Aging causes considerable changes in the optical and neural structures of the human eye.1 Visual acuity2 and contrast sensitivity3–5 decline with age, because of changes in both optical (increased monochromatic aberrations6–10 and intraocular light scattering11) and neural factors.12 On-axis higher order monochromatic aberrations increase with age whereas the lower order aberrations (refractive errors) show small changes of the order of 1 D throughout life.13,14 Studies have also investigated the contributions of corneal and internal aberrations and found that the balance between the corneal and internal aberrations is lost with aging.15 Most of the above studies have concentrated on the age-related changes in the optics associated with central vision.
Age-related changes in the optics affect both the central (on-axis) and peripheral vision (off-axis). In the periphery detection of pattern, movement and flicker are affected by the changes in the optical defocus,16–19 whereas changes in optical defocus19,20 or aberrations21 have little effect on resolution tasks in normal subjects. Peripheral resolution acuity is neurally limited. However, a recent study has shown that the low contrast resolution acuity declines with optical defocus in the periphery.22 Moreover, studies performed on subjects with central visual field loss have reported improvements in resolution acuity with peripheral (eccentric) refractive corrections at their preferred retinal locus.23–25 It would be interesting to know if resolution acuity in these subjects could be improved further by correcting both the lower and higher order aberrations for their eccentric fixation. It is possible that optical aberrations other than refractive errors could reduce peripheral image quality in these subjects. These subjects mostly correspond to an older age group whose preferred retinal locus can vary from 5 to 35° in the periphery.24,26 Therefore, it would be ideal to have normative data on the peripheral aberration profile of healthy older subjects.
There are few studies, which have explored age-related optical changes in the peripheral visual field. The influence of age on peripheral refractive errors along the horizontal visual field has been studied. The earlier studies by Millodot 27,28 and Scialfa et al.29 had conflicting results about the peripheral astigmatism with no details regarding the central refraction. Charman and Jennings30 measured peripheral refraction in two subjects with an interval of 26 years and found an increase in relative peripheral myopia and a small increase in peripheral astigmatism. The recent cross-sectional studies by Atchison et al.31,32 found that younger and older subjects with similar central refractive corrections had similar peripheral refraction profiles. There is only one study available in the literature that has shown the effect of age on peripheral higher order aberrations. Mathur et al.33 measured peripheral aberrations up to ±20° eccentricity (matrix of 38 points in the 20° visual field) in a small group of young and older emmetropes. They concluded that peripheral higher order aberrations increase with age, but peripheral visual performance deficits observed in normal older people is not attributable to this increase. Because their study was restricted in both sample size and eccentricity, it would be reasonable to measure peripheral aberrations in a larger sample of subjects with more highly eccentric angles. Therefore, the aim of this study is to compare peripheral lower and higher order aberrations across the horizontal (±40°) and inferior (−20°) visual field in a group of young and old emmetropes.
A prospective study was performed on the OD of 60 healthy subjects (29 females and 31 males). They were divided into two groups based on age. Group 1 contained 30 younger emmetropes (24 ± 3 years; age range: 20 to 29 years) with a mean subjective refraction of −0.23 diopter sphere (DS) (±0.39 DS) and −0.37 diopter cylinder (DC) (±0.19 DC). Group 2 contained 30 older presbyopic emmetropes (58 ± 5 years; age range: 52 to 67 years) with a mean subjective refractions +0.31 DS (±0.65 DS) and −0.55 DC (±0.26 DC), respectively. All subjects had distance visual acuities of 0.0 logarithm of the minimum angle of resolution or better. The older subjects were evaluated for lens changes based on Age-Related Eye Disease Study scales.34 All the older subjects had a lens grading of grade 1 (no opacity) or better for nuclear, cortical, and posterior subcapsular cataract. The subjects had no history of ocular surgery or pathology. No cycloplegic drugs were used for measurements. The subjects gave their informed consent after the nature and the intent of the study had been explained. The study was approved by the local ethics committee, and the study protocol was designed in accordance with the tenets of Declaration of Helsinki.
Monochromatic aberrations of the OD (OS occluded) were measured with a commercial open-view COAS-HD VR (AMO Wavefront Sciences, Albuquerque, NM) Shack-Hartmann aberrometer. The method used for measuring peripheral aberration with COAS-HD VR has been described in detail elsewhere.35 The measuring wavelength was 840 nm, and the resulting Zernike coefficients were converted for a wavelength of 555 nm. The aberrations were measured with natural pupils in a dim room illumination. The subjects positioned their head in a chin rest and fixated at a target through a glass slide hot mirror. The target consisted of 3 mm diameter red light-emitting diodes (LED) placed 3 m from the subject. The LEDs were placed in a radial geometry subtending a visual angle of ±40° horizontally and +20° superiorly. The measurements were performed at 11 different visual field locations: fovea (on-axis), out to ± 40° horizontally (temporal − and nasal +) and −20° inferiorly, in steps of 10°. The subjects turned their eyes to view each target during the measurement. Three readings were taken at each position. The Zernike analysis was restricted to a 4 mm circular central part of the wavefront. The above procedure for calculating Zernike coefficients has been discussed in detail elsewhere.35,36 All the analyses were reported according to Optical Society of America recommended standards.37
The higher order root mean square (HO RMS) and the individual Zernike coefficients from second- to sixth-order were exported from COAS-HD VR inbuilt software to Microsoft Excel (Microsoft, Redmond, WA). Statistical analysis was done with the SPSS software package version 126.96.36.199 for windows (SPSS, Chicago, IL). Graphs were plotted with GraphPad Prism software package version 188.8.131.527 for windows (GraphPad, San Diego, CA).
The Zernike coefficients from the three repeated readings at each off-axis angle for all subjects were averaged. The spherical equivalent M was calculated from Eq. 1. The regular astigmatic component J180 and oblique astigmatism J45 were calculated from Eqs. 2 and 3.
In the above equations C20, C40, C22, and C2−2 are Zernike coefficients for defocus, spherical aberration, regular astigmatism, and oblique astigmatism in micrometers (μm), and r is pupil radius in millimeter (mm). The relative peripheral refractive error (RPRE), the change in off-axis spherical equivalent relative to the on-axis spherical equivalent, was calculated for both groups.
The nine individual Zernike coefficients of third- and fourth-order aberrations for both groups were analyzed. The HO RMS from to third- to sixth-order was also computed. Mixed between-within subjects, repeated measures analysis of variance, with Geisser-Greenhouse adjustments were used to determine whether there were significant differences in the refraction and aberration components for the between-subjects variable age and the within-subjects variable eccentricity (off-axis). A p value of <0.05 was considered statistically significant.
Horizontal Visual Field
Age had significant effects on J45, J180 along the horizontal visual field, but no effect on RPRE. Eccentricity showed significant effect on all refraction components. There was a significant age-eccentricity interaction for J180 (Table 1).
J45 astigmatism increased linearly in both groups from the temporal to the nasal field. The rate of change was greater in the younger group (0.007 D/deg) than in the older group (0.003 D/deg). J45 astigmatism showed a very small variation (up to 0.5 D) across the visual field compared with J180 astigmatism (up to 2.35 D) (Fig. 1A, C). RPRE showed a myopic shift in the periphery for both groups with temporal-nasal asymmetry. Both the groups had maximum myopic shift of around 0.5 D in the temporal field whereas it was >1.5 D in the nasal field (Fig. 1B). J180 astigmatism increased quadratically along the horizontal visual field with temporal-nasal asymmetry for both groups. The older group had significantly higher astigmatism (up to 2.35 D) compared with the younger group (up to 2.1 D). This difference was more pronounced on the temporal field with the older group having astigmatism of 1.4 D compared with the 1.0 D of astigmatism in the younger group (Fig. 1C).
The aberration coefficients that changed significantly with age were trefoil (C3−3), horizontal coma (C31), spherical aberration (C40), and secondary astigmatism (C42). Eccentricity showed significant effects on all coefficients except C4−2. There was a significant age-eccentricity interactions for most coefficients except C4−4, and C4−2 (Table 1).
Among the higher order coefficients, horizontal coma (C31) differed most between the groups and across the field. Horizontal coma (C31) increased linearly in both groups from the nasal to the temporal field. The rate of change across the field was greater in the older group (−0.015 μm/deg) than in the younger group (−0.007 μm/deg) (Fig. 2C). Spherical aberration (C40) was more positive in the older group than in the younger group. Spherical aberration was positive up to ±20° then shifted to negative values in the younger group whereas it remained positive across the field for the older group except at +40° (Fig. 2G).
Higher Order Root Mean Square
Age and eccentricity had significant effects on HO RMS across the horizontal visual field (p < 0.05). HO RMS showed a quadratic rate of change with temporal-nasal asymmetry across the field for both the groups. The rate of change was greater in the older group than the younger group (Fig. 3).
Inferior Visual Field
Age had a significant effect on J45 astigmatism and no significant effect on RPRE and J180 astigmatism. Eccentricity showed significant effects on all refraction components. There was a significant age-eccentricity interaction for J45 (Table 2).
J45 astigmatism increased linearly in both groups with the rate of change higher in the younger group (0.015 D/deg) than older group (0.006 D/deg) (Fig. 4A). RPRE showed a myopic shift (up to −0.75 D) in both groups with no significant difference (Fig. 4B). J180 astigmatism increased toward the periphery in both groups with the young group having higher values (up to 0.72 D) than the old group (up to 0.58 D). However, this increase was not statistically significant (Fig. 4C).
Among the aberration coefficients in the inferior visual field, only vertical coma (C3−1) demonstrated significant effects of both age and eccentricity. Age had significant effect on horizontal coma (C31), but there was no significant effect of eccentricity. All the other coefficients showed significant effect of eccentricity except C4−2 and C44. There were significant age-eccentricity interactions for most coefficients (Table 2).
Vertical coma (C3−1) changed linearly in both groups, with rate of change higher in the old group (0.009 μm/deg) than in the young group (0.005 μm/deg) (Fig. 5B). Spherical aberration (C40) was slightly positive for the younger group (up to +0.021 μm) and more positive in the older group (up to +0.038 μm) with significant changes across the inferior visual field (Fig. 5G).
Higher Order Root Mean Square
HO RMS showed significant variation across the inferior visual field for both groups. The old group had significantly higher values than the young group at 10° and 20° eccentricity (p < 0.05) (Fig. 6).
This study shows that peripheral ocular aberrations increase with age across the horizontal and inferior visual fields. The result of our study is in agreement with the earlier study done by Mathur et al.33 We have also extended the findings along the horizontal visual field up to ± 40° in a larger sample of subjects. The changes in refraction components and aberration coefficients with age in the periphery are discussed below.
The peripheral refraction pattern was similar in both age groups along the horizontal and inferior visual field, which is in agreement with the earlier studies30–33 (Figs. 1 and 4). Age had a significant effect on J45 astigmatism. However, the amount of J45 astigmatism was only 0.22 D higher in the younger group (at nasal 40° and inferior 20°) than in the older group, which is a relatively small difference in the periphery.
As expected, RPRE showed myopic shift with no significant difference in both groups along the horizontal and inferior visual field. This finding is in line with earlier studies,38,39 which have shown emmetropes become relatively myopic in the periphery. The older subjects had slightly higher negative values of J180 astigmatism in the periphery than the younger group (−1.4 vs. −1.0 D at temporal 40°) along the horizontal visual field. However, there were no significant differences in J180 astigmatism between the groups in the inferior visual field. J180 astigmatism showed a significant quadratic increase with eccentricity in both groups along the horizontal visual field. Our results regarding J180 astigmatism agree with the results of Charman and Jennings30 study in which they reported slightly higher negative values in older eyes along the horizontal visual field. We also observed temporal-nasal asymmetry for RPRE and J180 along the horizontal visual field with greater changes in refraction for the nasal than for the temporal visual field in both groups.31 The nasal-temporal asymmetry is most probably attributable to the difference between the measurement axis (line of sight) and the eye's optical axis.40
In summary, the increases in peripheral refraction (lower order) with age across the horizontal and inferior visual field are relatively small. Even though we find no difference in peripheral refraction pattern between the two groups, it should be noted that refractive error in the periphery increases with eccentricity. Furthermore, it might be important to correct these peripheral refractive errors to achieve a better visual function in central visual field loss subjects.23–25
The dominant higher order aberration in the periphery was coma, and this varied significantly between the groups and across the field. The horizontal coma C31 along the horizontal visual field and vertical coma C3−1 along the inferior visual field increased linearly in both groups in agreement with Seidel theory. Furthermore, the horizontal and vertical coma slopes were twice as large in the older group than the younger group. This finding is consistent with the previous study by Mathur et al.33 who also reported a rapid increase in coma slopes for older emmetropes. However, the reason for this rapid increase of coma slopes in older emmetropes is not clearly understood, and currently available eye models cannot fully reproduce the observed age-related changes in coma.33
What is intriguing is why coma should increase with age—is this because of corneal, lenticular, or other changes? A recent axial study by Berrio et al.41 had found that in young eyes, the positive corneal coma is balanced by the negative internal (lenticular) coma. However, this balance is partly lost in the older eyes leading to increase of ocular (whole eye) horizontal coma. In addition, Atchison42 measured peripheral corneal and ocular aberrations in a middle-aged group and found that the corneal third-order coefficients were higher than the ocular third-order coefficients, indicating that the internal third-order coefficients provided a degree of balance to the corneal third-order coefficients. The studies by Bierro et al.41 and Atchison42 show that the balance between the corneal and internal third-order coefficients is present both axially and peripherally for the young and middle-aged groups. Furthermore, on-axis studies have shown that this balance is lost with aging thereby increasing the magnitude of ocular aberrations in old eyes.15 We could assume that the balance between corneal and lenticular coma is lost with aging also in the periphery. The loss of this balance could lead to both cornea and lens contributing to the increase of peripheral ocular coma in old eyes. This could be a reason for the increase in coma slopes that we observe in our study. Moreover, the loss of balance may not only affect coma but also other aberration coefficients. However, this assumption of loss of balance between the corneal and lenticular aberrations, and the consequent increase in total ocular aberrations in the periphery with aging needs to be investigated.
Among the fourth-order coefficients, the peripheral spherical aberration was significantly higher in the old group than the young group along the horizontal and inferior visual fields. However, in our study, the on-axis spherical aberration between the young (0.009 ± 0.020 μm) and old (0.012 ± 0.038 μm) group for a 4 mm pupil showed no significant age dependence in agreement with previous studies with emmetropic subjects.32,43 Studies that reported increase in spherical aberration with age included large refraction ranges, which could have influenced their results.44,45 The remaining coefficients of the third- and fourth-order aberrations did not show any major variation between the groups.
HO RMS showed quadratic field dependence in both groups along the horizontal visual field. The young and old group showed on average 1.5 and 2.1 times increase in HO RMS from center to ± 20° eccentricity (horizontal and inferior). This shows that the older group had higher rate of change in HO RMS than the younger group across the horizontal and inferior visual field. These results are in agreement with the previous study by Mathur et al.,33 who also reported a similar increase of HO RMS in their old group for the 20° visual field. However, we have extended the horizontal visual field to ± 40° and therefore considering a larger part of the visual field, the young and old group showed on average 3.1 and 5.4 times increase in HO RMS from center to periphery. This suggests that the rate of change in HO RMS from ± 20° to ± 40° is much more rapid in both groups with greater increase in the older group than the young group. This increase in HO RMS across the horizontal visual field is mainly because of the increase in horizontal coma (compare Fig. 2C with Fig. 3).
Does the increase in higher order aberrations influence visual performance in the periphery for old subjects? A previous study has shown that this amount of increase in higher order aberrations degrades the peripheral image quality.33 In addition, there are also other optical factors such as chromatic aberration,46 pupillary miosis,7 and intraocular light scattering,11 which could add to or partly mask the effect of increased monochromatic higher order aberrations. Nevertheless, some of the earlier studies47,48 have concluded that poor peripheral visual performance in older subjects is primarily neural in origin and optical factors play a minor role. However, a recent study by Rosen et al.22 has demonstrated that low contrast resolution acuity declines with optical defocus in the periphery of healthy young subjects. Further studies are needed to ascertain whether the increased higher order aberrations in combination with lower order aberrations reduce peripheral visual performance in older healthy subjects. In particular, this amount of increase in higher order aberrations could further degrade the peripheral vision in older central visual field loss subjects, who use their preferred retinal locus for reading or other resolution tasks. To understand this better, correction of higher order aberrations and evaluation of the visual function should be performed in older subjects with central visual field loss.
In conclusion, the peripheral higher order aberrations increase with age particularly coma and spherical aberration. However, the question of whether this increase in higher order aberrations and the corresponding decrease in retinal image quality have any impact on peripheral vision needs to be investigated further.
We thank Sebastian Carlström, Simon Dahlberg, and Roger Fransson for assistance with subject recruitment. We also thank Baskar Theagarayan, Robert Rosén, and Linda Lundström for their input and suggestions regarding the manuscript.
Vision Enabling Laboratory
Section of Optometry and Vision Science
School of Natural Sciences
391 82 Kalmar
1. Sekuler R, Sekuler AB. Age-related changes, optical factors, and neural processes. In: Kazdin AE, ed. Encyclopedia of Psychology, vol 8. Washington, DC: Oxford University Press; 2000:180–3.
2. Elliott DB, Yang KC, Whitaker D. Visual acuity changes throughout adulthood in normal, healthy eyes: seeing beyond 6/6. Optom Vis Sci 1995;72:186–91.
3. Elliott DB. Contrast sensitivity decline with ageing: a neural or optical phenomenon? Ophthalmic Physiol Opt 1987;7:415–9.
4. Elliott D, Whitaker D, MacVeigh D. Neural contribution to spatiotemporal contrast sensitivity decline in healthy ageing eyes. Vision Res 1990;30:541–7.
5. Owsley C, Sekuler R, Siemsen D. Contrast sensitivity throughout adulthood. Vision Res 1983;23:689–99.
6. Artal P, Ferro M, Miranda I, Navarro R. Effects of aging in retinal image quality. J Opt Soc Am (A) 1993;10:1656–62.
7. Calver RI, Cox MJ, Elliott DB. Effect of aging on the monochromatic aberrations of the human eye. J Opt Soc Am (A) 1999;16:2069–78.
8. McLellan JS, Marcos S, Burns SA. Age-related changes in monochromatic wave aberrations of the human eye. Invest Ophthalmol Vis Sci 2001;42:1390–5.
9. Applegate RA, Donnelly WJ, III, Marsack JD, Koenig DE, Pesudovs K. Three-dimensional relationship between high-order root-mean-square wavefront error, pupil diameter, and aging. J Opt Soc Am (A) 2007;24:578–87.
10. Fujikado T, Kuroda T, Ninomiya S, Maeda N, Tano Y, Oshika T, Hirohara Y, Mihashi T. Age-related changes in ocular and corneal aberrations. Am J Ophthalmol 2004;138:143–6.
11. Kuroda T, Fujikado T, Ninomiya S, Maeda N, Hirohara Y, Mihashi T. Effect of aging on ocular light scatter and higher order aberrations. J Refract Surg 2002;18:S598–602.
12. Elliott SL, Choi SS, Doble N, Hardy JL, Evans JW, Werner JS. Role of high-order aberrations in senescent changes in spatial vision. J Vis 2009;9:24.1–16.
13. Saunders H. Age-dependence of human refractive errors. Ophthalmic Physiol Opt 1984;4:107.
14. Saunders H. A longitudinal study of the age-dependence of human ocular refraction—I. Age-dependent changes in the equivalent sphere. Ophthalmic Physiol Opt 1986;6:39–46.
15. Artal P, Berrio E, Guirao A, Piers P. Contribution of the cornea and internal surfaces to the change of ocular aberrations with age. J Opt Soc Am (A) 2002;19:137–43.
16. Anderson RS, McDowell DR, Ennis FA. Effect of localized defocus on detection thresholds for different sized targets in the fovea and periphery. Acta Ophthalmol Scand 2001;79:60–3.
17. Artal P, Derrington AM, Colombo E. Refraction, aliasing, and the absence of motion reversals in peripheral vision. Vision Res 1995;35:939–47.
18. Leibowitz HW, Johnson CA, Isabelle E. Peripheral motion detection and refractive error. Science 1972;177:1207–8.
19. Wang YZ, Thibos LN, Bradley A. Effects of refractive error on detection acuity and resolution acuity in peripheral vision. Invest Ophthalmol Vis Sci 1997;38:2134–43.
20. Anderson RS. The selective effect of optical defocus on detection and resolution acuity in peripheral vision. Curr Eye Res 1996;15:351–3.
21. Lundström L, Manzanera S, Prieto PM, Ayala DB, Gorceix N, Gustafsson J, Unsbo P, Artal P. Effect of optical correction and remaining aberrations on peripheral resolution acuity in the human eye. Opt Express 2007;15:12654–61.
22. Rosen R, Lundström L, Unsbo P. Influence of optical defocus on peripheral vision. Invest Ophthalmol Vis Sci 2011;52:318–23.
23. Gustafsson J. The first successful eccentric correction. Vis Impair Res 2001;3:147–55.
24. Gustafsson J, Unsbo P. Eccentric correction for off-axis vision in central visual field loss. Optom Vis Sci 2003;80:535–41.
25. Lundström L, Gustafsson J, Unsbo P. Vision evaluation of eccentric refractive correction. Optom Vis Sci 2007;84:1046–52.
26. Lundström L, Unsbo P, Gustafsson J. Off-axis wave front measurements for optical correction in eccentric viewing. J Biomed Opt 2005;10:034002.
27. Millodot M. Effect of ametropia on peripheral refraction. Am J Optom Physiol Opt 1981;58:691–5.
28. Millodot M. Peripheral refraction in aphakic eyes. Am J Optom Physiol Opt 1984;61:586–9.
29. Scialfa CT, Leibowitz HW, Gish KW. Age differences in peripheral refractive error. Psychol Aging 1989;4:372–5.
30. Charman WN, Jennings JA. Longitudinal changes in peripheral refraction with age. Ophthalmic Physiol Opt 2006;26:447–55.
31. Atchison DA, Pritchard N, White SD, Griffiths AM. Influence of age on peripheral refraction. Vision Res 2005;45:715–20.
32. Atchison DA, Markwell EL. Aberrations of emmetropic subjects at different ages. Vision Res 2008;48:2224–31.
33. Mathur A, Atchison DA, Charman WN. Effects of age on peripheral ocular aberrations. Opt Express 2010;18:5840–53.
34. Age-Related Eye Disease Study Research Group. The Age-Related Eye Disease Study (AREDS) system for classifying cataracts from photographs: AREDS report no. 4. Am J Ophthalmol 2001;131:167–75.
35. Baskaran K, Theagarayan B, Carius S, Gustafsson J. Repeatability of peripheral aberrations in young emmetropes. Optom Vis Sci 2010;87:751–9.
36. Lundström L, Gustafsson J, Unsbo P. Population distribution of wavefront aberrations in the peripheral human eye. J Opt Soc Am (A) 2009;26:2192–8.
37. Thibos LN, Applegate RA, Schwiegerling JT, Webb R. Standards for reporting the optical aberrations of eyes. J Refract Surg 2002;18:S652–60.
38. Calver R, Radhakrishnan H, Osuobeni E, O'Leary D. Peripheral refraction for distance and near vision in emmetropes and myopes. Ophthalmic Physiol Opt 2007;27:584–93.
39. Lundström L, Mira-Agudelo A, Artal P. Peripheral optical errors and their change with accommodation differ between emmetropic and myopic eyes. J Vis 2009;9:17.1–11.
40. Charman WN, Atchison DA. Decentred optical axes and aberrations along principal visual field meridians. Vision Res 2009;49:1869–76.
41. Berrio E, Tabernero J, Artal P. Optical aberrations and alignment of the eye with age. J Vis 2010;10:pii:34.
42. Atchison DA. Anterior corneal and internal contributions to peripheral aberrations of human eyes. J Opt Soc Am (A) 2004;21:355–9.
43. Plainis S, Pallikaris IG. Ocular monochromatic aberration statistics in a large emmetropic population. J Mod Opt 2008;55:759–72.
44. Porter J, Guirao A, Cox IG, Williams DR. Monochromatic aberrations of the human eye in a large population. J Opt Soc Am (A) 2001;18:1793–803.
45. Thibos LN, Hong X, Bradley A, Cheng X. Statistical variation of aberration structure and image quality in a normal population of healthy eyes. J Opt Soc Am (A) 2002;19:2329–48.
46. Howarth PA, Zhang XX, Bradley A, Still DL, Thibos LN. Does the chromatic aberration of the eye vary with age? J Opt Soc Am (A) 1988;5:2087–92.
47. Whitaker D, Elliott DB. Simulating age-related optical changes in the human eye. Doc Ophthalmol 1992;82:307–16.
48. Morrison JD, McGrath C. Assessment of the optical contributions to the age-related deterioration in vision. Q J Exp Physiol 1985;70:249–69.