment processes to the photoreceptor cells’ outer segments. The variable has now changed from migration of melanin to variation in absolute amount to effect the proper screening in bright environments.
Does this hypothesis, though, really explain the variation? In the presence of a highly reactive, contractile pupil is there a need for melanin in the role of a lightscreener for the outer segments? There might not be except for the fact that the pupil has an absolute minimum size below which i t can contract no further. Once this limit is reached the melaninscreening mechanism may be of inestimable value in maintaining visual acuity. Also, in those extreme optically stressful environments such as deserts or snowfields, the combination of the mechanisms, pupil contractibility and melanin-screening, might be more beneficial and economical to the individual than just pupillary contraction alone. With some assistance from melanin-screening the pupil might be able to extend its range of contractibility into more extreme environments, thereby combatting pupillary fatigue. But here, too, we don’t know what the range of variation in pupil size is for various persons at the same level of illumination, persons who vary in the amount of melanin their retinae contain. This report presents the results of an investigation of the hypothesis that the amount of melanin in the retinal pigment epithelium of the human eye is adaptive as this relates to the maintenance of visual acuity in optically stressful environments, i.e., environments in which there are high or low intensities of sunlight striking the surroundings of the individual, as in snowfields and deserts or as in heavy forests and dimly lit, overcast skies. BACKGROUND
Retinal pigment epithelium (RPE). Good, detailed reviews of the histology and melanogenesis of the retinal pigment epithelial cell are readily available. This material has been summarized elsewhere (Hoffman, ’73). Moyer’s recent review article (‘69) on the RPE summarizes the present knowledge of the structure and function of this unique tissue. He concludes by stating the RPE functions almost entirely to support the neural retina by actively transporting ions, transporting large molecules, participating in the phagocytosis of visual cell material, synthesizing at least part of the extracellular matrix material, varying
RETINAL PIGMENTATION AND VISUAL ACUITY
visual sensitivity and acuity by the photomechanical response of melanin granules to meet varying conditions of illumination, and protecting the retina from damage resulting from sudden intense illumination by communicating its electrical response (for which melanin is probably the photopigment) directly to the iris muscles through a system of tight junctions. We note, however, the last two functions are probably not operative in man. Visual acuity. Contemporary knowledge of the specific details of the visual process are well documented in many reviews; this is reviewed in Hoffman (’73). The understanding of the visual process began more than one hundred years ago with the discovery of two kinds of sensory cells in the retina, the rods and cones. This observation led to the formulation of the “duplicity theory” of vision which forms the basis of our understanding of many visual processes. Riggs’ review (‘65) includes a good account of the major factors involved in visual acuity. The majority of the evidence to date points to the dimensions of the retinal mosaic, the actual size of the photoreceptors, as being so fine they cannot be considered as the principal factor influencing visual acuity. Pupil size, however, is one intrinsic factor which cannot be dismissed and is seen as exerting complex effects on visual acuity. A large pupillary aperture is favorable for visual acuity as it allows more light to stimulate the photoreceptors and minimizes the blur due to the diffraction of light produced by small openings. On the other hand, a small pupil will minimize the effects of spherical and other aberrations of the eye caused by abnormal shape of the globe, the cornea, the lens, etc. It seems likely, therefore, that visual acuity will be optimal when the pupil is of an intermediate size - the particular size dependent on conditions of illuminance, the form and size of the test object and individual differences in various eyes both within the same and among different individuals. Riggs notes that a constant level of acuity for pupil apertures between 2.5 and 5.0 mm diameter seems to represent a balance between the effects of diffraction and optical abberrations. Acuity will reach a maximum value at high intensities when the natural pupil has reached its minimum
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size. At even higher intensities the visual acuity will drop off as diffraction limits the ability of resolution (Foxell and Stevens, ’55; Leibowitz, ’52; Ogle, ’69). AS the discussion of pupil size implies, light intensity must be considered in a discussion of visual acuity. Visual acuity is poor at scotopic (low-light) levels and the parafoveal and peripheral rods predominate here. As the intensity of light increases, the threshold of the cone receptors is reached and visual acuity rises sharply. With further increases in intensity maximum acuity is reached and maintained over a wide range of high intensities at fixed pupil size. Again, beyond a certain intensity, acuity will begin to drop off. These latter intensities are roughly equivalent to those of bright sunlight and the surfaces of lighting fixtures (Foxell and Stevens, ’55). These results for pupil size and illumination are from experimentally controlled situations but as Foxell and Stevens (‘55) point out, observers in test settings consistently detect details much smaller than is encountered in normal work situations, including watch repair, where many conditions might limit performance. Pupil size and illumination, though, seem to be the principal factors influencing visual acuity. Others include the contrast of the test object, state of adaptation of the rods and cones, eye movements and monocular versus binocular vision. MATERIALS AND METHODS
The study group consisted of 84 students at the University of Colorado, Boulder campus; 49 were female, mean age 22.2 years; 35 were male, mean age 22.9 years. An important aspect of this investigation was the development and evaluation of a method for determining an estimate of the amount of melanin in the retina by ophthalmoscopic examination. The details of the method and its consistency of use, reported elsewhere (Hoffman, ’73), are briefly reviewed below. The basic parameter investigated is the amount of retinal pigmentation and its possible role in visual acuity under various intensities of light. Examination of the left ocular fundus was made with a hand-held, battery-powered, Welch Allyn No. 115 Ophthalmoscope with the pin-hold aperture in posi-
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tion. At this time the estimation of amount of retinal pigment was made according to criteria devised by this investigator. With an increase in the amount of melanin in the ocular fundus the general appearance and specific features thereof undergo change: color of overall fundus is altered from light red-orange to gray/brown, brightness of retinal vessels is decreased and fine terminal vessels and choroidal vessels are lost sight of. The criteria used to evaluate the amount of retinal pigmentation reflect these features and the apparent changes they undergo as amount of retinal melanin changes. Each of nine such criteria were scored from one to three, and the scores added to gain a total score for the individual’s overall retinal pigmentation. The total range of subject scores was divided into three groups and labeled “Light,” “Medium,” and “Heavy”retinal pigmentation. Binocular visual acuity examinations were conducted on each subject utilizing the Landolt C recognition test pattern on a chart designed and executed by the investigator and standardized at 20 feet. The visual acuity chart was illuminated by four Sylvania No. 2 Superflood EBV bulbs (no watt-rating given), two on each side, with the center of each bulb six inches in front of and eight inches lateral to the center line of the chart to give even lighting from the top to the bottom of the chart. Intensity of the photoflood bulbs was controlled by Leviton No. 6681, single pole, dimmer controls, 600 watts, 120 volts a.c. Each bulb had one control switch. The controls were calibrated for ten preselected intensities of light and recalibrated every five or six subjects because of the relatively short life span of the bulbs. Calibration was accomplished with a Salford Electrical Instruments (S.E.I.) Exposure Photometer. Table 1 lists the levels of brightness used in the study. Cahbration was done in terms of log foot-lamberts. (Note: one foot-lambert equals 0.318 candles per square foot.) It was originally hoped the brightness could be increased to about 10,000 foot-lamberts, the point at which visual acuity seems to drop off (Foxell and Stevens, ’55), but 2500 foot-lamberts was the maximum attainable. During visual acuity examination, the subject was seated in a straight-backed
TABLE 1
Brightness levels for visual acuity chart Level of brightness
Log foot-lamberts
0 1 2 3
2.0 2.5 1 .o 1.5 0.0 1 .o 1.5 2.0 2.5 3.4
chair so positioned that his eyes were 20 feet from the chart. Subjects were partially dark-adapted in a dimly-lit room for approximately five minutes. The visual acuity exam was begun at brightness level 7 and gradually decreased to level 0. The light was then brought to level 7 and the exam repeated here as an internal check on the performance of the subject. The brightness level was then increased to level 8 and finally level 9. For the acuity exam itself an incorrect response was noted when the individual made two successive errors on any one line. His visual acuity, for that level of brightness, was then the line he had correctly read just before the two successive errors. In order to control for the varying baselines of visual acuity between individuals, those subjects who normally wore glasses for distant viewing wore them during the exam to help correct for visual deficiencies and spherical aberrations. Those persons who didn’t wear glasses were assumed to have good visual acuity, but this was checked by having each individual attain at least 20-20 visual acuity at brightness level 7. For the levels of brightness where a measurement could be obtained, right pupil size was measured with a sliding caliper to determine the range of variation in pupil size response. The ophthalmoscopic examination was conducted following the visual acuity test to avoid forming an afterimage in the examined eye by the bright light of the ophthalmoscope and to avoid any possible bias in the results of the visual acuity exam from prior knowledge of a subject’s retinal pigmentation.
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RETINAL PIGMENTATION AND VISUAL ACUITY
Our basic task then is to measure the that there is no significant difference berelationships between visual acuity, pupil tween the mean visual acuities of any size and brightness levels and test for pos- two RPESCORE groups at any one level of sible significant differences in visual acu- brightness, only one t-value is found to be ity (and pupil size) at a particular level of significant - that between RPESCORE brightness between groups having differ- groups 2 and 3 at brightness level 4 for ent amounts of retinal pigmentation. the combined sample, at the 0.01 level. Student’s t-test was utilized to accomplish Since i t is an isolated result, perhaps due this. All frequency and descriptive sta- to the small sample sizes, no meaningful tistics were computed by the University of interpretation can be placed upon it. Only Colorado’s CDC 6400 utilizing the Statis- a series of significant t-values for any two tical Package for the Social Sciences (Nie RPESCORE groups over a wide range of et al.,’70). All t-values were calculated on brightness levels or between all three a Smith-Corona Cogito 1016PR program- RPESCORE groups at any one level of mable calculator. brightness would be considered meaningful. The lack of significant t-values within RESULTS either sex by itself also indicates that the In the following analyses all subjects degree of overall retinal pigmentation does are grouped into one of three retinal pig- not appear to influence visual acuity at mentation categories: RPESCORE 1, RPE- these levels of brightness. At the 0.05 level SCORE 2, and RPESCORE 3, each corre- there was one significant t-value between sponding to ‘light,’ ‘medium,’ and ‘heavy’ male and female mean visual acuities for degrees of retinal pigmentation respective- RPESCORE group 2; this is interpreted as ly as seen in table 2, which also presents a spurious result. the distribution of the RPESCORE groups Table 4 presents mean pupil sizes for for males and females. The chi-square test the sample, ungrouped as to RPESCORE. of independence indicates no significant The one significant t-value, between males difference between the sexes in the distri- and females at brightness level 6, and at bution of retinal pigmentation. the 0.05 level, is probably spurious. Table 3 presents mean visual actuities Mean pupil sizes by RPESCORE groups for the sample, ungrouped as to RPESCORE. are also presented in table 4. Utilizing the Of 87 subjects in the original study three t-test to examine the hypothesis of no sigwere eliminated because of visual acuity nificant difference between the mean pupil below 20/20 at brightness level 7, repre- sizes of any two RPESCORE groups at any senting a reduction of one subject in each one level of brightness, we note two sigof the RPESCORE groups. The most emer- nificant t-values: one in the combined gent feature of table 3 is the series of sig- sample between groups 1 and 3 at brightnificant t-values between male and female ness level 7 and one in the female sample mean visual acuities, ungrouped by RPE- between groups 1 and 3 at brightness level SCORE, at brightness levels 5 through 9, 7; both are considered spurious. No t-values all in the direction of higher male visual between male and female mean pupil sizes acuities at every level. broken down by RPESCORE groups were Mean visual acuities for each RPESCORE significant at the 0.05 level. group are also presented in table 3. UtilizFrom these results we conclude that the ing the t-test to examine the hypothesis degree of overall retinal pigmentation does TABLE 2
Formulation of RPESCORE g r o u p s
X2
Original total score
males
females
total
Group name
Degree of retinal pigmentation
8-12 13-18 19-23
11 17 7
16 17 16
27 34 23
RPESCORE 1 RPESCORE 2 RPESCORE 3
light medium heavy
N
(of sex difference) = 2.175 with 2 d.f., P
> 0.30.
J. MICHAEL HOFFMAN
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TABLE 3
M e u n visuul ucuities, V.A.1 Ungrouped data Brightness level
RPESCORE 1
RPESCORE 3
RPESCORE 2
S.D.
N
Mean
S.D.
N
Mean
S.D.
N
Mean
S.D.
0.097 0.075 0.084
0.077 0.069 0.073
11
0.082 0.075 0.078
0.060 0.058 0.058
17 17 34
0.105 0.082 0.093
0.094 0.094 0.093
7 16 23
0.100 0.069 0.078
0.058 0.048 0.052
1
0.298 0.311 0.305
0.089 0.107 0.099
0.315 0.321 0.318
0.099 0.108 0.102
0.295 0.333 0.314
0.094 0.112 0.104
0.280 0.277 0.278
0.068 0.097 0.088
2
0.500 0.500 0.500
0.089 0.139 0.131
0.499 0.509 0.505
0.099 0.135 0.133
0.519 0.509 0.514
0.122 0.165 0.143
0.453 0.481 0.472
0.103 0.118 0.088
3
0.707 0.661 0.680
0.180 0.165 0.172
0.714 0.669 0.687
0.198 0.149 0.169
0.708 0.695 0.702
0.190 0.202 0.193
0.693 0.616
0.640
0.150 0.133 0.139
0.962 0.859 0.902
0.250 0.233 0.244
0.940 0.876 0.902
0.248 0.266 0.256
1.019 0.922 0.971
0.273 0.248 0.262
0.859 0.773 0.799
0.176 0.158 0.165
Males 0 Females Total
Mean
N
35 49 84
4
16 27
5
2
1.227 1.101 1.153
0.276 0.193 0.238
1.210 1.103 1.147
0.166 0.158 0.167
1.292 1.078 1.185
0.330 0.219 0.297
1.094 1.124 1.115
0.249 0.204 0.214
6
3
1.407 1.236 1.307
0.325 0.203 0.272
1.331 1.247 1.281
0.258 0.148 0.200
1.449 1.234 1.341
0.333 0.282 0.323
1.427 1.227 1.288
0.418 0.158 0.271
7
3
1.512 1.304 1.391
0.347 0.244 0.298
1.544 1.331 1.417
0.374 0.21 1 0.302
1.508 1.331 1.419
0.337 0.289 0.322
1.474 1.247 1.317
0.379 0.148 0.256
8
3
1.613 1.419 1.500
0.386 0.271 0.336
1.635 1.435 1.516
0.350 0.292 0.326
1.596 1.409 1.503
0.438 0.302 0.382
1.617 1.414 1.476
0.358 0.229 0.283
9
2
1.670 1.488 1.564
0.390 0.321 0.361
1.695 1.519 1.591
0.350 0.345 0.351
1.636 1.409 1.523
0.443 0.302 0.390
1.713 1.539 1.592
0.358 0.321 0.334
1 Visual acuities are here expressed i n decimal form and are exactly equivalent to those expressed in standard Snellen units, i.e.,20120 = 1.00. 2 Significant t-values between male and female mean visual acuities at 0.05 level, d.f. = 82. 3 Significant t-values between male and female mean visual acuities at 0.01 level, d.f. = 82.
not influence pupil size under the levels of brightness used in this study nor is there a sexual difference noted in the phenomenon. DISCUSSION
We have seen that the degree of overall retinal pigmentation is associated with neither visual acuity nor pupil size, within the limits of brightness used in this study. Obviously, to conclude that no such association exists between these variables, the study design should be extended to brightness levels that are at once greater than
those attained here (at least to the point where visual acuity drops off under high light conditions due to the problems of small pupil size and diffraction) as well as to scotopic levels which were really not examined here except perhaps for the very lowest brightness level. We are still left with trying to explain the variation in amount of retinal melanin that obtains in human populations. In general the geographical distribution of retinal melanin appears to coincide roughly with skin color, i.e., those with the lightest retinae (least pigmented) appear to have
423
RETINAL PIGMENTATION AND VISUAL ACUITY TABLE 4
Mean p u p i l sizes, in mm RPESCORE 1
Ungrouped data
RPESCORE 2
Brightness level
N
Males 6Females Total
23 4.496 1 33 5.061 56 4.829
0.882 0.835 0.892
10 4.750 15 5.173 25 5.004
1.076 0.968 1.103
7
29 45 74
3.890 4.289 4.132
0.812 0.852 0.854
11 4.191 16 4.619 27 4.444
8
35 47 82
3.249 3.484 3.383
0.639 0.647 0.650
11 16 27
9
35 49 84
2.703 2.929 2.835
0.576 0.541 0.564
1
Mean
S.D.
N
S.D.
N
RPESCORE 3
S.D.
N
Mean
S.D.
10 4.360 11 5.109 21 4.752
0.696 0.853 0.854
3 7 10
4.100 4.743 4.550
0.721 0.408 0.568
1.023 1.033 1.032
13 3.754 17 4.265 30 4.043
0.680 0.814 0.789
5 12 17
3.580 3.883 3.794
0.427 0.381 0.407
3.327 3.687 3.541
0.575 0.863 0.768
17 3.176 17 3.471 34 3.324
0.618 0.545 0.593
7 14 21
3.300 3.264 3.276
0.847 0.388 0.559
11 2.681 16 3.050 27 2.900
0.549 0.610 0.604
17 2.706 17 2.988 34 2.847
0.632 0.573 0.611
7 2.729 16 2.744 23 2.739
0.550 0.397 0.439
Mean
Mean
Significant t-value between male and female mean pupil size at 0.05 level, d.f. = 54.
their origin in the northern and western sectors of the European subcontinent. Is there something unique about this environment which would have selected for lighter retinae in the past? Following the experimental observation that decreasing pigmentation of the fundus results in an increased sensitivity to longer wavelengths of light (greater than 600 mp), Daniels et al. (‘72) hypothesized that such an adaptive response might have arisen in the cave-dwelling periods of European prehistory where vision enhancement by firelight and embers would have been important. Daniels (‘64) has also suggested that such light retinae might prove to be advantageous for night or twilight vision, vision in fogs and during snowfalls. Intriguing as they are, these speculations must be put through the experimental gristmill. The observed significant difference between male and female mean visual acuities at the higher brightness levels is enigmatic. One could argue that the higher male visual acuity is the result of selection and training of males in tasks that require such ability. But this is obviously not the case since females have been courted routinely by industry to perform such minute tasks as assembling electronics components, tasks which require extreme visual acuity. Motivation may play some role here but it is beyond this investigation to inquire into such possibilities. Further, females may have felt uncomfortable in a dimly-lit room
with the investigator which resulted in their decreased performance. But this should also have mainfested itself at all brightness levels, not just the higher ones. We are left then with any number of possible explanations for this sexual dimorphism - genetic, environmental, psychological. None of them can be answered at present, and given our present knowledge about the genetic-environmental interactions of the visual system in man in general i t is likely to be some time in the future before we really gain an understanding. ACKNOWLEDGMENTS
I thank Drs. Alice Brues and David Greene for their helpful insights and criticisms during the completion of this study. Financial support was received from a Doctoral Dissertation Research Grant, GS37164, from the National Science Foundation and a grant from the Society of the Sigma Xi. LITERATURE CITED Birdsell, J. B. 1971 Human Evolution. A n Introduction to the New Physical Anthropology. Rand McNally, Chicago. Coon, C. S. 1965 The Living Races of Man. Knopf, New York. Coon, C. S., S. M. Garn and J. B. Birdsell 1950 Races. Knopf, New York. Daniels, F., Jr. 1964 Man and radiant energy: solar radiation. In: Handbook of Physiology,
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Section 4. Adaptation to the Environment. D. B. Dill, ed. American Physiological Society, Washington. Daniels, F., Jr., P. W. Post a n d B. E. Johnson 1972 Theories of the role of pigment in the evolution of h u m a n races. In: Pigmentation: Its Genesis a n d Biologic Control. V. Riley, ed. Appleton-Century-Crofts, New York. Foxell, C. A. P., and W. R. Stevens 1955 Measurements of visual acuity. Brit. J. Ophthal., 39; 5 1%533. Hoffman, J. M. 1973 Variation in Retinal Pigmentation: an Anthropological Perspective. Ph.D. Dissertation, University of Colorado, Boulder. Leibowitz, H. M. 1952 The effect of pupil size on visual acuity for photometrically equated test fields a t various levels of luminance. J. Optical SOC.Am., 42: 4 1 6 4 2 2 . Moyer, F. H. 1969 Development, structure, a n d function of the retinal pigmented epithelium. In: The Retina: Morphology, Function, a n d
Clinical Characteristics. B. R. Straatsma, M. 0. Hall, R. A. Allen and F. Crescitelli, eds. University Calif. Press, Berkeley. Nie, N. H., D. H. Bent and C. H. Hull 1970 Statistical Package for the Social Sciences. McGrawHill, New York. Ogle, K. N. 1969 Visual acuity. In: The Retina: Morphology, Function, a n d Clinical Characteristics. B. R. Straatsma et al., eds. University Calif. Press, Berkeley. Polyak, S. 1957 The Vertebrate Visual System. University Chicago Press, Chicago. Riggs, L. A. 1965 Visual acuity. In: Vision a n d Visual Perception. C. H. Graham, ed. John Wiley and Sons, New York. Walls, G. L. 1967 The Vertebrate Eye and its Adaptive Radiation. Hafner, New York. (Reprint of original 1942 edition.) Wolff, E. 1968 Anatomy of the Eye and Orbit, Sixth edition. Rev. by R. J. Last. W. B. Saunders, Philadelphia.
K E Y WORDS Brightness.
Eye . Melanin . Retina
. Vision
. Visual acuity
ABSTRACT This study investigates the hypothesis that the degree of retinal pigmentation i n the human eye is adaptive as it relates to the maintenance of visual acuity i n optically stressful environments, deserts and snowfields. Eightyfour subjects were examined, an estimation of their degree of retinal pigmentation made by ophthalmoscopic examination, and their binocular visual acuity tested over ten levels of brightness. The general level of retinal pigmentation did not influence mean visual acuity within the levels of brightness used in this study. The hypothesis was, therefore, rejected, but with the proviso that this study should be extended to even higher levels of brightness than were obtained here. There was no difference in mean pupil size at various levels of illumination between individuals grouped by degree of retinal pigmentation.
Primates are visual animals and, in this respect, man is no exception. In his work on the vertebrate visual system, Polyak ('57) lists that combination of characteristics specific to primate and human vision and then discusses the role of visual acuity in the phylogeny of primate vision. He sees primate vision as unique in its combination of diurnalism associated with a high visual acuity, well-differentiated sense of color and strictly binocular stereopsis, all coupled with richly developed mental attributes. As diurnal animals, most primates are faced with a great range of environments in terms of their overall illumination or brightness, from heavily canopied tropical forests which effectively screen nearly all direct sunlight, through various degrees of open woodland, to the extreme of highly illuminated deserts or near-deserts and snowfields. The ability of a primate to maintain its visual acuity when faced with such a range of potentially optically stressful environments, as well as with the variation in sunlight occurring between dawn and nightfall, is a problem to be mastered because optimal visual acuity will be maintained within a certain threshold and maximum intensity of illumination. On either side of this range of light intensities visual acuity drops dramatically. What mechaA M . J. P K Y S . ANTHROP.,4 3 ; 417-424.
nisms, then, are available to the primate faced with this problem? Obviously, adjustment of pupil size serves as an efficient regulatory mechanism over a wide range of light intensities, but is this the only method available for regulating the amount of light which eventually strikes the photoreceptors deep in the retina? An established biological phenomenon in some lower vertebrates and invertebrates is the migration of melanin from the basal aspect of the retinal pigment epithelium into processes surrounding the outer segments of the photoreceptors as the amount of light entering the eye increases. This phenomenon is assumed to increase visual acuity in these animals by reducing the scattering of light rays in the interior of the eye before the light reaches the photoreceptor cells' outer segments (Polyak, '57; Wolff, '68). Numerous authors state, although not without controversy, that this phenomenon either does not occur or has not been observed in higher vertebrates, especially the primates and man, arguing that this function has been superceded and replaced by a highly reactive and contractile pupil which serves to reduce the amount of incoming light as intensity increases (Walls, '67). However, the retina in all higher vertebrates, man not ex417
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J. MICHAEL HOFFMAN
cluded, still contains melanin in a discrete layer abutting the outer segments of the photoreceptor cells. The amount of melanin varies greatly therein when viewed ophthalmoscopically and microscopically. Why does the retinal pigment epithelium continue to possess melanin when no obvious function for i t remains and why does such variation remain in the amount of melanin in human retinae? Although numerous studies of the retinal pigment epithelium have been conducted, nowhere has anyone systematically examined the questions posed. Some biological studies do mention variability in the amount of melanin in the retinal pigment epithelium, but only to alert the physician to this normal variation, thereby begging the question why. Coon, Garn and Birdsell, collectively and individually, have addressed themselves to these questions but have not made the necessary tests of their hypotheses. As physical anthropologists they confront the question of variation in human retinal pigmentation, left begging by the biologists, and hypothesize that the amount of melanin in the retina is adaptive in maintaining visual acuity in optically stressful environments. Their basic argument is that an increase in the amount of melanin in the retina helps shield the photoreceptors’ outer segments thereby maintaining visual acuity in brightly lit environments, i.e., those with a great deal of sunlight and glare, by reducing the scattering of light within the eye and reducing the absolute amount of light which impinges on the photoreceptors. In their jointly-authored work Races (‘50), they implied by a diagram that pigment migration occurs in humans as in some invertebrates and lower vertebrates. However, Coon (’65) and Birdsell (‘71) do not mention this process in their individual works, nor do modern workers in vision research feel that i t is operative in man. Their basic argument, though, remains the same even in light of a change in mechanism, now implied to be the constant anatomical juxtaposition of the retinal pigment epithelial cells’ pigment processes to the photoreceptor cells’ outer segments. The variable has now changed from migration of melanin to variation in absolute amount to effect the proper screening in bright environments.
Does this hypothesis, though, really explain the variation? In the presence of a highly reactive, contractile pupil is there a need for melanin in the role of a lightscreener for the outer segments? There might not be except for the fact that the pupil has an absolute minimum size below which i t can contract no further. Once this limit is reached the melaninscreening mechanism may be of inestimable value in maintaining visual acuity. Also, in those extreme optically stressful environments such as deserts or snowfields, the combination of the mechanisms, pupil contractibility and melanin-screening, might be more beneficial and economical to the individual than just pupillary contraction alone. With some assistance from melanin-screening the pupil might be able to extend its range of contractibility into more extreme environments, thereby combatting pupillary fatigue. But here, too, we don’t know what the range of variation in pupil size is for various persons at the same level of illumination, persons who vary in the amount of melanin their retinae contain. This report presents the results of an investigation of the hypothesis that the amount of melanin in the retinal pigment epithelium of the human eye is adaptive as this relates to the maintenance of visual acuity in optically stressful environments, i.e., environments in which there are high or low intensities of sunlight striking the surroundings of the individual, as in snowfields and deserts or as in heavy forests and dimly lit, overcast skies. BACKGROUND
Retinal pigment epithelium (RPE). Good, detailed reviews of the histology and melanogenesis of the retinal pigment epithelial cell are readily available. This material has been summarized elsewhere (Hoffman, ’73). Moyer’s recent review article (‘69) on the RPE summarizes the present knowledge of the structure and function of this unique tissue. He concludes by stating the RPE functions almost entirely to support the neural retina by actively transporting ions, transporting large molecules, participating in the phagocytosis of visual cell material, synthesizing at least part of the extracellular matrix material, varying
RETINAL PIGMENTATION AND VISUAL ACUITY
visual sensitivity and acuity by the photomechanical response of melanin granules to meet varying conditions of illumination, and protecting the retina from damage resulting from sudden intense illumination by communicating its electrical response (for which melanin is probably the photopigment) directly to the iris muscles through a system of tight junctions. We note, however, the last two functions are probably not operative in man. Visual acuity. Contemporary knowledge of the specific details of the visual process are well documented in many reviews; this is reviewed in Hoffman (’73). The understanding of the visual process began more than one hundred years ago with the discovery of two kinds of sensory cells in the retina, the rods and cones. This observation led to the formulation of the “duplicity theory” of vision which forms the basis of our understanding of many visual processes. Riggs’ review (‘65) includes a good account of the major factors involved in visual acuity. The majority of the evidence to date points to the dimensions of the retinal mosaic, the actual size of the photoreceptors, as being so fine they cannot be considered as the principal factor influencing visual acuity. Pupil size, however, is one intrinsic factor which cannot be dismissed and is seen as exerting complex effects on visual acuity. A large pupillary aperture is favorable for visual acuity as it allows more light to stimulate the photoreceptors and minimizes the blur due to the diffraction of light produced by small openings. On the other hand, a small pupil will minimize the effects of spherical and other aberrations of the eye caused by abnormal shape of the globe, the cornea, the lens, etc. It seems likely, therefore, that visual acuity will be optimal when the pupil is of an intermediate size - the particular size dependent on conditions of illuminance, the form and size of the test object and individual differences in various eyes both within the same and among different individuals. Riggs notes that a constant level of acuity for pupil apertures between 2.5 and 5.0 mm diameter seems to represent a balance between the effects of diffraction and optical abberrations. Acuity will reach a maximum value at high intensities when the natural pupil has reached its minimum
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size. At even higher intensities the visual acuity will drop off as diffraction limits the ability of resolution (Foxell and Stevens, ’55; Leibowitz, ’52; Ogle, ’69). AS the discussion of pupil size implies, light intensity must be considered in a discussion of visual acuity. Visual acuity is poor at scotopic (low-light) levels and the parafoveal and peripheral rods predominate here. As the intensity of light increases, the threshold of the cone receptors is reached and visual acuity rises sharply. With further increases in intensity maximum acuity is reached and maintained over a wide range of high intensities at fixed pupil size. Again, beyond a certain intensity, acuity will begin to drop off. These latter intensities are roughly equivalent to those of bright sunlight and the surfaces of lighting fixtures (Foxell and Stevens, ’55). These results for pupil size and illumination are from experimentally controlled situations but as Foxell and Stevens (‘55) point out, observers in test settings consistently detect details much smaller than is encountered in normal work situations, including watch repair, where many conditions might limit performance. Pupil size and illumination, though, seem to be the principal factors influencing visual acuity. Others include the contrast of the test object, state of adaptation of the rods and cones, eye movements and monocular versus binocular vision. MATERIALS AND METHODS
The study group consisted of 84 students at the University of Colorado, Boulder campus; 49 were female, mean age 22.2 years; 35 were male, mean age 22.9 years. An important aspect of this investigation was the development and evaluation of a method for determining an estimate of the amount of melanin in the retina by ophthalmoscopic examination. The details of the method and its consistency of use, reported elsewhere (Hoffman, ’73), are briefly reviewed below. The basic parameter investigated is the amount of retinal pigmentation and its possible role in visual acuity under various intensities of light. Examination of the left ocular fundus was made with a hand-held, battery-powered, Welch Allyn No. 115 Ophthalmoscope with the pin-hold aperture in posi-
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J. MICHAEL HOFFMAN
tion. At this time the estimation of amount of retinal pigment was made according to criteria devised by this investigator. With an increase in the amount of melanin in the ocular fundus the general appearance and specific features thereof undergo change: color of overall fundus is altered from light red-orange to gray/brown, brightness of retinal vessels is decreased and fine terminal vessels and choroidal vessels are lost sight of. The criteria used to evaluate the amount of retinal pigmentation reflect these features and the apparent changes they undergo as amount of retinal melanin changes. Each of nine such criteria were scored from one to three, and the scores added to gain a total score for the individual’s overall retinal pigmentation. The total range of subject scores was divided into three groups and labeled “Light,” “Medium,” and “Heavy”retinal pigmentation. Binocular visual acuity examinations were conducted on each subject utilizing the Landolt C recognition test pattern on a chart designed and executed by the investigator and standardized at 20 feet. The visual acuity chart was illuminated by four Sylvania No. 2 Superflood EBV bulbs (no watt-rating given), two on each side, with the center of each bulb six inches in front of and eight inches lateral to the center line of the chart to give even lighting from the top to the bottom of the chart. Intensity of the photoflood bulbs was controlled by Leviton No. 6681, single pole, dimmer controls, 600 watts, 120 volts a.c. Each bulb had one control switch. The controls were calibrated for ten preselected intensities of light and recalibrated every five or six subjects because of the relatively short life span of the bulbs. Calibration was accomplished with a Salford Electrical Instruments (S.E.I.) Exposure Photometer. Table 1 lists the levels of brightness used in the study. Cahbration was done in terms of log foot-lamberts. (Note: one foot-lambert equals 0.318 candles per square foot.) It was originally hoped the brightness could be increased to about 10,000 foot-lamberts, the point at which visual acuity seems to drop off (Foxell and Stevens, ’55), but 2500 foot-lamberts was the maximum attainable. During visual acuity examination, the subject was seated in a straight-backed
TABLE 1
Brightness levels for visual acuity chart Level of brightness
Log foot-lamberts
0 1 2 3
2.0 2.5 1 .o 1.5 0.0 1 .o 1.5 2.0 2.5 3.4
chair so positioned that his eyes were 20 feet from the chart. Subjects were partially dark-adapted in a dimly-lit room for approximately five minutes. The visual acuity exam was begun at brightness level 7 and gradually decreased to level 0. The light was then brought to level 7 and the exam repeated here as an internal check on the performance of the subject. The brightness level was then increased to level 8 and finally level 9. For the acuity exam itself an incorrect response was noted when the individual made two successive errors on any one line. His visual acuity, for that level of brightness, was then the line he had correctly read just before the two successive errors. In order to control for the varying baselines of visual acuity between individuals, those subjects who normally wore glasses for distant viewing wore them during the exam to help correct for visual deficiencies and spherical aberrations. Those persons who didn’t wear glasses were assumed to have good visual acuity, but this was checked by having each individual attain at least 20-20 visual acuity at brightness level 7. For the levels of brightness where a measurement could be obtained, right pupil size was measured with a sliding caliper to determine the range of variation in pupil size response. The ophthalmoscopic examination was conducted following the visual acuity test to avoid forming an afterimage in the examined eye by the bright light of the ophthalmoscope and to avoid any possible bias in the results of the visual acuity exam from prior knowledge of a subject’s retinal pigmentation.
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RETINAL PIGMENTATION AND VISUAL ACUITY
Our basic task then is to measure the that there is no significant difference berelationships between visual acuity, pupil tween the mean visual acuities of any size and brightness levels and test for pos- two RPESCORE groups at any one level of sible significant differences in visual acu- brightness, only one t-value is found to be ity (and pupil size) at a particular level of significant - that between RPESCORE brightness between groups having differ- groups 2 and 3 at brightness level 4 for ent amounts of retinal pigmentation. the combined sample, at the 0.01 level. Student’s t-test was utilized to accomplish Since i t is an isolated result, perhaps due this. All frequency and descriptive sta- to the small sample sizes, no meaningful tistics were computed by the University of interpretation can be placed upon it. Only Colorado’s CDC 6400 utilizing the Statis- a series of significant t-values for any two tical Package for the Social Sciences (Nie RPESCORE groups over a wide range of et al.,’70). All t-values were calculated on brightness levels or between all three a Smith-Corona Cogito 1016PR program- RPESCORE groups at any one level of mable calculator. brightness would be considered meaningful. The lack of significant t-values within RESULTS either sex by itself also indicates that the In the following analyses all subjects degree of overall retinal pigmentation does are grouped into one of three retinal pig- not appear to influence visual acuity at mentation categories: RPESCORE 1, RPE- these levels of brightness. At the 0.05 level SCORE 2, and RPESCORE 3, each corre- there was one significant t-value between sponding to ‘light,’ ‘medium,’ and ‘heavy’ male and female mean visual acuities for degrees of retinal pigmentation respective- RPESCORE group 2; this is interpreted as ly as seen in table 2, which also presents a spurious result. the distribution of the RPESCORE groups Table 4 presents mean pupil sizes for for males and females. The chi-square test the sample, ungrouped as to RPESCORE. of independence indicates no significant The one significant t-value, between males difference between the sexes in the distri- and females at brightness level 6, and at bution of retinal pigmentation. the 0.05 level, is probably spurious. Table 3 presents mean visual actuities Mean pupil sizes by RPESCORE groups for the sample, ungrouped as to RPESCORE. are also presented in table 4. Utilizing the Of 87 subjects in the original study three t-test to examine the hypothesis of no sigwere eliminated because of visual acuity nificant difference between the mean pupil below 20/20 at brightness level 7, repre- sizes of any two RPESCORE groups at any senting a reduction of one subject in each one level of brightness, we note two sigof the RPESCORE groups. The most emer- nificant t-values: one in the combined gent feature of table 3 is the series of sig- sample between groups 1 and 3 at brightnificant t-values between male and female ness level 7 and one in the female sample mean visual acuities, ungrouped by RPE- between groups 1 and 3 at brightness level SCORE, at brightness levels 5 through 9, 7; both are considered spurious. No t-values all in the direction of higher male visual between male and female mean pupil sizes acuities at every level. broken down by RPESCORE groups were Mean visual acuities for each RPESCORE significant at the 0.05 level. group are also presented in table 3. UtilizFrom these results we conclude that the ing the t-test to examine the hypothesis degree of overall retinal pigmentation does TABLE 2
Formulation of RPESCORE g r o u p s
X2
Original total score
males
females
total
Group name
Degree of retinal pigmentation
8-12 13-18 19-23
11 17 7
16 17 16
27 34 23
RPESCORE 1 RPESCORE 2 RPESCORE 3
light medium heavy
N
(of sex difference) = 2.175 with 2 d.f., P
> 0.30.
J. MICHAEL HOFFMAN
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TABLE 3
M e u n visuul ucuities, V.A.1 Ungrouped data Brightness level
RPESCORE 1
RPESCORE 3
RPESCORE 2
S.D.
N
Mean
S.D.
N
Mean
S.D.
N
Mean
S.D.
0.097 0.075 0.084
0.077 0.069 0.073
11
0.082 0.075 0.078
0.060 0.058 0.058
17 17 34
0.105 0.082 0.093
0.094 0.094 0.093
7 16 23
0.100 0.069 0.078
0.058 0.048 0.052
1
0.298 0.311 0.305
0.089 0.107 0.099
0.315 0.321 0.318
0.099 0.108 0.102
0.295 0.333 0.314
0.094 0.112 0.104
0.280 0.277 0.278
0.068 0.097 0.088
2
0.500 0.500 0.500
0.089 0.139 0.131
0.499 0.509 0.505
0.099 0.135 0.133
0.519 0.509 0.514
0.122 0.165 0.143
0.453 0.481 0.472
0.103 0.118 0.088
3
0.707 0.661 0.680
0.180 0.165 0.172
0.714 0.669 0.687
0.198 0.149 0.169
0.708 0.695 0.702
0.190 0.202 0.193
0.693 0.616
0.640
0.150 0.133 0.139
0.962 0.859 0.902
0.250 0.233 0.244
0.940 0.876 0.902
0.248 0.266 0.256
1.019 0.922 0.971
0.273 0.248 0.262
0.859 0.773 0.799
0.176 0.158 0.165
Males 0 Females Total
Mean
N
35 49 84
4
16 27
5
2
1.227 1.101 1.153
0.276 0.193 0.238
1.210 1.103 1.147
0.166 0.158 0.167
1.292 1.078 1.185
0.330 0.219 0.297
1.094 1.124 1.115
0.249 0.204 0.214
6
3
1.407 1.236 1.307
0.325 0.203 0.272
1.331 1.247 1.281
0.258 0.148 0.200
1.449 1.234 1.341
0.333 0.282 0.323
1.427 1.227 1.288
0.418 0.158 0.271
7
3
1.512 1.304 1.391
0.347 0.244 0.298
1.544 1.331 1.417
0.374 0.21 1 0.302
1.508 1.331 1.419
0.337 0.289 0.322
1.474 1.247 1.317
0.379 0.148 0.256
8
3
1.613 1.419 1.500
0.386 0.271 0.336
1.635 1.435 1.516
0.350 0.292 0.326
1.596 1.409 1.503
0.438 0.302 0.382
1.617 1.414 1.476
0.358 0.229 0.283
9
2
1.670 1.488 1.564
0.390 0.321 0.361
1.695 1.519 1.591
0.350 0.345 0.351
1.636 1.409 1.523
0.443 0.302 0.390
1.713 1.539 1.592
0.358 0.321 0.334
1 Visual acuities are here expressed i n decimal form and are exactly equivalent to those expressed in standard Snellen units, i.e.,20120 = 1.00. 2 Significant t-values between male and female mean visual acuities at 0.05 level, d.f. = 82. 3 Significant t-values between male and female mean visual acuities at 0.01 level, d.f. = 82.
not influence pupil size under the levels of brightness used in this study nor is there a sexual difference noted in the phenomenon. DISCUSSION
We have seen that the degree of overall retinal pigmentation is associated with neither visual acuity nor pupil size, within the limits of brightness used in this study. Obviously, to conclude that no such association exists between these variables, the study design should be extended to brightness levels that are at once greater than
those attained here (at least to the point where visual acuity drops off under high light conditions due to the problems of small pupil size and diffraction) as well as to scotopic levels which were really not examined here except perhaps for the very lowest brightness level. We are still left with trying to explain the variation in amount of retinal melanin that obtains in human populations. In general the geographical distribution of retinal melanin appears to coincide roughly with skin color, i.e., those with the lightest retinae (least pigmented) appear to have
423
RETINAL PIGMENTATION AND VISUAL ACUITY TABLE 4
Mean p u p i l sizes, in mm RPESCORE 1
Ungrouped data
RPESCORE 2
Brightness level
N
Males 6Females Total
23 4.496 1 33 5.061 56 4.829
0.882 0.835 0.892
10 4.750 15 5.173 25 5.004
1.076 0.968 1.103
7
29 45 74
3.890 4.289 4.132
0.812 0.852 0.854
11 4.191 16 4.619 27 4.444
8
35 47 82
3.249 3.484 3.383
0.639 0.647 0.650
11 16 27
9
35 49 84
2.703 2.929 2.835
0.576 0.541 0.564
1
Mean
S.D.
N
S.D.
N
RPESCORE 3
S.D.
N
Mean
S.D.
10 4.360 11 5.109 21 4.752
0.696 0.853 0.854
3 7 10
4.100 4.743 4.550
0.721 0.408 0.568
1.023 1.033 1.032
13 3.754 17 4.265 30 4.043
0.680 0.814 0.789
5 12 17
3.580 3.883 3.794
0.427 0.381 0.407
3.327 3.687 3.541
0.575 0.863 0.768
17 3.176 17 3.471 34 3.324
0.618 0.545 0.593
7 14 21
3.300 3.264 3.276
0.847 0.388 0.559
11 2.681 16 3.050 27 2.900
0.549 0.610 0.604
17 2.706 17 2.988 34 2.847
0.632 0.573 0.611
7 2.729 16 2.744 23 2.739
0.550 0.397 0.439
Mean
Mean
Significant t-value between male and female mean pupil size at 0.05 level, d.f. = 54.
their origin in the northern and western sectors of the European subcontinent. Is there something unique about this environment which would have selected for lighter retinae in the past? Following the experimental observation that decreasing pigmentation of the fundus results in an increased sensitivity to longer wavelengths of light (greater than 600 mp), Daniels et al. (‘72) hypothesized that such an adaptive response might have arisen in the cave-dwelling periods of European prehistory where vision enhancement by firelight and embers would have been important. Daniels (‘64) has also suggested that such light retinae might prove to be advantageous for night or twilight vision, vision in fogs and during snowfalls. Intriguing as they are, these speculations must be put through the experimental gristmill. The observed significant difference between male and female mean visual acuities at the higher brightness levels is enigmatic. One could argue that the higher male visual acuity is the result of selection and training of males in tasks that require such ability. But this is obviously not the case since females have been courted routinely by industry to perform such minute tasks as assembling electronics components, tasks which require extreme visual acuity. Motivation may play some role here but it is beyond this investigation to inquire into such possibilities. Further, females may have felt uncomfortable in a dimly-lit room
with the investigator which resulted in their decreased performance. But this should also have mainfested itself at all brightness levels, not just the higher ones. We are left then with any number of possible explanations for this sexual dimorphism - genetic, environmental, psychological. None of them can be answered at present, and given our present knowledge about the genetic-environmental interactions of the visual system in man in general i t is likely to be some time in the future before we really gain an understanding. ACKNOWLEDGMENTS
I thank Drs. Alice Brues and David Greene for their helpful insights and criticisms during the completion of this study. Financial support was received from a Doctoral Dissertation Research Grant, GS37164, from the National Science Foundation and a grant from the Society of the Sigma Xi. LITERATURE CITED Birdsell, J. B. 1971 Human Evolution. A n Introduction to the New Physical Anthropology. Rand McNally, Chicago. Coon, C. S. 1965 The Living Races of Man. Knopf, New York. Coon, C. S., S. M. Garn and J. B. Birdsell 1950 Races. Knopf, New York. Daniels, F., Jr. 1964 Man and radiant energy: solar radiation. In: Handbook of Physiology,
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Section 4. Adaptation to the Environment. D. B. Dill, ed. American Physiological Society, Washington. Daniels, F., Jr., P. W. Post a n d B. E. Johnson 1972 Theories of the role of pigment in the evolution of h u m a n races. In: Pigmentation: Its Genesis a n d Biologic Control. V. Riley, ed. Appleton-Century-Crofts, New York. Foxell, C. A. P., and W. R. Stevens 1955 Measurements of visual acuity. Brit. J. Ophthal., 39; 5 1%533. Hoffman, J. M. 1973 Variation in Retinal Pigmentation: an Anthropological Perspective. Ph.D. Dissertation, University of Colorado, Boulder. Leibowitz, H. M. 1952 The effect of pupil size on visual acuity for photometrically equated test fields a t various levels of luminance. J. Optical SOC.Am., 42: 4 1 6 4 2 2 . Moyer, F. H. 1969 Development, structure, a n d function of the retinal pigmented epithelium. In: The Retina: Morphology, Function, a n d
Clinical Characteristics. B. R. Straatsma, M. 0. Hall, R. A. Allen and F. Crescitelli, eds. University Calif. Press, Berkeley. Nie, N. H., D. H. Bent and C. H. Hull 1970 Statistical Package for the Social Sciences. McGrawHill, New York. Ogle, K. N. 1969 Visual acuity. In: The Retina: Morphology, Function, a n d Clinical Characteristics. B. R. Straatsma et al., eds. University Calif. Press, Berkeley. Polyak, S. 1957 The Vertebrate Visual System. University Chicago Press, Chicago. Riggs, L. A. 1965 Visual acuity. In: Vision a n d Visual Perception. C. H. Graham, ed. John Wiley and Sons, New York. Walls, G. L. 1967 The Vertebrate Eye and its Adaptive Radiation. Hafner, New York. (Reprint of original 1942 edition.) Wolff, E. 1968 Anatomy of the Eye and Orbit, Sixth edition. Rev. by R. J. Last. W. B. Saunders, Philadelphia.
