Effects of Refractive Error on Detection Acuity and Resolution Acuity in Peripheral Vision

Yi-Zhong Wang, Larry N. Thibos, and Arthur Bradley

Purpose. To evaluate the effect of refractive error on detection acuity and resolution acuity in peripheral vision. Methods. Detection acuity, defined as the highest spatial frequency for which luminance gratings can be discriminated from a uniform field, and resolution acuity, defined as the highest spatial frequency for which spatial patterns are perceived veridically, was determined for vertical and horizontal gratings located at 20, 30, and 40 of eccentricity. Resolution was also measured for tumbling-E discrimination at these locations. Refractive state of the eye for test targets was manipulated by introducing an ophthalmic trial lens into the line of sight for the stimulus while holding accommodative state fixed. Results. Detection acuity in the periphery varied significandy with the amount of optical defocus, whereas acuity for grating resolution or letter discrimination was unaffected by defocus over a large range (up to 6 D). These results are consistent with the working hypothesis that detection acuity in the periphery is limited by contrast insufficiency under normal viewing conditions, but resolution is limited by ambiguity because of neural undersampling. Conclusions. The large depdi of focus for resolution acuity measured for peripheral vision indicates that spatial resolution is likely to remain sampling-limited even when peripheral refractive errors are not fully corrected, thus relaxing the methodologic requirements for obtaining noninvasive estimates of neural sampling density of the living eye in a clinical setting. Invest Ophthalmol Vis Sci. 1997;38:2134-2143.

.Diagnosis and monitoring of retinal diseases that cause a functional loss of optic nerve fibers would be enhanced by the development of noninvasive techniques for estimating the spatial density of the array of ganglion cells that samples the retinal image in the living eye.1'2 A body of experimental evidence indicates that psychophysical resolution acuity for highcontrast sinusoidal gratings viewed in the peripheral visual field fulfills this requirement. The argument has two parts: first, resolution is limited by the sampling density of visual neurons, and second, the neurons in question are the retinal ganglion cells. Evidence that peripheral resolution is sampling-limited comes primarily from reports of spatial aliasing and of motion aliasing.1'3"17 These experiments have shown that in peripheral vision, unlike foveal vision, acuity for deFrom the Visual Sciences Group, School of Optometry, Indiana University, liloomington, Indiana. Supported by National Eye. Institute grant R01 EY05109 (LNT). Submitted for publication. January 16, 1997; revised April 7, 1997; accepted April 9, 1997. Proprietary interest category: N. Reprint requests: Lany N. Thibos, Visual Sciences Optometry, Indiana University, 800 E. Atwater, Room 514, Bloominglon, IN 47405.

tecting the presence of a sinusoidal grating is much higher than acuity for resolving the grating's orientation, or the direction of motion when drifting. The common explanation for these results is that detection acuity is limited by the contrast-transfer properties of the eye's optical system, which are known to be nearly as good in the periphery as in the fovea when refractive errors are corrected. 18 " 20 On the contrary, resolution acuity is limited by the ambiguity of aliasing introduced when the retinal image is undersampled by the neural array of photoreceptors, which may be further undersampled by retinal ganglion cells.17 This explanation also accounts for the observation that perceptual aliasing occurs throughout the range of spatial frequencies from resolution cutoff to detection cutoff, and that contrast sensitivity for grating detection is much greater than unity at the cutoff frequency for resolution. 14 Saturation of resolution acuity with increasing stimulus contrast constitutes additional evidence that peripheral resolution is limited by neural undersampling, rather than by the contrast-attenuating effects of poor peripheral optics.14'18'20 In principle, the sampling limit to visual resoluInvestigative Ophthalmology & Visual Science, September 1997, Vol. 38, No. 10 Copyright Association for Research in Vision and Ophthalmology

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Effect of Defocus on Peripheral Acuity tion is set by the coarsest neural array in the early visual pathway because the highest spatial frequency that can be represented veridically by a neural array (i.e., the Nyquist frequency) varies directly with the sampling density of the array. In the human eye, the sampling density of retinal ganglion cells in the macular region exceeds that of cone photoreceptors21; therefore, resolution in the macula would be determined by cone density, not by ganglion cell density.5 However, starting at approximately 10 of eccentricity (or slightly less, depending on meridian), cones outnumber ganglion cells, and therefore we should expect resolution acuity in the periphery to be determined by the relatively low sampling density of the ganglion cell mosaic. This expectation has been confirmed experimentally by the close match discovered between psychophysical measurements of resolution acuity and anatomic predictions.3'1022 Thus, the evidence suggests that not only is visual resolution sampling-limited in the periphery, but the limiting array is the mosaic of retinal ganglion cells. It follows that the death of ganglion cells in peripheral retina due to diseases such as glaucoma23 should lower the behavioral resolution limit. Although experimental tests of this prediction have not yet been reported, we know that the technique is sensitive enough to reveal the subtle changes in ganglion cell density associated with the visual streak in healthy human eyes.24 If the sampling theory of visual resolution described above is to become useful in a clinical context (e.g., perimetry) to measure neural sampling density noninvasively in a diseased or normal eye, the potential for uncorrected refractive errors in the peripheral field to vitiate the technique must be clearly understood. Although sampling-limited performance for grating resolution can be achieved under laboratory conditions in which peripheral refractive errors are optically corrected (or avoided altogether by using interference fringes to stimulate the retina), the sampling limit might not be achievable in a clinical environment unless the substantial (and highly variable) refractive errors of the peripheral field25'26 are corrected. Anticipating the practical difficulty of optically correcting the entire visual field in clinical perimetry, it becomes important to establish the extent to which optical defocus differentially affects detection acuity and resolution acuity across the visual field. Some degree of tolerance to defocus is to be expected for the resolution task because previous studies using conventional acuity targets have shown that accurate correction of refractive errors in the periphery is unnecessary for achieving optimal resolution acuity.27"32 These earlier findings are consistent with a sampling-limited model because the effect of uncorrected refractive error is to attenuate retinal image contrast. Because grating resolution is limited by sampling rather than by contrast when refractive errors are corrected, a small

2135 amount of optical blur is of no consequence. For example, contrast sensitivity is approximately 10 for sinusoidal gratings at the resolution limit at 30 eccentricity in a well-corrected eye.14 Therefore, resolution acuity should be immune to optical blur, which produces as much as 10-fold attenuation of retinal image contrast. If the optical blur is large enough, however, retinal contrast will be attenuated so severely that insufficient contrast could become the limiting factor for visual resolution, thus defeating the clinical use of resolution acuity to estimate the sampling density of retinal ganglion cells. The aim of this study was to determine how much optical defocus can be tolerated in the peripheral field before contrast attenuation replaces neural undersampling as the critical factor limiting resolution acuity. We call the range of optical defocus for which resolution acuity remains constant the "depth of focus for resolution," and our main purpose was to measure its magnitude as a function of retinal eccentricity. Aside from the clinical applications mentioned above, knowledge of the depth of focus for resolution is important more generally for understanding the relevance of spatial and motion aliasing in human vision. Although it may be tempting to dismiss aliasing as a laboratory curiosity of no practical importance in daily life, on the grounds that objects in the peripheral field are habitually out of focus in an eye that accommodates on foveal targets, a rigorous approach requires that we investigate the amount of defocus required to abolish aliasing from visual experience. METHODS Three experienced subjects (the authors) participated in the study after their informed consent was obtained. The experimental protocol conformed to the tenets of the Declaration of Helsinki and was approved by an institutional review board. One subject (YZW) participated in all experiments; the other two subjects participated in selected experiments. High-contrast (80%) grating stimuli were generated on a computer monitor placed 20, 30, or 40 in the horizontal nasal field. Targets were 2.5 circular patches with mean luminance of 55 cd/m 2 . The subject viewed the peripheral stimulus with the right eye while maintaining constant fixation and accommodation on a distant target (3 meters). Pupil diameter during the experiment was typically 4 to 4.5 mm, and the fellow eye was occluded. Subjective refractive errors for central vision were determined with the experimental apparatus for each subject at the time of the experiments. The average refractions were +1.00/ -0.75X090 (AB), -0.50/-0.50X090 (LNT), and -3.37/-1.88X180 (YZW). Corrective lenses required for clear viewing of the fixation target were placed well in front of the subject's eye to avoid interfering

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with the peripheral field under study. Refractive state of the eye for the peripheral target was manipulated without inducing changes in accommodation by introducing an ophthalmic trial lens into the line of sight for the stimulus, but not for the fixation target. The distance from the back vertex of the peripheral trial lenses to the subject's cornea was 50 mm. Lens powers used in the experiment ranged from 7.00 D to +4.00 D. The effect of spectacle magnification on grating spatial frequency was corrected by dividing by factor m, defined as:
1

m = 1 - aF

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where 7?is the back vertex power of the trial lens and a is the back vertex distance of the trial lens to the center of the entrance pupil of the eye. F carries the sign of trial lens, and therefore m is greater than 1 for positive trial lenses. Detection acuity, defined as the highest spatial frequency for which gratings can be discriminated from a uniform field of the same mean luminance, was determined for vertical and horizontal gratings located at selected eccentricities as a function of spherical lens power. In a two-interval, forced-choice, contrast-detection paradigm,14 subjects were presented on each trial with either the grating or a uniform field of the same mean luminance. The subject's task was to say which interval contained spatial contrast (i.e., was not uniform). Detection acuity was measured either with full psychometric functions determined by the method of constant stimuli or with a dual staircase method. In the staircase method, vertical and horizontal gratings were randomly interleaved from trial to trial, and the responses to vertical and horizontal gratings were recorded separately. Detection acuity was taken as the average of seven reversal frequencies (the initial two reversals in staircase method were discarded). When the method of constant stimuli was used, detection acuity was interpolated with a Weibull function33'34 fit to the data using a least squares criterion. Resolution acuity for vertical and horizontal gratings was determined as a function of spherical lens power with a method of adjustment procedure.14 In each trial, the subject was presented with a grating stimulus oriented vertically or horizontally. The subject slowly changed the spatial frequency of the grating stimulus (starting from a low spatial frequency level where the grating's apparent orientation was clearly veridical) until the grating first appeared to alias.4 In this way, a lower-bound estimate of resolution acuity was obtained. Previous studies have documented the close agreement between the end point obtained by this method of adjustment and the grating resolution

limit obtained by forced-choice paradigms using tasks requiring discrimination of either motion direction or orientation.15 Anticipating a preference for letter targets in a clinical environment, we also measured discrimination acuity for high-contrast (80%) tumbling-E letters. Previous experiments35 indicated that the tumbling E is a suitable target for eliciting sampling-limited behavior in peripheral vision, and therefore we expected that letter and grating targets would yield similar estimates of resolution acuity. Two pairs of tumbling-E orientations were used: right E versus up E, and right E versus left E. The aspect ratio of the letters was 1:1, with stroke width equal to one fifth the dimension of the letter. For comparison with grating resolution, the threshold size of the tumbling Es was converted to letter discrimination acuity in terms of the characteristic frequency of the letter (2.5 cyc/letter). Minimum resolvable letter size was measured as a function of spherical lens power by using a single-presentation, two-alternative, forced-choice paradigm. On each trial, subjects were presented with a single stimulus, and the task was to indicate the letter's orientation. The size of the smallest discriminable letter was determined by a single staircase method, which averaged seven reversals (the initial two reversals in the staircase method were discarded).

RESULTS Effect of Spherical Defocus on Grating Resolution Acuity Figure 1 shows the resolution acuities measured for vertical and horizontal gratings for three subjects at 20 horizontal nasal field as a function of trial lens power. Higher resolution for horizontal gratings is evident for each subject, as expected from previous work.143236 Maximum resolution acuities were 3.0, 3.4, and 3.5 cyc/deg for vertical gratings and 4.3, 4.2, and 5.2 cyc/deg for horizontal gratings, respectively, for subjects AB, LNT, and YZW. These results are consistent with the resolution limits obtained from the same subjects at the same eccentricity using other psychophysical methods.15 Little or no change in grating resolution acuity occurred over a large range of optical defocus (6 D or more). Similar results obtained from one subject (YZW) tested at two other eccentricities (30 and 40 horizontal nasal field) are shown in Figure 2. Again, the resolution acuity for horizontal gratings is higher than that for vertical gratings at each eccentricity. Although grating resolution acuity decreased at more eccentric locations, grating resolution acuity was largely independent of defocus over a range of 6 to 8 D at every eccentricity tested.

Effect of Defocus on Peripheral Acuity

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by optical defocus. To test this prediction, tumblingE acuities were determined as a function of trial lens power for our three subjects at 20 eccentricity. The results are compared in Figure 3 with the resolution acuities for horizontal gratings shown in Figure 1. Each data point for letter acuity in Figure 3 is the average result of right E versus up E and right E versus left E discrimination. As predicted, tumbling-E acuity is independent of defocus over a range of approximately 6 D (letter acuity changes <0.5 cyc/deg, or 0.06 log MAR). A slightly better acuity (approximately 5%) was found for the discrimination of right E versus up E. The systematic inferiority of letter acuity to grating acuity (even when averaged across orientations) can be traced to the reduced number of cycles in a letter stimulus and is consistent with the claim that resolution acuity for tumbling-E targets is samplinglimited.37 Despite correction of systematic magnifica-

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FIGURE l. Grating resolution (open symbols) and detection (filled symbols) acuities as functions of trial lens power measured at 20 horizontal nasal field for three subjects. Open circles and open triangles indicate resolution acuities for vertical and horizontal gratings, respectively. Each resolution acuity was the average of at least five settings by the method of adjustment. The standard errors of means for resolution acuity are less than symbol radius in most cases. Detection acuities estimated by the dual staircase method for vertical and horizontal gratings are represented by filled circles and filled triangles, respectively. Detection acuities also were determined with the method of constant stimuli for subject YZW (bottom panel; filled squares represent vertical gratings and filled inverted triangles represent horizontal gratings). Error bars for the latter data set represent 1 SEM of three measures and are smaller than symbols in most cases.

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FIGURE 2. Grating resolution (open symbols) and detection (filled symbols) acuities as functions of trial lens power measured at 30 (a) and 40 (b) eccentricities for subject YZW. Open circles and open triangles indicate resolution acuities for vertical and horizontal gratings, respectively. Each resolution acuity was the average of 10 settings by the method of adjustment. The standard errors of means for resolution acuity are less than symbol radius in most cases. Filled circles and filled triangles represent detection acuities for vertical and horizontal gratings, respectively, derived from psychometric functions. Error bars for detection acuities are 1 SEM of three measures.

Effect of Spherical Defocus on Letter Discrimination Acuity If letter acuity for the tumbling-E alphabet is sampling-limited in peripheral vision, as suggested by Anderson,35 then it too should be relatively unaffected

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30 in the horizontal nasal field. The squares indicate performance when the target is well focused, the circles when the target is approximately 4 D out of focus. Curves are Weibull functions fit to the data points. The major effect of defocus was a shift of the psychometric function to lower spatial frequencies, with a secondary effect of increased slope of the psychometric function when plotted on semilogarithmic axes. Accordingly, the loss of detection acuity due to defocus could be quantified by the horizontal location of the psychometric function, which was interpolated from the Weibull functions at the 82% correct level. Psychometric functions of the kind illustrated in Figure 4 were collected for a series of defocus powers for one subject (YZW) and each result was summarized by the change in detection acuity. This effect of defocus on detection acuity is compared with the corresponding effect on resolution acuity in the bottom panel of Figure 1 for targets located at 20 of eccentricity. A similar comparison is drawn in Figure 2 for the same subject tested also at 30 and 40 eccentricities. These results clearly demonstrate that unlike resolution, grating detection acuity depends strongly on optical blur in the periphery. This result was confirmed on all three subjects using a more efficient staircase methodology for measuring detection acuity (see Fig. 1). Although the detection curves show a less pronounced peak for the more eccentric target locations, an optimal lens power that maximizes detection acuity is clearly evident at each eccentricity tested. The presence of off-axis astigmatism is revealed by the difference between optimal lens powers for vertical and horizontal gratings. One potential clinical application suggested by these results is the use of a con-

Power of Trial Lens (diopter)

FG R 3. Effect of optical blur on letter discrimination [filled IUE squares) and resolution acuity for horizontal gratings (open squares) at 20 eccentricity for three subjects. Each letter discrimination acuity is the average result for right E versus up E and right E versus left E, and it is represented by the characteristic frequency of the tumbling Es (2.5 cyc/letter). The standard errors of means are less than symbol radius in most cases. Open arrows indicate the optimal correcting lens (dioptric power that maximized detection acuity) for horizontal gratings at the peripheral test location. Filled arrows indicate the optimal correcting lens for horizontal gratings in central vision.

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tion effects, positive spherical defocus had a larger effect than negative defocus on letter acuity; this might be due to the interaction of defocus with positive spherical aberration in our subjects' eyes.38 Effect of Spherical Defocus on Grating Detection Acuity Figure 4 shows typical examples of psychometric functions for the detection of vertical gratings obtained at

Spatial Frequency (cyc/deg)

FIGURE 4. Typical examples of psychometric functions for contrast detection of vertical gratings by subject YZW. Target location was 30 in the horizontal nasal field. Squares represent the data for a well-focused grating; circles represent the data for a defocused grating. Threshold (82% correct) was interpolated using Weibull functions (smooth curves) fit to the experimental data.

Effect of Defocus on Peripheral Acuity

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trast-detection task for subjective refraction of the peripheral visual field.39 At any given lens power, the vertical separation between detection and resolution curves in Figures 1 and 2 defines the aliasing zone, a range of spatial frequencies over which subjects experienced subjective aliasing.4 For subjects AB and LNT, the aliasing zone is nearly the same for vertical and horizontal gratings. However, for subject YZW, the aliasing zone depended strongly on stimulus orientation. A - 1 D lens, for example, nearly abolished aliasing for horizontal gratings but maximized the aliasing zone for vertical gratings. This effect, which we call meridional aliasing, is evidently caused by the much larger degree of astigmatism in the peripheral field for YZW than for the other subjects. In the clearly focused meridian, high-frequency targets produce high-contrast retinal images that are subject to aliasing, whereas the orthogonal meridian may be spared aliasing because of the blurring effect of unconnected peripheral astigmatism. DISCUSSION The results of this study demonstrate that the effect of optical defocus on peripheral visual acuity is much greater for the psychophysical task of contrast detection than it is for spatial resolution. This strong impact of defocus on detection acuity indicates that detection is contrast-limited in peripheral vision, just as it is in central vision. Resolution acuity, however, is immune to several diopters of defocus in the periphery because peripheral resolution is limited by neural sampling density, which is independent of retinal image quality. With sufficient defocus, detection acuity falls to the level of resolution acuity and perceptual aliasing is precluded. Further blurring would be expected to attenuate retinal contrast to a level below the minimum required to support sampling-limited performance, causing resolution acuity and detection acuity to fall in concert. In this study, we did not systematically explore this domain of large refractive errors, nor did we attempt to evaluate the extent to which phase reversals may have been present in the blurred retinal images of the test stimuli. One clinical implication of our results is that careful correction of peripheral refractive errors is critical for obtaining optimal performance from patients undergoing diagnostic tests based on contrast detection (e.g., conventional perimetry using differential light sensitivity for small spots of light). Although Frankhauser and Enoch demonstrated this fact in a clinical environment many years ago,40 the correction of peripheral refractive errors during perimetry has not yet become standard clinical practice. Recognition of this shortcoming is important also for newer forms of perimetry based on the detection of contrast in vanishing optotypes.41 Another clinical implication of our results is that

correction of the entire visual field using the prescription appropriate for central refractive errors may be sufficient to elicit sampling-limited performance from patients performing visual resolution tasks in peripheral vision. As illustrated in Figure 3 for our three subjects, peripheral resolution acuity for gratings measured with optimal correction of refractive error is the same as acuity measured with the foveal correction. This forgiving nature of peripheral resolution would seem to be responsible for the general agreement between numerous studies of peripheral visual acuity in the literature,42 which is remarkable considering the large variability in experimental protocols pertaining to the correction of refractive errors. Exceptions to this rule are described below, however, so it is not always true that correcting central refractive error is adequate for measuring sampling-limited performance in the periphery. Verification of Sampling-Limited Behavior Sampling-limited performance in a psychophysical resolution task is akin to diffraction-limited performance of an optical system: it is the highest level of performance attainable given the physical constraints of unavoidable limitations. Achieving sampling-limited performance is a prerequisite for psychophysically estimating neural sampling density because if sampling is not the limiting factor, then some other mechanism (e.g., spatial filtering by optical defocus or neural spatial summation) must be, thus defeating the rationale of the test. Our finding that resolution acuity is insensitive to defocus increases the likelihood that sampling-limited performance will be attained in a clinical testing environment, but it is not a guarantee. Therefore, it is important to have methods available to verify that an individual patient has achieved sampling-limited performance on any given test of spatial resolution. The accepted method of verification is to show that stimuli beyond the measured resolution limit lead to perceptual aliasing, which may be demonstrated in several different ways. The first is to show that detection acuity exceeds resolution acuity, the second is to show that contrast sensitivity for detection exceeds that for resolution, and the third is to show that errors are made in judging the direction of motion of a drifting grating. Other ideas for verifying the presence of aliasing have proved to be less useful. For example, asking subjects to detect the jagged edges of lines or bars does not work well because of die low contrast present in the higher-frequency components of such stimuli."16 Checking for perceived motion reversal of drifting gratings is also problematic,13 but this idea is easily rescued by testing instead for evidence of nonveridical motion perception.15 In this paper we concentrated on the first method mentioned above, and show, in agreement with previous research,13'20 that

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Horizontal Nasal Visual heici 40* 30" 20" 10' i-tonzontal Nasal Visual Field 0" 40" 30" 20* 10' 0'

uncorrected peripheral refractive errors reduce the cutoff spatial frequency for detection. Therefore, when refractive errors are large, detection acuity falls to the level of resolution acuity, which unfortunately produces uncertainties in the verification process. Thus, the ideal situation is to correct peripheral refractive errors as accurately as possible. In the next section we introduce a method for quantifying acceptable tolerance levels for residual defocus. Depth of Field for Resolution We define depth of field for resolution as the range of viewing distances over which high-contrast gratings with spatial frequency just beyond the resolution limit can be positioned without affecting their resolvability. Our results indicate that the depth of field for peripheral resolution is approximately 6 D in the midperiphery (20 to 40 eccentricity). This is an extremely large range that, under favorable conditions, may encompass nearly all of visual space. The linear range is maximized when the eye is accommodated to the dioptric midpoint (33 cm), in which case the visual resolution of objects placed anywhere from 16 cm in front of the eye to infinity would be limited by neural undersampling. In general, however, the range of viewing distances encompassed by depth of field depends on the eye's state of accommodation and peripheral refractive error. Fortunately, with such a large depth of field available, it should be easy to position this range optically so as to include target distances typically used in clinical perimetry and campimetry. To visualize how depth of field for resolution changes across the visual field, it is convenient to use a dioptric scale for object distances so that distances beyond optical infinity can be illustrated. Figure 5 shows such a depth of field plot for die horizontal nasal field of the right eye of subject YZW. The data are plotted relative to the central refractive error, which is tantamount to assuming the refractive error of the eye has been corrected widi prescription lenses appropriate for central vision. (For subject YZW, the lens powers that maximized detection acuity for vertical and horizontal gratings in central vision were 3.37 D and 5.25 D, respectively). The sign convention for the object distance scale is the same as the sign of blurring lenses used in the experiments. Zero on the scale represents optical infinity, negative blurring lenses create virtual objects closer to the subject, and positive lenses create virtual objects farther away. Depth of field for resolution by an eye corrected for central vision depends on the subject's natural refractive error in the peripheral field. This information can be deduced from the experimental data by noting the lens that maximized detection acuity for vertical or for horizontal gratings at each eccentricity tested. The dioptric difference between these optimal lens values for peripheral vision and the optimal lenses

Depth of field for vertical gratings

Depth of field for horizontal gratings

FIGURE 5. Depth of field for resolution in dioptric space in the horizontal nasal field of the right eye of subject YZW. Results for vertical and horizontal gratings are shown separately. Zero diopters on the vertical axis represents central emmetropia or corrected ametropia (i.e., diopters on the vertical axis are relative to the subject's central correction). Thick lines indicate the optimal lens power (i.e., power that maximizes detection acuity). Thin lines indicate the lens power that reduces detection acuity to match resolution acuity (i.e., eliminates aliasing). Shaded area indicates the depth of field for resolution (i.e., dioptric range for which resolution acuity remains constant and sampling-limited). Also shown are symbols representing the lens power that reduces detection acuity to match resolution acuity for subjects AB {filled circles) and LNT {filled squares) at 20 eccentric-

ity. Detailed shape of the shaded region between 0 and 20 eccentricity is unknown. for central vision are shown by the thick lines in Figure 5. These thick lines are interpreted as the locus of object distances that are conjugate to the retina for a centrally corrected eye. Because subject YZW is hyperopic in his peripheral field when the eye is optimally corrected for central vision, the thick line lies beyond optical infinity in the figure. Thin lines in this illustration indicate the lens power that reduces detection acuity to the level of resolution acuity at any given eccentricity. Thus, the shaded region bounded by thin lines is the depth of field for resolution and corresponds to the range of distances over which high-contrast gratings just beyond the resolution limit can be positioned without affecting their resolvability. Although resolution acuity is constant throughout the shaded region, detection acuity varies significantly, peaking at the retinal conjugate distance marked by the thick line. Outside the shaded region, gratings at the resolution limit are so badly blurred that they are not detectable, which prevents aliasing and reduces resolution acuity below the retinal sampling limit. Consequently, targets located outside the shaded region would not be suitable for estimating the sampling density of retinal neural arrays. Two interesting features of depth of focus for resolution are evident for subject YZW. First, the dioptric extent of the interval at any given eccentricity is

Effect of Defocus on Peripheral Acuity 6 4

2141 Under these conditions, aliasing will not occur and resolution acuity will not reach the levels expected of a sampling-limited task. In this case, a diagnostic perimetry test using horizontal gratings would not be a valid indicator of neural sampling density for this patient. Conversely, if the stimulus is oriented vertically forYZW, then his depth of field for resolution is more symmetrically placed about the 0 D line, and samplinglimited performance would be expected. For this reason, the condition of meridional aliasing mentioned above can have important practical implications for estimating neural sampling density psychophysically. The presence of large amounts of uncorrected off-axis astigmatism in the general population 25 ' 26 ' 43 suggests that meridional aliasing, in which spatial frequency components of one orientation are focused clearly enough to cause aliasing but components of another orientation are blurred sufficiently to prevent aliasing, may be common. The asymmetric nature of the depth of field for resolution for subject YZW is probably due to his high degree of central myopia in the horizontal meridian (5.25 D), which changes rapidly toward hyperopia with increasing eccentricity. More symmetric fields were obtained for the other two subjects, who are nearly emmetropic centrally. Although a less extensive data set was obtained for these subjects, Figure 5 shows that the near and far boundaries of depth of field for resolution for AB and LNT at 20 eccentricity are more evenly spaced about 0 D for both target orientations. Importance of Correcting Off-Axis Astigmatism This study demonstrates that over a large dioptric range (approximately 3 D), resolution acuity is independent of optical blur of the retinal image in peripheral vision. The existence of such a large depth of field for resolution suggests that correction of peripheral refractive errors may not be critical for obtaining sampling-limited performance from patients, provided that peripheral test targets are not more than 2 or 3 D out of focus. This condition, in turn, depends on the refractive errors of the natural eye in the peripheral field. Therefore, to appreciate the clinical implications of our findings, our results n ust be interpreted in the context of individual differences in the refractive errors of the peripheral visual field found in the general population. Ocular astigmatism is typically described as mixed, myopic, or hyperopic, depending on whether the principal image planes straddle the retina or are entirely anterior or posterior to the retina, respectively. Ferree et al2D'44'45 further classified the pattern of peripheral refractive errors into three types: mixed astigmatism at all eccentricities (type A); typically hyperopic astigmatism at all eccentricities, or myopic astigmatism centrally, which changes to hyperopic astigmatism for

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(solid thick curves) and for horizontal gratings (broken thick

curves). Thin curves are drawn parallel to the thick curves at a distance of 2.5 D. Regions filled with 45 oblique lines (/) represent the depth of field for resolution of vertical gratings; areas filled with 135 oblique lines (\) represent the depth of field for resolution of horizontal gratings. Horizontal line drawn through the data point at 0 eccentricity indicates average central correction. Detailed shapes of the shaded regions between 0 and 20 of eccentricity are unknown.

greater for vertical gratings than for horizontal gratings. This is probably because resolution tends to be radially organized in the peripheral field (e.g., resolution acuity is highest for horizontal gratings on the horizontal meridian).24'32'311 Consequently, because optical defocus has a greater impact on higher spatial frequencies, the tolerance of resolution acuity to defocus is greater for vertical gratings than for horizontal gratings on the horizontal meridian. The second feature to note in Figure 5 is that the shaded region for horizontal gratings lies beyond the 0 D reference line. This implies that when this subject wears corrective lenses appropriate for his central refractive error and his accommodation is relaxed, objects at finite distances will lie outside the depth of field for resolution.

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high eccentricities (type B), or asymmetric astigmatism (type C). According to Ferree et al2D and Rempt et al,26 the nominal conjugate surface (i.e., plane containing the circle of least confusion) changes by less than 2.5 D for eccentricities up to 40, which is within the 3 D depth of field for resolution we measured in the periphery. Therefore, we conclude that for the average patient, peripheral refractive error is too small to affect the measurement of resolution acuity in the periphery when tested with targets located at a distance appropriate for central vision (i.e., at optical infinity for an eye corrected for central vision). However, Sturm's interval for off-axis astigmatism also increases to 2.5 D at 40 of eccentricity. Consequently, depending on the type of astigmatism in the subject's eye, one extreme or the other of Sturm's interval may exceed the depth of field for resolution. The result would be meridional aliasing, which implies that sampling-limited performance could be achieved at some stimulus orientations but not at others. To estimate the likelihood of encountering sampling-limited resolution in the general population, we show in Figure 6 the effect of peripheral astigmatism on depth of field for resolution using the mean population data of Ferree et al23 (their Fig. 5) and the present depth of focus results. Solid thick curves show the mean refraction for the horizontal meridian (which images vertical gratings), and the broken thick curves show the mean refraction for the vertical meridian (which images horizontal gratings) determined by Ferree et al.25 Thus, Sturm's interval is the difference between solid and broken thick curves. Thin curves delimit the depth of field for resolution, taking a conservative estimate of 5 D (2.5 D) for eccentricity > 20. Depth of field regions for vertical and horizontal gratings are filled with different patterns in the figure so that the region of overlap is marked by cross-hatching. This diagram may be used to predict the suitability of central refractive correction on peripheral vision by drawing a horizontal reference line through the zero-eccentricity data point. For any other eccentricity, if this horizontal line lies within the cross-hatched area, then central correction is good enough to ensure that resolution acuities for both horizontal and vertical gratings will be sampling-limited. If the reference line lies inside the depth of field region for one target orientation only, then meridional aliasing exists and resolution acuity will be sampling-limited for one orientation but contrast-limited for the other. Figure 6 indicates that over the range of eccentricities from 10 to 40 (the region of visual field of greatest interest for measuring the loss of retinal ganglion cells in glaucoma), sampling-limited behavior is the expected norm for the population even when peripheral refractive errors are imperfecdy corrected using prescriptions appropriate for central vision. This result bodes well for the success of clinical applications

of resolution perimetry to estimate ganglion cell density. It would also explain why previous experiments using conventional acuity targets have obtained results consistent with sampling-limited behavior, despite the fact that no special precautions were taken to ensure that neural undersampling (rather than insufficient contrast sensitivity) would be the physiological factor limiting visual performance.29"32'41
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