Development of Visual Resolution11 RICHARD HELD Massachusetts Institute of Technology
ABSTRACT
Increased interest in early visual development has been triggered by new findings concerning the neuronal mechanisms of the visual system and the control of their development by both maturational and environmental influences. Visual acuity is the most basic measure of the developing pattern vision of the human infant. Methods of measuring acuity in infants have been improved in recent years and new data have been produced. These methods include the visually evoked potential, use of the optokinetic response, and application of the preferential looking procedure. The preferential looking procedure is based upon the assumption that an infant will prefer to look at a patterned stimulus over an otherwise equivalent but blank stimulus as long as the former is resolvable. Our research group has found evidence that the assumption is not always true, a result which indicates that the method as generally used yields conservative measures of acuity. It also implies that a fast method of measurement can be used reliably. Procedures for measuring acuity in infants have been applied not only to infants without visual problems but also to study the effects of ocular anomalies, including astigmatism, occlusion, and strabismus. The ability to resolve detail is fundamental to pattern perception and to all the capaci-
ties that depend upon it: recognition of objects, faces, print, script, and so on. Consequently, measures of resolution tell us about a basic capacity that limits many achievements of a higher order and the increase of resolution during development allows progressive improvement of these achievements. The most common measure of resolution is visual acuity (Riggs, 1965), and perhaps the best known test of acuity involves the Snellen chart and its variants. Letters or numbers of graded size are presented at a fixed distance to an observer who reports the smallest that he can discern. The Snellen number represents the fraction of normal vision, defined as unity (20/20), shown by an observer. A more precise technique of measuring acuity will be discussed in this paper; it consists of presenting gratings of alternating dark and light stripes of equal width. The acuity threshold, then, is the grating with the narrowest stripes that can be detected 50% of the time it is presented. When it is not detected, it appears indiscriminable from a blank field of equal luminance (brightness). Gratings are usually specified by their spatial frequency in cycles per degree of visual angle, where a cycle consists of one dark and one light stripe. Normal adult acuity is considered 30 cycles per degree corresponding to 20/20 Snellen. The gratings used for research often consist of changes in luminance that are sinusoidal (Braddick, Campbell, & Atkinson, 1978), but, for practical purposes, square wave gratings consisting of abrupt transitions from higher to lower luminances are frequently used.1
*The research reported from the laboratory of the author was supported by grants from the National Institutes of Health (No. EY-02649, No. EY-01191, and No. EY-02621) and from the Spencer Foundation (No. LTR-DTD71373)-
'It should be mentioned here that visual acuity is but the extreme value on a function that defines what is called contrast sensitivity. Acuity is tested with the use of high contrast (black-white) test patterns (gratings or otherwise). When the contrast is lowered, only coarser detail can be detected and the highest spatial frequency of a grating that can be seen is lowered. The contrast sensitivity function describes the variation in the maximum detectable spatial frequency of the test grating as contrast is varied from low to high (Braddick et al., 1978).
Canad. J. Psychol./Rev. canad. Psychol., 1979, 33 (4)
213
ACUITY IN INFANTS AND YOUNG CHILDREN
With individuals who understand verbal instructions, standard psychophysical procedures are used to measure acuity. With human infants as with animals, other procedures must be used. But, unlike research with animals, prolonged and arduous experimentation is out of the question with human infants. Given these requirements, three procedures have proven useful although they by no means exhaust the possibilities. Preference Method
It has long been known that an infant prefers to gaze at a patterned region in his field of vision rather than a blank area, under a variety of experimental conditions (Stirnimann, 1944; Fantz, Ordy, & Udelf, 1962). Various procedures have been developed in recent years to exploit this preference for pattern. If a grating stimulus is paired with an otherwise equivalent blank field, the infant should preferentially look at the grating as long as it is resolvable. When no longer resolvable the preference should be 50%. Much of the research using this method to measure acuity is summarized by Dobson and Teller (1978). Contrast sensitivity functions have been obtained by Atkinson, Braddick, and Moar (1977) and by Banks and Salapatek (1978). If two gratings which differ in some respect such as stripe orientation are presented together, a difference in their visibilities results in preferential fixation on the more visible one (Gwiazda, Brill, Mohindra, & Held, 1978; Leehey, Moskowitz-Cook, Brill, & Held, 1975). This procedure has proven quite sensitive to small differences in visibility. We have also developed a five-minute preferential viewing procedure which allows us to test the acuity of infants between birth and one year (Gwiazda, Wolfe, Brill, Mohindra, & Held, in press (a)). It has been valuable in studying infants with ocular anomalies such as astigmatism, in which 214
the optically uncorrected retinal image can never be focused simultaneously in all orientations; occlusion, in which one eye is covered for a period of time; strabismus, in which the eyes do not look in the same direction at the object of regard; and anisometropia, in which the refractive power of the two eyes differs. Visually Evoked Potential
Patterns that are flashed on and off evoke an electrical response in the visual part of the brain which can be recorded with electrodes placed on the subject's scalp. By varying the size of the pattern elements and observing the parameters of the electrical response, it is possible to derive a measure of sensitivity in adults that correlates well with measures of visual acuity (Campbell & Maffei, 1970). This technique is usable with infants since no instructions are required (Pirchio, Spinelli, Fiorentini, & Maffei, 1978). The procedure has generally shown substantially higher acuity in infants and earlier achievement of adult levels than the preference technique (Dobson & Teller, 1978). Optokinetic Response
If a patterned stimulus moves across the retina at an appreciable velocity, it induces a series of pursuit eye movements followed by a saccade back to the original position. No other voluntary response is needed on the part of the observer aside from gazing at the stimulus to effect the appropriate accommodation of the lens of the eye needed to focus the stimulus on the retina. This procedure has been used extensively to study acuity in infants since the optokinetic response ceases when the detail of the pattern that evokes it becomes too fine to be detected. Measures of acuity taken by means of this response agree rather well with those obtained using the looking preference procedure (Dobson & Teller, 1978). R. Held
20 30 AGE (weeks)
FIGURE 1 Median spatial frequencies of looking preferences from grouped data as a function of age and grating orientation. Main axes medians combined those from horizontal and vertical gratings. Error bars represent semi-interquartile ranges. (Reprinted by permission of American Journal of Optometry and Physiological Optics)
DEVELOPMENT OF ACUITY
THE PATTERN PREFERENCE
Beginning at birth, growth of acuity with age is universally observed (Dobson & Teller, 1978), and explanation of this growth is an important subject for research. The preferential viewing technique developed by our group allows us to test infants ranging in age from a few weeks up to at least one year. This technique differs from others in at least one important respect. The grating stimulus is paired with either a blank field or another grating of equal space-averaged luminance in an otherwise darkened room (Leehey et al., 1975; Gwiazda et al., 1978). In the absence of other illuminated objects, the infants have little to attend to other than the intended stimuli. Using this technique we have demonstrated the growth of acuity during the first year as well as the differential rate of growth of acuity for oblique as opposed to main axis gratings. Using the fast procedure developed recently, we have obtained the data shown in Figure 1 from a group of infants without serious refractive or other ocular problems (Gwiazda, Brill, Mohindra, & Held, in press (b)). These data constitute a norm against which can be compared the acuities of infants suffering from ocular anomalies.
ASSUMPTION
Development of visual resolution
Anomalous findings recently led us to question the assumption that infants always prefer to gaze at a visible pattern over a blank field. Using the method of constant stimuli, we therefore gathered data over a set of frequencies ranging to higher values than appeared to be necessary in order to approach 50% preference. A typical subject's results are shown in Figure 2. The infant clearly did not prefer to look at the grating at the higher frequencies. The infant preferred to look at the blank field at at least one frequency, a response that is just as indicative of discrimination and detection of the grating as is a preference for looking at it. This result has since been replicated many times (Held, Gwiazda, Brill, Mohindra, & Wolfe, 1979)- We do not yet know why the preference is reversed at the higher spatial frequencies, but the result has two important implications. The dip below 50% stabilizes the termination of the staircase process used in the fast procedure for measuring acuity (Gwiazda et al., in press (a)). And the preference method will underestimate acuity if the stimulus set does not include gratings of frequencies
215
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higher than those that elicit a preference of 50% or more. The underestimation may in part account for the discrepancy between the values of acuity obtained with preference techniques and those obtained with the visually evoked potential. Differences in threshold criteria may also help account for it. While the preference method remains of great value, we must bear in mind that it has yielded conservative values for acuity. ANOMALIES OF VISION AND OCULOMOTOR COORDINATION
During the last two decades discoveries in the visual system, particularly in the cortex, have set the stage for discoveries concerning the effects of anomalous conditions of vision. Most of this work has involved the cat and monkey visual system (Wiesel & Hubel, 1965; von Noorden, 1973)- It is now known that monocular occlusion soon after birth can result in irreversible loss of bino216
cularity and of the ability for stimulation of the deprived eye to excite cortical cells. Furthermore, the behaviour of monocularly deprived animals demonstrates losses in acuity and discrimination that parallel the single cell results (Dews & Wiesel, 1970; Mitchell, 1978). Artificially induced strabismus has been shown to reduce greatly the number of cells that respond to stimulation of both eyes (Hubel & Wiesel, 1965; Baker, Grigg, & von Noorden, 1974). And it has been claimed that such strabismus can cause amblyopia (reduced acuity not attributable to either optical or peripheral problems) in the deviating eye (von Noorden & Dowling, 1970). Only during a critical period (approximately the fourth through twelfth week in the cat) does the animal display adverse reactions to these forms of visual deprivation (Wiesel & Hubel, 1963, 1965). Older animals deprived of pattern vision for long periods of time show few, if any, of the R. Held
morphological, physiological, and behavioural deficits found in animals deprived during the critical period. Thus, it is thought that once the visual pathways are fully developed, they remain intact even when not in use for prolonged periods of time. Following demonstration of the impressive effects of deprivation on binocular vision, attempts have been made to demonstrate that development of other aspects of vision depend upon exposure to the normal environment. The best known of these are the stripe-reared kittens of Blakemore and Cooper (1970) and of Hirsch and Spinelli (1971). It was claimed that kittens able to view stripes of only one orientation failed to develop cells responsive to edges of other orientations, particularly those near the orthogonal axis. However, a somewhat amended view of this claim is presented in a more recent publication (Stryker, Sherk, Leventhal, & Hirsch, 1978). In the wake of these demonstrations of the plasticity of the developing visual system in animals, researchers have actively sought to explore possible parallels in human vision, and several have been proposed and studied. The new techniques for studying infants' acuity enable researchers to study the development of vision under normal and anomalous conditions and to look for results analogous to those of the animal studies. We have been interested in four of the proposed human parallels: the oblique effect, the meridional amblyopia apparently resulting from chronic astigmatism, the amblyopia resulting from the form of strabismus known as esotropia (crosseyedness in which one eye turns in towards the nose), and the effects of occlusion of one eye. These four will be discussed in turn. The Oblique Effect
Visual acuity in adult human observers can be tested with gratings of varied orientations in the frontal plane. When this is done, gratings tilted off the vertical and Development of visual resolution
horizontal axes are resolved less effectively than those aligned with them; acuity for oblique gratings is generally reduced by 1 o to 20%. Following announcement of the results from experiments with stripereared kittens, claims were made that the oblique effect resulted from exposure to the urban world since horizontal and vertical lines occur more frequently than obliques in city environments. The argument appeared to be clinched by the claim that Cree Indians of northern Canada who live in huts with oblique sides have less of an oblique effect than a sample of urbanliving Caucasians (Annis & Frost, 1973). Using the technique for measuring acuity in infants, we tested whether exposure to the environment produces the oblique effect. If experience were responsible, then reduced acuity on the oblique should not occur until some time after birth when sufficient exposure to the environment had occurred. One of the results of measuring acuity for both main axis and oblique gratings is shown in Figure 1, summarizing data for a group of normal infants. By six months of age, acuity for oblique gratings is less than that for vertical and horizontal ones and remains so (Gwiazda et al., in press (a)). Other tests directly pairing oblique and main-axes gratings indicate a preference for the main-axes gratings as early as the second month (Leehey et al., 1975; Gwiazda et al., 1978). Given this early onset of the oblique effect, it is safe to conclude that its underlying substrate develops independently of specially biased environments. It seems unlikely that infants are systematically exposed to the appropriately biased set of oriented contours prior to a few months of age. Recently, Timney and Muir (1976) discovered that a group of Chinese individuals from Hong Kong showed reduced oblique effect relative to a Caucasian group. If we ask what is common to Cree Indians and Hong Kong Chinese the answer is, of course, that they are both of Mongoloid origin. Taken together with our argument 217
that the effect develops endogenously, the racial difference suggests a genetic origin for the difference in magnitude of the oblique effect between Cree Indians and urban Caucasians.
sate for the high incidence of astigmatism early in life (Mohindra, Held, Gwiazda, 8c Brill, 1978). In any event, this high incidence has allowed us to measure acuity and its development in a large number of astigmatic infants. Meridional Amblyopia The optical blurring effects of the astigA second analogy to the stripe-reared kitten matism are made quite evident by the reexperiment is the very considerable loss of duced acuity along selected orientations. acuity (as much as one-half normal) in the However, we have yet to detect any sign of habitually blurred meridia of chronic amblyopia in astigmatic infants (up to one astigmatic observers. In astigmatism, the year of age). The earliest evidence we have optics of the eye are not perfectly spherical found for this form of amblyopia occurred but possess a cylindrical component. in a child two years, ten months old. ConseTherefore, only edges of one orientation in quently, we tentatively conclude that susthe frontal plane can be sharply focused at ceptibility to this form of amblyopia has its any given time. Moreover, certain orientaonset sometime after the first year and betions tend to be habitually out of focus and fore the third year of life. This delayed consequently blurred. Many astigmatic susceptibility contrasts strongly, as we shall adults show losses of acuity despite optical discuss, with the earlier onset of amblyopia correction for edges in the habitually blurred resulting from either strabismus or occluorientations (Mitchell, Freeman, Millodot, sion of one eye. & Haegerstrom, 1973), a state of affairs known as meridional amblyopia. The Amblyopia Accompanying Esotropia amblyopia is specific to the blurred meridia It has long been known that amblyopia frealthough the meridia may vary widely quently accompanies crosseyedness, but the among different observers. There is consecausal relation between the two has been quently a strong presumption that the ambiguous. It is unclear whether one amblyopia is produced by the habitual blurcauses the other or whether both are caused ring. by a third factor. The availability of a technique for measuring acuity, hence The questions to be answered then are: amblyopia, in infants may help to establish When does astigmatism induce meridional at least one causal sequence. amblyopia and what is the critical period during which the visual system is sensitive We have tested the acuity of each eye of a to blurring on selected orientations? The series of infants with constant esotropia. In answers are to be found by studying a samthese infants one eye (the deviating one) ple of astigmats from as early as possible turns too far inward towards the nose and until the onset and cessation of susceptibilremains that way. The non-deviating eye ity to amblyopia. The procedure involves fixates objects of interest. Some of these using our tests of acuity with and without infants appear in the clinic at a few months optical correction for the astigmatism. of age and at first testing may show no appreciable difference in acuity between The incidence of clinically significant the two eyes. However, byfiveor six months astigmatism in the adult population is of age, all of those whom we have tested approximately 10%; we expected to find a begin to show significant differences in similar incidence in infants. To our surprise acuity between the eyes in favour of the we found that the incidence was roughly five times the adult amount, implying that non-deviating (fixating) eye (Fig. 3). The fact that the strabismic condition existed for some naturally corrective process occurs some time before the development of during the first few years of life to compen218
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amblyopia hints that the former caused the latter, although this conclusion is far from firm. Both conditions might have a common and independent underlying cause, but the amblyopia may not appear until the level of acuity appropriate to the five- or six-month-old (between 4 and 6 cycles/degree) is reached. The effects of strabismus on binocularity, including loss of stereovision and lessened interocular transfer of tilt aftereffects, have been documented in the literature on adult vision (Banks, Aslin, & Letson, 1975; Hohmann & Creutzfeld, 1975). Discovery of the consequences of strabismus for infant vision await the development of simple and efficient procedures for measuring binocularity in infants. Fox, Aslin, Shea, and Dumais (1980) have developed a stereopsis test which may prove useful in this connection. Very recently we have developed a test for stereoacuity in infants which promises to provide a very sensitive test for binocularity (Birch, Gwiazda, & Held, in press). The Effects of Monocular Occlusion
At least one retrospective analysis of the consequences of monocular occlusion has Development of visual resolution
been made (Awaya, Miyake, Shiose, Kanda, & Kawase, 1976); it suggests that even very short periods (one week) of occlusion can cause permanent visual deficits. We have studied the acuities of several infants who have had one eye patched for varying periods of time as a common form of therapy for early strabismus. All of these infants were constant esotropes showing differences in acuity favouring the non-deviating eye. The result, without exception, was an increase in acuity of the deviating eye with a concomitant reduction of acuity in the patched eye (Thomas, Mohindra, & Held, 1979). In other words, a tradeoff of acuities took place in which the acuity of one eye appeared to gain at the expense of the other eye (Fig. 3). Such a tradeoff has been suggested in the clinical literature (Michaels, 1975), but to the best of our knowledge this is the first demonstration of it. The deviating eye appears to return to its previous level of acuity following permanent removal of the occluder in the absence of complicating factors. However, the acuity of the previously patched eye may increase to levels above what is normally to be expected (Fig. 3). We have so far no adequate explanation of the latter phenomenon. The early strabismus, followed by the patching treatment, and finally by removal of the patch, seems to release the nondeviating eye from an inhibitory influence. Perhaps a reduction of binocularity, such as is seen in adult esotropes, accounts for this release. SUMMARY AND DISCUSSION
We have reviewed the state of the art with regard to measures of visual resolution in infants. These measures can now be made quickly and reliably with a number of procedures including visual preference which we have emphasized. Normative data have been obtained on a large number of infants using the preference procedure which shows that acuity begins at about 20/1200 Snellen (1/2 cycle/degree) soon after birth
219
and rises monotonically to at least 20/50 Snellen (12 cycles/degree) by the end of the first year. Acuity for oblique gratings begins to fall below that of main axes gratings at about six months of age. These data probably underestimate acuity because of the reversal of preference from grating to blank field at the upper end of the range of spatial frequencies. The results obtained on infants without serious ocular anomalies have been followed up with studies of infants suffering from astigmatism. The blurring effects of astigmatism can be detected quite early in the form of reduced acuity in the blurred meridia. But we have not found meridional amblyopia occurring in the first year of life; the earliest we have seen it is late in the third year. Infants suffering from a form of strabismus known as constant esotropia are found to develop differences in acuity between the eyes in the first semester of life. The deviating eye always shows the lower acuity, which we presume represents an early form of amblyopia. When the non-deviating eye is occluded by patching, the other eye improves in acuity but at the expense of the occluded eye. Finally, removal of the patch can result in a return to the earlier difference between the acuities of the two eyes. Our experience with the esotropic infants strikingly demonstrates the plasticity of the visual system with regard to visual function during this stage of life. Compared to this early susceptibility, meridional amblyopia runs a much delayed time course. Visual deprivation studies using animals have clearly demonstrated consequent changes at the cellular level. To understand the consequences of these changes for vision, alterations in the functioning of the whole system must be studied. The research discussed above on the development of vision in the human infant and child represents one step in this direction. RESUME L'interet accru pour le developpement visuel
220
precoce s'est declenche par de nouvelles donnees concernant les mecanismes neurologiques du systeme visuel et le controle du developpement de ces mecanismes par des influences relevant aussi bien de la maturation que de l'environnement. L'acuite visuelle est la mesure la plus fondamentale du developpement de la vision des patterns par le nourrisson. Les methodes employees pour obtenir cette mesure se sont ameliorees au cours des dernieres annees et de nouvelles donnees ont ete recueillies. Parmi ces methodes, on peut souligner le potentiel evoque, la reponse optocinetique et l'observation differentielle. Cette derniere technique est fondee sur le postulat qu'un nourrisson preferera regarder un stimulus complexe (un pattern) qu'un stimulus uni, mais equivalent par ailleurs, dans la mesure ou le premier peut etre analyse. Notre groupe de recherche a pu montrer que ce postulat n'est pas toujours vrai, ce qui indiquerait que l'usage habituel qu'on fait de cette methode donne une mesure conservatrice de l'acuite et done qu'une technique de mesure rapide peut etre fiable. Des techniques de mesure de l'acuite ont ete appliquees non seulement a des nourrissons non affectes de problemes visuels, mais aussi a des nourrissons atteints de troubles oculaires tels que 1'astigmatisme, Pocclusion, et le strabisme. REFERENCES ANNIS, R.c, & FROST, B. Human visual ecology and orientation anisotropies in acuity. Science, 1973,182, 729-731 ATKINSON, j . , BRADDICK, o., & MOAR, K. Development of
contrast sensitivity over thefirstthree months of life in the human infant. VisionRes., 1977,17(9), 10371044 AWAYA, S., MIYAKE, Y., SHIOSE, Y., KANDA, T . , & KAWASE,
Y. Stimulus deprivation amblyopia in man. Proc. Second Congress ofInternational StrabismologicalAssoc.,
1976 BAKER, F.H., GRIGG, P., & VON NOORDEN, G.K. Effects o f
visual deprivation and strabismus on the response of neurons in the visual cortex of the monkey, including studies on the striate and prestriate cortex in the normal animal. BrainRes., 1974,66,185—208 BANKS, M., ASLIN, R., Be LETSON, R. Sensitive period for
the development of human binocular vision. Science, 1975,190,675-677 BANKS, M.S., & SALAPATEK, P. Acuity and contrast sensitivity in 1,2, and 3 month old human infants. Investigative Ophthal., 1978,17(4), 361-365 BIRCH, E.E., GWIAZDA.J., & HELD, R. Stereoacuity of
human infants. To be presented at meeting of Optical Society, 30 April—3 May, 1980 BLAKEMORE, c , & COOPER, G.F. Development of the
brain depends on the visual environment. Nature, 1970,8*8,477-478
R. Held
BRADDICK, o., CAMPBELL, F.W., & ATKINSON,]. Channels
in vision: Basic aspects. In R. HELD, H.W. LEIBOWITZ, & H.-L. TEUBER (eds.), Perception. (Handbook of sensory physiology; Vol. 8). Berlin-Heidelberg: Springer-Verlag, 1978 CAMPBELL, F.w., & MAFFEi, L. Electrophysiological evidence for the existence of orientation and size detectors in the human visual system. Journal ofPhysiology, 1970,207,635-652 DEWS, P.B., & WIESEL, T.N. Consequences of monocular
deprivation on visual behaviour in kittens.y. Physiol., 1970,206,437-455 DOBSON, v., & TELLER, D. Y. Visual acuity in human infants: A review and comparison of behavioral and electrophysiological studies. Vision Res., 1978,18, 1469-1483 FANTZ, R.L., ORDY, J.M., & UDELF, M.S. Maturation of
pattern vision in infants during the first six months. J. comp. physiol. Psychol., 1962,55(6), 907—917 FOX, R., ASLIN, R.N., SHEA, S.L., & DUMAIS, S.T. Stereopsis
in human infants. Science, 1980,207,323—324 GWIAZDA,J., BRILL, S., MOHINDRA, I., & HELD, R. I n f a n t
visual acuity and its meridional variation. Vision Res., 1978,18,1557-1564 GWIAZDA,J., BRILL, s., MOHINDRA, i., & HELD, R. Pre-
ferential looking acuity in infants from 2 to 58 weeks of age. Am.]. Optom. physiol. Optics, in press, (a) GWIAZDA,J., WOLFE,J., BRILL, S., MOHINDRA, I., & HELD,
R. Quick assessment of preferential looking acuity in infants. Am.J. Optom. physiol. Optics, in press, (b)
MICHAELS, D.D. Visual optics and refraction: A clinical approach. San Pedro: Mosby, 1975 MITCHELL, D.E. Effect of early visual experience on the development of certain perceptual abilities in animals and man. In R.D. WALK & H. j . PICK, JR. (Eds.),
Perception and experience. New York: Plenum Publishing Corp., 1978. MITCHELL, D.E., FREEMAN, R.D., MILLODOT, M., &
HAEGERSTROM, G. Meridional amblyopia: Evidence for modification of the human visual system by early visual experience. VisionRes., 1973,13,535-558 MOHINDRA, L, HELD, R., GWIAZDA,J., & BRILL, s. Astig-
matism in infants. Science, 1978,202,329—331 PIRCHIO, M., SPINELLI, D., FIORENTINl, A., & MAFFEI, L.
Infant contrast sensitivity evaluated by evoked potentials. Brain Res., 1978,141,179-184 RIGGS, L.A. Visual Acuity. In C.H. GRAHAM (Ed.), Vision and visual perception. New York: Wiley, 1965 STIRNIMANN, F. Ueberdas Farbenempfinden Neugeborener. Ann. Paedia., 1944,163,1—25 STRYKER, M.P., SHERK, H., LEVENTHAL, A.G., & HIRSCH, H.
Physiological consequences for the cat's visual cortex of effectively restricting early visual experience with oriented contours. J. Neurophysiol., 1978,41, 8g6— 99 THOMAS,J., MOHINDRA, I., & HELD, R. S t r a b i s m i c
amblyopia in infants. Am.J. Optom. physiol. Optics, 1
979.56
ABSTRACT
Increased interest in early visual development has been triggered by new findings concerning the neuronal mechanisms of the visual system and the control of their development by both maturational and environmental influences. Visual acuity is the most basic measure of the developing pattern vision of the human infant. Methods of measuring acuity in infants have been improved in recent years and new data have been produced. These methods include the visually evoked potential, use of the optokinetic response, and application of the preferential looking procedure. The preferential looking procedure is based upon the assumption that an infant will prefer to look at a patterned stimulus over an otherwise equivalent but blank stimulus as long as the former is resolvable. Our research group has found evidence that the assumption is not always true, a result which indicates that the method as generally used yields conservative measures of acuity. It also implies that a fast method of measurement can be used reliably. Procedures for measuring acuity in infants have been applied not only to infants without visual problems but also to study the effects of ocular anomalies, including astigmatism, occlusion, and strabismus. The ability to resolve detail is fundamental to pattern perception and to all the capaci-
ties that depend upon it: recognition of objects, faces, print, script, and so on. Consequently, measures of resolution tell us about a basic capacity that limits many achievements of a higher order and the increase of resolution during development allows progressive improvement of these achievements. The most common measure of resolution is visual acuity (Riggs, 1965), and perhaps the best known test of acuity involves the Snellen chart and its variants. Letters or numbers of graded size are presented at a fixed distance to an observer who reports the smallest that he can discern. The Snellen number represents the fraction of normal vision, defined as unity (20/20), shown by an observer. A more precise technique of measuring acuity will be discussed in this paper; it consists of presenting gratings of alternating dark and light stripes of equal width. The acuity threshold, then, is the grating with the narrowest stripes that can be detected 50% of the time it is presented. When it is not detected, it appears indiscriminable from a blank field of equal luminance (brightness). Gratings are usually specified by their spatial frequency in cycles per degree of visual angle, where a cycle consists of one dark and one light stripe. Normal adult acuity is considered 30 cycles per degree corresponding to 20/20 Snellen. The gratings used for research often consist of changes in luminance that are sinusoidal (Braddick, Campbell, & Atkinson, 1978), but, for practical purposes, square wave gratings consisting of abrupt transitions from higher to lower luminances are frequently used.1
*The research reported from the laboratory of the author was supported by grants from the National Institutes of Health (No. EY-02649, No. EY-01191, and No. EY-02621) and from the Spencer Foundation (No. LTR-DTD71373)-
'It should be mentioned here that visual acuity is but the extreme value on a function that defines what is called contrast sensitivity. Acuity is tested with the use of high contrast (black-white) test patterns (gratings or otherwise). When the contrast is lowered, only coarser detail can be detected and the highest spatial frequency of a grating that can be seen is lowered. The contrast sensitivity function describes the variation in the maximum detectable spatial frequency of the test grating as contrast is varied from low to high (Braddick et al., 1978).
Canad. J. Psychol./Rev. canad. Psychol., 1979, 33 (4)
213
ACUITY IN INFANTS AND YOUNG CHILDREN
With individuals who understand verbal instructions, standard psychophysical procedures are used to measure acuity. With human infants as with animals, other procedures must be used. But, unlike research with animals, prolonged and arduous experimentation is out of the question with human infants. Given these requirements, three procedures have proven useful although they by no means exhaust the possibilities. Preference Method
It has long been known that an infant prefers to gaze at a patterned region in his field of vision rather than a blank area, under a variety of experimental conditions (Stirnimann, 1944; Fantz, Ordy, & Udelf, 1962). Various procedures have been developed in recent years to exploit this preference for pattern. If a grating stimulus is paired with an otherwise equivalent blank field, the infant should preferentially look at the grating as long as it is resolvable. When no longer resolvable the preference should be 50%. Much of the research using this method to measure acuity is summarized by Dobson and Teller (1978). Contrast sensitivity functions have been obtained by Atkinson, Braddick, and Moar (1977) and by Banks and Salapatek (1978). If two gratings which differ in some respect such as stripe orientation are presented together, a difference in their visibilities results in preferential fixation on the more visible one (Gwiazda, Brill, Mohindra, & Held, 1978; Leehey, Moskowitz-Cook, Brill, & Held, 1975). This procedure has proven quite sensitive to small differences in visibility. We have also developed a five-minute preferential viewing procedure which allows us to test the acuity of infants between birth and one year (Gwiazda, Wolfe, Brill, Mohindra, & Held, in press (a)). It has been valuable in studying infants with ocular anomalies such as astigmatism, in which 214
the optically uncorrected retinal image can never be focused simultaneously in all orientations; occlusion, in which one eye is covered for a period of time; strabismus, in which the eyes do not look in the same direction at the object of regard; and anisometropia, in which the refractive power of the two eyes differs. Visually Evoked Potential
Patterns that are flashed on and off evoke an electrical response in the visual part of the brain which can be recorded with electrodes placed on the subject's scalp. By varying the size of the pattern elements and observing the parameters of the electrical response, it is possible to derive a measure of sensitivity in adults that correlates well with measures of visual acuity (Campbell & Maffei, 1970). This technique is usable with infants since no instructions are required (Pirchio, Spinelli, Fiorentini, & Maffei, 1978). The procedure has generally shown substantially higher acuity in infants and earlier achievement of adult levels than the preference technique (Dobson & Teller, 1978). Optokinetic Response
If a patterned stimulus moves across the retina at an appreciable velocity, it induces a series of pursuit eye movements followed by a saccade back to the original position. No other voluntary response is needed on the part of the observer aside from gazing at the stimulus to effect the appropriate accommodation of the lens of the eye needed to focus the stimulus on the retina. This procedure has been used extensively to study acuity in infants since the optokinetic response ceases when the detail of the pattern that evokes it becomes too fine to be detected. Measures of acuity taken by means of this response agree rather well with those obtained using the looking preference procedure (Dobson & Teller, 1978). R. Held
20 30 AGE (weeks)
FIGURE 1 Median spatial frequencies of looking preferences from grouped data as a function of age and grating orientation. Main axes medians combined those from horizontal and vertical gratings. Error bars represent semi-interquartile ranges. (Reprinted by permission of American Journal of Optometry and Physiological Optics)
DEVELOPMENT OF ACUITY
THE PATTERN PREFERENCE
Beginning at birth, growth of acuity with age is universally observed (Dobson & Teller, 1978), and explanation of this growth is an important subject for research. The preferential viewing technique developed by our group allows us to test infants ranging in age from a few weeks up to at least one year. This technique differs from others in at least one important respect. The grating stimulus is paired with either a blank field or another grating of equal space-averaged luminance in an otherwise darkened room (Leehey et al., 1975; Gwiazda et al., 1978). In the absence of other illuminated objects, the infants have little to attend to other than the intended stimuli. Using this technique we have demonstrated the growth of acuity during the first year as well as the differential rate of growth of acuity for oblique as opposed to main axis gratings. Using the fast procedure developed recently, we have obtained the data shown in Figure 1 from a group of infants without serious refractive or other ocular problems (Gwiazda, Brill, Mohindra, & Held, in press (b)). These data constitute a norm against which can be compared the acuities of infants suffering from ocular anomalies.
ASSUMPTION
Development of visual resolution
Anomalous findings recently led us to question the assumption that infants always prefer to gaze at a visible pattern over a blank field. Using the method of constant stimuli, we therefore gathered data over a set of frequencies ranging to higher values than appeared to be necessary in order to approach 50% preference. A typical subject's results are shown in Figure 2. The infant clearly did not prefer to look at the grating at the higher frequencies. The infant preferred to look at the blank field at at least one frequency, a response that is just as indicative of discrimination and detection of the grating as is a preference for looking at it. This result has since been replicated many times (Held, Gwiazda, Brill, Mohindra, & Wolfe, 1979)- We do not yet know why the preference is reversed at the higher spatial frequencies, but the result has two important implications. The dip below 50% stabilizes the termination of the staircase process used in the fast procedure for measuring acuity (Gwiazda et al., in press (a)). And the preference method will underestimate acuity if the stimulus set does not include gratings of frequencies
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higher than those that elicit a preference of 50% or more. The underestimation may in part account for the discrepancy between the values of acuity obtained with preference techniques and those obtained with the visually evoked potential. Differences in threshold criteria may also help account for it. While the preference method remains of great value, we must bear in mind that it has yielded conservative values for acuity. ANOMALIES OF VISION AND OCULOMOTOR COORDINATION
During the last two decades discoveries in the visual system, particularly in the cortex, have set the stage for discoveries concerning the effects of anomalous conditions of vision. Most of this work has involved the cat and monkey visual system (Wiesel & Hubel, 1965; von Noorden, 1973)- It is now known that monocular occlusion soon after birth can result in irreversible loss of bino216
cularity and of the ability for stimulation of the deprived eye to excite cortical cells. Furthermore, the behaviour of monocularly deprived animals demonstrates losses in acuity and discrimination that parallel the single cell results (Dews & Wiesel, 1970; Mitchell, 1978). Artificially induced strabismus has been shown to reduce greatly the number of cells that respond to stimulation of both eyes (Hubel & Wiesel, 1965; Baker, Grigg, & von Noorden, 1974). And it has been claimed that such strabismus can cause amblyopia (reduced acuity not attributable to either optical or peripheral problems) in the deviating eye (von Noorden & Dowling, 1970). Only during a critical period (approximately the fourth through twelfth week in the cat) does the animal display adverse reactions to these forms of visual deprivation (Wiesel & Hubel, 1963, 1965). Older animals deprived of pattern vision for long periods of time show few, if any, of the R. Held
morphological, physiological, and behavioural deficits found in animals deprived during the critical period. Thus, it is thought that once the visual pathways are fully developed, they remain intact even when not in use for prolonged periods of time. Following demonstration of the impressive effects of deprivation on binocular vision, attempts have been made to demonstrate that development of other aspects of vision depend upon exposure to the normal environment. The best known of these are the stripe-reared kittens of Blakemore and Cooper (1970) and of Hirsch and Spinelli (1971). It was claimed that kittens able to view stripes of only one orientation failed to develop cells responsive to edges of other orientations, particularly those near the orthogonal axis. However, a somewhat amended view of this claim is presented in a more recent publication (Stryker, Sherk, Leventhal, & Hirsch, 1978). In the wake of these demonstrations of the plasticity of the developing visual system in animals, researchers have actively sought to explore possible parallels in human vision, and several have been proposed and studied. The new techniques for studying infants' acuity enable researchers to study the development of vision under normal and anomalous conditions and to look for results analogous to those of the animal studies. We have been interested in four of the proposed human parallels: the oblique effect, the meridional amblyopia apparently resulting from chronic astigmatism, the amblyopia resulting from the form of strabismus known as esotropia (crosseyedness in which one eye turns in towards the nose), and the effects of occlusion of one eye. These four will be discussed in turn. The Oblique Effect
Visual acuity in adult human observers can be tested with gratings of varied orientations in the frontal plane. When this is done, gratings tilted off the vertical and Development of visual resolution
horizontal axes are resolved less effectively than those aligned with them; acuity for oblique gratings is generally reduced by 1 o to 20%. Following announcement of the results from experiments with stripereared kittens, claims were made that the oblique effect resulted from exposure to the urban world since horizontal and vertical lines occur more frequently than obliques in city environments. The argument appeared to be clinched by the claim that Cree Indians of northern Canada who live in huts with oblique sides have less of an oblique effect than a sample of urbanliving Caucasians (Annis & Frost, 1973). Using the technique for measuring acuity in infants, we tested whether exposure to the environment produces the oblique effect. If experience were responsible, then reduced acuity on the oblique should not occur until some time after birth when sufficient exposure to the environment had occurred. One of the results of measuring acuity for both main axis and oblique gratings is shown in Figure 1, summarizing data for a group of normal infants. By six months of age, acuity for oblique gratings is less than that for vertical and horizontal ones and remains so (Gwiazda et al., in press (a)). Other tests directly pairing oblique and main-axes gratings indicate a preference for the main-axes gratings as early as the second month (Leehey et al., 1975; Gwiazda et al., 1978). Given this early onset of the oblique effect, it is safe to conclude that its underlying substrate develops independently of specially biased environments. It seems unlikely that infants are systematically exposed to the appropriately biased set of oriented contours prior to a few months of age. Recently, Timney and Muir (1976) discovered that a group of Chinese individuals from Hong Kong showed reduced oblique effect relative to a Caucasian group. If we ask what is common to Cree Indians and Hong Kong Chinese the answer is, of course, that they are both of Mongoloid origin. Taken together with our argument 217
that the effect develops endogenously, the racial difference suggests a genetic origin for the difference in magnitude of the oblique effect between Cree Indians and urban Caucasians.
sate for the high incidence of astigmatism early in life (Mohindra, Held, Gwiazda, 8c Brill, 1978). In any event, this high incidence has allowed us to measure acuity and its development in a large number of astigmatic infants. Meridional Amblyopia The optical blurring effects of the astigA second analogy to the stripe-reared kitten matism are made quite evident by the reexperiment is the very considerable loss of duced acuity along selected orientations. acuity (as much as one-half normal) in the However, we have yet to detect any sign of habitually blurred meridia of chronic amblyopia in astigmatic infants (up to one astigmatic observers. In astigmatism, the year of age). The earliest evidence we have optics of the eye are not perfectly spherical found for this form of amblyopia occurred but possess a cylindrical component. in a child two years, ten months old. ConseTherefore, only edges of one orientation in quently, we tentatively conclude that susthe frontal plane can be sharply focused at ceptibility to this form of amblyopia has its any given time. Moreover, certain orientaonset sometime after the first year and betions tend to be habitually out of focus and fore the third year of life. This delayed consequently blurred. Many astigmatic susceptibility contrasts strongly, as we shall adults show losses of acuity despite optical discuss, with the earlier onset of amblyopia correction for edges in the habitually blurred resulting from either strabismus or occluorientations (Mitchell, Freeman, Millodot, sion of one eye. & Haegerstrom, 1973), a state of affairs known as meridional amblyopia. The Amblyopia Accompanying Esotropia amblyopia is specific to the blurred meridia It has long been known that amblyopia frealthough the meridia may vary widely quently accompanies crosseyedness, but the among different observers. There is consecausal relation between the two has been quently a strong presumption that the ambiguous. It is unclear whether one amblyopia is produced by the habitual blurcauses the other or whether both are caused ring. by a third factor. The availability of a technique for measuring acuity, hence The questions to be answered then are: amblyopia, in infants may help to establish When does astigmatism induce meridional at least one causal sequence. amblyopia and what is the critical period during which the visual system is sensitive We have tested the acuity of each eye of a to blurring on selected orientations? The series of infants with constant esotropia. In answers are to be found by studying a samthese infants one eye (the deviating one) ple of astigmats from as early as possible turns too far inward towards the nose and until the onset and cessation of susceptibilremains that way. The non-deviating eye ity to amblyopia. The procedure involves fixates objects of interest. Some of these using our tests of acuity with and without infants appear in the clinic at a few months optical correction for the astigmatism. of age and at first testing may show no appreciable difference in acuity between The incidence of clinically significant the two eyes. However, byfiveor six months astigmatism in the adult population is of age, all of those whom we have tested approximately 10%; we expected to find a begin to show significant differences in similar incidence in infants. To our surprise acuity between the eyes in favour of the we found that the incidence was roughly five times the adult amount, implying that non-deviating (fixating) eye (Fig. 3). The fact that the strabismic condition existed for some naturally corrective process occurs some time before the development of during the first few years of life to compen218
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amblyopia hints that the former caused the latter, although this conclusion is far from firm. Both conditions might have a common and independent underlying cause, but the amblyopia may not appear until the level of acuity appropriate to the five- or six-month-old (between 4 and 6 cycles/degree) is reached. The effects of strabismus on binocularity, including loss of stereovision and lessened interocular transfer of tilt aftereffects, have been documented in the literature on adult vision (Banks, Aslin, & Letson, 1975; Hohmann & Creutzfeld, 1975). Discovery of the consequences of strabismus for infant vision await the development of simple and efficient procedures for measuring binocularity in infants. Fox, Aslin, Shea, and Dumais (1980) have developed a stereopsis test which may prove useful in this connection. Very recently we have developed a test for stereoacuity in infants which promises to provide a very sensitive test for binocularity (Birch, Gwiazda, & Held, in press). The Effects of Monocular Occlusion
At least one retrospective analysis of the consequences of monocular occlusion has Development of visual resolution
been made (Awaya, Miyake, Shiose, Kanda, & Kawase, 1976); it suggests that even very short periods (one week) of occlusion can cause permanent visual deficits. We have studied the acuities of several infants who have had one eye patched for varying periods of time as a common form of therapy for early strabismus. All of these infants were constant esotropes showing differences in acuity favouring the non-deviating eye. The result, without exception, was an increase in acuity of the deviating eye with a concomitant reduction of acuity in the patched eye (Thomas, Mohindra, & Held, 1979). In other words, a tradeoff of acuities took place in which the acuity of one eye appeared to gain at the expense of the other eye (Fig. 3). Such a tradeoff has been suggested in the clinical literature (Michaels, 1975), but to the best of our knowledge this is the first demonstration of it. The deviating eye appears to return to its previous level of acuity following permanent removal of the occluder in the absence of complicating factors. However, the acuity of the previously patched eye may increase to levels above what is normally to be expected (Fig. 3). We have so far no adequate explanation of the latter phenomenon. The early strabismus, followed by the patching treatment, and finally by removal of the patch, seems to release the nondeviating eye from an inhibitory influence. Perhaps a reduction of binocularity, such as is seen in adult esotropes, accounts for this release. SUMMARY AND DISCUSSION
We have reviewed the state of the art with regard to measures of visual resolution in infants. These measures can now be made quickly and reliably with a number of procedures including visual preference which we have emphasized. Normative data have been obtained on a large number of infants using the preference procedure which shows that acuity begins at about 20/1200 Snellen (1/2 cycle/degree) soon after birth
219
and rises monotonically to at least 20/50 Snellen (12 cycles/degree) by the end of the first year. Acuity for oblique gratings begins to fall below that of main axes gratings at about six months of age. These data probably underestimate acuity because of the reversal of preference from grating to blank field at the upper end of the range of spatial frequencies. The results obtained on infants without serious ocular anomalies have been followed up with studies of infants suffering from astigmatism. The blurring effects of astigmatism can be detected quite early in the form of reduced acuity in the blurred meridia. But we have not found meridional amblyopia occurring in the first year of life; the earliest we have seen it is late in the third year. Infants suffering from a form of strabismus known as constant esotropia are found to develop differences in acuity between the eyes in the first semester of life. The deviating eye always shows the lower acuity, which we presume represents an early form of amblyopia. When the non-deviating eye is occluded by patching, the other eye improves in acuity but at the expense of the occluded eye. Finally, removal of the patch can result in a return to the earlier difference between the acuities of the two eyes. Our experience with the esotropic infants strikingly demonstrates the plasticity of the visual system with regard to visual function during this stage of life. Compared to this early susceptibility, meridional amblyopia runs a much delayed time course. Visual deprivation studies using animals have clearly demonstrated consequent changes at the cellular level. To understand the consequences of these changes for vision, alterations in the functioning of the whole system must be studied. The research discussed above on the development of vision in the human infant and child represents one step in this direction. RESUME L'interet accru pour le developpement visuel
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precoce s'est declenche par de nouvelles donnees concernant les mecanismes neurologiques du systeme visuel et le controle du developpement de ces mecanismes par des influences relevant aussi bien de la maturation que de l'environnement. L'acuite visuelle est la mesure la plus fondamentale du developpement de la vision des patterns par le nourrisson. Les methodes employees pour obtenir cette mesure se sont ameliorees au cours des dernieres annees et de nouvelles donnees ont ete recueillies. Parmi ces methodes, on peut souligner le potentiel evoque, la reponse optocinetique et l'observation differentielle. Cette derniere technique est fondee sur le postulat qu'un nourrisson preferera regarder un stimulus complexe (un pattern) qu'un stimulus uni, mais equivalent par ailleurs, dans la mesure ou le premier peut etre analyse. Notre groupe de recherche a pu montrer que ce postulat n'est pas toujours vrai, ce qui indiquerait que l'usage habituel qu'on fait de cette methode donne une mesure conservatrice de l'acuite et done qu'une technique de mesure rapide peut etre fiable. Des techniques de mesure de l'acuite ont ete appliquees non seulement a des nourrissons non affectes de problemes visuels, mais aussi a des nourrissons atteints de troubles oculaires tels que 1'astigmatisme, Pocclusion, et le strabisme. REFERENCES ANNIS, R.c, & FROST, B. Human visual ecology and orientation anisotropies in acuity. Science, 1973,182, 729-731 ATKINSON, j . , BRADDICK, o., & MOAR, K. Development of
contrast sensitivity over thefirstthree months of life in the human infant. VisionRes., 1977,17(9), 10371044 AWAYA, S., MIYAKE, Y., SHIOSE, Y., KANDA, T . , & KAWASE,
Y. Stimulus deprivation amblyopia in man. Proc. Second Congress ofInternational StrabismologicalAssoc.,
1976 BAKER, F.H., GRIGG, P., & VON NOORDEN, G.K. Effects o f
visual deprivation and strabismus on the response of neurons in the visual cortex of the monkey, including studies on the striate and prestriate cortex in the normal animal. BrainRes., 1974,66,185—208 BANKS, M., ASLIN, R., Be LETSON, R. Sensitive period for
the development of human binocular vision. Science, 1975,190,675-677 BANKS, M.S., & SALAPATEK, P. Acuity and contrast sensitivity in 1,2, and 3 month old human infants. Investigative Ophthal., 1978,17(4), 361-365 BIRCH, E.E., GWIAZDA.J., & HELD, R. Stereoacuity of
human infants. To be presented at meeting of Optical Society, 30 April—3 May, 1980 BLAKEMORE, c , & COOPER, G.F. Development of the
brain depends on the visual environment. Nature, 1970,8*8,477-478
R. Held
BRADDICK, o., CAMPBELL, F.W., & ATKINSON,]. Channels
in vision: Basic aspects. In R. HELD, H.W. LEIBOWITZ, & H.-L. TEUBER (eds.), Perception. (Handbook of sensory physiology; Vol. 8). Berlin-Heidelberg: Springer-Verlag, 1978 CAMPBELL, F.w., & MAFFEi, L. Electrophysiological evidence for the existence of orientation and size detectors in the human visual system. Journal ofPhysiology, 1970,207,635-652 DEWS, P.B., & WIESEL, T.N. Consequences of monocular
deprivation on visual behaviour in kittens.y. Physiol., 1970,206,437-455 DOBSON, v., & TELLER, D. Y. Visual acuity in human infants: A review and comparison of behavioral and electrophysiological studies. Vision Res., 1978,18, 1469-1483 FANTZ, R.L., ORDY, J.M., & UDELF, M.S. Maturation of
pattern vision in infants during the first six months. J. comp. physiol. Psychol., 1962,55(6), 907—917 FOX, R., ASLIN, R.N., SHEA, S.L., & DUMAIS, S.T. Stereopsis
in human infants. Science, 1980,207,323—324 GWIAZDA,J., BRILL, S., MOHINDRA, I., & HELD, R. I n f a n t
visual acuity and its meridional variation. Vision Res., 1978,18,1557-1564 GWIAZDA,J., BRILL, s., MOHINDRA, i., & HELD, R. Pre-
ferential looking acuity in infants from 2 to 58 weeks of age. Am.]. Optom. physiol. Optics, in press, (a) GWIAZDA,J., WOLFE,J., BRILL, S., MOHINDRA, I., & HELD,
R. Quick assessment of preferential looking acuity in infants. Am.J. Optom. physiol. Optics, in press, (b)
MICHAELS, D.D. Visual optics and refraction: A clinical approach. San Pedro: Mosby, 1975 MITCHELL, D.E. Effect of early visual experience on the development of certain perceptual abilities in animals and man. In R.D. WALK & H. j . PICK, JR. (Eds.),
Perception and experience. New York: Plenum Publishing Corp., 1978. MITCHELL, D.E., FREEMAN, R.D., MILLODOT, M., &
HAEGERSTROM, G. Meridional amblyopia: Evidence for modification of the human visual system by early visual experience. VisionRes., 1973,13,535-558 MOHINDRA, L, HELD, R., GWIAZDA,J., & BRILL, s. Astig-
matism in infants. Science, 1978,202,329—331 PIRCHIO, M., SPINELLI, D., FIORENTINl, A., & MAFFEI, L.
Infant contrast sensitivity evaluated by evoked potentials. Brain Res., 1978,141,179-184 RIGGS, L.A. Visual Acuity. In C.H. GRAHAM (Ed.), Vision and visual perception. New York: Wiley, 1965 STIRNIMANN, F. Ueberdas Farbenempfinden Neugeborener. Ann. Paedia., 1944,163,1—25 STRYKER, M.P., SHERK, H., LEVENTHAL, A.G., & HIRSCH, H.
Physiological consequences for the cat's visual cortex of effectively restricting early visual experience with oriented contours. J. Neurophysiol., 1978,41, 8g6— 99 THOMAS,J., MOHINDRA, I., & HELD, R. S t r a b i s m i c
amblyopia in infants. Am.J. Optom. physiol. Optics, 1
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