Light levels, refractive development, and myopia – A speculative review
Introduction
Recent studies from numerous groups have reported that outdoor activity is protective against myopia development in children (Deng et al., 2010; Dirani et al., 2009; French et al., 2013; Guggenheim et al., 2012; Jones et al., 2007; Mutti et al., 2002; Rose et al., 2008a) and, in animal models of myopia, that elevated light levels slow the rate of myopia development (Ashby et al., 2009; Ashby and Schaeffel, 2010; Siegwart et al., 2012; Smith et al., 2012). These results raise the issue of the how ambient light levels may affect the emmetropization mechanism, including normal refractive development and the response to myopiagenic stimuli.
In comparison with illuminance levels outdoors, indoor lighting experienced by humans is typically less than 1000 lux and often much less – in the range of 100–500 lux. This, of course, is far less than the light levels experienced outdoors during the daytime (130,000 lux and above in direct sun on a clear day, about 15,000 lux in the shade). Indeed, these are the levels that presumably were experienced by terrestrial vertebrate eyes throughout the evolution of the primate line. Most terrestrial creatures develop in a visual environment that ranges from high photopic light levels outdoors during the day to mesopic levels at dawn and dusk (or inside buildings) and scotopic levels at night unless artificial lighting is provided. Rather than considering outdoor illuminance levels to be “high” or “bright” or “elevated,” it is more appropriate to consider them as normal, and to consider “standard” indoor illuminance as low.
With the development of towns and cities, one may suppose that humans began to spend more time indoors, in lower-illuminance conditions; time spent indoors also appears to have increased with the development of indoor lighting and the development of non-agricultural indoor employment. Good visual acuity, needed for reading and other visual tasks that involve fine detail, is achieved with illuminances of approximately 100 lux–500 lux (Norton et al., 2002). Based at least in part on the increased costs involved in providing light levels above this point, indoor lighting for humans, and the lighting provided in the vivaria housing many of the animals used in studies of refractive development, are in this same illuminance range (Feldkaemper et al., 1999; Li and Howland, 2003; Morgan et al., 2004; Norton and McBrien, 1992; Schmid and Wildsoet, 1997; Smith, III et al., 2001) and, rarely, up to 1000 lux (Bitzer et al., 2000). The emerging reports of the protective effects of outdoor activity on myopia suggest that it is important to systematically explore the effect of illuminance levels above the low photopic levels experienced indoors.
In this review we suggest, as have Cohen et al. (2011, 2012) that the effects of illuminance on the emmetropization mechanism may form a continuum from scotopic and low photopic light levels, which foster the development myopic refractive errors, to the much higher illuminance levels experienced in the outdoors that affect refractive development, keeping eyes slightly hyperopic, and reduce the impact of myopiagenic stimuli. Indeed, in a 1999 paper on the effect of light levels on form-deprivation myopia in chicks, Feldkaemper et al. (1999) concluded, “Experiments show that the eye becomes more sensitive to image degradation at low light, the human eye may also be more prone to develop myopia if the light levels are low during extended periods of near work.”
Although the amount of light reaching the retina is presumably the key factor, it is difficult to measure the μW/cm2 of the many visible wavelengths that enter through the pupil and reach the retina. For convenience, illuminance (light falling on a surface) is a more easily measured quantity, indicating the amount of visible light (lumens) reaching an area of a surface (square meters) and corrected for the spectral sensitivity of humans: the lux. Illuminance levels from the sun on a clear day are approximately 130,000 lux (Birmingham, Alabama). Higher levels have also been reported (Dharani et al., 2012). In the shade on a sunny day, lux measured at the ground is typically 15,000–25,000 lux. Outdoors on a cloudy day it ranges from 10,000 to 40,000 lux. By comparison, indoor illuminance (100–500 lux) is very low.
Of course, most eyes are not pointed constantly toward the sky, but are aimed roughly parallel to the ground and mostly receive light reflected from objects. Light reaching the retina in this manner is lower, sometimes considerably so. Changes in pupil diameter also can alter the retinal illuminance by over 1 log unit. That said, the illuminance in lux can serve as an indicator of the upper limit of available light. This review will examine the relatively few studies that have varied the illuminance levels above and (in animal studies) slightly below standard indoor levels. Even though these indoor illuminance levels are, in an evolutionary sense, “low”, they are the levels at which most human and animal observations have been made and therefore serve as a standard level. By comparison, outdoor illuminance levels and the levels used in a few animal studies are “elevated” and we will refer to them as such.
Section snippets
Normal refractive development
The effects of illuminance on human refractive development occur against a background of changing refractive state in the months and years after birth. At birth, refractive state, measured with cycloplegia, is broadly distributed, ranging from low myopia (−1 to −4 D) to high hyperopia (up to 8 D) with a mean refraction of low (2 D) to moderate (3.5 D) hyperopia (Chen et al., 2011; Cook and Glasscock, 1951). This may reflect genetic factors that determine the location of the focal plane (corneal
Animal studies
Over the past 35 years there has been extensive characterization of the emmetropization mechanism in animal models, examining normal refractive development and induced myopia produced with form deprivation or negative lens-wear. However, the majority of these studies have used “standard” colony lighting that, from the present perspective, is quite low, in the range of 100–500 lux. Currently, we have only a very limited understanding of ambient illuminance as a variable that may affect the
Blur, and/or vitamin D levels
Several potential mechanisms have been suggested to explain the protective effects of outdoor activity against myopia in children. To the extent that hyperopic defocus on the retina from near targets contributes to axial elongation and myopia development in children, being outside with few nearby objects could remove that stimulus. In addition, the pupils would be expected to be smaller in the higher outdoor light levels, increasing the depth of focus and further reducing blur. These factors
Illuminance as a continuous variable
The research reviewed in the previous sections leads us to suggest that ambient light levels act as a continuous variable that, as light levels rise through the photopic range, has an increasing impact on the emmetropization mechanism (Fig. 2). The effect of rising illuminance is to shift the endpoint of normal refractive development toward hyperopia and to slow the response to myopiagenic stimuli. In this model it is assumed that illuminance varies on a circadian cycle with a period of low
Concluding comments
In this review, we have tried to integrate information from human epidemiological studies, from investigations using animals models of refractive development and myopia, and from studies of retinal circuitry to suggest ways in which illuminance levels may impact normal refractive development and the response to environmental myopiagenic stimuli. We recognize that the resulting model is incomplete and, no doubt, contains some incorrect conclusions. The intersection of illuminance levels,
Acknowledgments
Supported by NIH grants R01 EY005922 and P30 EY003039 (Core). We thank Alexander H. Ward for participation in the tree shrew elevated light level study and in preliminary dopamine studies and Dr. Michael R. Frost for helpful comments on the manuscript and assistance in figure preparation. We also thank two anonymous reviewers for their insightful and helpful comments.
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