Abstract

Scanning laser ophthalmoscopy has been used to measure individual cone-photoreceptor directionalities in the living human eye. The directionality is determined at different retinal eccentricities where it is expected that cones have diameters ranging between 5–10μm, comparable to the spot size of the incident beam. Individual cone directionality values are compared with the predicted directionalities obtained by using the waveguide model of light coupling to and from photoreceptors for the case of a focused incident beam.

© 2011 OSA

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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. London, Ser. B 112, 428–450 (1933).
    [CrossRef]
  2. G. Toraldo di Francia and L. Ronchi, “Directional scattering of light by the human retina,” J. Opt. Soc. Am. 42, 782–783 (1952).
  3. J. M. Enoch, “Optical properties of the retinal receptors,” J. Opt. Soc. Am. 53, 71–85 (1963).
    [CrossRef]
  4. A. W. Snyder and C. Pask, “The Stiles-Crawford effect explanation and consequences,” Vision Res. 13, 1115–1137 (1973).
    [CrossRef] [PubMed]
  5. A. Roorda and D. R. Williams, “Optical fiber properties of individual human cones,” J. Vision 2, 404–412 (2002).
    [CrossRef]
  6. B. Vohnsen and D. Rativa, “Absence of an integrated Stiles-Crawford function for coherent light,” J. Vision 11, 1–10 (2011).
    [CrossRef]
  7. B. Vohnsen, I. Iglesias, and P. Artal, “Guided light and diffraction model of human-eye photoreceptors,” J. Opt. Soc. Am. A 22, 2318–2328 (2005).
    [CrossRef]
  8. D. Rativa and B. Vohnsen, “Simulating human photoreceptor optics using a liquid-filled photonic crystal fiber,” Biomed. Opt. Express 2, 543–551 (2011).
    [CrossRef] [PubMed]
  9. J. M. Enoch and G. M. Hope, “Directional sensitivity of the foveal and parafoveal retina,” Invest. Ophthalmol. Visual Sci. 12, 497–503 (1973).
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  11. J. M. Gorrand and F. C. Delori, “A reflectometric technique for assessing photoreceptor alignment,” Vision Res. 3, 990–1010 (1995).
  12. P. J. Delint, T. T. J. M. Berendschot, and D. van Norren, “Local photoreceptor alignment measured with a scanning laser ophthalmoscope,” Vision Res. 37, 243–248 (1997).
    [CrossRef] [PubMed]
  13. S. A. Burns, S. Wu, F. C. Delori, and A. E. Elsner, “Direct measurement of human cone-photoreceptor alignment,” J. Opt. Soc. Am. A 12, 2329–2338 (1996).
    [CrossRef]
  14. 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, 6486–6501 (2008).
    [CrossRef] [PubMed]
  15. W. Gao, R. S. Jonnal, B. Cense, O.P. Kocaoglu, Q. Wang, and D. T. Miller, “Measuring directionality of the retinal reflection with a Shack-Hartmann wavefront sensor,” Opt. Express 17, 23085–23097 (2009).
    [CrossRef]
  16. C. A. Curcio, K. R. Sloan, R. E. Kalina, and A. E. Hendrickson, “Human photoreceptor topography,” J. Comp. Neurol. 292, 497–523 (1990).
    [CrossRef] [PubMed]
  17. B. Vohnsen and D. Rativa, “Ultrasmall spot size scanning laser ophthalmoscopy,” Biomed. Opt. Express . Submitted.
  18. H. Hofer, P. Artal, B. Singer, J. L. Aragon, and D. R. Williams, “Dynamics of the eyes wave aberration,” J. Opt. Soc. Am. A 18, 497–506 (2000).
    [CrossRef]
  19. A. Ghatak and K. Thyagarajan, “Introduction to fiber optics,” (Cambridge, U.K., 1998), pp. 149–156.
  20. D. Marcuse, “Loss analysis of single-mode fiber splices,” Bell Syst. Tech. J. 56, 56, 703–718 (1977).
  21. J. M. Gorrand, M. Doly, and F. Bacin, “Macular pigment density assessed by directional fundus reflectance,” J. Opt. Soc. Am. A 26, 1847–1854 (2009).
    [CrossRef]
  22. S. A. Burns, S. Wu, J. Chang, and A. E. Elsner, “Variations in photoreceptor directionality across the central retina,” J. Opt. Soc. Am. A 14, 2033–2040 (1997).
    [CrossRef]
  23. G. Westheimer, “Dependence of the magnitude of the Stiles-Crawford effect on retinal location,” J. Physiol. (London) 192, 309–315 (1967).
  24. J. A. Van Loo and J. M. Enoch, “The scotopic Stiles-Crawford effect,” Vision Res. 15, 1005–1009 (1975).
    [CrossRef] [PubMed]
  25. B. Lochocki, D. Rativa, and B. Vohnsen, “Spatial and spectral characterisation of the first and second Stiles-Crawford effects using tuneable liquid-crystal filters,” J. Mod. Opt. (in press).

2011

B. Vohnsen and D. Rativa, “Absence of an integrated Stiles-Crawford function for coherent light,” J. Vision 11, 1–10 (2011).
[CrossRef]

D. Rativa and B. Vohnsen, “Simulating human photoreceptor optics using a liquid-filled photonic crystal fiber,” Biomed. Opt. Express 2, 543–551 (2011).
[CrossRef] [PubMed]

2009

2008

2005

2002

A. Roorda and D. R. Williams, “Optical fiber properties of individual human cones,” J. Vision 2, 404–412 (2002).
[CrossRef]

2000

1997

S. A. Burns, S. Wu, J. Chang, and A. E. Elsner, “Variations in photoreceptor directionality across the central retina,” J. Opt. Soc. Am. A 14, 2033–2040 (1997).
[CrossRef]

P. J. Delint, T. T. J. M. Berendschot, and D. van Norren, “Local photoreceptor alignment measured with a scanning laser ophthalmoscope,” Vision Res. 37, 243–248 (1997).
[CrossRef] [PubMed]

1996

1995

J. M. Gorrand and F. C. Delori, “A reflectometric technique for assessing photoreceptor alignment,” Vision Res. 3, 990–1010 (1995).

1990

J. M. Gorrand and F. C. Delori, “A method for assessing the photoreceptor directionality,” Invest. Ophthalmol. Visual Sci. 31 (suppl.), 425 (1990).

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

1977

D. Marcuse, “Loss analysis of single-mode fiber splices,” Bell Syst. Tech. J. 56, 56, 703–718 (1977).

1975

J. A. Van Loo and J. M. Enoch, “The scotopic Stiles-Crawford effect,” Vision Res. 15, 1005–1009 (1975).
[CrossRef] [PubMed]

1973

A. W. Snyder and C. Pask, “The Stiles-Crawford effect explanation and consequences,” Vision Res. 13, 1115–1137 (1973).
[CrossRef] [PubMed]

J. M. Enoch and G. M. Hope, “Directional sensitivity of the foveal and parafoveal retina,” Invest. Ophthalmol. Visual Sci. 12, 497–503 (1973).

1967

G. Westheimer, “Dependence of the magnitude of the Stiles-Crawford effect on retinal location,” J. Physiol. (London) 192, 309–315 (1967).

1963

1952

1933

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

Aragon, J. L.

Artal, P.

Bacin, F.

Berendschot, T. T. J. M.

P. J. Delint, T. T. J. M. Berendschot, and D. van Norren, “Local photoreceptor alignment measured with a scanning laser ophthalmoscope,” Vision Res. 37, 243–248 (1997).
[CrossRef] [PubMed]

Burns, S. A.

Cense, B.

Chang, J.

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. London, Ser. B 112, 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, 497–523 (1990).
[CrossRef] [PubMed]

Delint, P. J.

P. J. Delint, T. T. J. M. Berendschot, and D. van Norren, “Local photoreceptor alignment measured with a scanning laser ophthalmoscope,” Vision Res. 37, 243–248 (1997).
[CrossRef] [PubMed]

Delori, F. C.

S. A. Burns, S. Wu, F. C. Delori, and A. E. Elsner, “Direct measurement of human cone-photoreceptor alignment,” J. Opt. Soc. Am. A 12, 2329–2338 (1996).
[CrossRef]

J. M. Gorrand and F. C. Delori, “A reflectometric technique for assessing photoreceptor alignment,” Vision Res. 3, 990–1010 (1995).

J. M. Gorrand and F. C. Delori, “A method for assessing the photoreceptor directionality,” Invest. Ophthalmol. Visual Sci. 31 (suppl.), 425 (1990).

Doly, M.

Elsner, A. E.

Enoch, J. M.

J. A. Van Loo and J. M. Enoch, “The scotopic Stiles-Crawford effect,” Vision Res. 15, 1005–1009 (1975).
[CrossRef] [PubMed]

J. M. Enoch and G. M. Hope, “Directional sensitivity of the foveal and parafoveal retina,” Invest. Ophthalmol. Visual Sci. 12, 497–503 (1973).

J. M. Enoch, “Optical properties of the retinal receptors,” J. Opt. Soc. Am. 53, 71–85 (1963).
[CrossRef]

Gao, W.

Ghatak, A.

A. Ghatak and K. Thyagarajan, “Introduction to fiber optics,” (Cambridge, U.K., 1998), pp. 149–156.

Gorrand, J. M.

J. M. Gorrand, M. Doly, and F. Bacin, “Macular pigment density assessed by directional fundus reflectance,” J. Opt. Soc. Am. A 26, 1847–1854 (2009).
[CrossRef]

J. M. Gorrand and F. C. Delori, “A reflectometric technique for assessing photoreceptor alignment,” Vision Res. 3, 990–1010 (1995).

J. M. Gorrand and F. C. Delori, “A method for assessing the photoreceptor directionality,” Invest. Ophthalmol. Visual Sci. 31 (suppl.), 425 (1990).

Hendrickson, A. E.

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

Hofer, H.

Hope, G. M.

J. M. Enoch and G. M. Hope, “Directional sensitivity of the foveal and parafoveal retina,” Invest. Ophthalmol. Visual Sci. 12, 497–503 (1973).

Iglesias, I.

Jonnal, R. S.

Kalina, R. E.

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

Kocaoglu, O.P.

Marcuse, D.

D. Marcuse, “Loss analysis of single-mode fiber splices,” Bell Syst. Tech. J. 56, 56, 703–718 (1977).

Miller, D. T.

Pask, C.

A. W. Snyder and C. Pask, “The Stiles-Crawford effect explanation and consequences,” Vision Res. 13, 1115–1137 (1973).
[CrossRef] [PubMed]

Rativa, D.

B. Vohnsen and D. Rativa, “Absence of an integrated Stiles-Crawford function for coherent light,” J. Vision 11, 1–10 (2011).
[CrossRef]

D. Rativa and B. Vohnsen, “Simulating human photoreceptor optics using a liquid-filled photonic crystal fiber,” Biomed. Opt. Express 2, 543–551 (2011).
[CrossRef] [PubMed]

Ronchi, L.

Roorda, A.

A. Roorda and D. R. Williams, “Optical fiber properties of individual human cones,” J. Vision 2, 404–412 (2002).
[CrossRef]

Singer, B.

Sloan, K. R.

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

Snyder, A. W.

A. W. Snyder and C. Pask, “The Stiles-Crawford effect explanation and consequences,” Vision Res. 13, 1115–1137 (1973).
[CrossRef] [PubMed]

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. London, Ser. B 112, 428–450 (1933).
[CrossRef]

Thyagarajan, K.

A. Ghatak and K. Thyagarajan, “Introduction to fiber optics,” (Cambridge, U.K., 1998), pp. 149–156.

Toraldo di Francia, G.

Van Loo, J. A.

J. A. Van Loo and J. M. Enoch, “The scotopic Stiles-Crawford effect,” Vision Res. 15, 1005–1009 (1975).
[CrossRef] [PubMed]

van Norren, D.

P. J. Delint, T. T. J. M. Berendschot, and D. van Norren, “Local photoreceptor alignment measured with a scanning laser ophthalmoscope,” Vision Res. 37, 243–248 (1997).
[CrossRef] [PubMed]

Vohnsen, B.

Wang, Q.

Westheimer, G.

G. Westheimer, “Dependence of the magnitude of the Stiles-Crawford effect on retinal location,” J. Physiol. (London) 192, 309–315 (1967).

Williams, D. R.

A. Roorda and D. R. Williams, “Optical fiber properties of individual human cones,” J. Vision 2, 404–412 (2002).
[CrossRef]

H. Hofer, P. Artal, B. Singer, J. L. Aragon, and D. R. Williams, “Dynamics of the eyes wave aberration,” J. Opt. Soc. Am. A 18, 497–506 (2000).
[CrossRef]

Wu, S.

Zhang, Y.

Bell Syst. Tech. J.

D. Marcuse, “Loss analysis of single-mode fiber splices,” Bell Syst. Tech. J. 56, 56, 703–718 (1977).

Biomed. Opt. Express

Invest. Ophthalmol. Visual Sci.

J. M. Enoch and G. M. Hope, “Directional sensitivity of the foveal and parafoveal retina,” Invest. Ophthalmol. Visual Sci. 12, 497–503 (1973).

J. M. Gorrand and F. C. Delori, “A method for assessing the photoreceptor directionality,” Invest. Ophthalmol. Visual Sci. 31 (suppl.), 425 (1990).

J. Comp. Neurol.

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

J. Opt. Soc. Am.

J. Opt. Soc. Am. A

J. Physiol. (London)

G. Westheimer, “Dependence of the magnitude of the Stiles-Crawford effect on retinal location,” J. Physiol. (London) 192, 309–315 (1967).

J. Vision

A. Roorda and D. R. Williams, “Optical fiber properties of individual human cones,” J. Vision 2, 404–412 (2002).
[CrossRef]

B. Vohnsen and D. Rativa, “Absence of an integrated Stiles-Crawford function for coherent light,” J. Vision 11, 1–10 (2011).
[CrossRef]

Opt. Express

Proc. R. Soc. London, Ser. B

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

Vision Res.

A. W. Snyder and C. Pask, “The Stiles-Crawford effect explanation and consequences,” Vision Res. 13, 1115–1137 (1973).
[CrossRef] [PubMed]

J. M. Gorrand and F. C. Delori, “A reflectometric technique for assessing photoreceptor alignment,” Vision Res. 3, 990–1010 (1995).

P. J. Delint, T. T. J. M. Berendschot, and D. van Norren, “Local photoreceptor alignment measured with a scanning laser ophthalmoscope,” Vision Res. 37, 243–248 (1997).
[CrossRef] [PubMed]

J. A. Van Loo and J. M. Enoch, “The scotopic Stiles-Crawford effect,” Vision Res. 15, 1005–1009 (1975).
[CrossRef] [PubMed]

Other

B. Lochocki, D. Rativa, and B. Vohnsen, “Spatial and spectral characterisation of the first and second Stiles-Crawford effects using tuneable liquid-crystal filters,” J. Mod. Opt. (in press).

B. Vohnsen and D. Rativa, “Ultrasmall spot size scanning laser ophthalmoscopy,” Biomed. Opt. Express . Submitted.

A. Ghatak and K. Thyagarajan, “Introduction to fiber optics,” (Cambridge, U.K., 1998), pp. 149–156.

Supplementary Material (10)

» Media 1: MOV (2817 KB)     
» Media 2: MOV (2686 KB)     
» Media 3: MOV (5245 KB)     
» Media 4: MOV (2579 KB)     
» Media 5: MOV (2007 KB)     
» Media 6: MOV (1683 KB)     
» Media 7: MOV (1854 KB)     
» Media 8: MOV (3984 KB)     
» Media 9: MOV (3396 KB)     
» Media 10: MOV (2965 KB)     

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Figures (7)

Fig. 1
Fig. 1

Experimental method. (a) Experimental setup and (b) CCD images of the beam profile at the conjugated (P’) and subject’s (P) pupil position. * Further details about the SLO are given in Ref. [17].

Fig. 4
Fig. 4

Retinal images of the subject BV and directionality values at different retinal regions: (a) eccentricity from 0° to 1.5° ( Media 1), the blue zones are the areas selected to measure the averaged value of directionality, the directionality coefficient of the areas selected is given in mm −2 units; (b) superior retinal eccentricities of 5° ( Media 2), 10°* ( Media 3), 15° ( Media 4), and 20° ( Media 5). The individual directionality values are represented by: (Yellow box) ρ = 0.10 – 0.15mm −2, (Red box) ρ = 0.15 – 0.20mm −2, (Yellow star) ρ = 0.20 – 0.30mm −2, (Red star) ρ > 0.30mm −2. The opened square represents the area selected to calculate the directionality averaged values with (Yellow square) ρ = 0.10 – 0.15mm −2 and (Red square) ρ = 0.15 – 0.20mm −2. * The media shows a processed (intensity-constant artificial pupil) (a) and an unprocessed (uncorrected for the Gaussian laser beam profile) video (b).

Fig. 2
Fig. 2

Schematic of light coupling to the cone-photoreceptors at the retina plane for an SLO system.

Fig. 3
Fig. 3

Dependence of the predicted directionality coefficient with the photoreceptor size. The values are estimated for an illumination spot-size of wr = 2.5μm, 3.5μm and 5.5μm.

Fig. 5
Fig. 5

Retinal images of the subject DR and directionality values at different retinal regions: (a) eccentricity from 0° to 1.5° ( Media 6), the blue zones are the areas selected to measure the averaged value of directionality, the directionality coefficient of the areas selected is given in mm −2 units; (b) superior retinal eccentricities of 5° ( Media 7), 10° ( Media 8), 15° ( Media 9), and 20° ( Media 10). The individual directionality values are represented by: (Yellow box) ρ = 0.10 – 0.15mm −2, (Red box) ρ = 0.15 – 0.20mm −2, (Yellow star) ρ = 0.20 – 0.30mm −2, (Red star) ρ > 0.30mm −2. The opened square represents the area selected to calculate the directionality averaged values since (Yellow square) ρ = 0.10 – 0.15mm −2 and (Red square) ρ = 0.15 – 0.20mm −2

Fig. 6
Fig. 6

Reflected average image intensity as a function of pupil entrance point of the imaging beam for the subject BV: (a) total average for superior retinal eccentricities of 5°, 10°, 15°, and 20°, the error values represent the standard deviation; (b) Two examples of individual cone values compared with the value obtained analyzing an area containing the same cones for an eccentricity of 10°, the error values have not been represented such that variations in peak locations can be easily observed.

Fig. 7
Fig. 7

Individual and total area-averaged directionalities of both subjects at different superior parafoveal eccentricities. The solid line corresponds to the predicted dependence of the directionality coefficient with the eccentricity using Eq. (3) for the special case of a = wm using the retinal mosaic reported by Curcio et al. [16].

Equations (4)

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η = 10 ρ ( r r 0 ) 2
T ( θ ) = [ 2 w r w m w r 2 + w m 2 ] 2 exp [ 2 ( π n eye w r w m ) 2 θ 2 λ 2 ( w r 2 + w m 2 ) ]
ρ ( w r , w m ) = 2 log ( e ) ( π n eye λ f eye ) 2 ( w r 2 w m 2 w r 2 + w m 2 )
a w m ( 0.65 + 1.619 V 3 / 2 + 2.879 V 6 ) 1

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