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Psychophysical assessment of visual acuity in infants with visual disorders
Beha vioural Brain Research, 10 ( 19 8 3 ) 51- 5 8 Elsevier
51
PSYCHOPHYSICAL A S S E S S M E N T OF VISUAL ACUITY IN INFANTS WITH VISUAL D I S O R D E R S
I. M O H I N D R A l, S.G. J A C O B S O N 2, J. Z W A A N 2 and R. H E L D 1
~Department of Psychology, Massachusetts Institute of Technology, Cambridge, MA 02139, and ZMassachusetts Eye and Ear Infirmary, Boston. MA 02114 (U.S.A.) (Reccived June 18th, 1983) (Accepted July 7th, 1983)
Key words'." visual acuity development - visual form deprivation - preferential looking - h u m a n
SUMMARY
The measurement of visual acuity is an essential part of the eye examination of adults, but is rarely attempted in infants being examined for presumed or known eye disease. We have used a preferential looking technique to test visual acuity of infants attending a hospital eye clinic. Serial measurements of acuity of infants attending a hospital eye clinic. Serial measurements of acuity in infants with certain eye diseases can provide examples of the effects of visual deprivation on the developing human visual system. Amongst 14 cases of monocular visual form deprivation in early life, there were 9 infants who had monocular occlusion as therapy for esotropia; 3 infants who had unilateral opacities of the ocular media; and 2 infants who had unilateral eyelid closure from infection or bums. Despite differences in exact mode of deprivation, the effects on visual acuity were similar. There was a reduction of visual acuity in the deprived eye and a simultaneous increase in acuity of the non-deprived eye. These effects of monocular deprivation were not permanent. Recovery occurred with reverse deprivation or by simple cessation of the deprivation. Of l0 children with binocular visual form deprivation, there were 5 who had bilateral congenital cataracts and 5 who had bilateral uncorrected high refractive errors. Infants with cataract surgery before 2 months of age showed normal early development of visual acuity. A 4-6 month delay before treatment resulted in reduced acuity, but recovery subsequently occurred. Infants with high hyperopia or astigmatism showed no acuity deficits in the first year of life when tested with optical correction. One case of early meridional amblyopia was detected in the 0166-4328/83/$03.00 © 1983 Elsevier Science Publishers B.V.
52 third year of life. After a period of optical correction there was recovery of visual acuity to normal levels. This suggests that this deficit at this age is reversible.
INTRODUCTION
Recent advances in techniques for psychophysical assessment of vision in human infants have permitted evaluations in the clinic of children with a variety of visual disorders [6]. Amongst the many ocular diseases in a pediatric population are some that cause asymmetric visual deprivation such as strabismus and monocular opacities of the ocular media. Therapeutic monocular occlusion also can produce such deprivation. The major initial effect of this deprivation is a 'trade-off of acuities between the eyes, i.e. a decrease in visual acuity of the deprived eye along with an increase in acuity of the non-deprived eye [ 12]. In this paper we present examples oftrade-offs resulting from a number of different types of asymmetric visual deprivation, and describe the associated phenomenon of 'superacuity' that we have observed in a number of infants undergoing such deprivation [ 13 ]. METHODS
The psychophysical method for measuring visual acuity in infants is the two-alternative forced-choice preferential looking technique. Details of this method, the norms achieved with it, and applications to clinical cases have been previously described [2, 3, 6]. The technique is based on the premise that, when given the choice, infants will prefer to fixate patterned rather than unpatterned stimuli. In the procedure, two stimuli, a square wave grating and a blank field, are presented simultaneously to the infant who sits in a parent's lap 50 cm from a screen onto which the stimuli are projected. An observer of the infant is behind the screen and is forced to decide at which of the stimuli the infant prefers to look. If this decision coincides with the side of presentation of the grating stimulus, then the infant's response is considered correct. The stimuli are presented according to a modified staircase procedure or a constant stimulus method, both of which have been shown to give similar results [2, 6]. Monocular acuities are measured using a disposable patch over the eye not being tested. All aphakic infants were tested either with spectacle or contact lense correction and overplussed for the testing distance; thresholds for these eyes were corrected for magnification resulting from the optical correction. RESULTS
Fig. 1 shows 12 examples of serial visual acuity measurements from 11 infants with various eye disorders. Visual acuity is plotted as spatial frequency
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54 (cycles per degree) along the vertical axis and age (weeks) on the horizontal axis. Figures 1A and 1B are examples of infants with ocular diseases but no asymmetry in visual input during the period when the acuity measurements were made. Infant 1A had bilateral congenital cataracts that were successfully removed at an early age. Three successive acuity measures with optical correction showed equal acuities for the two eyes. Infant 1B had congenital alternating esoptropia and on 3 separate visits showed equal acuities for both eyes. In contrast, the other 10 examples are from infants that experienced some degree of asymmetric visual deprivation and all showed the trade-off phenomenon. Infants 1C and 1D represent examples of the trade-off effect resulting from the visual deprivation of strabismus. These infants had esotropia detected shortly after birth and both had a preference for fixation with one eye. When visual acuity was first measured, both eyes were equal. On a subsequent visit, however, acuity of the eye preferred for fixation (left eye in both cases) had increased while that of the non-preferred eye had decreased. Monocular form deprivation also can result in the trade-off phenomenon. Infants 1E and 1F had esotropia and unequal acuities. Monocular occlusion was prescribed for the eye with higher acuity (right eye in 1E; left eye in 1F) and on the following visit, the occluded eye was lower in acuity and the unoccluded eye had become higher. Infant 1G had monocular form deprivation from a pupillary membrane (ocular media opacity) and acuity of the deprived left eye fell. The last acuity plotted in the graph was measured after removal of the opacity and with full optical correction. The non-deprived right eye showed an increase in acuity concurrently. Infant 1H had equal acuities after bilateral cataract surgery but experienced defocussed imagery in the left eye because of an ill-fitting contact lens. This monocular deprivation caused a trade-off of acuities again: a dramatic increase in acuity occurred in the eye with the well-fitted contact lens (right eye) while the left eye lost acuity. The measure of acuity in the deprived left eye was made with a properly fitting lens. A trade-off of acuities has also been observed during reversal of deprivation effects and after cessation of monocular deprivation. Infants 1I and 1J both received monocular occlusion as therapy to reverse the deprivation caused by unilateral ocular media opacification of the right eye (Infant 1I) and extended occlusion therapy of the right eye for strabismus (Infant 1J). Again, the pattern of acuity change was a trade-off. Infant 1K had extended occlusion therapy of the left eye for strabismus and was found to have unequal acuities as a result. Cessation of this occlusion led to an increase in acuity of the previously occluded eye and a decrease in acuity of the fellow eye. After some further acuity changes [7] both eyes increased to equality. Infant 1L, the same infant as 1H, showed a similar pattern of acuity changes once the contact lens fit in the left eye was corrected. Fig. 2 shows monocular acuity results from 11 infants, ranging in age from 9 to 45 weeks, with visual disorders that caused a large difference in acuity between
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Fig. 2. Visual acuity measurements in 11 infants with unequal acuities due to asymmetric visual input. Open symbols represent infants with visual deprivation; circles, deprived eye; squares, non-deprived eye. Closed symbols are infants with unilateral congenital ocular abnormalities; circles, affected eye; squares, unaffected eye. Shaded symbols are results from an infant with one eye enucleated (circle) because of an ocular tumor. Filled triangles are normative acuity results for the first year of life [3]. NM, not measurable.
the two eyes. Six of these infants had asymmetric visual experience due to some type of deprivation in the first year of life; 4 infants had unilateral developmental ocular abnormalities; and 1 infant had one eye removed in the second month of life. Also on this graph are plotted normative results for visual acuity in the first year of life [3]. These data points represent median spatial frequencies at 7 mean ages (ranging from 4 to 54 weeks) for 24 normal infants; error bars are the semi-interquartile range. Table I lists the clinical condition and the type of asymmetric visual input at the time of testing for the 11 infants with visual disorders. The 4 infants with developmental abnormalities had no measurable vision in the affected eye; acuities of the unaffected eyes were distributed around the norm with small deviations. In contrast, the 6 infants with asymmetric visual deprivation showed acuity in the undeprived eye that was higher than what would be expected from the normative data, averaging more than one octave. The acuity of the deprived eye in these infants was usually measurable and lower than the norm, averaging about two octaves below the norm. In most of these cases, the acuity difference was the result of a trade-off. The infant with recent surgical removal of one eye because of an ocular tumor had a higher than expected acuity in the remaining eye. DISCUSSION
The phenomenon of trade-off of visual acuity during asymmetric visual deprivation in human infants is now well established. The original observations were made using psychophysical techniques [ 12, 15] and more recent studies with
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Retinoblastoma Severe unilateral microophthalmos Unilateral microophthalmos with coloboma Unilateral optic nerve coloboma Severe unilateral microophthalmos Unilateral congenital cataract (after surgery) Bilateral congenital cataracts (after surgery) Congenital esotropia Bilateral congenital cataracts (after surgery) Persistent hyperplastic primary vitreous (after surgery) Congenital esotropia
Clinical condition
Defocus in one eye due to incorrect contact lens Preference for fixation Pupillary membrane occluding visual axis in one eye 3 weeks after cessation of therapeutic occlusion of unaffected eye After monocular occlusion therapy
Before full optical correction of aphakic eye
2 weeks after enucleation of right eye
Type of asymmetric visual input
57 electrophysiological methods have confirmed the finding [ 14]. The present report emphasizes the fact that the trade-off of acuities occurs in response to a wide variety of unilateral visual deprivations of eyes that otherwise appeared capable of normal visual function. The pattern of change of acuities is similar in strabismus with eye preference; in monocular form deprivation from ocular media opacification (cataract or pupillary membrane) or therapeutic occlusion; and in unilateral defocus of retinal imagery. The most parsimonious interpretation of the trade-off effect is in terms of an interocular interaction. The interesting coincidence of the onset age for enhanced binocularity with the age when acuity differences first occur in esotropic infants like 1C and 1D has led to the suggestion that this particular trade-off may be the result of a competitive interaction between eyes [4, 5]. Neuronal mechanisms for the trade-off phenomenon are not known, but the literature on visual deprivation in young animals is replete with physiological and morphological evidence for an increase in function and structure of the undeprived visual pathway at the expense of the deprived pathway [9]. Behavioral evidence for a tradeoff in visually deprived animals has also recently been provided [ 11 ]. Some infants that experienced asymmetric visual input in the first year of life showed higher than expected acuity in their undeprived eye during the time when the deprived eye was lower than the norm. This 'superacuity' of the undeprived eye was not seen, however, in every instance of a trade-off of acuities. The effect seemed unrelated to the type and severity of the visual deprivation and it occurred in infants of varied ages during the first year of life. The finding of superacuity, first reported by Mohindra, et al. [13], has more recently been demonstrated using the visual evoked response [8]. Unlike the psychophysical results, the electrophysiological measures suggested that the superacuity phenomenon is only present in the first 3 months of life. It is of interest that studies in some adults with monocular visual deprivation have also demonstrated a form of superacuity in the undeprived eye [1]. The mechanism for this transiently accelerated development of resolution in the undeprived eye of some infants with asymmetry of visual input is not known. It is of significant interest, however, that the 4 infants with congenital developmental abnormalities of one eye showed no superacuity in their remaining eye. Asymmetry of visual input alone is therefore not the only prerequisite for superacuity; there may be a need for two functioning visual pathways and possibly an interocular interaction. A binocular interaction would not be possible in infants with disorders such as severe unilateral microophthalmos in which there is partial if not complete absence of the visual pathways from the affected eye [ 10]. A hypothesis implicating binocular interaction gains some further strength from the results of the infant that was born with two intact visual pathways but had an enucleation early in life. The finding of superacuity in the remaining eye of this infant suggests that this case may represent the most extreme form of imbalanced visual input.
58 The effect of subsequent degeneration of the pathway from the enucleated eye might be expected to eliminate this 'interocular interaction' and a pattern more like those of the 4 infants with congenital developmental abnormalities could occur. ACKNOWLEDGEMENTS
We thank Miss A.E. Stromberg, Dr. E. Mobilia, Mrs. Francis Zwaan and Professor C.H. Dohlman for their help throughout this study; we are also grateful to Mr. J. Bauer for his help with the analysis of some of the data. This work was supported by grants from the National Institutes of Health (EY02649) and (EY02621). REFERENCES 1 Freeman, R.D. and Bradley, A., Monocularly deprived humans: nondeprived eye has supernormal vernier acuity, J. Neurophysiol., 43 (1980) 1645-1653. 2 Gwiazda, J., Wolfe, J., Brill, S. Mohindra, I. and Held, R., Quick assessment of preferential looking acuity in infants, Amer. J. Optom. physiol. Optics, 57 (1980) 420--427. 3 Gwiazda, J., Brill, S., Mohindra, I. and Held, R., Preferential looking acuity in infants from two to fifty-eight weeks of age, Amer. J. Optom. physiol. Optics, 57 (1980) 428-432. 4 Held, R., Binocular vision...behavioral and neuronal development. In J. Mehler and R. Fox (Eds.), Neonate Cognition: Beyond the Blooming, Buzzing Confusion, Lawrence Erlbaum, Hillsdale, NJ, in press. 5 Jacobson, S.G., Mohindra, I. and Held, R., Age of onset of amblyopia in infants with esotropia. Documenta Ophthalmologica, Proe. Series, 30 (1981) 210-216. 6 Jacobson, S.G., Mohindra, I. and Held, R., Visual acuity of infants with ocular diseases, Amer. J. Ophthalmol., 93 (1982) 198-209. 7 Jacobson, S.G., Mohindra, I. and Held, R., Monocular visual form deprivation in human infants, Documenta Ophthalmologica, in press. 8 Jastrzebski, G.B., Marg, E., and Hoyt, C.S., Superacuity in monocular deprivation amblyopes. Proc. Second int. Syrup. Visual Optics, Tucson, Arizona (October 23-25, 1982). 9 Lund, R.D., Environmental influences on visual responsiveness. In R.D. Lund (Ed.), Development and Plasticity of the Brain, Oxford Univ. Press, New York, 1978, pp. 253-284. 10 Mann, 1., Developmental Abnormalities of the Eye, Cambridge Univ. Press, Cambridge, 1937, pp. 60-93. 11 Mitchell, D., et al., The labile nature of the visual recovery prompted by reverse occlusion in monocularly deprived kittens, Inv. Ophthalmol. Vis. Sci., Suppl., 24 (1983) 22. 12 Mohindra, I., Jacobson, S.G., Thomas, J., and Held, R., Development of amblyopia in infants, Trans. Ophthal. Soc. U.K., 99 (1979) 344-346. 13 Mohindra, I., Held, R. and Jacobson, S.G., Interocular interaction and superacuity in human infants with monocular visual deprivation, Inv. Ophthalmol. Vis. Sci., Suppl., 20 (1981) 119. 14 Odom, J.V., Hoyt, C.S., and Marg, E., Effect of natural deprivation and unilateral eye patching on visual acuity of infants and children: evoked potential measurements, Arch. Ophthalmol., 99 (1981) 1412-1416. 15 Thomas, J., Mohindra, I., and Held, R., Strabismic amblyopia in infants, Amer. J. Optom. physiol. Optics, 56 (1979) 197-201.
51
PSYCHOPHYSICAL A S S E S S M E N T OF VISUAL ACUITY IN INFANTS WITH VISUAL D I S O R D E R S
I. M O H I N D R A l, S.G. J A C O B S O N 2, J. Z W A A N 2 and R. H E L D 1
~Department of Psychology, Massachusetts Institute of Technology, Cambridge, MA 02139, and ZMassachusetts Eye and Ear Infirmary, Boston. MA 02114 (U.S.A.) (Reccived June 18th, 1983) (Accepted July 7th, 1983)
Key words'." visual acuity development - visual form deprivation - preferential looking - h u m a n
SUMMARY
The measurement of visual acuity is an essential part of the eye examination of adults, but is rarely attempted in infants being examined for presumed or known eye disease. We have used a preferential looking technique to test visual acuity of infants attending a hospital eye clinic. Serial measurements of acuity of infants attending a hospital eye clinic. Serial measurements of acuity in infants with certain eye diseases can provide examples of the effects of visual deprivation on the developing human visual system. Amongst 14 cases of monocular visual form deprivation in early life, there were 9 infants who had monocular occlusion as therapy for esotropia; 3 infants who had unilateral opacities of the ocular media; and 2 infants who had unilateral eyelid closure from infection or bums. Despite differences in exact mode of deprivation, the effects on visual acuity were similar. There was a reduction of visual acuity in the deprived eye and a simultaneous increase in acuity of the non-deprived eye. These effects of monocular deprivation were not permanent. Recovery occurred with reverse deprivation or by simple cessation of the deprivation. Of l0 children with binocular visual form deprivation, there were 5 who had bilateral congenital cataracts and 5 who had bilateral uncorrected high refractive errors. Infants with cataract surgery before 2 months of age showed normal early development of visual acuity. A 4-6 month delay before treatment resulted in reduced acuity, but recovery subsequently occurred. Infants with high hyperopia or astigmatism showed no acuity deficits in the first year of life when tested with optical correction. One case of early meridional amblyopia was detected in the 0166-4328/83/$03.00 © 1983 Elsevier Science Publishers B.V.
52 third year of life. After a period of optical correction there was recovery of visual acuity to normal levels. This suggests that this deficit at this age is reversible.
INTRODUCTION
Recent advances in techniques for psychophysical assessment of vision in human infants have permitted evaluations in the clinic of children with a variety of visual disorders [6]. Amongst the many ocular diseases in a pediatric population are some that cause asymmetric visual deprivation such as strabismus and monocular opacities of the ocular media. Therapeutic monocular occlusion also can produce such deprivation. The major initial effect of this deprivation is a 'trade-off of acuities between the eyes, i.e. a decrease in visual acuity of the deprived eye along with an increase in acuity of the non-deprived eye [ 12]. In this paper we present examples oftrade-offs resulting from a number of different types of asymmetric visual deprivation, and describe the associated phenomenon of 'superacuity' that we have observed in a number of infants undergoing such deprivation [ 13 ]. METHODS
The psychophysical method for measuring visual acuity in infants is the two-alternative forced-choice preferential looking technique. Details of this method, the norms achieved with it, and applications to clinical cases have been previously described [2, 3, 6]. The technique is based on the premise that, when given the choice, infants will prefer to fixate patterned rather than unpatterned stimuli. In the procedure, two stimuli, a square wave grating and a blank field, are presented simultaneously to the infant who sits in a parent's lap 50 cm from a screen onto which the stimuli are projected. An observer of the infant is behind the screen and is forced to decide at which of the stimuli the infant prefers to look. If this decision coincides with the side of presentation of the grating stimulus, then the infant's response is considered correct. The stimuli are presented according to a modified staircase procedure or a constant stimulus method, both of which have been shown to give similar results [2, 6]. Monocular acuities are measured using a disposable patch over the eye not being tested. All aphakic infants were tested either with spectacle or contact lense correction and overplussed for the testing distance; thresholds for these eyes were corrected for magnification resulting from the optical correction. RESULTS
Fig. 1 shows 12 examples of serial visual acuity measurements from 11 infants with various eye disorders. Visual acuity is plotted as spatial frequency
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54 (cycles per degree) along the vertical axis and age (weeks) on the horizontal axis. Figures 1A and 1B are examples of infants with ocular diseases but no asymmetry in visual input during the period when the acuity measurements were made. Infant 1A had bilateral congenital cataracts that were successfully removed at an early age. Three successive acuity measures with optical correction showed equal acuities for the two eyes. Infant 1B had congenital alternating esoptropia and on 3 separate visits showed equal acuities for both eyes. In contrast, the other 10 examples are from infants that experienced some degree of asymmetric visual deprivation and all showed the trade-off phenomenon. Infants 1C and 1D represent examples of the trade-off effect resulting from the visual deprivation of strabismus. These infants had esotropia detected shortly after birth and both had a preference for fixation with one eye. When visual acuity was first measured, both eyes were equal. On a subsequent visit, however, acuity of the eye preferred for fixation (left eye in both cases) had increased while that of the non-preferred eye had decreased. Monocular form deprivation also can result in the trade-off phenomenon. Infants 1E and 1F had esotropia and unequal acuities. Monocular occlusion was prescribed for the eye with higher acuity (right eye in 1E; left eye in 1F) and on the following visit, the occluded eye was lower in acuity and the unoccluded eye had become higher. Infant 1G had monocular form deprivation from a pupillary membrane (ocular media opacity) and acuity of the deprived left eye fell. The last acuity plotted in the graph was measured after removal of the opacity and with full optical correction. The non-deprived right eye showed an increase in acuity concurrently. Infant 1H had equal acuities after bilateral cataract surgery but experienced defocussed imagery in the left eye because of an ill-fitting contact lens. This monocular deprivation caused a trade-off of acuities again: a dramatic increase in acuity occurred in the eye with the well-fitted contact lens (right eye) while the left eye lost acuity. The measure of acuity in the deprived left eye was made with a properly fitting lens. A trade-off of acuities has also been observed during reversal of deprivation effects and after cessation of monocular deprivation. Infants 1I and 1J both received monocular occlusion as therapy to reverse the deprivation caused by unilateral ocular media opacification of the right eye (Infant 1I) and extended occlusion therapy of the right eye for strabismus (Infant 1J). Again, the pattern of acuity change was a trade-off. Infant 1K had extended occlusion therapy of the left eye for strabismus and was found to have unequal acuities as a result. Cessation of this occlusion led to an increase in acuity of the previously occluded eye and a decrease in acuity of the fellow eye. After some further acuity changes [7] both eyes increased to equality. Infant 1L, the same infant as 1H, showed a similar pattern of acuity changes once the contact lens fit in the left eye was corrected. Fig. 2 shows monocular acuity results from 11 infants, ranging in age from 9 to 45 weeks, with visual disorders that caused a large difference in acuity between
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Fig. 2. Visual acuity measurements in 11 infants with unequal acuities due to asymmetric visual input. Open symbols represent infants with visual deprivation; circles, deprived eye; squares, non-deprived eye. Closed symbols are infants with unilateral congenital ocular abnormalities; circles, affected eye; squares, unaffected eye. Shaded symbols are results from an infant with one eye enucleated (circle) because of an ocular tumor. Filled triangles are normative acuity results for the first year of life [3]. NM, not measurable.
the two eyes. Six of these infants had asymmetric visual experience due to some type of deprivation in the first year of life; 4 infants had unilateral developmental ocular abnormalities; and 1 infant had one eye removed in the second month of life. Also on this graph are plotted normative results for visual acuity in the first year of life [3]. These data points represent median spatial frequencies at 7 mean ages (ranging from 4 to 54 weeks) for 24 normal infants; error bars are the semi-interquartile range. Table I lists the clinical condition and the type of asymmetric visual input at the time of testing for the 11 infants with visual disorders. The 4 infants with developmental abnormalities had no measurable vision in the affected eye; acuities of the unaffected eyes were distributed around the norm with small deviations. In contrast, the 6 infants with asymmetric visual deprivation showed acuity in the undeprived eye that was higher than what would be expected from the normative data, averaging more than one octave. The acuity of the deprived eye in these infants was usually measurable and lower than the norm, averaging about two octaves below the norm. In most of these cases, the acuity difference was the result of a trade-off. The infant with recent surgical removal of one eye because of an ocular tumor had a higher than expected acuity in the remaining eye. DISCUSSION
The phenomenon of trade-off of visual acuity during asymmetric visual deprivation in human infants is now well established. The original observations were made using psychophysical techniques [ 12, 15] and more recent studies with
9
14 32 38 41 17.5
22
27 31, 41
38
45
1
7
8 9
10
11
(weeks)
Age
2 3 4 5 6
Case
TABLEI
Retinoblastoma Severe unilateral microophthalmos Unilateral microophthalmos with coloboma Unilateral optic nerve coloboma Severe unilateral microophthalmos Unilateral congenital cataract (after surgery) Bilateral congenital cataracts (after surgery) Congenital esotropia Bilateral congenital cataracts (after surgery) Persistent hyperplastic primary vitreous (after surgery) Congenital esotropia
Clinical condition
Defocus in one eye due to incorrect contact lens Preference for fixation Pupillary membrane occluding visual axis in one eye 3 weeks after cessation of therapeutic occlusion of unaffected eye After monocular occlusion therapy
Before full optical correction of aphakic eye
2 weeks after enucleation of right eye
Type of asymmetric visual input
57 electrophysiological methods have confirmed the finding [ 14]. The present report emphasizes the fact that the trade-off of acuities occurs in response to a wide variety of unilateral visual deprivations of eyes that otherwise appeared capable of normal visual function. The pattern of change of acuities is similar in strabismus with eye preference; in monocular form deprivation from ocular media opacification (cataract or pupillary membrane) or therapeutic occlusion; and in unilateral defocus of retinal imagery. The most parsimonious interpretation of the trade-off effect is in terms of an interocular interaction. The interesting coincidence of the onset age for enhanced binocularity with the age when acuity differences first occur in esotropic infants like 1C and 1D has led to the suggestion that this particular trade-off may be the result of a competitive interaction between eyes [4, 5]. Neuronal mechanisms for the trade-off phenomenon are not known, but the literature on visual deprivation in young animals is replete with physiological and morphological evidence for an increase in function and structure of the undeprived visual pathway at the expense of the deprived pathway [9]. Behavioral evidence for a tradeoff in visually deprived animals has also recently been provided [ 11 ]. Some infants that experienced asymmetric visual input in the first year of life showed higher than expected acuity in their undeprived eye during the time when the deprived eye was lower than the norm. This 'superacuity' of the undeprived eye was not seen, however, in every instance of a trade-off of acuities. The effect seemed unrelated to the type and severity of the visual deprivation and it occurred in infants of varied ages during the first year of life. The finding of superacuity, first reported by Mohindra, et al. [13], has more recently been demonstrated using the visual evoked response [8]. Unlike the psychophysical results, the electrophysiological measures suggested that the superacuity phenomenon is only present in the first 3 months of life. It is of interest that studies in some adults with monocular visual deprivation have also demonstrated a form of superacuity in the undeprived eye [1]. The mechanism for this transiently accelerated development of resolution in the undeprived eye of some infants with asymmetry of visual input is not known. It is of significant interest, however, that the 4 infants with congenital developmental abnormalities of one eye showed no superacuity in their remaining eye. Asymmetry of visual input alone is therefore not the only prerequisite for superacuity; there may be a need for two functioning visual pathways and possibly an interocular interaction. A binocular interaction would not be possible in infants with disorders such as severe unilateral microophthalmos in which there is partial if not complete absence of the visual pathways from the affected eye [ 10]. A hypothesis implicating binocular interaction gains some further strength from the results of the infant that was born with two intact visual pathways but had an enucleation early in life. The finding of superacuity in the remaining eye of this infant suggests that this case may represent the most extreme form of imbalanced visual input.
58 The effect of subsequent degeneration of the pathway from the enucleated eye might be expected to eliminate this 'interocular interaction' and a pattern more like those of the 4 infants with congenital developmental abnormalities could occur. ACKNOWLEDGEMENTS
We thank Miss A.E. Stromberg, Dr. E. Mobilia, Mrs. Francis Zwaan and Professor C.H. Dohlman for their help throughout this study; we are also grateful to Mr. J. Bauer for his help with the analysis of some of the data. This work was supported by grants from the National Institutes of Health (EY02649) and (EY02621). REFERENCES 1 Freeman, R.D. and Bradley, A., Monocularly deprived humans: nondeprived eye has supernormal vernier acuity, J. Neurophysiol., 43 (1980) 1645-1653. 2 Gwiazda, J., Wolfe, J., Brill, S. Mohindra, I. and Held, R., Quick assessment of preferential looking acuity in infants, Amer. J. Optom. physiol. Optics, 57 (1980) 420--427. 3 Gwiazda, J., Brill, S., Mohindra, I. and Held, R., Preferential looking acuity in infants from two to fifty-eight weeks of age, Amer. J. Optom. physiol. Optics, 57 (1980) 428-432. 4 Held, R., Binocular vision...behavioral and neuronal development. In J. Mehler and R. Fox (Eds.), Neonate Cognition: Beyond the Blooming, Buzzing Confusion, Lawrence Erlbaum, Hillsdale, NJ, in press. 5 Jacobson, S.G., Mohindra, I. and Held, R., Age of onset of amblyopia in infants with esotropia. Documenta Ophthalmologica, Proe. Series, 30 (1981) 210-216. 6 Jacobson, S.G., Mohindra, I. and Held, R., Visual acuity of infants with ocular diseases, Amer. J. Ophthalmol., 93 (1982) 198-209. 7 Jacobson, S.G., Mohindra, I. and Held, R., Monocular visual form deprivation in human infants, Documenta Ophthalmologica, in press. 8 Jastrzebski, G.B., Marg, E., and Hoyt, C.S., Superacuity in monocular deprivation amblyopes. Proc. Second int. Syrup. Visual Optics, Tucson, Arizona (October 23-25, 1982). 9 Lund, R.D., Environmental influences on visual responsiveness. In R.D. Lund (Ed.), Development and Plasticity of the Brain, Oxford Univ. Press, New York, 1978, pp. 253-284. 10 Mann, 1., Developmental Abnormalities of the Eye, Cambridge Univ. Press, Cambridge, 1937, pp. 60-93. 11 Mitchell, D., et al., The labile nature of the visual recovery prompted by reverse occlusion in monocularly deprived kittens, Inv. Ophthalmol. Vis. Sci., Suppl., 24 (1983) 22. 12 Mohindra, I., Jacobson, S.G., Thomas, J., and Held, R., Development of amblyopia in infants, Trans. Ophthal. Soc. U.K., 99 (1979) 344-346. 13 Mohindra, I., Held, R. and Jacobson, S.G., Interocular interaction and superacuity in human infants with monocular visual deprivation, Inv. Ophthalmol. Vis. Sci., Suppl., 20 (1981) 119. 14 Odom, J.V., Hoyt, C.S., and Marg, E., Effect of natural deprivation and unilateral eye patching on visual acuity of infants and children: evoked potential measurements, Arch. Ophthalmol., 99 (1981) 1412-1416. 15 Thomas, J., Mohindra, I., and Held, R., Strabismic amblyopia in infants, Amer. J. Optom. physiol. Optics, 56 (1979) 197-201.