Few would dispute that if the human visual system is to function at its maximal potential efficiency under all conditions without the use of optical aids, a sharply focused optical image on the retina is required. Thus, we might naively expect that the long process of evolution would have led to an eye which, with accommodation relaxed, was emmetropic. Furthermore, the eye would possess a rapidly responding accommodation system capable of producing an appropriate change in focus when near objects were observed. Although, in practice, these “ideal” goals are not perfectly achieved, actual performance approximates reasonably closely to the ideal, at least in younger eyes. In particular, rather than refractive errors being normally distributed, in adulthood, they show a strong excess near emmetropia, even though in infancy this is much less well marked.1 Moreover, under photopic conditions, the young eye changes focus in the correct direction within about 1 s when viewing objects at different distances, even though geometrical optical blur is nominally independent of the sign of defocus.
How, then, does the growing eye develop toward an approximately emmetropic state, so that distant objects are in reasonable focus on the retina? How is the correct balance in the growth rates of the components of the eye's optical system maintained? How does the accommodation system resolve the sign ambiguity inherent in optical defocus and respond in the correct direction with the right change in ocular power? Do these processes have anything in common or are the mechanisms entirely different? Much effort has been devoted to attempts to find answers to these questions, not least because the solutions might aid our understanding of the problem of the increasing prevalence of myopia in many parts of the modern world.1–3
It is pertinent here to compare first the accuracies of emmetropization and accommodation. Extensive 20th century studies in unselected populations confirmed that although individual ocular parameters were each normally distributed, the combined refractions were not: they showed an excess of low hyperopia (including about 75% of the population) in the refractive range 0 to +2 diopters (D).4 Given the fact that most eyes show a tonic accommodation of about 1 D in the absence of an adequate accommodative stimulus,5 this suggests that normal refractive development can produce the required distance focus to an accuracy of around ±1 D. It is also striking that the refraction of both eyes develops similarly, with roughly 75% of the population having anisometropia ≤0.25 D.6 The accuracy of accommodation is more variable, because it depends on the stimulus and observing conditions. Although sometimes errors are very small, lags of up to 1 D are not unusual.7 Thus, the errors of focus inherent in the emmetropization and accommodation mechanisms are broadly similar. It must, of course, be remembered that, in the presence of ocular monochromatic and chromatic aberration, there is some ambiguity in what constitutes “best” focus. In the presence of spherical aberration, for example, “best” focus will be spatial frequency dependent, whereas longitudinal chromatic aberration means that there is a focus difference of around 2 D across the visible spectrum, with the eye being relatively hyperopic for the red and myopic for the blue. These factors, in combination with the influence of diffraction, mean that ocular depth of focus approaches ±0.5 D under many circumstances and that larger amounts of defocus blur are often acceptable, particularly when the pupil diameter is small.8–10 In general, then, emmetropization and accommodation are capable of achieving an accuracy of focus which, until the onset of presbyopia, is acceptable for the needs of a substantial proportion of the population.
How emmetropization is achieved has long been a matter of dispute, with both genetic and environmental factors having their supporters. For example, Sorsby11 was a strong advocate of a genetic origin and felt justified in stating robustly “The traditional emphasis on environmental factors as productive of refractive error finds no support in the detailed studies of today.” Subsequent experiments with animals have, however, firmly established that final refractive state depends on both genetics and on visual experience after birth12–14: it may be that other, as yet inadequately explored, factors such as diet15 also play a role. Earlier animal work concentrated on the effects of foveal form deprivation. Later, manipulation by lenses of the axial state of focus showed that appropriately accelerated or retarded eye growth could occur to minimize the resultant errors of focus.12,13 Thus emmetropization must involve an active feedback process, dependent in some way on the retinal image, which can potentially be manipulated, either by accident or design, to produce a non-emmetropic refractive endpoint. Further animal studies showed that appropriate eye growth could still be achieved in the absence of an intact optical nerve or accommodation system. This implies that control of growth must be at the retinal level,16 although there is evidence that some refinement appears to be possible if the higher centers are also involved.17
This picture of development in terms of foveal focus alone underwent radical modification when it was shown that application of lenses that covered only part of the visual field produced growth changes only in the corresponding part of the eye.18,19 Moreover, the long-neglected work of Hoogerheide et al.20 had earlier suggested that the peripheral refraction of trainee pilots was a good predictor of whether they would tend to become more myopic during the course of their training. Those pilots with relative hyperopia in their peripheral field were more likely to undergo a myopic change. These findings, and other related work, have led to the suggestions that, by analogy with the axial findings in animals, a “hyperopic” image, which lay behind the peripheral retina would cause excessive local growth which, because of the general constraints on eyeball shape, would in turn tend to increase the axial length and lead to myopia.14,21–23 Animal experiments with monkeys support the view that the retinal periphery plays a substantial role in refractive development and that an intact fovea is not necessary for emmetropization to occur.24–26 It may also be relevant that children suffering from diseases causing peripheral or peripheral plus central impairment of vision tend to become myopic.27
The idea that peripheral focus is an important part of normal emmetropization still does not answer the basic question of how the signals to control growth might be derived from an initially defocused optical image.28 Here, Howland has recently made what may be a significant contribution to the debate.29 Although there has been a tendency to talk about peripheral hyperopia or myopia, as though peripheral refractive errors are purely spherical, Howland points out that, like all optical systems, the eye suffers from oblique astigmatism. It, therefore, has two image surfaces containing the sagittal (radial) and tangential focal lines, separated by the interval of Sturm. The magnitude of the astigmatism in dioptric terms varies roughly as the square of the field angle, and amounts to about 5 D at a field angle of 60°: the tangential focus is relatively myopic with respect to the sagittal focus.30 Howland notes further that there is good evidence for the existence of neurons tuned to different orientations in the peripheral retina. Suppose, then, that the signals from those neurons responding to radially and tangentially oriented edges or other structures are compared. If the eyeball is too short, the “tangential” neurons will respond strongly and the “radial” neurons more weakly. Comparison of these outputs will yield a difference signal which tells the eyeball to grow. If, however, the eyeball is already too long, the signal from the “radial” neutrons will dominate over the “tangential” signal, yielding a difference signal that slows growth. Only when the difference in the output signals of the two neuron populations approaches zero will growth stabilize, this corresponding to the situation where the two image surfaces lie symmetrically in front and behind the retina. In this situation, which is typical of emmetropic eyes,30,31 the circle of least confusion lies close to the retina. This is advantageous, because detection is quite sensitive to focus in the periphery although resolution is not.32
One attractive feature of this suggested mechanism is that it is robust against changes in pupil diameter with light level, whereas this is not the case with possible mechanisms involving the Stiles-Crawford effect, higher order aberrations or chromatic aberration.22,28 The retina is known to be able to perform quite complex local processing, e.g., for the detection of looming objects,33 so the existence of the appropriate circuitry for comparing local radial and tangential image quality is plausible. Note too that the parsimonious assumption is made that the proposed mechanism controls only the growth of the vitreous chamber, the growth of the other components of the eye's optical system being under genetic control. Within limits, this automatically achieves the correct balance between the different growth rates, which is required for emmetropia, and gives the appropriate correlation between component values. A variety of different combinations of anterior component values can still lead to an emmetropic eye, as observed in practice.34,35 From the clinical point of view, if further work supports the concept that the peripheral refraction influences refractive development, then measures to control myopia development by modifying the peripheral refraction in an appropriate way, through such means as specially designed contact or spectacle lenses, become attractive.36,37
Could there be links here with the way in which accommodation resolves the ambiguity of blur information to respond with the appropriate magnitude of accommodation or disaccommodation response? This appears unlikely in view of the different demands on the two focusing mechanisms. Although in emmetropization defocus signals must be integrated over considerable periods of time, in accommodation, the response occurs in <1 s. Moreover, accommodation responses must be dominated by the foveal image. This necessity can be appreciated if we consider a typical domestic indoor visual environment, where there will be wide variations in the accommodation stimuli presented at different points in the field. A task like threading a needle would become impossible if the accommodation response was influenced by the disparate competing accommodation stimuli in the peripheral field. In fact, studies in which isolated peripheral accommodation stimuli are presented in an otherwise stimulus-free field suggest that the response weakens steadily with the target's field angle, to fall to a low level at about 15°. When the field contains both peripheral and axial stimuli, the response is largely controlled by the axial stimulus, although peripheral stimuli within a few degrees of the axial stimulus do have some influence on the response.38
Note here a further important difference from emmetropization, assuming that the latter does depend on focus in the peripheral retina. In this case, if the eye was only exposed to an indoors environment, with its typical variation in distance of objects from the eye across the visual field, there could be no systematic pattern of defocus across the retina. Indeed, each time fixation was varied across the visual scene the defocus on different parts of the peripheral retina would vary, even if accommodation maintained an accurate foveal focus. Only in an outdoor environment, with most of the object field lying close to optical infinity, will there be a consistent pattern of focus across the retina, this pattern being essentially unchanged as fixation changes to bring the images of different distant objects onto the fovea. Such a situation is obviously required for relatively slow-acting, peripherally driven emmetropization to be effective. Thus, it would be anticipated that a condition for any emmetropization mechanism based on peripheral imagery is that there should be reasonable periods of outdoor activity. This accords with studies suggesting that longer periods of outdoor activity inhibit myopia development.39–41
Returning to accommodation, what sort of odd-error cues does the system make use of to guide the direction of the dynamic response? Although claims are sometimes made that one particular cue is of major importance, it appears probable that different individuals place different weights on different cues and that this weighting may change when the cue that they normally use is absent. Thus experiments under monocular conditions show that although chromatic aberration may be useful, most people soon learn to use other cues, like small amounts of astigmatism or higher order aberration, as alternatives.42,43 Under binocular conditions, disparity cues become available. Most real-world situations additionally contain a rich variety of proximity and other perceptual cues. What is, perhaps, surprising is that some subjects in monocular laboratory studies fail to accommodate at all to changes in real-space stimuli, despite their having normal accommodation as judged by clinical tests. This suggests the possible absence of any true reflex accommodation and that all accommodation may demand a voluntary input.
To summarize, although the mechanisms of emmetropization and accommodation both involve the ideal end point of a well-focused retinal image, they differ in many respects. The hypothesis that the state of focus in the peripheral retina plays an important role in the emmetropization process appears promising. There is the exciting possibility that, if further studies support this suggestion, control of myopia development might become possible through, e.g., the wear of corrections designed to modify relative peripheral refraction as well as correcting axial errors.36,37
W. Neil Charman
Faculty of Life Sciences
University of Manchester PO Box 88
Manchester M60 1QD, United Kingdom
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