Abstract

The directional sensitivity of the retina, known as the Stiles-Crawford effect (SCE), originates from the waveguide property of photoreceptors. This effect has been extensively studied in normal and pathologic eyes using highly customized optical instrumentation. Here we investigate a new approach based on a Shack-Hartmann wavefront sensor (SHWS), a technology that has been traditionally employed for measuring wave aberrations (phase) of the eye and is available in clinics. Using a modified research-grade SHWS, we demonstrate in five healthy subjects and at four retinal eccentricities that intensity information can be readily extracted from the SHWS measurement and the spatial distribution of which is consistent with that produced by the optical SCE. The technique is found sufficiently sensitive even at near-infrared wavelengths where the optical SCE is faint. We demonstrate that the optical SCE signal is confined to the core of the SHWS spots with the tails being diffuse and non-directional, suggesting cones fail to recapture light that is multiply scattered in the retina. The high sensitivity of the SHWS to the optical SCE raises concern as to how this effect, intrinsic to the retina, may impact the SHWS measurement of ocular aberrations.

© 2009 OSA

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References

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  1. W. S. Stiles and B. H. Crawford, “The luminous efficiency of rays entering the eye pupil at different points,” Proc. R. Soc. Lond., B 112(778), 428–450 (1933).
    [CrossRef]
  2. G. J. van Blokland, “Directionality and alignment of the foveal receptors, assessed with light scattered from the human fundus in vivo,” Vision Res. 26(3), 495–500 (1986).
    [CrossRef] [PubMed]
  3. S. A. Burns, S. Wu, F. Delori, and A. E. Elsner, “Direct measurement of human-cone-photoreceptor alignment,” J. Opt. Soc. Am. A 12(10), 2329–2338 (1995).
    [CrossRef]
  4. J. M. Gorrand and F. Delori, “A reflectometric technique for assessing photoreceptor alignment,” Vision Res. 35(7), 999–1010 (1995).
    [CrossRef] [PubMed]
  5. N. P. Zagers, J. van de Kraats, T. T. Berendschot, and D. van Norren, “Simultaneous measurement of foveal spectral reflectance and cone-photoreceptor directionality,” Appl. Opt. 41(22), 4686–4696 (2002).
    [CrossRef] [PubMed]
  6. W. Gao, B. Cense, Y. Zhang, R. S. Jonnal, and D. T. Miller, “Measuring retinal contributions to the optical Stiles-Crawford effect with optical coherence tomography,” Opt. Express 16(9), 6486–6501 (2008).
    [CrossRef] [PubMed]
  7. W. Gao, R. S. Jonnal, B. Cense, and D. T. Miller, “Measuring directionality of the retinal reflection with a Shack-Hartmann wavefront sensor,” in Society of Photo-Optical Instrumentation Engineers' 2009 International Symposium on Ophthalmic Technologies XIX(San Jose, CA, 2009).
  8. W. Gao, R. S. Jonnal, B. Cense, O. Kocaoglu, Q. Wang, and D. T. Miller, “Photoreceptor directionality measured with Shack-Hartmann wavefront sensing,” Invest. Ophthalmol. Vis. Sci. 50, 2741 (2009).
  9. S. Marcos, and S. A. Burns, “Cone directionality from laser ray tracing in normal and LASIK patients,” Journal of Modern Optics, 1–8, iFirst (2009).
  10. “American National Standard for Safe Use of Lasers ANSI Z136.1,” (Laser Institute of America, Orlando, FL) (2000).
  11. J. Porter, H. Queener, J. Lin, K. Thorn, and A. A. S. Awwal, Adaptive Optics for Vision Science: Principles, Practices, Design and Applications (Wiley, 2006).
  12. N. López-Gil and P. Artal, “Comparison of double-pass estimates of the retinal-image quality obtained with green and near-infrared light,” J. Opt. Soc. Am. A 14(5), 961–971 (1997).
    [CrossRef]
  13. J. M. Gorrand and M. Doly, “Alignment parameters of foveal cones,” J. Opt. Soc. Am. A 26(5), 1260–1267 (2009).
    [CrossRef]
  14. S. Marcos, S. A. Burns, and J. C. He, “Model for cone directionality reflectometric measurements based on scattering,” J. Opt. Soc. Am. A 15(8), 2012–2022 (1998).
    [CrossRef]
  15. S. Marcos and S. A. Burns, “Cone spacing and waveguide properties from cone directionality measurements,” J. Opt. Soc. Am. A 16(5), 995–1004 (1999).
    [CrossRef]
  16. N. P. A. Zagers, T. T. J. M. Berendschot, and D. van Norren, “Wavelength dependence of reflectometric cone photoreceptor directionality,” J. Opt. Soc. Am. A 20(1), 18–23 (2003).
    [CrossRef]
  17. J. van de Kraats and D. van Norren, “Directional and nondirectional spectral reflection from the human fovea,” J. Biomed. Opt. 13(2), 024010 (2008).
    [CrossRef] [PubMed]
  18. C. A. Curcio, K. R. Sloan, R. E. Kalina, and A. E. Hendrickson, “Human photoreceptor topography,” J. Comp. Neurol. 292(4), 497–523 (1990).
    [CrossRef] [PubMed]
  19. W. Gao, B. Cense, C. Zhu, R. S. Jonnal, and D. T. Miller, “Impact of fundus structure on wavefront sensing of ocular aberrations,” Invest. Ophthalmol. Vis. Sci. 49, 2836 (2008).
  20. H. Song, Y. Zhao, X. Qi, Y. T. Chui, and S. A. Burns, “Stokes vector analysis of adaptive optics images of the retina,” Opt. Lett. 33(2), 137–139 (2008).
    [CrossRef] [PubMed]
  21. E. Götzinger, M. Pircher, W. Geitzenauer, C. Ahlers, B. Baumann, S. Michels, U. Schmidt-Erfurth, and C. K. Hitzenberger, “Retinal pigment epithelium segmentation by polarization sensitive optical coherence tomography,” Opt. Express 16(21), 16410–16422 (2008).
    [CrossRef] [PubMed]
  22. B. B. Cense, W. Gao, J. M. Brown, S. M. Jones, R. S. Jonnal, M. Mujat, B. H. Park, J. F. de Boer, and D. T. Miller, “Retinal Imaging with polarization-sensitive optical coherence tomography and adaptive optics,” Opt. Express 17(24), 21634–21651 (2009).
    [CrossRef] [PubMed]

2009

2008

2003

2002

1999

1998

1997

1995

S. A. Burns, S. Wu, F. Delori, and A. E. Elsner, “Direct measurement of human-cone-photoreceptor alignment,” J. Opt. Soc. Am. A 12(10), 2329–2338 (1995).
[CrossRef]

J. M. Gorrand and F. Delori, “A reflectometric technique for assessing photoreceptor alignment,” Vision Res. 35(7), 999–1010 (1995).
[CrossRef] [PubMed]

1990

C. A. Curcio, K. R. Sloan, R. E. Kalina, and A. E. Hendrickson, “Human photoreceptor topography,” J. Comp. Neurol. 292(4), 497–523 (1990).
[CrossRef] [PubMed]

1986

G. J. van Blokland, “Directionality and alignment of the foveal receptors, assessed with light scattered from the human fundus in vivo,” Vision Res. 26(3), 495–500 (1986).
[CrossRef] [PubMed]

1933

W. S. Stiles and B. H. Crawford, “The luminous efficiency of rays entering the eye pupil at different points,” Proc. R. Soc. Lond., B 112(778), 428–450 (1933).
[CrossRef]

Ahlers, C.

Artal, P.

Baumann, B.

Berendschot, T. T.

Berendschot, T. T. J. M.

Brown, J. M.

Burns, S. A.

Cense, B.

W. Gao, R. S. Jonnal, B. Cense, O. Kocaoglu, Q. Wang, and D. T. Miller, “Photoreceptor directionality measured with Shack-Hartmann wavefront sensing,” Invest. Ophthalmol. Vis. Sci. 50, 2741 (2009).

W. Gao, B. Cense, Y. Zhang, R. S. Jonnal, and D. T. Miller, “Measuring retinal contributions to the optical Stiles-Crawford effect with optical coherence tomography,” Opt. Express 16(9), 6486–6501 (2008).
[CrossRef] [PubMed]

W. Gao, B. Cense, C. Zhu, R. S. Jonnal, and D. T. Miller, “Impact of fundus structure on wavefront sensing of ocular aberrations,” Invest. Ophthalmol. Vis. Sci. 49, 2836 (2008).

Cense, B. B.

Chui, Y. T.

Crawford, B. H.

W. S. Stiles and B. H. Crawford, “The luminous efficiency of rays entering the eye pupil at different points,” Proc. R. Soc. Lond., B 112(778), 428–450 (1933).
[CrossRef]

Curcio, C. A.

C. A. Curcio, K. R. Sloan, R. E. Kalina, and A. E. Hendrickson, “Human photoreceptor topography,” J. Comp. Neurol. 292(4), 497–523 (1990).
[CrossRef] [PubMed]

de Boer, J. F.

Delori, F.

S. A. Burns, S. Wu, F. Delori, and A. E. Elsner, “Direct measurement of human-cone-photoreceptor alignment,” J. Opt. Soc. Am. A 12(10), 2329–2338 (1995).
[CrossRef]

J. M. Gorrand and F. Delori, “A reflectometric technique for assessing photoreceptor alignment,” Vision Res. 35(7), 999–1010 (1995).
[CrossRef] [PubMed]

Doly, M.

Elsner, A. E.

Gao, W.

W. Gao, R. S. Jonnal, B. Cense, O. Kocaoglu, Q. Wang, and D. T. Miller, “Photoreceptor directionality measured with Shack-Hartmann wavefront sensing,” Invest. Ophthalmol. Vis. Sci. 50, 2741 (2009).

B. B. Cense, W. Gao, J. M. Brown, S. M. Jones, R. S. Jonnal, M. Mujat, B. H. Park, J. F. de Boer, and D. T. Miller, “Retinal Imaging with polarization-sensitive optical coherence tomography and adaptive optics,” Opt. Express 17(24), 21634–21651 (2009).
[CrossRef] [PubMed]

W. Gao, B. Cense, C. Zhu, R. S. Jonnal, and D. T. Miller, “Impact of fundus structure on wavefront sensing of ocular aberrations,” Invest. Ophthalmol. Vis. Sci. 49, 2836 (2008).

W. Gao, B. Cense, Y. Zhang, R. S. Jonnal, and D. T. Miller, “Measuring retinal contributions to the optical Stiles-Crawford effect with optical coherence tomography,” Opt. Express 16(9), 6486–6501 (2008).
[CrossRef] [PubMed]

Geitzenauer, W.

Gorrand, J. M.

J. M. Gorrand and M. Doly, “Alignment parameters of foveal cones,” J. Opt. Soc. Am. A 26(5), 1260–1267 (2009).
[CrossRef]

J. M. Gorrand and F. Delori, “A reflectometric technique for assessing photoreceptor alignment,” Vision Res. 35(7), 999–1010 (1995).
[CrossRef] [PubMed]

Götzinger, E.

He, J. C.

Hendrickson, A. E.

C. A. Curcio, K. R. Sloan, R. E. Kalina, and A. E. Hendrickson, “Human photoreceptor topography,” J. Comp. Neurol. 292(4), 497–523 (1990).
[CrossRef] [PubMed]

Hitzenberger, C. K.

Jones, S. M.

Jonnal, R. S.

B. B. Cense, W. Gao, J. M. Brown, S. M. Jones, R. S. Jonnal, M. Mujat, B. H. Park, J. F. de Boer, and D. T. Miller, “Retinal Imaging with polarization-sensitive optical coherence tomography and adaptive optics,” Opt. Express 17(24), 21634–21651 (2009).
[CrossRef] [PubMed]

W. Gao, R. S. Jonnal, B. Cense, O. Kocaoglu, Q. Wang, and D. T. Miller, “Photoreceptor directionality measured with Shack-Hartmann wavefront sensing,” Invest. Ophthalmol. Vis. Sci. 50, 2741 (2009).

W. Gao, B. Cense, Y. Zhang, R. S. Jonnal, and D. T. Miller, “Measuring retinal contributions to the optical Stiles-Crawford effect with optical coherence tomography,” Opt. Express 16(9), 6486–6501 (2008).
[CrossRef] [PubMed]

W. Gao, B. Cense, C. Zhu, R. S. Jonnal, and D. T. Miller, “Impact of fundus structure on wavefront sensing of ocular aberrations,” Invest. Ophthalmol. Vis. Sci. 49, 2836 (2008).

Kalina, R. E.

C. A. Curcio, K. R. Sloan, R. E. Kalina, and A. E. Hendrickson, “Human photoreceptor topography,” J. Comp. Neurol. 292(4), 497–523 (1990).
[CrossRef] [PubMed]

Kocaoglu, O.

W. Gao, R. S. Jonnal, B. Cense, O. Kocaoglu, Q. Wang, and D. T. Miller, “Photoreceptor directionality measured with Shack-Hartmann wavefront sensing,” Invest. Ophthalmol. Vis. Sci. 50, 2741 (2009).

López-Gil, N.

Marcos, S.

Michels, S.

Miller, D. T.

B. B. Cense, W. Gao, J. M. Brown, S. M. Jones, R. S. Jonnal, M. Mujat, B. H. Park, J. F. de Boer, and D. T. Miller, “Retinal Imaging with polarization-sensitive optical coherence tomography and adaptive optics,” Opt. Express 17(24), 21634–21651 (2009).
[CrossRef] [PubMed]

W. Gao, R. S. Jonnal, B. Cense, O. Kocaoglu, Q. Wang, and D. T. Miller, “Photoreceptor directionality measured with Shack-Hartmann wavefront sensing,” Invest. Ophthalmol. Vis. Sci. 50, 2741 (2009).

W. Gao, B. Cense, Y. Zhang, R. S. Jonnal, and D. T. Miller, “Measuring retinal contributions to the optical Stiles-Crawford effect with optical coherence tomography,” Opt. Express 16(9), 6486–6501 (2008).
[CrossRef] [PubMed]

W. Gao, B. Cense, C. Zhu, R. S. Jonnal, and D. T. Miller, “Impact of fundus structure on wavefront sensing of ocular aberrations,” Invest. Ophthalmol. Vis. Sci. 49, 2836 (2008).

Mujat, M.

Park, B. H.

Pircher, M.

Qi, X.

Schmidt-Erfurth, U.

Sloan, K. R.

C. A. Curcio, K. R. Sloan, R. E. Kalina, and A. E. Hendrickson, “Human photoreceptor topography,” J. Comp. Neurol. 292(4), 497–523 (1990).
[CrossRef] [PubMed]

Song, H.

Stiles, W. S.

W. S. Stiles and B. H. Crawford, “The luminous efficiency of rays entering the eye pupil at different points,” Proc. R. Soc. Lond., B 112(778), 428–450 (1933).
[CrossRef]

van Blokland, G. J.

G. J. van Blokland, “Directionality and alignment of the foveal receptors, assessed with light scattered from the human fundus in vivo,” Vision Res. 26(3), 495–500 (1986).
[CrossRef] [PubMed]

van de Kraats, J.

van Norren, D.

Wang, Q.

W. Gao, R. S. Jonnal, B. Cense, O. Kocaoglu, Q. Wang, and D. T. Miller, “Photoreceptor directionality measured with Shack-Hartmann wavefront sensing,” Invest. Ophthalmol. Vis. Sci. 50, 2741 (2009).

Wu, S.

Zagers, N. P.

Zagers, N. P. A.

Zhang, Y.

Zhao, Y.

Zhu, C.

W. Gao, B. Cense, C. Zhu, R. S. Jonnal, and D. T. Miller, “Impact of fundus structure on wavefront sensing of ocular aberrations,” Invest. Ophthalmol. Vis. Sci. 49, 2836 (2008).

Appl. Opt.

Invest. Ophthalmol. Vis. Sci.

W. Gao, R. S. Jonnal, B. Cense, O. Kocaoglu, Q. Wang, and D. T. Miller, “Photoreceptor directionality measured with Shack-Hartmann wavefront sensing,” Invest. Ophthalmol. Vis. Sci. 50, 2741 (2009).

W. Gao, B. Cense, C. Zhu, R. S. Jonnal, and D. T. Miller, “Impact of fundus structure on wavefront sensing of ocular aberrations,” Invest. Ophthalmol. Vis. Sci. 49, 2836 (2008).

J. Biomed. Opt.

J. van de Kraats and D. van Norren, “Directional and nondirectional spectral reflection from the human fovea,” J. Biomed. Opt. 13(2), 024010 (2008).
[CrossRef] [PubMed]

J. Comp. Neurol.

C. A. Curcio, K. R. Sloan, R. E. Kalina, and A. E. Hendrickson, “Human photoreceptor topography,” J. Comp. Neurol. 292(4), 497–523 (1990).
[CrossRef] [PubMed]

J. Opt. Soc. Am. A

Opt. Express

Opt. Lett.

Proc. R. Soc. Lond., B

W. S. Stiles and B. H. Crawford, “The luminous efficiency of rays entering the eye pupil at different points,” Proc. R. Soc. Lond., B 112(778), 428–450 (1933).
[CrossRef]

Vision Res.

G. J. van Blokland, “Directionality and alignment of the foveal receptors, assessed with light scattered from the human fundus in vivo,” Vision Res. 26(3), 495–500 (1986).
[CrossRef] [PubMed]

J. M. Gorrand and F. Delori, “A reflectometric technique for assessing photoreceptor alignment,” Vision Res. 35(7), 999–1010 (1995).
[CrossRef] [PubMed]

Other

S. Marcos, and S. A. Burns, “Cone directionality from laser ray tracing in normal and LASIK patients,” Journal of Modern Optics, 1–8, iFirst (2009).

“American National Standard for Safe Use of Lasers ANSI Z136.1,” (Laser Institute of America, Orlando, FL) (2000).

J. Porter, H. Queener, J. Lin, K. Thorn, and A. A. S. Awwal, Adaptive Optics for Vision Science: Principles, Practices, Design and Applications (Wiley, 2006).

W. Gao, R. S. Jonnal, B. Cense, and D. T. Miller, “Measuring directionality of the retinal reflection with a Shack-Hartmann wavefront sensor,” in Society of Photo-Optical Instrumentation Engineers' 2009 International Symposium on Ophthalmic Technologies XIX(San Jose, CA, 2009).

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Figures (7)

Fig. 1
Fig. 1

Layout of the laboratory SHWS for measuring the optical SCE. The beam of a 788 nm pigtailed SLD (linearly polarized) passes through an artificial pupil, limiting the beam size to 2 mm at the eye’s pupil. The XY position of the beam at the eye’s pupil is controlled via a tip-tilt mirror that is conjugate to the retina. After entering the eye, the beam focuses to a small spot on the retina. The fixation target and pupil camera are used to align the eye to the system. The camera also confirms location of the beam entry position. Light reflected from the retina, exits the eye and after a relay telescope is sampled by a lenslet array and captured by a CCD camera. ‘p’ refers to planes conjugate to the pupil; ‘r’ refers to planes conjugate to the retina. The system contains no polarization controlling components. See text for additional system details.

Fig. 2
Fig. 2

(left) Raw SHWS image acquired on one subject using the Fig. 1 system. Colored boxes are superimposed across (middle) the entire spot array and (right) an enlarged subsection. Red and blue boxes are positioned to sample the core and tail portions of the spots, respectively, and are the regions used for data analysis in this study. The raw image is displayed using an inverted grayscale. T, N, S and I represent temporal, nasal, superior and inferior sides of the pupil, respectively.

Fig. 3
Fig. 3

Wavefront (a) aberration and (b) amplitude maps reconstructed from the same raw SHWS data on one subject. The wavefront aberration map is composed of 18 Zernike modes (3rd through 6th order). The contour interval is 0.2 μm, and the peak-to-valley across the 6.8 mm pupil is 3.56 μm. Data points in the amplitude map correspond to intensity measurements, one per lenslet (red boxes in Fig. 2). The superimposed surface is a least-squares fit of Eq. (1) to the data points.

Fig. 4
Fig. 4

Wavefront amplitude reconstructed from SHWS images acquired at 2 degree retinal eccentricity on the same subject. The four plots represent the four possible combinations of pupil entry position (on and off the optical SCE peak) and summation box location (core and tail of SHWS spots): (a) on SCE peak and core, (b) off SCE peak and core, (c) on SCE peak and tail, and (d) off SCE peak and tail. Beam entry positions differed by 2 mm. Data points correspond to intensity measurements, one per lenslet.

Fig. 5
Fig. 5

Pupil intensity (wavefront amplitude) reconstructed from raw SHWS images for (a) fovea, (b) 1 degree, (c) 2 degree, and (d) 3 degree retinal eccentricity of the superior retinal field. Data points correspond to intensity measurements, one per lenslet, with corneal reflex removed.

Fig. 6
Fig. 6

Fit of the SHWS measurements on five subjects to the five-parameter model (Eq. (1). (left) Average directionality is plotted as a function of retinal eccentricity and summation box location (core, tail). Error bars represent +/− one standard deviation. (right) A simplified Eq. (1) (defined in text) is plotted as a function of pupil position. The simplified equation captures the relative contribution (I/(I + B)) and the directional strength ρcore of the Gaussian portion.

Fig. 7
Fig. 7

The filled squares are the measurements from the SHWS. Error bars represent the +/−1 standard deviation. The open circles, upward-pointing triangles and downward-pointing triangles stand for equivalent measurements from Zagers et al. (2003), Marcos et al. (1998) and Marcos and Burns (1999), respectively.

Tables (1)

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Table 1 Relevant parameters of the different reflectometric techniques.

Equations (1)

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R ( x ) = B + I * 10 ρ [ ( x x 0 ) 2 + ( y y 0 ) 2 ]

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