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Abstract
An adaptive optics (AO) system was used to investigate the effect of long-term neural adaptation to the habitual optical profile on neural contrast sensitivity in pseudophakic eyes after the correction of all aberrations, defocus, and astigmatism. Pseudophakic eyes were assessed at 4 and 8 months postoperatively for changes in visual performance. Visual benefit was observed in all eyes at all spatial frequencies after AO correction. The average visual benefit across spatial frequencies was higher in the pseudophakic group (3.31) at 4 months postoperatively compared to the normal group (2.41). The average contrast sensitivity after AO correction in the pseudophakic group improved by a factor of 1.73 between 4 and 8 months postoperatively. Contrast sensitivity in pseudophakic eyes was poorer, which could be attributed to long-term adaptation to the habitual optical profiles before the cataract surgery, in conjunction with age-related vision loss. Improved visual performance in pseudophakic eyes suggests that the aged neural system can be re-adapted for altered ocular optics.
© 2022 Optica Publishing Group under the terms of the Optica Open Access Publishing Agreement
1. Introduction
Age-related vision loss has been studied extensively, and many studies have shown that contrast sensitivity decreases with the progression of age [1–8]. This decrease in contrast sensitivity tends to show the highest prominence at middle to high spatial frequencies [2,3,8]. The etiology of this decrease in contrast sensitivity is not completely understood, but it can be explained by a combination of both optical and neural factors [3]. The optical factors include an increase in both higher-order aberrations (HOAs), especially coma and primary spherical aberrations (SA) [9–11], and light scatter due to the high-density of the crystalline lens with age advancement [12–17]. Based on the Mie scattering theory, Costello et al. reported that multilamellar bodies observed in age-related nuclear cataracts might be major origins of light scattering [18]. Further, a decrease in transmission because of a decrease in pupil size and an increase in ocular media density plays a major role [19]. The contribution of neural factors has also been studied. Based on the interference fringes formed on the retina after the visual stimulus bypasses the effect of ocular optics, Burton et al. found that the neural contrast sensitivity of normal eyes was mildly lower in older subjects than in younger subjects [4]. Furthermore, other studies indicated the presence of neural factors that limit spatial vision with an increase in age [5,6,19].
Cataract, a major age-related optical change, has significant effects on visual perception and the optical properties of the eye, including a reduction in contrast sensitivity especially at higher spatial frequencies [20], and an increase in light scatter and HOAs [21]. Elliot et al. used adaptive optics (AO) to correct the HOAs and showed that AO compensation improves older subjects’ spatial contrast sensitivity, but this increase is not comparable to that of young subjects even if the latter had not undergone AO correction [7]. They also suggested that optical factors other than monochromatic aberrations, especially light scatter due to increased lens density, could be a major barrier to improving contrast sensitivity once AO corrections are conducted. A pseudophakic eye is a good approach to overcome light scatter as cataract surgery removes intraocular scattering induced by the aged lens. This makes it possible to solely investigate neural performance with AO correction.
The main experimental challenge stems from the difficulty in empirically separating neural from optical factors [22]. The application of AO provides a method to minimize the limitations imposed by optical factors [23]. Furthermore, AO can be used to evaluate how alterations in the optical quality modify neural functions by assessing visual processing with fully corrected optics in both young ‘normal’ eyes [24,25] and those with optical abnormalities [26–29].
It has been hitherto reported that optical factors, rather than neural factors, play a major role in the loss of spatial contrast sensitivity in elderly patients [8,30]. However, the role of neural adaptation and/or plasticity in improving spatial contrast sensitivity is not well understood. Few studies have demonstrated an improvement in vision after cataract surgery due to neural re-adaptation to a new set of optical factors. After cataract extraction with the implantation of monofocal and multifocal IOLs, uncorrected visual acuity (VA) and near and distance contrast sensitivity, respectively, were found to improve over time [31,32]. Although these studies reported no remarkable refractive errors after surgery, they did not evaluate changes in total aberrations including HOAs, and the optical changes may not fully explain the improvement in visual performance. Postoperatively, the neural system may be stimulated by the richness of spatial information afforded by new optics, allowing for improved vision over time.
Considering that the density of the crystalline lens increases progressively, and aging adults are gradually exposed to degraded retinal input, aged adult eyes, especially with cataracts, may represent another interesting model of long-term neural adaptation to intraocular scatter. Retinal images in such individuals may be more deprived of fine spatial details than in those with typical optical blur induced by aberrations [33]. It is plausible that long-term exposure to this poor optical quality modifies the neural processing mechanism to compensate for the optical blur, failing to obtain the full benefits of the optical blur correction. Nevertheless, little is known about this adaptation/re-adaptation process in the aging visual system. Clinically, the knowledge gained from such studies will guide how optical treatments with advanced wavefront-guided and/or multifocal IOLs need to be applied to individual patients. Therefore, this study aimed to assess the visual benefit of correcting HOAs that may be limited by adapted neural processing in pseudophakic aged eyes. Furthermore, to evaluate the potential neural re-adaptation effect, additional contrast sensitivity measurements were performed 4 and 8 months after cataract surgery.
2. Experimental procedure
2.1 Subjects
Four normal young eyes and five pseudophakic aged eyes from nine subjects (one eye from each subject) were studied. They were assigned to the normal (age, 26 ± 2 years; uncorrected VA, better than 20/20) and pseudophakic (age, 68 ± 7 years; best-corrected VA, 20/25 or better). All normal eyes were emmetropic. All eyes underwent a recent dilated ophthalmological examination, and no pathology was identified in the normal eyes. Pseudophakic eyes with abnormal ocular media and/or retinal diseases were excluded except for four with blepharitis and one with mild dry eye. All pseudophakic eyes had monofocal IOLs implanted, and none had documented findings of posterior capsule opacification at the last visit to the clinic before enrollment. One patient experienced a posterior capsule tear during surgery; however, the IOL was still placed in the capsular bag without the need for a vitrectomy. The IOLs implanted in the pseudophakic eyes were spherical acrylic SN60AT (3 eyes; Alcon, Fort Worth, TX, USA), aspheric silicone LI61AO (1 eye; Bausch + Lomb, Rochester, NY, USA), and spherical silicone LI61SE (1 eye; Bausch + Lomb, Rochester, NY, USA). All patients were administered drops containing 1% tropicamide and 2.5% phenylephrine to achieve dilation and paralysis of accommodation in the normal eyes. Head movements were stabilized with a bite bar, and a phoropter was used, to partially compensate for the sphere and cylinder in some patients, along with a Badal system before closed-loop AO. Pseudophakic subjects were evaluated 4 and 8 months after cataract surgery. At each visit, the same parameters of optical and visual performance were measured. Written informed consent was obtained from all patients, and approval was obtained from the University of Rochester Research Review Board. The study adhered to the tenets of the Declaration of Helsinki and was performed in accordance with the US Health Insurance Portability and Accountability Act.
2.2 Aberration correction
The AO system used in this study is described elsewhere [26]. It comprises a large-stroke deformable mirror (Mirao 52D; Imagine Eyes, Orsay, France) [34] and a custom-made in-house Shack–Hartmann wavefront sensor. Contrast sensitivity was measured using a two-alternate forced-choice method with QUEST. A psychometric function based on 40 trials was derived, and the contrast threshold was determined as that at which at least 75% of the responses were correct. Gabor functions subtending to a 2° visual angle were displayed on a digital light projector (Sharp PG-M20X; Sharp Corporation, Japan) as the visual stimulus. The spatial frequencies used were 4, 8, 12, and 16 cycles/degree. The subjects viewed the stimulus through an artificial adjustable pupil that was conjugated to the pupil of the eye. Aberrations were corrected for the largest available pupil with AO, while vision testing was performed for an artificial pupil, the size of which ranged from 5.5 to 6.0 mm and was 0.5 mm smaller than the maximum pupil size. To evaluate the visual benefit (defined below) of correcting HOA and the neural adaptation effect, contrast sensitivity was measured with closed-loop correction of second-order aberrations with and without AO correction of all aberrations at two different time points: 4 and 8 months postoperatively.
2.3 Visual performance testing
Prior to the visual performance test, each subject adapted to a uniform field of 13 cd/m2 (luminance measured at the subject’s pupil plane) for 5 min. A practice session involved 5–8 measures of contrast threshold; after this session, most of the subjects reported familiarity with the test, and the measured values did not vary significantly. After the practice session, the contrast threshold was measured twice under each condition in a randomized order. The mean luminance of the test stimuli was the same as that of the adaptation field (photopic light condition). When inconsistencies > −0.2 log units were noted between measurements, additional measurements were obtained. The measurements were excluded and repeated when unreliable convergence of psychometric function, inconsistent closed-loop correction, or excessive eye movements were noted. Aberrations were corrected continuously throughout the visual performance test in a closed loop to maintain stable optical quality. The participants were asked to blink at their discretion during psychophysical evaluation, at which point the correction was temporarily suspended.
2.4 Visual benefit and neural enhancement
To improve the characterization of the changes in contrast sensitivity (CS) with AO-based HOA correction, we defined the visual benefit as follows:
Visual performance was also assessed using the contrast sensitivity function measured at 4 and 8 months postoperatively in pseudophakic eyes after AO-based HOA correction. This enabled us to exclude the contributions of HOAs to visual performance and to estimate the effect of neural re-adaptation to the changed optics. We define this “neural enhancement” as follows:
2.5 Statistical analysis
Differences in continuous variables between normal eyes and pseudophakic eyes (two different time points) were compared using mixed ANOVA once normality was verified using the Kolmogorov–Smirnov test. Bartlett’s test was performed to verify the assumption of equal variances, while the Tukey method was used for post-hoc multiple comparisons. Statistical significance was set as P values less than 0.05. Data are presented as mean ± standard deviation. All analyses were performed using Statistical Package for the Social Sciences software (version 25.0).
3. Results
3.1 Total aberrations and specific prominent HOAs
Figure 1(A) shows total wavefront maps for individual pseudophakic eyes at the 4-month and 8-months timepoints. In general, differences in root mean square (RMS) of total aberrations between the two time points were not significant, except for subjects 1 and 3. In subject 1, a remarkable decrease in defocus and astigmatism was observed, which may be explained by the reduction of the tilt angle of the tilted IOL by capsular contraction. In subject 3, vertical coma decreased from 0.76 µm at 4 months postoperatively to 0.16 µm at 8 months postoperatively, which was the main contributor to the reduced total RMS. The decrease in the coma might have been caused by the decentration of the IOL between the two time points.
Fig. 1. (A) Total wavefront maps and difference maps for individual pseudophakic eyes at 4 months and 8 months postoperatively. Each number under individual maps represents a root mean square (RMS) of total aberrations including both lower-order aberration and higher-order aberration (HOA). In subject 1, a large decrease in defocus and astigmatism was observed. In subject 3, a significant decrease in total RMS was noted due mainly to vertical coma. Pupil sizes used for each participant’s wavefront map across the subjects were also provided. (B) Bar graph presenting the total HOA RMS and the mean magnitude of three Zernike coefficients (trefoil, coma, primary spherical aberration (SA)) that contributed most to the HOA RMS in microns for the normal eyes (black oblique, n = 4) and pseudophakic eyes (n = 5) at 4 months (blue) and 8 months (red) after cataract surgery. Significant differences from normal eyes were indicated with (*). Error bars represent the standard deviation.
The HOA RMS values were 0.38 ± 0.18 µm, 0.56 ± 0.25 µm, and 0.50 ± 0.15 µm in the normal and pseudophakic (4 and 8 months postoperatively) groups, respectively (Fig. 1(B)). Individual Zernike modes (trefoil, coma, and primary SA) are depicted in Fig. 1(B) as the absolute average for both groups, defined following the OSA convention [35]. Trefoil and coma were calculated by the quadratic means of the vertical and oblique trefoil, and the vertical and horizontal coma, respectively. The normal eyes had lower magnitudes of individual aberrations than did the pseudophakic eyes, except for coma, the magnitude of which was higher in the normal than in the pseudophakic eyes at 8 months postoperatively. In pseudophakic eyes, magnitudes of aberrations were slightly higher at 4 months postoperatively than at 8 months postoperatively, possibly because of the change in the coma. However, none of the differences in individual HOAs and the HOA RMS between 4 and 8 months postoperatively were significant. Excluding subject 3 did not affect the statistical significance of the difference, since the exclusion induced more similarity in terms of coma and HOA RMS between the two time points. There was a significant difference in the trefoil between the normal and pseudophakic eyes at 4 and 8 months postoperatively (P = 0.021 and 0.012, respectively).
3.2 Contrast sensitivity after HOA correction using AO
Contrast sensitivity improved significantly in both pseudophakic and normal eyes at all spatial frequencies after the correction of HOA (Fig. 2). Overall, the pseudophakic eyes had lower contrast sensitivity at all spatial frequencies than normal eyes with and without AO correction, except at a spatial frequency of 12 cycles/degree at 8 months postoperatively. Both with and without AO correction, contrast sensitivity at 8 months postoperatively was better than that at 4 months postoperatively. Statistically significant improvements at higher spatial frequencies were observed from 4 months to 8 months postoperatively, at 12 and 16 cycles/degree without AO correction (P = 0.042 and 0.028, respectively), and at 8, 12, and 16 cycles/degree with AO correction (P = 0.037, 0.014, and 0.012, respectively). The improvement in contrast sensitivity after AO correction was not explained by changes in HOA because the correction was nearly diffraction-limited and the residual HOAs were similar (residual RMS with AO was approximately 0.095 µm at both time points in the pseudophakic group and 0.082 µm in the normal group).
Fig. 2. Average contrast sensitivity as a function of spatial frequency (cycles/degree) for normal eyes (black, n = 4), pseudophakic eyes (n = 5) at 4 months postoperatively (blue), and pseudophakic eyes at 8 months postoperatively (red). Solid curves and symbols indicate measurements without AO compensation; dashed curves and open symbols indicate measurements with AO compensation. All eyes showed a significant improvement in contrast sensitivity after AO correction, and all pseudophakic eyes showed lower contrast sensitivity than normal eyes with and without AO correction at all spatial frequencies at 12 c/deg at 8 months postoperatively. A (*) indicates the significant difference between values 4 months and 8 months postoperatively. Error bars represent standard deviation.
3.3 Visual benefit after AO correction
Despite substantial intersubject variability, all eyes experienced visual benefits at all spatial frequencies (Fig. 3). There were no statistically significant differences in the visual benefit between normal and pseudophakic eyes at 4 and 8 months postoperatively. The average visual benefits across spatial frequencies were comparable between normal eyes (2.4) and pseudophakic eyes (3.3 and 2.9 at 4 and 8 months postoperatively, respectively). The slight difference in the visual benefits experienced by pseudophakic eyes at 4 and 8 months postoperatively was not statistically significant. Notably, at the 4-month time point, the visual benefit increased with a decrease in spatial frequency (4 and 8 cycles/degree) compared to those of normal and 8 months postoperatively, suggesting that neural compensation occurs towards lower spatial frequencies before re-adaptation towards better optics occurs. Furthermore, the less visual benefit was achieved with AO at 8 months than at 4 months postoperatively, which may indicate the re-adaptation effect. In contrast, the average neural enhancements calculated between 4 and 8 months postoperatively were 1.2, 1.5, 2.2, and 2.1 at 4, 8, 12, and 16 cycles/degree, respectively. At all spatial frequencies, neural enhancements >1 indicated the effect of neural re-adaptation to the changed optics.
Fig. 3. Average visual benefit according to spatial frequency (cycles/degree) in normal eyes (black triangles, n = 4), pseudophakic eyes (n = 5) at four months postoperatively (blue squares), and pseudophakic eyes at eight months postoperatively (red circles). The visual benefit is equal to the contrast sensitivity of each eye at a specific spatial frequency after adaptive optics (AO) correction divided by that same measurement without AO correction. No significant differences between normal eyes and pseudophakic eyes at postoperative 4 and 8 months were noted. Error bars represent standard deviation.
4. Discussion
Our study showed that pseudophakic eyes had HOAs that are similar in magnitude to young normal eyes. It was also found that these uncorrected aberrations limited contrast sensitivity in both groups. Pseudophakic eyes showed improvement in contrast sensitivity from 4 months to 8 months postoperatively, which indicates that plasticity was well-maintained even in aged eyes. Furthermore, the long-term improvement in visual perception after minimizing the ocular wavefront aberrations with AO in pseudophakic aged eyes also highlights the importance of neural re-adaptation to an altered retinal image quality after cataract surgery in aged eyes.
Owing to technological advances in customized refractive and cataract surgery, it became possible to estimate the visual benefit of correcting HOAs in aging eyes. Although prior studies have shown the benefit of compensating for specific HOAs (e.g. SA) in pseudophakic eyes, they could not encompass the benefit of other HOAs [31]. Furthermore, the SA correction was equally applied to all subjects with the same aspheric design regardless of the magnitude of the preoperative HOA [36–39]. Another limitation was that those studies did not allow adequate comparison of contrast sensitivity among different postoperative time points, even though total HOAs fluctuate with time [36,37,40]. The beauty of using AO is to avoid these deficiencies by correcting aberrations in a customized fashion to ensure that all aberrations can be controlled individually and separately at any time point [41]. By using AO compensation, we could reproduce the potential visual benefit of customized refractive and/or cataract surgeries in both young and aged eyes.
The HOA RMS was higher in pseudophakic eyes than in normal controls in our study; this result is consistent with that of the previous studies [36–38,42]. The magnitudes of trefoil and SA in our normal eyes were also consistent with those of previous studies [42,43]; however, the magnitude of coma in our study was biased by one outlier who might have subclinical keratoconus. The statistically significant difference in the magnitudes of trefoil in our pseudophakic eyes and normal eyes may be due to differences in IOL properties, as two pseudophakic eyes (subjects 3 and 5) with 3-piece silicone IOLs (LI61AO and LI61SE) showed higher trefoil than eyes with 1-piece acrylic IOLs. Other potential factors include anterior capsular contraction of the silicone optic or a warped optic due to the exertion of increased tension force by capsular folds or wrinkles along the axis of the PMMA haptics (+ haptic angulation). These unpredictable factors may limit the outcomes of future customized HOA-correcting cataract surgeries. Further investigations are necessary to clarify if these are potential factors.
We did not measure contrast sensitivity in young subjects at the two different time points because their contrast sensitivity was unlikely to change within 4 months. Without AO correction, the contrast sensitivity of aged pseudophakic eyes was lower than that of young normal eyes. Interestingly, even after AO correction, this parameter remained poorer in pseudophakic eyes than in young normal eyes. This result suggests that HOAs are not the sole factors accounting for reduced contrast sensitivity. In addition to the age-related neural decay, other optical factors that were not improved by AO correction and cataract surgery, such as residual intraocular scatter, may override the benefit of this correction along with all spatial frequencies. We clinically ruled out a small pupil size and the posterior capsular opacification in all pseudophakic eyes, but residual intraocular scatter due to the ocular media, such as the cornea and vitreous, is still possible.
Notably, AO provided a significant visual benefit by correcting HOA in aged pseudophakic eyes, although this was lower than that of normal eyes. This result was comparable to a previous finding that visual benefit was nearly identical for aged phakic individuals without cataracts and young normal eyes [7]. However, our study’s aged pseudophakic eyes were exposed to poorer optics related to cataracts over a long period and might be adapted to the long-lasting blur [44]. This long-term adaptation effect might be supported by a decrease and increase in the visual benefit of pseudophakic eyes at the 4-month time point at higher (12 and 16 cycles/degree) and lower frequencies (4 and 8 cycles/degree), respectively, by boosting the low spatial frequency signal. This finding is similar to that of neurotypically developed subjects with keratoconus [22], who demonstrate impaired sensitivity to fine details (compromise) and improved sensitivity to coarse spatial details (compensation). These gains and losses in visual benefit resemble those in patients with advanced keratoconus who experience poor optical quality in their lives and might be mediated by changes in signal enhancement.
In addition to yielding short-term (4 months postoperatively) visual benefit, AO correction showed a significant improvement in the visual benefit at 8 months postoperatively at higher spatial frequencies (12 and 16 cycles/degree). This cannot be explained by changes only in HOAs because the difference maps and the total RMS difference between the two time points showed non-trivial changes in lower-order aberrations (LOAs) observed in at least two out of five study participants. There has been evidence for neural adaptation to LOAs, HOAs, and a combination of both [45–48]. Even though we observed non-trivial refractive errors in at least two out of five participants, all of the participants did not need to correct them, making it difficult to separate the contribution of individual aberrations to neural adaptation. Instead, we concluded that the improvement in visual performance over time is due mainly to the neural adaptation mechanism that the visual system can be re-adapted to the new habitual optics over time. The human visual system is well known to be plastic; it can be re-adapted to the new optical blur by changing optics, especially in young adults [22]. However, it is unclear whether this neural re-adaptation is also effective in aged adults. In our study, the human visual system, even in aged adults, might remain plastic; therefore, it could be re-adapted to new optics over time. We wanted to highlight this neural factor and named it “neural enhancement.” The calculated neural enhancement (> 1) conspicuously showed persistent sensory plasticity in aged pseudophakic eyes.
However, the age-related neural decline may lead to the deterioration of spatial vision. Theoretically, the visual benefit can be expected to increase with an increase in HOA magnitude; therefore, the correction of HOA should correspondingly provide a greater visual benefit. Conversely, the visual benefit in pseudophakic eyes at 8 months postoperatively decreased at the highest spatial frequency (16 cycles/degree). Additionally, even after AO correction, the aged pseudophakic eyes showed a poorer contrast sensitivity than did the young normal eyes, which received no AO compensation. In other words, despite the improvement in retinal image quality after AO correction in aged pseudophakic eyes, age-related recession in contrast sensitivity was still evident. These results are consistent with the consensus that various neural factors contribute to the senescent recession of spatial vision. Loss of ganglion cells in the central retina has been reported to reduce spatial sampling in aged subjects [45,46]. Furthermore, functional modifications beyond the retina may lead to the age-related decline in spatial contrast sensitivity. Evidence from monkey models [47,48] implies the occurrence of an age-related functional deficit in cortical channel tunings, such as a loss of direction and orientation selectivity of cells in the striate cortex, and a decrease in the neural signal-to-noise ratio. HOA correction might improve contrast sensitivity at higher spatial frequencies, but these neural deficits might impose an upper limit on the improvement yielded by AO correction. However, these findings are yet to be confirmed in aged human subjects.
The effect of learning the procedure cannot be ruled out. To minimize the procedural learning effect, subjects had multiple practice trials before collecting the study data to ensure that they were fully familiar and comfortable with the visual task and that their performance was stable. Therefore, it seems unlikely that the measured performance improvement was due to the learning effect over repetitive measurements.
In conclusion, similar to normal eyes in young adults, pseudophakic eyes in aged adults had a visual perception limited by imperfect optics, and they benefited from HOA correction. Moreover, the intrinsic neural system in aged subjects is not fully compromised and is still re-adaptable to altered optics. These findings will help us rationalize the practical necessity of customized HOA correction to guarantee a visual benefit to aged eyes, especially pseudophakic eyes. However, age-related neural deficits may degrade visual performance. Additional research is needed to address the potential mechanism underlying the senescent neural deficits, the neural adaptation to intraocular scatter, and their impact on vision in patients with cataracts.
Funding
National Institute of Health (EY014999); Research to Prevent Blindness.
Disclosures
The authors declare no conflicts of interest.
Data availability
Data underlying the results presented in this paper are not publicly available at this time but may be obtained from the authors upon reasonable request.
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