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University of Houston, College of Optometry, Houston, Texas 77204-2020
Submitted 28 October 2002; accepted in final form 1 August 2003
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ABSTRACT |
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INTRODUCTION |
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; Ogle 1952; Schor et al. 1984a). However, normal stereopsis is a biologically expensive process that requires exquisite coordination between well-developed motor and sensory processes. For optimal stereopsis, each eye must have good spatial vision, binocular eye coordination must be sufficient to maintain bifoveal fixation, sensory fusion must be capable of combining right and left eye images into a stable single percept, and there must be sensitive disparity-tuned mechanisms that can signal both crossed and uncrossed disparities. Each of these components requires normal visual experience to mature, and if any component fails to develop normally as a result of abnormal visual experience, stereopsis is compromised (Birch and Stager 1985; Birch and Swanson 2000; Blake and Hirsch 1975; Brooks et al. 1996; Harwerth et al. 1997a; Hess 1996; Holopigian and Blake 1986; Peters 1969; Wensveen 2001).
Anisometropia is a difference in the refractive errors between the two eyes. Because the accommodative effort is largely equal for each of the two eyes in both humans (Campbell 1960; Marran and Schor 1998) and monkeys (Flitcroft et al. 1992), an interocular difference in refractive error will cause the retinal image of one eye to be defocused relative to the other. Defocus affects spatial vision, progressively attenuating the contrast of high to low spatial frequencies with increasing magnitudes of defocus. Monocular defocus associated with either naturally occurring or simulated anisometropia essentially deprives monocular mechanisms associated with the defocused eye of high spatial-frequency information (Williams and Boothe 1983) but at the same time deprives binocular mechanisms of the same high spatial-frequency information (Westheimer and McKee 1980). If one eye is consistently defocused during early development, that eye may develop the permanent visual deficits associated with anisometropic amblyopia.
Anisometropic amblyopia manifests clinically and is largely defined as a reduction in the best-corrected monocular visual acuity of the previously defocused eye. This reduction in resolution is associated with a decrease in contrast sensitivity over progressively higher spatial frequencies. Individuals with anisometropic amblyopia also frequently have deficits in binocular vision. It has long been known that unequal image contrast in the two eyes has a deleterious effect on stereopsis (Halpern and Blake 1988; Legge and Gu 1989; Schor and Heckmann 1989; Simons 1984), and studies using clinical tests of stereopsis have shown a correlation between the degree of anisometropia, the depth of anisometropic amblyopia, and measured reductions in stereopsis (Goodwin and Romano 1985; Rutstein 1999; Weakley 2001). Laboratory investigations, however, have suggested that anisometropic amblyopia involves deficits in binocular processing that exist beyond what can be attributed to reduced monocular contrast sensitivity (Hess 1996; Holopigian and Blake 1986; Levi et al. 1979; Sireteanu et al. 1981). Little is known about the nature of binocular vision deficits in anisometropic amblyopia that are not secondary to monocular spatial vision deficits. Thus, in this study, we investigated the binocular deficits produced by early anisometropia in the absence of the monocular limitations associated with amblyopia. To dissociate uniquely binocular deficits from monocular deficits associated with anisometropic amblyopia, an alternating defocus strategy was used to provide adequate visual experience for the normal development of monocular mechanisms, but that consistently deprived binocular mechanisms of experience with high spatial frequencies. An abstract of part of these results has been published (Wensveen et al. 1997).
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METHODS |
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MONKEYS. The primary subjects were 11 rhesus monkeys (Macaca mulatta); 2 normally reared control monkeys and 9 experimental monkeys reared with alternating monocular defocus. During the rearing period, which extended from 3 wk to 9 mo of age, each of the experimental monkeys wore a negative-powered, continuous-wear contact lens (Fernandes et al. 1988) on alternate eyes on successive days. The contact lenses effectively produced an interocular imbalance in refractive error, which optically simulated an anisometropia. The lenses were alternated between eyes on successive days to allow each eye normal monocular visual experience every other day, thus reducing the likelihood that either eye would develop amblyopia. However, the rearing strategy ensured that the monkeys never experienced clear simultaneous binocular vision during the treatment period. The lens-rearing regime was purposefully delayed until the subjects were 3 wk old because visual manipulations like anisometropia that are initiated in infant monkeys after 3 wk of age are unlikely to produce a secondary strabismus (Harwerth et al. 1990; Quick et al. 1989; Smith et al. 1985). To investigate whether any effects would be graded depending on the magnitude of anisometropia, three monkeys wore a –1.50 diopter (D) lens, three monkeys wore a –3.00 D lens, and three monkeys wore a –6.00 D lens. Lens-reared monkeys are identified by the power of the lens worn and an assigned number within their treatment group (i.e., 6LR-2 was the second monkey in the group of three reared with –6 D lenses). After the 9-month period of lens rearing, the monkeys were allowed unrestricted binocular vision. Behavioral training and testing was started when the monkeys were 
2 yr old.
The refractive-error history of the lens-reared monkeys is presented in Table 1. The refractive-error data at 3 wk and at 9 mo of age are the retinoscopic results obtained at the Yerkes Regional Primate Center immediately before and after the lens rearing regimen. The refractive errors at 2 yr were determined through a subjective refraction procedure (Smith et al. 1985).
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All of the procedures used in this investigation conformed to the APS Guiding Principles for Research Involving Animals and Human Beings and followed protocols approved by the University of Houston's Institutional Animal Care and Use Committee.
Subjects
HUMANS. Two humans served as comparison subjects for a subset of the experiments. The experimental protocol for the human subjects was reviewed and approved by the University of Houston Committee for the Protection of Human Subjects and informed consent was obtained from each of the subjects. Both human subjects showed normal stereopsis by clinical testing and were experienced psychophysical observers aware of the aims of the study. Both subjects were optically corrected low myopes and 33 yr of age.
Apparatus and visual stimuli
During the daily experimental sessions, the monkeys were seated in a primate chair inside a lightproof, sound-attenuating chamber. The primate chair was fitted with a response lever on the waist plate and a drink spout on the neck plate through which orange drink reinforcement was delivered. The animal's optimal spectacle correction, which was determined for each eye independently via retinoscopy and a subjective refraction procedure (Smith et al. 1985), was held in a facemask at about a 14-mm vertex distance. For monocular viewing, the lens well for one of the eyes could be occluded with an opaque disc.
Spatial contrast sensitivity
Knowledge of the integrity of monocular spatial mechanisms was crucial for the interpretation of the binocular stereoscopic data. Consequently, to determine whether the lens-rearing paradigm had compromised our subjects' spatial visual development, spatial contrast-sensitivity functions were determined for each eye of each monkey. The basic apparatus and operant procedures were similar to those employed in previous investigations (Harwerth et al. 1980, 1990; Smith et al. 1999).
The detection stimuli were 9 x 14° patches of vertical sinusoidal gratings generated on a high brightness Joyce monitor run at a space-average luminance of 80 cd/m2. Contrast was defined as (Lmax – Lmin)/(Lmax + Lmin), where Lmax and Lmin represent the maximum and minimum luminances of the grating, respectively.
The behavioral paradigm was a temporal-interval detection task that required the monkey to press and hold down the response lever to initiate a trial, and then to release the lever within a criterion response interval following the 500-ms grating stimulus presentation. Contrast detection thresholds were measured as a function of spatial frequency from 0.25 to 16 c/° in 0.15 log unit steps. Data were collected using an adaptive staircase where contrast was reduced by 0.1 log units after each hit but was increased by 
0.3 log units following two consecutive misses. Thresholds were defined as the descending reversals, which corresponded to a hit rate of 25%.
Contrast-sensitivity functions were generated from the geometric means of a minimum of 10 threshold measurements at each spatial frequency. Each contrast-sensitivity function was fit with the following double-exponential function using an iterative routine that minimized the sum of squared errors (Movshon and Kiorpes 1988)
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Fixation disparity and interocular alignment
Eye-alignment information was also critical for the interpretation of the stereoscopic threshold data. Inspection of the positions of the first Purkinje images produced by a bright fixation target indicated that all of the experimental monkeys were orthotropic. However, to ensure that the dichoptic stereoscopic stimuli were presented to corresponding retinal points, fixation disparities were measured behaviorally as a function of prism-induced forced vergence (Harwerth et al. 1995, 1997a). In essence, the monkeys made dichoptic vernier judgments for line stimuli presented against a background that promoted binocular fusion. The offset of the dichoptically viewed line stimuli at perceptual alignment (fixation disparity) was determined over a range of horizontal prism powers. The plot of prism power (forced vergence) versus fixation disparity provided an indication of the monkey's motor fusion capabilities (Ogle et al. 1967) and, more importantly, the prism power that minimized the monkey's fixation disparity to zero (the associated phoria; Table 1).
Stereopsis:
Stereoscopic stimuli were generated by computer graphics (VSG 2/3, Cambridge Research Systems, Cambridge, UK) and were dichoptically viewed through liquid-crystal shutters (model LV 100P, DisplayTech, Longmont, CO) that were synchronized with the video frames to present alternate, noninterlaced frames at 60 Hz to each eye.
The stereoscopic stimuli were one-dimensional Gabor patches that consisted of a vertical carrier grating that was windowed by a Gaussian envelope along the horizontal meridian only, leaving the top and bottom edges sharp. The size of the Gaussian envelope was varied to maintain a spatial bandwidth of 0.5 octaves so that about four cycles of the carrier grating were visible for all carrier grating spatial frequencies (Hess and Wilcox 1994). The upper reference Gabor pattern was centered horizontally and was presented at a horizontal retinal disparity of zero to define the reference plane. The test Gabor pattern was located below the reference by a 2-arcmin gap and was presented with crossed or uncrossed disparity with respect to the reference. The binocular disparities of the stereoscopic stimuli were positioned with subpixel resolution (0.056 arcmin) using the methods of Krauskopf and Farell (1991). To eliminate monocular positional cues, the overall position of the test pattern was jittered randomly between trials, rightward or leftward by 0.5–1 times the trial disparity magnitude. We were certain that monkeys were basing their responses on binocular disparity because when one of the monkey's eyes was occluded, performance fell to chance levels.
Monkeys performed a "go/no-go" discrimination task that incorporated the essential features of a two-alternative forced-choice paradigm. An 8-Hz clicker prompted the monkey to press down on the lever to initiate a 1-s fixation cue, followed by the 0.5-s presentation of the reference and test stimuli. Correct behavior was defined as a lever release (a go response) if the test stimulus was offset in crossed disparity or a maintained lever press (a no-go response) if the test stimulus was offset in uncrossed disparity. Correct responses were reinforced with a tone and with orange drink on a percentage basis.
During a daily experimental session, five crossed and five uncrossed disparities that were equally spaced along the disparity continuum were presented in accordance with the method of constant stimuli. The resulting psychometric functions were fitted with a logistic function (Berkson 1953), and the semi-intraquartile range was taken as the disparity threshold. The results reported are the means of at least four threshold determinations.
To define the influence of spatial frequency on stereopsis, disparity thresholds (i.e., stereoacuities) were measured for a range of carrier grating spatial frequencies with the contrast of the stimulus pattern set at 100%. During each daily session, the spatial frequency of the stimulus was constant, but it was varied from 0.25 to 16 c/° between sessions. Disparity thresholds measured with 100% contrast represent the smallest disparity or the "resolution" limit for a given spatial frequency. To extend the range of our investigations of stereoscopic vision, we also investigated the effects of contrast on stereo performance for disparities that were within the normal resolution limit (Simmons and Kingdom 1994; Smallman and MacLeod 1994). First, we measured disparity thresholds as a function of stimulus contrast. In a given daily session, the stimulus contrast was held constant, but it was varied from 3.12 to 100% between sessions. Next, we measured the contrast required to support stereoscopic discrimination as a function of disparity. For these experiments, the binocular disparity of the test stimulus was held constant during a given session, but it was varied from 1 to 128 arcmin between sessions, and the contrast threshold for depth discrimination was determined. For either measurement, the method of constant stimuli was employed with 10 stimulus values equally spaced along the disparity or contrast continuum. The discrimination data were analyzed from the function of the "percent nearer" response versus stimulus magnitude. The semi-intraquartile ranges determined from logistic functions (Berkson 1953) fit to the data were used to construct composite contrast threshold versus binocular disparity functions for stimuli with spatial frequencies of 0.5, 2, and 8 c/°.
For all experiments, the data reported were collected after practicerelated improvements in performance had stabilized, and thus the visual deficits represent the irresolvable deficits caused by early abnormal visual experience.
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RESULTS |
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The spatial contrast-sensitivity functions show that the anisometropic rearing strategy was largely successful in preventing the development of significant degrees of amblyopia. Figure 1 illustrates the spatial contrast-sensitivity functions for both eyes of all of the lens-reared monkeys (
and 
) and for the left eyes of the two control monkeys (
and 
). For six monkeys, monocular contrast sensitivities were indistinguishable from normal, confirming that the alternating defocus strategy did not disrupt the development of spatial vision or the normal balance between the two eyes. However, one of the 3 D lens-reared monkeys (3LR-3) and two of the 6 D lens-reared monkeys (6LR-1 and 6LR-2) demonstrated reduced but similar monocular contrast sensitivities for high spatial-frequency stimuli. It is perhaps important that these three monkeys had large hyperopic refractive errors at the beginning of the lens-rearing period (Table 1). Thus it is possible that during early development these monkeys did not accommodate to obtain clear retinal images even with the eye not wearing the defocusing lens, which would explain their mild bilateral reductions in contrast sensitivity over the high spatial frequencies (Schoenleber and Crouch 1987; Werner and Scott 1985).
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Fixation disparity
On the basis of their rearing histories, symmetrical corneal reflexes (Quick and Boothe 1989) and behaviorally determined fixation disparities, the lens-reared monkeys appeared to be orthotropic. The range of fixation disparities determined for the lens-reared monkeys extended from 6.04 arcmin overconverged to 3.78 arcmin underconverged. These measures of fixation disparity are well below the limiting value of 33.3 arcmin, which defines a small-angle strabismus (Morgan 1969). The amount of prism required to correct for any measured fixation disparity was mounted in the viewing mask during all subsequent dichoptic testing so that the stimuli were imaged on corresponding retinal points (Table 1). Although there is no indication to the affirmative, it is important to note that it is impossible to be absolutely certain that the experimental monkeys did not have small angle strabismus with anomalous retinal correspondence.
Stereopsis across spatial frequency
Figure 2 illustrates the effects of spatial frequency on the stereopsis of normal monkey (left) and human observers (right). For descriptive purposes, the disparity versus spatial-frequency data have been fit by two-line functions using an iterative routine that evaluated the slopes and the x-y coordinates of the intersection of the two line segments, terminating with the minimum 
2 (IGOR software version 3.01, Wave-metrics, LakeOswego, OR). The pattern of results was similar for humans and monkeys. For both monkey and human subjects, the disparity thresholds decreased from low to mid spatial frequencies with slopes of less than –1 on the log-log axes (monkeys: –0.59 and –0.39; humans: –0.67 and –0.65). Disparity thresholds then increased over the higher spatial frequencies with slopes of 0.28 and 0.30 for the monkeys and 0.69 and 0.98 for the human subjects. The intersection of the two segments defined the subjects' best stereoacuity and the spatial frequency that supported optimal stereo performance. The lowest disparity thresholds for the normal monkeys were similar (0.11 and 0.17 arcmin) but slightly higher than those for the human observers (0.08 and 0.10 arcmin). Likewise the optimal spatial frequencies for stereopsis were comparable but slightly lower for the monkeys (monkeys: 3.9 and 4.9 c/° vs. humans: both at 5.3 c/°).
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In Fig. 3 top, disparity-threshold versus spatial-frequency functions are shown for each monkey segregated by treatment group along with the disparity thresholds for the normal monkeys, replotted from Fig. 2 as thick solid lines. The functions for the treated monkeys were qualitatively similar in shape to those obtained from the normal monkeys and adequately conformed to the two-line fit. However, the functions for all of the treated monkeys revealed quantitative departures from normal that generally increased in magnitude with the degree of imposed anisometropia. For the 1.5 D lens-reared monkeys (top left), elevations in the disparity threshold were primarily restricted to the higher spatial frequencies. The 3 D lens-reared monkeys (top middle) exhibited larger elevations in threshold that extended across a larger range of spatial frequencies, and the most severe deficits in stereopsis were found in two of the 6 D lens-reared monkeys (top right). In all of the treated animals, the spatial frequencies that yielded the optimal stereoacuity were lower that those observed in normal monkeys and the best disparity thresholds were elevated. The average best disparity thresholds for the 1.5 D and 3 D lens-reared monkeys were 0.32 ± 0.07 and 0.88 ± 0.45 arcmin, respectively. Although one of the 6 D lens-reared monkeys exhibited stereo deficits that were similar in degree to those found in the three 1.5 D lens-reared monkeys, the other animals reared with 6 D of anisometropia exhibited disparity thresholds that were 45 times (monkey 6LR-1, 5.8 arcmin at 1.2 c/°) and 23 times higher than normal (monkey 6LR-2, 3.2 arcmin at 1.6 c/°).
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Figure 3, bottom, compares, relative to normal, the monocular contrast detection thresholds (open symbols) and the disparity discrimination thresholds (filled symbols) for each treated monkey. The open symbols show the ratios of the monocular contrast thresholds for the poorest eye of each of the lens-reared monkeys divided by the average monocular contrast thresholds for normal monkeys. The filled symbols show the ratios of the disparity threshold for each of the lens-reared monkeys divided by the average disparity threshold for the normal monkeys. In each of the top and bottom pairs, individual monkeys are represented by the same symbols.
For the 1.5 D lens-reared monkeys (bottom left), 
, 
, and 
lay approximately along the unity line, indicating that there were no differences in contrast detection thresholds between the 1.5 D lens-reared monkeys and the normal monkeys. Disparity discrimination thresholds (, 
, and ) also show only minor differences from normal over low spatial frequencies but increasing deficits over high spatial frequencies. It is important to note that the relative elevations in disparity threshold for the 1.5 D lens-reared monkeys cannot be attributed to elevations in contrast detection threshold as there were none. Other monkeys demonstrating this pattern of results include monkeys 3LR-1 ( and ) and 3LR-2 ( and ) shown in bottom middle, and monkey 6LR-3 ( and ) shown in bottom right. For all of these monkeys, deficits in disparity processing over high spatial frequencies cannot be attributed to deficits in monocular contrast sensitivity.
On the other hand, monkey 3LR-3 ( and 
, middle), and monkeys 6LR-1 and 6LR-2 ( and and and 
, respectively, right panel) demonstrated elevations in contrast threshold that probably did contribute to the elevation in disparity threshold observed over high spatial frequencies. Across low spatial frequencies, however, the monocular contrast thresholds demonstrated by these three monkeys were normal or better than normal and therefore cannot account for the elevation in binocular disparity thresholds.
Although the observed disparity-threshold elevations cannot be accounted for entirely by a reduction in contrast sensitivity, they may reflect the relative inefficiency of the disparity discriminating mechanisms (Legge and Gu 1989), which would be revealed by a reduced gain in stereoacuity as a function of stimulus contrast. In the next set of experiments, the relationship between contrast and stereopsis was investigated to determine if there was evidence of reduced contrast gain of the disparity-sensitive mechanisms in the treated monkeys.
Contrast threshold for binocular disparity
In the previous experiment, each of the monkeys reared with alternating monocular defocus showed a deficit in stereoacuity with high (100%) contrast grating stimuli. However, measures of stereoacuity do not provide a complete characterization of stereoscopic depth perception, because sensitivities to disparities larger than the stereoacuity limit are not represented. To extend the characterization of stereopsis over a larger range of disparities, contrast thresholds for depth discrimination were measured for disparities that exceeded each subject's stereoacuity limit for stimuli of 0.5, 2, and 8 c/°.
In Fig. 4, columns of graphs represent the data from monkeys in the same lens power group (1.5, 3, or 6 D), and rows of graphs show data for the same spatial frequency (0.5, 2, or 8 c/°) across groups. In each graph, contrast threshold is plotted against disparity threshold (arcmin). The filled symbols connected by lines represent disparity thresholds measured for a series of fixed contrasts, which were varied from 100 to 3.12%. The absolute disparity thresholds are represented by the filled symbols that lie on the top line of the graphs at 100% contrast. The open symbols represent contrast thresholds measured for a series of fixed disparities, which were varied between 1 and 128 arcmin. The confluence of the two sets of data is expected as both sets of measurements probed the relationship between contrast and disparity for depth discrimination. The area contained within the bowl of the curve includes all of the combinations of contrast and disparity that can be reliably discriminated, while the area outside the curve represents combinations of contrast and disparity that cannot be discriminated. In essence, the curve represents the envelope of stereoscopic depth discrimination. The symbols on the right-hand y axis are contrast detection thresholds for the Gabor patterns used in the depth discrimination task. For each of the lens-reared monkeys, the contrast detection thresholds shown on the right-hand axes were consistently lower than the contrast threshold required for depth discrimination indicated by the plateau in the functions, indicating that, as in humans (Frisby and Mayhew 1978), depth discrimination required a reliably visible target.
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The solid lines representing the data for the two normal monkeys extend gradually down and to the right signifying that with decreasing contrast levels, larger disparities are required for depth discrimination. However, as the contrast approaches the contrast detection threshold each of the functions plateau, indicating that even as the disparity is made larger, the contrast required for discriminating depth remains constant. The contrast required over this range of larger disparities appears to be spatial-frequency dependent as higher contrasts were required for depth discrimination with the 8 c/° gratings than for either the 0.5 or 2 c/° gratings.
The extent to which the relationship between contrast and disparity for depth discrimination deviated from normal depended on the amount of anisometropia the monkeys experienced during rearing. The functions for the 1.5 D lens-reared monkeys (left) are relatively normal, whereas functions for the 3 D lens-reared monkeys (middle) are shifted toward larger disparities and higher contrasts, but the deficits in depth discrimination are most obvious for monkeys 6LR-1 ( and ) and 6LR-2 ( and ; right). These monkeys have very little area contained within their functions, indicating that they can only discriminate larger disparities at relatively high contrasts. Monkey 6LR-3 ( and ), however, only shows mild deficits similar to those demonstrated by monkeys reared with 1.5 D of defocus (left).
Monkey 6LR-3 consistently showed only minor deficits in binocular function despite having been reared with the strongest defocusing lens. There was no notable difference in his lens rearing history compared with the other two monkeys in the 6 D group. There was, however, a difference between his initial refractive error and the refractive errors of the other two monkeys reared with 6 D defocusing lenses (Table 1).
The deficits in the contrast and disparity domains for depth discrimination depended on the spatial frequency of the stimulus, where thresholds for the highest spatial frequency investigated (8 c/°) were consistently the most severely degraded. The thresholds measured for the all of the lens-reared monkeys with 0.5 c/° (top) and 2 c/° (middle) deviated from normal by approximately the same amount while thresholds for 8c/° (bottom) were elevated to a greater extent from normal and could not be measured for monkey 3LR-3.
The contrast versus disparity functions for the lens-reared monkeys were most obviously shifted upward to higher contrasts, but there may also have been increases in disparity threshold that either caused a rightward shift of the functions to larger disparities or a change in the slope of the functions. To investigate the possibility of these extra deficits in disparity processing, the upward shifts were effectively eliminated for the 2 c/° grating stimuli data by vertically re-scaling the functions so that the contrast thresholds for disparities between 8 and 64 arcmin for experimental monkeys were similar to those of normal monkeys (Fig. 5). For all of the lens-reared monkeys, stereo deficits were still apparent when the contrast disparity functions were normalized for larger disparities. Over the range of small disparities (filled symbols), the individual curves do not overlie the normal average curve but are instead displaced rightward toward larger disparities. Simply shifting the curves to the left toward smaller disparities will not superimpose the experimental data on the curves from normal monkeys because the slopes of the contrast versus disparity functions for the lens-reared monkeys are steeper than normal.
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To further examine how disparity thresholds varied as a function of contrast for the lens-reared and normal monkeys, disparity thresholds for the 2 c/° stimuli were plotted against contrast (Fig. 6). As contrast was increased from the lowest contrast tested (3.12%), disparity thresholds decreased for all monkeys, as indicated by the negative slopes of functions in Fig. 6. For normal monkeys ([hexagonblack]), the slope of the function (–0.54) follows the square-root law observed in human subjects (Halpern and Blake 1988; Legge and Gu 1989; Schor and Heckmann 1989) where the disparity threshold varies with the square root of the contrast. Although several of the treated monkeys had similar normal slopes (1.5LR-1, 1.5LR-2, and 6LR-3) all of the 3 D lens-reared monkeys (middle) showed an initial steep decrease in disparity threshold to 10% contrast. Monkeys 3LR-1 () and 3LR-2 () showed disparity thresholds that then remained relatively constant from 10 to 100% contrast. For monkeys 1.5LR-3 (, left), 6LR-1 (, right), and 6LR-2 (, right), the slopes of the disparity-threshold functions were shallow (–0.29, –0.30, and –0.33, respectively) over the entire range of contrasts compared with normal monkeys. For all of these monkeys, as the contrast of the stimulus was increased, the disparity threshold improved at a slower rate than normal.
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DISCUSSION |
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; Levi et al. 1979; Sireteanu et al. 1981). The main findings were that, with one exception, the experimental monkeys exhibited deficits in local stereopsis, the severity of which varied with the amount of induced anisometropia. Further characterization of the deficits in disparity processing showed that reduced contrast sensitivity and reduced contrast gain of disparity-sensitive mechanisms contributed to the observed behavioral deficits. Stereopsis across spatial frequency
The disparity-threshold versus spatial-frequency function represents an envelope defined by the operational limits of an array of spatial-frequency-tuned disparity-sensitivity mechanisms. The departure from the normal shape and position of the function demonstrated by the lens-reared monkeys implies that there are abnormalities in how disparity is processed in these individuals. In the following sections, specific features of the disparity-threshold versus spatial-frequency function for experimental subjects will be compared with functions for normal subjects to shed light on how disparity might be processed differently as a result of early abnormal binocular visual experience.
The two distinct segments of the disparity-threshold versus spatial-frequency function imply that there is a difference in how disparity is processed depending of the spatial frequency of the stimulus (see Fig. 4). From low to mid spatial frequencies, disparity threshold decreases proportionally (slope = –1), suggesting that a constant phase shift between the dichoptically viewed carrier gratings limits stereopsis, and from mid to high spatial frequencies, the disparity threshold remains constant (slope = 0), suggesting that a constant positional shift between the Gaussian envelopes limits stereopsis (Harwerth et al. 1995; Schor et al. 1984a).
The average slope from low to mid spatial frequencies for all our monkeys was –0.56 ± 0.13, which is lower than the slope of –1 (Harwerth et al. 1995; Schor et al. 1984a). Stimulus contrast can influence the slope of the threshold versus spatial-frequency functions through "off-frequency viewing" (Yang and Stevenson 1997). With high contrast stimuli, the measured threshold is erroneously low for the nominal spatial frequency because filters most sensitive to higher spatial frequencies, rather than the optimally tuned filters, determine the disparity threshold. Thresholds measured with low contrast stimuli are considered to provide a clearer isolation of spatial-frequency-tuned filters. To determine whether off-frequency viewing may have influenced our slope, disparity thresholds measured with low contrast (4.4%) gratings of 0.5 and 2 c/° were re-plotted (Fig. 7). The diagonal line indicates a slope of –1. Of the nine monkeys that had low contrast thresholds for both spatial frequencies (not 3LR-3 and 6LR-1), only one monkey (6LR-2) showed a slope that was not close to 1. And so, with low contrast Gabor stimuli, disparity thresholds decrease proportionally with spatial frequency, thus supporting the phase shift model over low to mid spatial frequencies.
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Over high spatial frequencies, the average slope for treated monkeys was 0.64 ± 0.4, supporting the proposal that disparity sensitivity is mediated by a mechanism sensitive to positional disparity (Schor et al. 1984a), which predicts a slope of zero but allows for a shallow positive slope due to the reduction in the effective contrast of the stimulus at high spatial frequencies (Harwerth et al. 1995; Legge and Gu 1989).
The intersection of the two line segments fit to the data demarcates the transition from a phase to a position-sensitive mechanism and identifies the spatial frequency each subject required to reliably discriminate their minimum binocular disparity. All of the lens-reared monkeys achieved their best stereoacuity with spatial frequencies between 1.14 and 2.58 c/° compared with 3.58 and 4.90 c/° for normal monkeys. The phase-sensitive mechanisms that the normal monkeys used for these higher frequencies were unavailable to the lens-reared monkeys, presumably because these mechanisms did not develop due to the selective deprivation of binocular high spatial frequencies caused by monocular defocus. Without these mechanisms, the lens-reared monkeys could not achieve the same minimum disparity thresholds that normal monkeys did. Instead, lens-reared monkeys reverted to processing the positional disparity between the Gaussian envelopes, which would not support disparity thresholds as low as those ordinarily supported by phase-disparity processing. There must also be a deficit in these mechanisms using positional disparity because the plateaus of the functions were elevated from normal.
Contrast threshold for binocular disparity
Because defocus during rearing would have attenuated contrast to binocular mechanisms, the relationship between contrast and disparity for depth discrimination was investigated to determine if the observed abnormalities in disparity thresholds could be due to faulty contrast processing of the disparity-sensitive mechanisms. The vertical displacements of the contrast threshold for binocular disparity functions certainly indicate a deficit in contrast sensitivity of the disparity-sensitive mechanisms, but the residual departure from the normal curve following scaling for reduced contrast sensitivity implies additional contrast processing deficits (Fig. 5).
Two features of the disparity versus contrast functions distinguished lens-reared monkeys from normal (Fig. 6): the steep initial slope over low contrasts (3 D lens-reared monkeys) and the shallow overall slopes. The steep initial slope indicates that when the contrast of the stimulus is increased by a small amount, the disparity threshold improves dramatically. This high contrast gain has been reported near the binocular contrast detection threshold of normal observers (Halpern and Blake 1988). Examination of the proximity of detection thresholds to contrast thresholds for depth discrimination (Fig. 4, center) reveals that the 3 D lens-reared monkeys were operating close to their contrast detection thresholds.
The slope of the disparity versus contrast functions were shallow compared with normal for monkeys 1.5LR-3, 3LR-1, 3LR-2, 6LR-1, and 6LR-2. As a consequence, increasing the contrast for these treated monkeys produced smaller than normal improvements in disparity threshold, which implies that the contrast gain of the disparity-sensitive mechanisms had been decreased. It is also clear that it is not possible to overcome the stereo deficiency for small disparities simply by increasing the contrast of the stimulus. The apparently low contrast gain for depth discrimination is at odds with the higher than normal contrast gain reported for contrast perception in amblyopes (Hess and Bradley 1980; Loshin and Levi 1983). Contrast perception is most anomalous at threshold, but as the stimulus contrast is increased incrementally, the change in perceived contrast increases at twice the normal rate, so that at high contrasts, the contrast perception of the amblyopic eye is essentially normal. Unlike the contrast perception of an amblyopic eye that typically normalizes at suprathreshold contrasts (Georgeson and Sullivan 1975; Hess and Bradley 1980; Hess et al. 1983; Loshin and Levi 1983), relative depth discrimination, like contrast discrimination (Bradley and Ozhawa 1986; Levi 1991), reaction times (Levi et al. 1979; Loshin and Levi 1983), and visually evoked potentials (Levi and Harwerth 1978), does not appear to normalize at suprathreshold contrasts.
Implications for humans
The visual system of the rhesus monkeys closely approximates the human visual system (Boothe 1982; Boothe et al. 1985; Harwerth and Smith 1985a,b; Movshon and Kiorpes 1988; Smith et al. 1982). This has proven to be true when comparing visual functions in normal individuals and, increasingly, when comparing visual functions in monkeys that have undergone some visual perturbation approximating a disorder of human vision (Harwerth and Smith 1993; Harwerth et al. 1997a, 1981; O'Dell et al. 1989; Smith et al. 1985, 2000; Tusa et al. 2002). The similarities observed between human and normal monkey subjects in this study further substantiates the rhesus monkey as a model of human vision and allows us to consider the implications of the results from our treated monkeys for human anisometropes.
Patients with anisometropic amblyopia show deficits in stereopsis. Simulating anisometropia in normal observers reasonably approximates the deficits in monocular processes, and these deficits undoubtedly contribute to a reduction in stereopsis (Brooks et al. 1996; Davson 1962; Donzis et al. 1983; Goodwin and Romano 1985; Larson and Lachance 1983; Levy and Glick 1974; Lovasik and Szymkiw 1985; Ong and Burley 1972; Simons 1984; Westheimer and McKee 1980; Wood 1983). Our results, however, show that in addition to these effects, there are additional deficits in binocular processing that are the result of the incongruence of neural input associated with early anisometropia. Patients with anisometropic amblyopia would have these deficits in binocular function in addition to the deficits that follow from their reduced visual acuity and clinical suppression, and these deficits in stereopsis would vary with the magnitude of the early anisometropia. Patients with a history of early anisometropia but with normal visual acuity (myopic anisometropes, for example, or anisometropic amblyopes who have been successfully treated for their amblyopia) are also expected to show these deficits in binocular function.
In the visual world where most scenes are not high contrast but do have rich spatial-frequency content, these deficits in stereopsis may only limit performance of tasks that require a high degree of stereopsis. In everyday life, however, deficits in stereopsis would probably be compensated for by a general reduction in reliance on binocular depth information and a greater reliance on monocular depth cues (Harwerth et al. 1998; O'Shea et al. 1994; Schor and Howarth 1986).
Conclusions
These investigations have demonstrated that, apart from the monocular sensory deficits associated with amblyopia, there are binocular sensory deficits that occur as a result of the incongruous neural input associated with early anisometropia. The severity of the observed deficits vary directly with the magnitude of the simulated anisometropia experienced during the rearing period and the target spatial frequency. For a given spatial frequency, the treated monkeys generally required more contrast to support stereopsis even for large disparities, suggesting that the observed deficits in stereopsis is, in part, due to reduced contrast sensitivity of the disparity-sensitive mechanism. Additionally, a given increase in contrast produced smaller-than-normal improvements in stereo discrimination in our treated subjects, which suggests that in addition to deficits in contrast sensitivity, disparity-sensitive mechanisms exhibited low contrast gains. The spatial-frequency-selective nature of the binocular deficits produced by the imposed anisometropia indicate that disparity-processing mechanisms are normally spatial-frequency selective and that mechanisms tuned to different spatial frequencies can be differentially affected by abnormal binocular visual experience. The deficits in binocular functioning documented here add to our growing awareness of the complex and pervasive nature of the visual deficits associated with anisometropic amblyopia. The following paper reports on the physiology of neurons in cortical area VI of these anisometropic subjects (Zhang et al. 2003).
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DISCLOSURES |
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Address for reprint requests and other correspondence: J. M. Wensveen, University of Houston, College of Optometry, 505 J. Davis Armistead Bldg., Houston, TX. 77204-2020 (E-mail: Jwensveen{at}uh.edu).
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, and 
, the average for the 2 normal monkeys. Error bars are the SD. The slopes of the line segments fitted to the data and the R2 values indicating the goodness of fit are shown in parentheses beside the legend.