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near and mid-distance objects, images from more distant objects will be focused in front of the retina so producing myopic blur that is known to act against the development of myopia in experimental animals. This is an everyday corollary to the experimental work in chicks that included both in-focus near targets and distance information.34 The situation is quite different in close work where images of objects from a distance are largely prevented from reaching the eye, being obscured by the reading material that will occupy a significant proportion of the visual field. In addition to the elimination of the protective myopic blur from distant objects, reading material being in-focus across a significant proportion of the visual field will reduce the out of focus content of the visual image. Currently, however, there is no experimental work assessing whether a totally in-focus image on its own can induce changes in eye growth.
Light vergence and photon catch
In relation to the ability of the retina to differentiate between myopic and hyperopic blur, as has already been noted, an obvious difference between these two situations is that in hyperopic defocus, light passing through the retina to come to a focus behind it is convergent, whereas in myopic defocus with images of distant objects focused in front of the retina, light passing through the retina is divergent. In considering how the retina might be able to differentiate between the blurred images caused by convergent or divergent light, the effect of these two optical conditions on the distribution of photons along the lengths of the photoreceptor outer segments appears to offer a possible explanation.
In conditions of convergent light, photons will become more closely packed as the convergent light nears its point of focus posterior to the photoreceptor outer segments so that in the case of hyperopic blur, as convergent light passes through the retina, photon density and absorption in the photoreceptors will increase towards the tips of the photoreceptor outer segments and decrease in their more proximal bases.
Conversely in conditions of myopic blur with focus in front of the retina and divergent light passing through the retina, photon density will decrease along the length of the photoreceptor outer segments so that there will be an increased photon catch at the bases of the photoreceptor outer segments rather than the tips.
It may be asked whether the Stiles Crawford effect,61 in which photons are thought preferentially to enter the proximate ends of the outer
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segments and be transmitted axially in the outer segments as a result of their waveguide properties, would prevent any skewed distribution of photons within the receptor outer segments. There is good evidence, however, that photons can be transmitted transversely through the lateral outer segment membrane and induce depolarisation limited to a very localised section of the outer segment.62
In conditions of myopic or hyperopic defocus with an enlarged blur circle in the retina for either condition, very few photons would be travelling in a path normal to the plane of the retina, and as a result, very few would be admitted to the receptor outer segments if only those arriving normal to the inner surface of the outer segment were able to enter the outer segment.
Defocus does reduce contrast sensitivity for spatial frequencies in the range 3–38 cycles/degree but not lower frequencies.63 Defocus, however, does not reduce total retinal illuminance. In personal experiments in which there was rapid alternation of viewing an illuminated target with a focused or a defocused eye, it was noted that optical defocus with plus or minus lenses up to ± 10 D had no effect on the perceived brightness of the illuminated target, thus indicating that photons arriving at the retina along convergent or divergent paths were captured by the outer segments. Thus it would be possible, that the differing vergences of light reaching the retina in hyperopic or myopic defocus could be identified in the retina as a result of a skewed distribution of photon catch along the photoreceptor outer segments.
Where there was an increased photon catch in the tips of the outer segments, such would occur in hyperopic defocus; elongation of the eye would act to even out the distribution of photon catch along the outer segments by moving the maximal photon absorption towards the mid-points of the photoreceptor outer segments.
In visual deprivation myopia in chicks, there is an elongation of the photoreceptor outer segments that has been suggested as a driving force for ocular elongation.64 In the short-term, a skewed distribution of photon catch along the photoreceptor outer segments might be a stimulus to accommodation and in the longer term to eye growth.
Thus, it is possible that the young eye may be programmed to elongate in response to hyperopic blur in an attempt to overcome an unequal distribution of photons along the length of photoreceptor outer segments. Conversely, an increased photon catch at the bases of the photoreceptor outer segments in conditions of myopic blur would inhibit ocular axial
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growth and if growth characteristics of the lens or cornea were unaffected, this might account for the development of hyperopia in experimental animals in which myopic blur has been induced by the wearing of positive lenses. It is known that the response to an alteration in the vergence of light reaching the eye is almost immediate65 as would be expected if the compensatory response to positive or negative lens wear were a function of photon distribution in the receptor outer segments. In the short-term a skewed distribution of photon catch along the photoreceptor outer segments might be a stimulus to accommodation and in the longer term to eye growth.
Chromaticity
The effects of longitudinal and transverse chromatic aberration on the focus and location of the retinal image are well known, longitudinal chromatic aberration forming the basis of the duochrome test, red light being focused in the eye more posteriorly than green or blue light. The retinal effect of chromatic aberration may also be increased by dispersion of shorter wavelengths by the lens.66
In white light where all the colors of the spectrum are present in an image, some of the red wavelengths will be focused behind the photoreceptor layer of the retina, while some of the shorter wavelength blue light will be focused in front of the photoreceptor layer of the retina, a situation that has been identified as a factor involved in the elongation of the eye in the development of myopia.38
In the human eye, there are three types of cones: L-cones that preferentially absorb long wavelength red photons; M-cones absorbing maximally mid-wavelength photons; and S-cones preferentially absorbing short wavelength blue photons. In the chick, there are five colour sensitive cone types and a double cone responding to movement67 but the spectral sensitivity curve of the chick eye is similar to that of the human.68
L-cones and M-cones greatly outnumber S-cones but this may be a reflection of the fact that blue photons are significantly more energetic than green or red photons, so likely to stimulate a photochemical effect in the photoreceptor outer segments in excess of their numbers, the energy of a photon acting as a wave, being proportional to its frequency and its momentum being inversely proportional to its wavelength.
As the human (and chick) eye is most sensitive to mid-wavelength yellow/green light in photopic conditions, the probability is that
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accommodation is largely influenced by these wavelengths. If green light absorbed in the M-cones determines accommodation so as to maximize luminance contrast, this would ensure that green wavelengths were focused in the mid-points of the M-cone photoreceptor outer segments and, additionally, that most of the red and blue wavelengths would be accommodated within the lengths of the outer segments so that the whole visible spectrum, with the exception of the longest red wavelengths or the shortest blue wavelengths, could be accomodated within the length of the outer segments with red light absorbed in the tips of L-cones, blue light absorbed in the bases of S-cones and green light in the mid-points of M- cones. In conditions of white light with all the wavelengths of the visible spectrum present, if accommodation were largely determined by M-cones and green light to which the retina is the most sensitive, there would be an equal distribution of photon catch of red photons in the distal tips and of blue photons in the proximal bases of the outer segments (or perhaps an equal photochemical effect allowing for the increased energy of short wavelength photons as compared with longer wavelengths and the reduced number of S-cones).
In spite of the fact that there is good evidence that the degree of accommodative effort is unlikely to be directly involved in the etiology of myopia, a number of studies have used assessments of accommodation in relation to chromatic aberration as an indication of myopia risk.
It has been shown that the accommodation response is sensitive to the chromatic properties of the stimulus, the degree of accommodation being determined by the relative sensitivities of L- and M-cones.36 It has been suggested that if luminance contrast is maximized by accommodation, the longest red wavelengths will be focused behind the photoreceptor layer of the retina and the shortest blue wavelengths infront ot it. It has also been suggested that in individuals in whom luminance contrast is dominated by L-cones, this would result in increased accommodation, elongation of the eye and myopia.36 It has also been shown that the use of green paper (absorbing longer wavelengths) during reading reduces accommodative effort and may thus protect against myopia.69
In another study35 it was shown that humans and chicks accommodated more in red light and less in blue light in accordance with chromatic aberration and that in chicks, a small compensatory change in refractive error could be demonstrated when chicks were refracted in total darkness but not in white light unless refracted under cycloplegia. The difference between the results of this study and an earlier study,68 where no change in
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accommodative tonus or of refraction was found in chicks raised in red or blue near monochromatic light, was ascribed to the fact that the wavelengths of blue light used in the later study were longer than those used in the earlier study.
Longitudinal chromatic aberration in conditions of retinal blur leading to visual deprivation myopia, has been held to provide complex color-coded cues for reflexive accommodation.62 As these chromatic cues are most sensitive to spatial frequencies between 3 and 5 cycles/degree, it has been suggested as a possibility that a change in the spatial frequency composition of the retinal image will reduce the sensitivity to chromatic cues, resulting in inadequate accommodation leading to a hyperopic blur and myopia.70
Although a number of features of the retinal image in lid closure such as reduced luminance, reduced contrast, loss of higher frequency spatial content, the effect of altered chromaticity has received little if any attention. In lid closure, the eyelid with its rich blood supply is effectively a red filter. Additionally, as white light traverses the closed eyelids, shorter wavelengths are more likely to be dispersed than are longer wavelengths. An alteration in the spectral composition of light reaching the retina with a preponderance of longer wavelength red light and a deficit of shorter wavelength blue light would be an expected result.
Alterations in the spectral composition in which developing animals are raised can lead to structural changes in the eye. Thus, blue acara fish raised for two years in near monochromatic light of various wavelengths71 showed a marked increase in the length of the photoreceptor outer segments of L-cones and M-cones when raised in shorter wavelength blue light. This was ascribed to a compensatory response to long and medium wavelength deprivation. It had previously been shown that fish reared in light of longer wavelengths had increased ocular nasotemporal diameters as compared with those raised in shorter wavelength light.72
In the enhanced S-cone syndrome,73 it is believed that there is an actual increase in the number of S cones in the retina and that these replace some of the L- and M-cones.74 In this condition, the affected eyes are usually hyperopic as would be expected with a greater photon catch in the bases of the increased number of S-cone photoreceptor outer segments as compared with photon catch in the tips of the photoreceptor outer segments of the reduced number of L-cones.
It is interesting that growth in other biological systems can be influenced by the spectral composition of incident light, for in experiments related to the production of food plants for space exploration, it was
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found that although plants (lettuces) could be grown in red and blue light, or in white light, their growth was greatly enhanced beyond that in white light by the addition of 24% green light to red and blue growing conditions.75
A possible explanation for the effects that chromaticity might have on ocular or refractive development would be a differential stimulation of red or blue sensitive cones. This explanation however is rendered highly unlikely as in experiments in which chicks were raised in narrow band near monochromatic red light or narrow band near UV blue light,68 ocular and refractive development was similar in each of the two chromatic conditions. In these experiments, only very restricted red wavelengths of 650–700 nm or blue light of 350–425 nm were used and the probability is that the chicks accommodated to whatever wavelengths were available so that those raised in purely red light would accommodate to the degree necessary to focus the available red light in the mid-points of the red sensitive cone outer segments and, similarly, those raised in blue light would accommodate to ensure the focus of blue light in the mid-points of the blue sensitive cone outer segments. There would thus be no imbalance of photon catch along the length of the outer segments, with most of the photon catch being in the mid-points of the outer segments and very little photon catch in either their tips or the bases.
To test whether an unequal distribution of photon catch along the photoreceptor outer segments affects ocular growth and, therefore, refractive development in the young animal, we investigated in chicks the effect of chromatic manipulation designed to increase photon catch in the tips of the outer segments or alternatively in their bases. This would also explain the fact that chicks can emmetropise in monochromatic light.
In preliminary experiments carried out to test the hypothesis that ocular growth and refractive development might be influenced by the distribution of photon catch along photoreceptor outer segments, we have raised newborn chicks in lighting conditions that contained either an excess of longer wavelength red light or of shorter wavelength blue light, together with an adequate amount of mid-wavelength green light, to ensure that the focal plane for mid-wavelength green light was focused in the outer segment mid-points. Where chicks were raised in lighting conditions containing red and green wavelengths but little blue, if accommodation were determined by the green wavelengths, there would be a preponderance of red photons in the tips of relevant photoreceptor outer segments with a lack of balancing blue photons in the S-cone photoreceptor outer segment
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bases. Where chicks were raised in combined blue and green light without red wavelengths, the opposite would be the case.
Chicks were raised in a light-tight enclosure with a 12 hours on/12 hour off illumination cycle from banks of either red or blue emitting light emitting diodes (LEDs). The emission spectrum of red emitting LEDs contained wavelenghts between 575 nm and 700 nm with a peak emission at 640 nm. The emission spectrum of the blue emitting LEDs ranged between 430 nm and 550 nm with a peak emission at 490 nm. Luminance of red and blue emitting LEDs was equal. The enclosure was lined with high contrast black and white stripes, giving a range of spatial frequencies (depending on location of chicks within the enclosure) of 4–8 cycles/degree.
Our initial results support the hypothesis that development of the young eye is influenced by the distribution of photon catch along the photoreceptor outer segments, for those raised in light with a preponderance of longer wavelength red light (with some green) were myopic (–1.50 D to –2. 50 D at 14 days). In contrast those raised in light containing a preponderance of shorter wavelength blue light (and some green) that were hyperopic (+2.50 D to +3.50 D at 14 days). There was a highly significant difference in mean refraction between the two lighting conditions (p < 0.001) and a significant difference in mean vitreous chamber lengths, that in the myopic eyes of chicks raised in red plus green light were significantly longer than in the hyperopic eyes of chicks raised in blue plus green light (p < 0.01).
As already indicated an alternative explanation for the effect of chromaticity upon refractive development could be that a preponderance of red or blue light might produce an effect on ocular development by altering the balance between stimulated L-cones and S-cones rather than an imbalance of photon catch along the lengths of the outer segments. The fact that raising chicks in either pure monochromatic red or pure blue light (without the addition of any intermediate wavelenghts) has no effect upon eye growth or refractive development68 makes this explanation unlikely.
When the spectral emission characteristics of artificial light (tungsten lamps and the more recently introduced long-life fluorescent lamps) were examined, both types of artificial lighting were found to have a preponderance of red light in their emission spectra, a significant amount of midwavelength green emission and very little blue emission that might explain why indoor activity rather than close work is associated with the development of myopia, for a large proportion of indoor activity will be undertaken in conditions of artificial lighting.
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In contrast, when the spectral characteristics of outdoor scenes were analysed, they were found to contain a preponderance of shorter wavelengths of light in virtue of their predominately blue skies and green foliage. The spectral composition of light experienced during outdoor activity could be one explanation for the protective effect against myopia reported in recent studies. A study comparing time spent in outdoor activity with time spent in artificial light rather than time spent in reading might provide some interesting results.
We have investigated the spectral composition of outdoor scenes in various climatic conditions. In cloudy conditions, there is an equal amount of red, green or blue in the average outdoor scene. Not unexpectedly, in sunset scenes there is a preponderance of red light while in the average sunlit outdoor scene the largest contribution to spectral content is of blue wavelengths followed by a significant amount of green and a much reduced contribution of red. Thus, the average daylight scene with a predominantly blue sky and green foliage offers an additional explanation as to why outdoor activity appears to protect against the development of myopia. The studies that identified the protective role of outdoor activity were carried out in Ohio, USA,26 Australia25 and Singapore,27 locations where blue skies are the norm.
In a very large study of 3,636 school children aged between 6 and 18 years of age76 it was found that those children whose homes were lit by fluorescent lighting had an increased prevalence of hyperopia as compared to those whose homes were lit by tungsten lighting. The older types of fluorescent lights had a rather discontinuous emission spectrum with strong emission peaks at 450 nm and 550 nm and a broad less intense emission from 500 nm to 700 nm. The strong emission peaks at 450 nm and 550 nm might account for the increased hyperopia that was associated with fluorescent lighting. More recent types of fluorescent lamps have colour temperatures varying from 2700K to 6000K. Each has a different spectral emission depending on the phosphor coating. Those with lower colour temperatures with an excess of longer wavelength emission might be conducive to the development of myopia while those with a high colour temperature with more blue in their emission spectrum might be protective. In the absence of well designed trials the possible effects of different types of fluorescent lighting on refractive development remains speculative.
An interesting and as yet unexplained finding is that in more northerly or southerly countries (but not in near equatorial countries) those born in
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late summer months, when examined as adults, have a higher prevalence of myopia than those born in the winter.77,78
For the first few months of life, babies spend a large proportion of the day asleep and it is only by three months of age or so that the eyes are open for a large part of the day. Babies born in August (in northern countries) or in April (in southern latitudes) will be entering winter conditions by the time their eyes are open for most of the day. In winter, with a shortened period of daylight in non-tropical latitudes, babies of three months plus of age will be exposed for a significant part of the day to artificial lighting with a preponderance of longer wavelengths that could provide a ready explanation for the finding of an increased prevalence of myopia in those born in the summer but only in high and low latitudes where short days occur in the winter. In equatorial or near equatorial countries, the length of the day does not vary significantly with the season and this would explain the lack of any correlation between dates of birth and refraction in such countries, for there would be no seasonal variation in the amount of time throughout the year spent indoors or outdoors.
As already indicated, during outdoor activity with accommodative effort sufficient to achieve a sharp retinal image of near-to mid-distance objects, the images of distant objects will be focused in front of the retina, so inducing the myopic blur that appears to be protective against myopia. Thus, both the chromaticity of the light reaching the retina as suggested by others79 and its vergence from distant objects when the eye is accommodated for near-to mid-distance objects, are likely to play a role in the protective effect against myopia associated with outdoor activity.
If an increased photon catch in the tips of the photoreceptor outer segments as compared with their bases is a factor stimulating ocular elongation and myopia, it might be expected that those with protanopia or protonomaly in whom there is an absent or reduced sensitivity to red light might be more hyperopic (or less myopic) than the average person with normal color vision. A recent extensive study in high school students80 found a lower prevalence of myopia among students with red/green color deficiency than among normal controls with a significant difference in refractive error between the two groups. Additionally, those with protanopia or protanomaly had shorter axial lengths than did color normal students, confirming that ocular growth and refractive development is different among those with red/green color deficiency as compared with those with normal colour vision. This finding is in keeping with the