19:842, 1980. 2. Kiorpes L, Boothe R, Carlson M, and Alfi D: Frequency of naturally occurring strabismus in monkeys. J Pediatr Oph- thalmol Strabismus 22:60, ...
Investigative Ophthalmology & Visual Science, Vol. 31, No. 6, June 1990 Copyright © Association for Research in Vision and Ophthalmology
Accessory Lateral Rectus Orbital Geometry in Normal and Naturally Strabismic Monkeys R. G. Boothe, M. W. Quick, M. V. Joosse, M. A. Abbas, and D. C. Anderson We conducted anatomic dissections of macaque monkey orbits and made a quantitative assessment of the orbital geometry of the accessory lateral rectus muscle. Our results show that the expected effect of this muscle on rotations of the globe is to produce elevation and abduction. The abducting component could counteract nasal drifts, and thus our findings provide support for the hypothesis that this muscle could render monkeys resistant to the development of esodeviations. Dissections of the orbits from two naturally esotropic monkeys also are consistent with this hypothesis. The accessory lateral rectus muscle was absent in one of them and abnormally small in the other. Humans do not have an accessory lateral rectus muscle, and we speculate that the high prevalence of esodeviations in humans may be related to an evolutionary loss of this muscle system. Invest Ophthalmol Vis Sci 31: 1168-1174,1990
The only reports of naturally occurring strabismus in monkeys come from a screening project that was conducted during the past decade at the University of Washington Regional Primate Center.1"3 This is surprising given the widespread prevalence of strabismus in humans4 and given the similarities between the visual systems of humans and monkeys, including many aspects of both normal and abnormal visual development.5"10 In a major review of this topic, Jampolsky speculated that there must be some fundamental difference(s) between human and monkey oculomotor systems that makes most monkeys impervious to the factors that cause strabismus in humans." One fundamental difference between human and monkey oculomotor systems is evident at the level of gross anatomy. Monkeys have an accessory lateral rectus extraocular muscle (ALR), which is not present in humans (Fig. 1). The presence of the ALR in monkeys is documented in the comparative anatomy literature,12"18 but its existence does not appear to be widely appreciated in the ophthalmology literature. For example, there is mention of it neither in Jampolsky's review paper," nor in major ophthalmology textbooks that deal with strabismus.19'20 From the Yerkes Regional Primate Research Center, and the Departments of Psychology and Ophthalmology, Emory University, Atlanta, Georgia. Supported by National Institutes of Health grant RR-00165 to Yerkes Regional Primate Research Center. Submitted for publication: August 18, 1989; accepted October 9, 1989. Reprint requests: Ronald G. Boothe, Yerkes Regional Primate Research Center, Emory University, Atlanta, GA 30322.
Previous papers that have discussed the functional role of the ALR have tended to discount it as being too small and weak to have a significant influence on monkey eye movements.15 Nevertheless, a qualitative assessment of its size and position in relation to the other extraocular muscles suggests that the ALR may be well suited to help prevent the eye from drifting nasally (Fig. 1). For this reason, we hypothesized that this muscle might be able to function as a stabilizing force that helps prevent esodeviations from occurring in monkeys, regardless of whether or not the muscle makes a significant contribution to patterned eye movements. The purpose of this study was to make a more rigorous assessment of the viability of this hypothesis. We used quantitative dissection methods, similar to those described by Miller and Robins,21 to specify the expected effects, based on orbital geometry, of the ALR on rotations of the globe. We first made these assessments on a group of normal control macaque monkeys. When two naturally esotropic macaque monkeys, which were located during the screening project,1"3 had to be euthanatized for health reasons unrelated to their strabismus, we also conducted anatomic dissections of their orbits. Some preliminary results from this project have been presented previously in abstract form.22 Materials and Methods We conducted quantitative dissections on the orbits from ten macaque monkeys: four normal control Macaca mulatta, four normal control Macaca nemestrina, and two Macaca nemestrina monkeys that had naturally occurring esodeviations. Strabis-
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Fig. 1. A top view of the exposed orbits from a normal macaque monkey. The exposed muscle/tendons that can be seen attaching to the globe from this view are the superior obliques (O), superior recti (S), lateral recti (L), and the accessory lateral recti (A). All of these muscles would be found attached to similar positions on the globe of a human, except for the accessory lateral rectus (ALR), which is absent in humans. The ALR of the right eye has been exposed and pulled away from the globe to reveal the optic nerve (arrow), which lies beneath it. The ALR inserts onto the globe superior and posterior to the LR, inferior and posterior to the superior rectus, and superior and anterior to the optic nerve. The origins of all three muscles are near the optic foramen where the optic nerve enters the orbit from the brain cavity.
mic monkey M75038 exhibited an accommodative esotropia with a magnitude up to 35 prism diopters during near fixation. Recent retinoscopy and cover testing revealed a refractive error of +1.75 D in the right eye and -1.5 D in the left eye, and a fixation preference for the right eye. Strabismic monkey T82265 exhibited an alternating esotropia of about 14 prism diopters, and had a refractive error of+3.00 D in the right eye and +1.00 D in the left eye.23 The cadaver heads were fixed in formalin or paraformaldehyde and placed in a stereotaxic device. The eyes were in the anatomic position of rest (ie, the pupillary axes were directed approximately straight ahead). The top of the cranium and the brain were removed to expose the orbital bones which were removed with rongeurs to expose the globe and extraocular tissue. The lateral rectus muscle (LR) and the ALR were carefully dissected, and the stereotaxic locations of their anatomic origins and insertions measured and specified using the same methods as described by Miller and Robins.21 We compared our values obtained for the LR to the values reported by Miller and Robins in order to confirm that our meth-
odology was similar to theirs. The coordinates for the origin and insertion of the ALR then were used to calculate unit moment vectors for an eye in the primary position as described by Miller and Robins.21 These unit moment vectors specify the direction of rotation away from the primary position that would be produced by contraction of the muscle. The widths of both the LR and the ALR were measured with a ruler near their attachments to the globe. Since the ALR follows an essentially straight course, we were able to calculate its length directly from the coordinates of its origin and insertion. Then, the ALR was removed by cutting it near its origin and insertion, and a water reservoir used to determine its volume. Average cross-sectional area calculations were made based on length and volume. Finally, each ALR was processed for histology and confirmed to be skeletal muscle tissue. All procedures were performed in compliance with the ARVO Resolution on the Use of Animals in Research. The Yerkes Regional Primate Research Center is fully accredited by the American Association for Accreditation of Laboratory Animal Care.
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Results We made measurements from both eyes of each of our subjects, but in all cases the results from the left and right eyes of the same monkey were identical or differed by only a slight amount. For brevity, we present here only the results for the left eyes. The locations of the origins and insertions of the ALR can be expressed in a left-hand Cartesian coordinate system relative to the approximate center of rotation of the eye, as described by Miller and Robins.21 We determined these values separately for each of our control monkeys, and also calculated separate mean values for the M. nemestrina and M. mulatta normal control groups. A student t-test did not reveal any differences between the two groups at the 0.01 level of confidence, and therefore we combined the results to obtain mean control values. We plot these mean values, along with error bars indicating their standard deviations, for the ALR origins and insertions, in Figure 2. This plot of the positions of the origin and insertion relative to the center of rotation of the eye illustrates that the primary action of the ALR in normal monkeys is to abduct (Fig. 2a) and to elevate (Fig. 2b) the eye. As a standard for comparison, we also present mean values and standard deviation error bars for the LR insertions of our normal controls. In order to make a more quantitative assessment of the expected effects of the ALR on rotations of the globe, we calculated unit moment vectors of the ALR for the eye in primary position. We did this separately for each monkey, and the individual values are shown in Table 1. These results demonstrate quantitatively that the primary action of the ALR in normal macaque monkeys is to abduct and elevate the eye. Sizes of the ALR in normal monkeys are presented in Table 2. The three data columns show average cross sectional area for the ALR, the width of the ALR at its attachment to the globe, and the relative width of the ALR attachment compared to the LR attachment. We calculated this last value primarily as a control to demonstrate that our results are not simply a reflection of absolute differences in muscle sizes between individual animals. We calculated separate mean values for the M. nemestrina and M. mulatta control groups for each column in Table 2. A student t-test did not reveal any differences between the two species that were statistically significant at the 0.01 level of confidence on any of these measures. Therefore, we combined results from all animals to arrive at a single overall mean control value for each of the three columns. The sizes of the ALRs in the two monkeys with esodeviations were outside of the range of values
Fig. 2. Thisfigureshows the positions of the attachments of the ALR and LR muscles in a left-hand Cartesian coordinate system where the center of rotation of the eye is located at the intersection of the X, Y, and Z axes, (a) A top view where the X axis represents medial-lateral and Y posterior-anterior, (b) A lateral view where the Y axis is the same as in (a) and Z represents inferior-superior. Large open square symbols plot the mean values of the ALR insertions for our group of normal control monkeys, and the error bars around these symbols indicate ± one standard deviation along the X, Y, and Z axes. Similarly, large open circle symbols indicate LR insertions for the normal controls, and large closed square symbols are for the ALR origins. LR origins overlap with those shown for the ALR and are not shown. The small square symbols are the ALR origin and insertion values for naturally strabismic monkey T82265, and the LR insertions are indicated by the small closed circles (T82265) and the small open circles (M75038). Much of the interanimal variability shown is accounted for by individual differences in absolute sizes of the orbits. To illustrate the magnitude of this factor we present two circles which represent globe size. The inner circle represents the monkey with the smallest globe, and the outer circle represents the largest globe.
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Table 1. Unit moment vectors for the ALR in normal control monkeys Monkey
Macaque species
Z Y X (elevation) (intorsion) (abduction)
YN88279 YN88271 YN8831 YN8833
mulatta mulatta mulatta mulatta
0.57 0.69 0.74 0.48
-0.07 0.16 -0.03 0.03
0.83 0.71 0.68 0.87
YN88270 YN88192 YBP3 YBP4
nemestrina nemestrina nemestrina nemestrina
0.71 0.75 0.69 0.73
-0.04 0.27 0.02 -0.08
0.71 0.61 0.73 0.68
found for any of the normal control monkeys of either species. In strabismic monkey M75038, the ALR was absent, and in monkey T82265 the ALR was smaller than in any of the normal control monkeys. The values for ALR area, ALR width, and the ratio of ALR width to LR width for T82265 were 0.8 mm2, 1.0 mm, and 0.17 respectively. We used z-scores to evaluate the null hypothesis that these values fall within the range of normal variation. The probabilities that a monkey from our normal control population would have an ALR cross sectional area as small as 0.8 mm2, or an ALR width as narrow as 1.0 mm, or an ALR/LR proportion as low as 0.17, are each less than 1 out of 100. We also compared the LR widths of the two naturally strabismic monkeys to the normal control group. Based on z-scores, the LR width for monkey M75038 was significantly (P < 0.01) larger than expected for a normal control monkey. The width of T82265's LR fell within the normal range. The orbital geometry of the LR also was examined in the strabismic monkeys. The positions of the LR insertions of the naturally strabismic monkeys in relation to the mean values for the normal controls are illustrated in Figure 2. None of the coordinate values of LR origin or insertion for either monkey was significantly different from the normal controls at the 0.01 level of confidence. Finally, the coordinates for the ALR origin and insertion of esotropic monkey T82265 were determined, and are shown in Figure 2. It is apparent that the action of the ALR in this monkey would result in elevation and abduction of the eye, similar to the normal control monkeys. A z-score test revealed that none of strabismic monkey T82265's origin or insertion values was significantly different from those of our normal control population at the 0.01 level of confidence. Calculation of unit moment vectors for monkey T82265 confirmed this conclusion: abduction = 0.76, elevation = 0.65, and intorsion = 0.03. Therefore, the primary abnormalities in the orbits of
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our two naturally strabismic monkeys were the absence of the ALR in M75038 and a reduction in its size in T82265. There is also some evidence that the LR may have shown an increase in size in monkey M75038. However, the abnormalities in these orbits did not appear to involve changes in the positions of origins or insertions of the ALR or the LR. Discussion Our assessment of the orbital geometry of normal monkeys demonstrates that the ALR has the potential to contribute to elevation and abduction of the eye. We conclude that one function of the ALR may be to help stabilize the eyes of monkeys under conditions that would otherwise lead to esodeviations. Similarly, we conclude that monkeys in which the ALR is abnormally small or absent will exhibit an increased susceptibility to esodeviations. Our finding that the ALR was small or absent in both naturally esotropic monkeys is consistent with these conclusions. Fuchs and Luschei15 used a transducer to measure isometric tension characteristics of the monkey ALR while stimulating the abducens nerve with a train of electrical impulses, and determined that maximal tension developed by the ALR is only about one seventh of the amount developed by the LR. Furthermore, it developed its maximal tension more slowly and at much lower stimulus frequencies. They concluded that the ALR can be expected to play only a minor role in lateral movements of the eye. The role of this muscle then was largely ignored in subsequent studies of monkey eye movements. However, even if the active force generated by the ALR is relatively small and develops slowly compared to that of the LR, the influence of its passive force on resisting nasal drifts is likely to be relatively larger. Our direct measurements of muscle widths at insertions reveal that the width of the ALR is almost Table 2. Size of the ALR in normal control monkeys
Monkey
Macaque species
ALR area (mm2)
ALR width (mm)
ALR width/ LR width
YN88279 YN88271 YN8831 YN8833
mulatta mulatta mulatta mulatta
4.1 4.6 4.2 4.2
3.0 3.0 2.5 4.0
0.38 0.43 0.50 0.67
YN88270 YN88192 YBP3 YBP4
nemestrina nemestrina nemestrina nemestrina
5.8 5.7 4.5 4.7
2.5 2.0 2.5 3.5
0.42 0.40 0.36 0.44
4.7 0.7
2.9 0.6
0.45 0.10
Mean SD
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half that of the LR (Table 2). Comparisons of our cross-sectional measurements of the ALR to similar measurements of the LR by Miller and Robins21 indicate that the cross-sectional area of the ALR is about one third that of the LR. The ALR generates relatively little active force for its size most likely because it is highly tendinous. This can be noted from the gross observation that the ALR has a whitish appearance similar to the superior oblique (Fig. 1). Since the ALR is not present in humans, our findings may also have relevance for human strabismus. We do not claim that a small or missing ALR is a sufficient condition for causing esodeviations in primates. All humans are purported to lack this muscle, and yet only a small percentage of humans develop esotropia. Therefore, it is clear that most human eyes are able to maintain alignment, even in the absence of an ALR. However, our results can be related to multifactorial models of the causes of strabismus in which the strength of latent strabismus (phoria) is a function of the sum of a number of predisposing factors. If this latent tendency exceeds some threshold amount, the strabismus becomes manifest (tropia). Given a multifactorial threshold model, it is helpful to distinguish between the factors that operate directly to increase the magnitude of the latent tendency (predisposing causal factors) and the factors that operate primarily to influence an individual's threshold level. Examples of the kinds of predisposing causal factors that frequently have been implicated in human esotropia include refractive error and abnormal accommodative convergence.19"20'24"27 An example of a factor that has been proposed to operate primarily to influence threshold level is a subject's fusional divergence amplitude.2425 We assume that the predisposing causal factors that can lead to esodeviations have a similar frequency of occurrence in monkeys and humans. This assumption seems reasonable based on the similarities of human and monkey visual systems.5"10 However, we propose that the presence of the ALR in most monkeys acts to raise their threshold level, and that it is this factor which accounts for the infrequent occurrence of esodeviation in monkeys. Similarly, we propose that the absence of the ALR in humans results in a lowered threshold (increased susceptibility to esodeviations), which accounts for the relatively higher prevalence of esodeviations in humans. Another issue is whether the loss or reduction in size of the ALR might be a secondary effect caused by the strabismus. This possibility seems unlikely because in our two naturally esotropic monkeys the ALRs were abnormally small, but the LRs, which also function to abduct the eye, were either of normal size (T82265) or slightly enlarged (M75038). Our
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studies of monkeys that have had a strabismus induced by early visual deprivation28 may help to resolve this issue. We can safely assume that a normal ALR was initially present in these monkeys since they were drawn from a normal population. Anatomic dissections of these monkeys' orbits may determine whether the sizes of their ALRs remain normal after the deviation has appeared, but we have not yet performed these dissections. Our monkeys that developed induced strabismus were raised under conditions of visual deprivation that were moderately severe and began shortly after birth.28 It is noteworthy that under these conditions, in which the predisposing factors probably are not biased towards either esodeviations or exodeviations (visual deprivation), and in which the threshold level for esodeviations was not altered (the ALRs were presumably normal—see discussion above), we produced a combination of eso- and exodeviations. These results are consistent with our multifactorial threshold model, which predicts that it should be possible to produce strabismus in monkeys with the same predisposing causal factors that operate in humans, as long as the magnitude of their effects is sufficient to exceed the monkey threshold level. The negative findings that were previously interpreted as evidence that monkeys are impervious to many of the factors that lead to strabismus in humans'' may need to be reevaluated in terms of this threshold interpretation. Previous investigators have argued that the ALR in monkeys might be a transitional form of the retractor bulbus system that is present in lower mammals, but that has been lost during the course of human evolution.1718 Our results are consistent with the hypothesis that the high prevalence of strabismus in humans is related to an evolutionary loss of this muscle system. For example, suppose primate oculomotor systems evolved in such a way that they could maintain alignment in the presence of the ALR. When the ALR subsequently was lost during the course of human evolution, one resulting weakness would be in the direction to allow esodeviations. Tychsen and Lisberger29 proposed a theory of the causes of human strabismus that is based on a nasaltemporal asymmetry in movement/motion processing systems. Tychsen and Lisberger pointed out that one advantage of their theory is that the direction of the asymmetry provides a potential explanation for the preponderance of esodeviations over exodeviations in human infantile strabismus. Our model complements this theory by providing a potential explanation for the direction of the asymmetry. Suppose that the oculomotor systems of early primates evolved nasal-temporal asymmetries to balance or
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compensate for the abducting force generated by the ALR. Furthermore, suppose that at the current stage of the evolutionary process, humans have lost the ALR, but still maintain the asymmetry. Thus, this isolated asymmetry has now become a predisposing causal factor of strabismus in humans, as outlined by Tychsen and Lisberger.29 In other words, the prevalence of strabismus in humans may have been exacerbated in a dual manner by evolution—first, a lowered threshold (due to loss of the ALR), and second, the operation of an additional predisposing causal factor (nasal-temporal asymmetry). The fact that the ALR generates elevation in addition to abduction leads to the prediction that loss of the ALR should produce a weakness for drifting downward in addition to nasally. However, this downward weakness would be the same in both eyes, and thus would not be expected to increase the likelihood of eye misalignment, unless the ALR was abnormally small in only one eye. If we are correct in speculating that the prevalence of human strabismus is related to an evolutionary loss of the ALR, then the elevation component may be related in some way to the enigmatic finding that infantile esodeviations often exhibit dissociated vertical deviations (DVD). The simplest prediction of our model would probably be that the eye that drifts nasally should also drift downward. In DVD, the nonfixating eye does drift vertically, but it does so in an upward direction.20 This simple model can no doubt be modified in order to yield predictions in the proper direction as well. We have not done so to date, but think this issue is worthy of further study. We have not yet had an opportunity to determine whether the ALR is abnormal in our remaining monkeys with naturally occurring esodeviations. Experiments currently in progress in our laboratory are aimed at determining the distribution of the ALR across primate species and across individual family lines within species, and include comparisons between monkeys obtained from different breeding colonies. This information may provide an answer to the puzzle of why, to date, there have been no other reports of naturally occurring esotropia in monkeys. It may be that frequent esodeviations will be found only in genetic lines of primates in which the ALR is small or absent. These could include entire species, such as humans, and also genetic lines within species, such as the monkeys detected by our previous screening project.1"3* * Dr. Alcides Pissinatti at the Centro De Primatologia Do Rio De Janeiro has identified two Callithrix monkeys that have convergent strabismus (personal communication). We have conducted dissections on the orbits of four normal Callithrix cadavers and found the ALR to be absent in each of them. Based on these preliminary
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observations, we speculate that Callithrix species of monkeys are susceptible to esodeviations. Key words: strabismus, visual development, comparative anatomy, accessory lateral rectus, extraocular muscle
Acknowledgments We thank R. Bohlinger and Drs. M. Slattery and A. Fernandes for assistance with some dissections, and Drs. J. Tigges, M. Tigges, J. Wilson, J. Wallman, and L. Tychsen for providing comments on earlier versions of this manuscript. The first author expresses particular appreciation to Dr. Orville Smith, Director of the Washington Primate Center when the original monkey screenings took place, and Dr. Frederick King, Director of the Yerkes Primate Center where the current studies were conducted, for their unflagging support at all stages of this project.
References 1. Kiorpes L and Boothe R: Naturally occurring strabismus in monkeys {Macaca nemestrina). Invest Ophthalmol Vis Sci 19:842, 1980. 2. Kiorpes L, Boothe R, Carlson M, and Alfi D: Frequency of naturally occurring strabismus in monkeys. J Pediatr Ophthalmol Strabismus 22:60, 1985. 3. Boothe R, Kiorpes L, and Carlson M: Studies of strabismus and amblyopia in infant monkeys. J Pediatr Ophthalmol Strabismus 22:206, 1985. 4. National Advisory Eye Council, editors: Report of the strabismus, amblyopia, and visual processing panel. In Reports of the Program Panels. Vision Research—A National Plan. Evaluation and Update, 1987, p. 279. 5. Polyak S: The Vertebrate Visual System. Chicago, University of Chicago Press, 1957, p. 957. 6. Boycott B and Dowling J: Organization of the primate retina: Light microscopy. Philos Trans R Soc Lond [Biol] 255:109, 1969. 7. Harwerth R and Smith E: Rhesus monkey as a model for normal vision of humans. Am J Optom Physiol Optics 62:633, 1985. 8. Boothe R, Dobson V, and Teller D: Postnatal development of vision in human and nonhuman primates. Annu Rev Neurosci 8:495, 1985. 9. Boothe R: Visual development: Central neural aspects. In Handbook of Human Growth and Developmental Biology, Vol 1: Part 1. Development of the Nervous System: Sensory, Motor and Integration Development, Meisami E and Timeras P, editors. Boca Raton, Florida, CRC Press, 1989, p. 179. 10. Boothe R: Experimentally induced and naturally occurring monkey models of human amblyopia. In Comparative Perception, Vol 1: Basic Mechanisms, Berkley M and Stebbins W, editors. New York, John Wiley & Sons, 1990, p. 461. 11. Jampolsky A: Unequal visual inputs and strabismus management: A comparison of human and animal strabismus. In Symposium on Strabismus: Transactions of the New Orleans Academy of Ophthalmology. Mosby, St. Louis, 1978, p. 358. 12. Hartman C and Straus W: The Anatomy of the Rhesus Monkey. Baltimore, Williams & Wilkins, 1933, p. 344. 13. Haines K, Holmes J, and Bollert J: Eye-muscle in monkey and man. Michigan Academician 1:13, 1969. 14. Wojtowicz Z, Sadowski T, and Kurek D: The external ocular muscles in Macacus rhesus. Folia Morphologica 28:3, 1969. 15. Fuchs A and Luschei E: Development of isometric tension in simian extraocular muscle. J Physiol (Lond) 219:155, 1971.
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16. Isomura G: Comparative anatomy of the extrinsic ocular muscles in vertebrates. Anat Anz 150:498, 1981. 17. Spencer R and Porter J: Innervation and structure of extraocular muscles in the monkey in comparison to those of the cat. J CompNeurol 198:649, 1981. 18. Schnyder H: The innervation of the monkey accessory lateral rectus muscle. Brain Res 296:139, 1984. 19. von Noorden G: Binocular Vision and Ocular Motility: Theory and Management of Strabismus. St. Louis, CV Mosby, 1985. 20. Lang J: Strabismus. Cibis G, translator. Thorofare, NJ, Slack, 1984. 21. Miller J and Robins D: Extraocular muscle sideslip and orbital geometry in monkeys. Vision Res 27:381, 1987. 22. Boothe R, Joosse M, and Quick M: Orbital geometry of the accessory lateral rectus muscle in monkeys. Society for Neuroscience Abstracts 14:958, 1988. 23. Eggers H and Boothe R: Naturally occurring accommodative
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esotropia in macaques. ARVO Abstracts. Invest Ophthalmol VisSci28(Suppl):103, 1987. Parks M and Wheeler M: Concomitant esodeviations. In Clinical Ophthalmology, Vol 1, Duane T and Jaeger E, editors. Philadelphia, JB Lippincott, 1988, ch. 12. Parks M and Mitchell P: Comcomitant exodeviations. In Clinical Ophthalmology, Vol 1, Duane T and Jaeger E, editors. Philadelphia, JB Lippincott, 1988, ch. 13. Dobson V and Sebris L: Longitudinal study of acuity and stereopsis in infants with or at-risk for esotropia. Invest Ophthalmol Vis Sci 30:1146, 1989. Ingram R, Walker C, Wilson J, Arnold P, and Dally S: Prediction of refraction at age 1 year. Br J Ophthalmol 70:12, 1986. Quick M, Tigges M, Gammon J, and Boothe R: Early abnormal visual experience induces strabismus in infant monkeys. Invest Ophthalmol Vis Sci 30:1012, 1989. Tychsen L and Lisberger S: Maldevelopment of visual motion processing in humans who had strabismus with onset in infancy. J Neuroscience 6:2495, 1985.
