Abstract

Cones show a differential sensitivity to light coming from different portions of the pupil, typically being most sensitive to light from the center of the pupil. We measured the directional properties of the cones across the central 6 deg of the retina, using an optical imaging technique. We find that the cones in the center of the fovea have the broadest tuning. The width of the angular tuning changes rapidly from 0 deg to 1 deg retinal eccentricity, with cones at 1 deg being much more narrowly tuned than the cones in the center of the fovea. Directional tuning of the cones remains relatively constant from 1 deg to 3 deg retinal eccentricity. Receptoral disarray contributes minimally to the measured directional properties of the foveal cones, and there is no evidence of asymmetry between horizontal and vertical retinal locations. There are only small differences among the five subjects in the change in angular tuning of the cones with retinal location. We find that at the foveal center the directional tuning of the cones is limited by the diameter of the cone apertures.

© 1997 Optical Society of America

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References

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    [CrossRef]
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1997 (1)

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

1996 (1)

J. van der Kraats, T. T. J. M. Berendschot, D. V. Norren, “The pathways of light measured in fundus reflectometry,” Vision Res. 15, 2229–2247 (1996).
[CrossRef]

1995 (2)

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

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

1994 (1)

1993 (3)

1992 (2)

M. A. Wilson, M. C. W. Campbell, P. Simonet, “Change of pupil centration with change of illumination and pupil size,” Optom. Vision Sci. 69, 129–136 (1992).
[CrossRef]

D. I. A. MacLeod, D. R. Williams, W. Makous, “A visual nonlinearity fed by single cones,” Vision Res. 32, 347–363 (1992).
[CrossRef] [PubMed]

1990 (2)

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

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

1989 (1)

B. Chen, W. Makous, “Light capture by human cones,” J. Physiol. 414, 89–109 (1989).
[PubMed]

1988 (1)

1986 (1)

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

1985 (2)

1982 (1)

D. G. Birch, M. A. Sandberg, “Psychophysical studies of cone optical bandwidth in patients with retinitis pigmentosa,” Vision Res. 22, 1113–1117 (1982).
[CrossRef] [PubMed]

1980 (1)

D. R. Williams, “Visual consequences of the foveal pit,” Invest. Ophthalmol. Visual Sci. 19, 653–667 (1980).

1979 (2)

H. E. Bedell, J. M. Enoch, “A study of the Stiles–Crawford (S–C) function at 35° in the temporal field and the stability of the foveal S–C function peak over time,” J. Opt. Soc. Am. 69, 435–442 (1979).
[CrossRef] [PubMed]

S. J. Starr, F. W. Fitzke, R. W. Massof, “The Stiles–Crawford effect in the central fovea,” Invest. Ophthalmol. Visual Sci. (Suppl.) 20, 172 (1979).

1978 (1)

J. E. Bailey, G. G. Heath, “Flicker effects on receptor directional sensitivity,” Am. J. Optom. Physiol. Opt. 55, 807–812 (1978).
[CrossRef]

1976 (1)

1975 (1)

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

1974 (1)

D. I. A. MacLeod, “Directionally selective light adaptation a visual consequence of receptor disarray?” Vision Res. 14, 369–378 (1974).
[CrossRef] [PubMed]

1973 (2)

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

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

1972 (1)

J. M. Enoch, G. M. Hope, “An analysis of retinal receptor orientation IV. Center of the entrance pupil and the center of convergence of orientation and directional sensitivity,” Invest. Ophthalmol. 11, 1017–1021 (1972).
[PubMed]

1971 (1)

A. M. Laties, J. M. Enoch, “An analysis of retinal receptor orientation,” Invest. Ophthalmol. Visual Sci. 10, 69–77 (1971).

1969 (1)

1968 (1)

W. L. Makous, “A transient Stiles–Crawford effect,” Vision Res. 8, 1271–1284 (1968).
[CrossRef] [PubMed]

1967 (1)

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

1949 (1)

1947 (1)

1937 (1)

B. H. Crawford, “The luminous efficiency of light entering the pupil at different points and its relation to brightness threshold measurements,” Proc. R. Soc. London Ser. B 124, 81–96 (1937).
[CrossRef]

1933 (1)

W. S. Stiles, 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]

Applegate, R. A.

Bailey, J. E.

J. E. Bailey, G. G. Heath, “Flicker effects on receptor directional sensitivity,” Am. J. Optom. Physiol. Opt. 55, 807–812 (1978).
[CrossRef]

Bedell, H. E.

Berendschot, T. T. J. M.

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

J. van der Kraats, T. T. J. M. Berendschot, D. V. Norren, “The pathways of light measured in fundus reflectometry,” Vision Res. 15, 2229–2247 (1996).
[CrossRef]

Birch, D. G.

D. G. Birch, M. A. Sandberg, “Psychophysical studies of cone optical bandwidth in patients with retinitis pigmentosa,” Vision Res. 22, 1113–1117 (1982).
[CrossRef] [PubMed]

Blokland, G. J. V.

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

Burns, S. A.

Campbell, M. C. W.

M. A. Wilson, M. C. W. Campbell, P. Simonet, “Change of pupil centration with change of illumination and pupil size,” Optom. Vision Sci. 69, 129–136 (1992).
[CrossRef]

Chen, B.

B. Chen, W. Makous, “Light capture by human cones,” J. Physiol. 414, 89–109 (1989).
[PubMed]

Crawford, B. H.

B. H. Crawford, “The luminous efficiency of light entering the pupil at different points and its relation to brightness threshold measurements,” Proc. R. Soc. London Ser. B 124, 81–96 (1937).
[CrossRef]

W. S. Stiles, 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, A. E. Hendrickson, “Human photoreceptor topography,” J. Comp. Neurol. 292, 497–523 (1990).
[CrossRef] [PubMed]

C. A. Curcio, “Diameters of presumed cone apertures in human retina, in Annual Meeting, Vol. 20 of 1987 OSA Technical Digest Series (Optical Society of America, Washington, D.C., 1987), p. 83.

Delint, P. J.

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

Delori, F. C.

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

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

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

S. A. Burns, A. E. Elsner, J.-M. Gorrand, M. R. Kreitz, F. C. Delori, “Comparison of reflectometric and psychophysical measures of cone orientation,” in Noninvasive Assessment of the Visual System, Vol. 1 of 1992 OSA Technical Digest Series (Optical Society of America, Washington, D.C., 1992), pp. 160–163.

Diddie, K. R.

Easter, S. S. J.

Elsner, A. E.

Engheta, N.

Enoch, J. M.

H. E. Bedell, J. M. Enoch, “A study of the Stiles–Crawford (S–C) function at 35° in the temporal field and the stability of the foveal S–C function peak over time,” J. Opt. Soc. Am. 69, 435–442 (1979).
[CrossRef] [PubMed]

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

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

J. M. Enoch, G. M. Hope, “An analysis of retinal receptor orientation IV. Center of the entrance pupil and the center of convergence of orientation and directional sensitivity,” Invest. Ophthalmol. 11, 1017–1021 (1972).
[PubMed]

A. M. Laties, J. M. Enoch, “An analysis of retinal receptor orientation,” Invest. Ophthalmol. Visual Sci. 10, 69–77 (1971).

J. M. Enoch, F. L. Tobey, “Waveguide properties of retinal receptors,” in Techniques and Observations in Vertebrate Photoreceptor Optics, Vol. 23 of Springer Series in Optical Science, J. M. Enoch, F. L. Tobey, eds. (Springer-Verlag, Berlin, 1981).

Fitzke, F. W.

S. J. Starr, F. W. Fitzke, R. W. Massof, “The Stiles–Crawford effect in the central fovea,” Invest. Ophthalmol. Visual Sci. (Suppl.) 20, 172 (1979).

Gorrand, J. M.

J. M. Gorrand, “Directional effects of the retina appearing in the aerial image,” J. Opt. 16, 279–287 (1985).
[CrossRef]

Gorrand, J.-M.

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

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

S. A. Burns, A. E. Elsner, J.-M. Gorrand, M. R. Kreitz, F. C. Delori, “Comparison of reflectometric and psychophysical measures of cone orientation,” in Noninvasive Assessment of the Visual System, Vol. 1 of 1992 OSA Technical Digest Series (Optical Society of America, Washington, D.C., 1992), pp. 160–163.

Heath, G. G.

J. E. Bailey, G. G. Heath, “Flicker effects on receptor directional sensitivity,” Am. J. Optom. Physiol. Opt. 55, 807–812 (1978).
[CrossRef]

Hendrickson, A. E.

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

Hope, G. M.

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

J. M. Enoch, G. M. Hope, “An analysis of retinal receptor orientation IV. Center of the entrance pupil and the center of convergence of orientation and directional sensitivity,” Invest. Ophthalmol. 11, 1017–1021 (1972).
[PubMed]

Hyams, L.

Kalina, R. E.

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

Krauskopf, J.

J. Krauskopf, “Some experiments with a photoelectric ophthalmoscope,” M. A. Bouman, J. J. Vos, eds. Excerpta Medica International Congress Series 125 (Excepta Medica Foundation, Amsterdam, 1965).

Kreitz, M. R.

S. A. Burns, A. E. Elsner, J.-M. Gorrand, M. R. Kreitz, F. C. Delori, “Comparison of reflectometric and psychophysical measures of cone orientation,” in Noninvasive Assessment of the Visual System, Vol. 1 of 1992 OSA Technical Digest Series (Optical Society of America, Washington, D.C., 1992), pp. 160–163.

Lakshminarayanan, V.

Laties, A. M.

A. M. Laties, J. M. Enoch, “An analysis of retinal receptor orientation,” Invest. Ophthalmol. Visual Sci. 10, 69–77 (1971).

MacLeod, D. I. A.

D. I. A. MacLeod, D. R. Williams, W. Makous, “A visual nonlinearity fed by single cones,” Vision Res. 32, 347–363 (1992).
[CrossRef] [PubMed]

D. I. A. MacLeod, “Directionally selective light adaptation a visual consequence of receptor disarray?” Vision Res. 14, 369–378 (1974).
[CrossRef] [PubMed]

Makous, W.

D. I. A. MacLeod, D. R. Williams, W. Makous, “A visual nonlinearity fed by single cones,” Vision Res. 32, 347–363 (1992).
[CrossRef] [PubMed]

B. Chen, W. Makous, “Light capture by human cones,” J. Physiol. 414, 89–109 (1989).
[PubMed]

Makous, W. L.

W. L. Makous, “A transient Stiles–Crawford effect,” Vision Res. 8, 1271–1284 (1968).
[CrossRef] [PubMed]

Massof, R. W.

S. J. Starr, F. W. Fitzke, R. W. Massof, “The Stiles–Crawford effect in the central fovea,” Invest. Ophthalmol. Visual Sci. (Suppl.) 20, 172 (1979).

Norren, D. V.

J. van der Kraats, T. T. J. M. Berendschot, D. V. Norren, “The pathways of light measured in fundus reflectometry,” Vision Res. 15, 2229–2247 (1996).
[CrossRef]

O’Brien, B.

Pask, C.

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

Pokorny, J.

Polyak, S. L.

S. L. Polyak, The Retina (University of Chicago Press, Chicago, Ill., 1941).

Pugh, E. N. J.

Rowe, M. P.

Safir, A.

Sandberg, M. A.

D. G. Birch, M. A. Sandberg, “Psychophysical studies of cone optical bandwidth in patients with retinitis pigmentosa,” Vision Res. 22, 1113–1117 (1982).
[CrossRef] [PubMed]

Simonet, P.

M. A. Wilson, M. C. W. Campbell, P. Simonet, “Change of pupil centration with change of illumination and pupil size,” Optom. Vision Sci. 69, 129–136 (1992).
[CrossRef]

Sloan, K. R.

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

Smith, V. C.

Snyder, A. W.

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

Starr, S. J.

S. J. Starr, F. W. Fitzke, R. W. Massof, “The Stiles–Crawford effect in the central fovea,” Invest. Ophthalmol. Visual Sci. (Suppl.) 20, 172 (1979).

Stiles, W. S.

W. S. Stiles, 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]

Tobey, F. L.

J. M. Enoch, F. L. Tobey, “Waveguide properties of retinal receptors,” in Techniques and Observations in Vertebrate Photoreceptor Optics, Vol. 23 of Springer Series in Optical Science, J. M. Enoch, F. L. Tobey, eds. (Springer-Verlag, Berlin, 1981).

Toraldo de Francia, G.

van der Kraats, J.

J. van der Kraats, T. T. J. M. Berendschot, D. V. Norren, “The pathways of light measured in fundus reflectometry,” Vision Res. 15, 2229–2247 (1996).
[CrossRef]

Van Loo, J. A.

J. A. Van Loo, 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, D. van Norren, “Local photoreceptor alignment measured with a scanning laser ophthalmoscope,” Vision Res. 37, 243–248 (1997).
[CrossRef] [PubMed]

Webb, R. H.

Westheimer, G.

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

Williams, D. R.

D. I. A. MacLeod, D. R. Williams, W. Makous, “A visual nonlinearity fed by single cones,” Vision Res. 32, 347–363 (1992).
[CrossRef] [PubMed]

D. R. Williams, “Visual consequences of the foveal pit,” Invest. Ophthalmol. Visual Sci. 19, 653–667 (1980).

Wilson, M. A.

M. A. Wilson, M. C. W. Campbell, P. Simonet, “Change of pupil centration with change of illumination and pupil size,” Optom. Vision Sci. 69, 129–136 (1992).
[CrossRef]

Wu, S.

Am. J. Optom. Physiol. Opt. (1)

J. E. Bailey, G. G. Heath, “Flicker effects on receptor directional sensitivity,” Am. J. Optom. Physiol. Opt. 55, 807–812 (1978).
[CrossRef]

Invest. Ophthalmol. (1)

J. M. Enoch, G. M. Hope, “An analysis of retinal receptor orientation IV. Center of the entrance pupil and the center of convergence of orientation and directional sensitivity,” Invest. Ophthalmol. 11, 1017–1021 (1972).
[PubMed]

Invest. Ophthalmol. Visual Sci. (3)

D. R. Williams, “Visual consequences of the foveal pit,” Invest. Ophthalmol. Visual Sci. 19, 653–667 (1980).

A. M. Laties, J. M. Enoch, “An analysis of retinal receptor orientation,” Invest. Ophthalmol. Visual Sci. 10, 69–77 (1971).

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Figures (7)

Fig. 1
Fig. 1

Profiles of the distribution of light measured in the plane of the pupil when different retinal locations are illuminated. Each line in a profile represents the intensity distribution along a single column of pixels. Thus the overall distribution is oriented vertically with the upper half of the pupil plotted as positive numbers and the lower half plotted as negative numbers. Left, illumination of the central fovea with a 1-deg-diameter illumination spot; center, illumination of a region of retina 1 deg nasal to the fovea with a 1-deg illumination spot; right, illumination of a region of retina 2 deg nasal to the fovea with a 1-deg illumination spot.

Fig. 2
Fig. 2

Best fitting ρ values as a function of retinal location. The measurement field size was 1 deg in diameter. Top, mean ±2 standard errors of the mean for a single subject. Data were collected in four separate measurement sessions over four months. Bottom, average results for five subjects. Error bars represent ±2 standard errors of the mean. Circles, values collected with a 1-deg-diameter illumination spot; diamonds, measurements made with a 0.5-deg spot.

Fig. 3
Fig. 3

Comparison of the average of the best-fitting ρ values for horizontal and vertical traverses of the central retina for three subjects. All data for each subject were collected on the same date with use of a 1-deg-diameter illumination spot.

Fig. 4
Fig. 4

Variation in the location of the maximum in light exiting the eye with changes in the entry pupil location. Each panel represents multiple measurements made for a single subject on one day. A single measurement is represented by a single arrow. The solid symbol at the base of each arrow is the location of the entry pupil for a single measurement. The point of each arrow is located at the peak in the distribution of light exiting the eye for that entry pupil position. The large solid circles represent the average peak in light returning out of the pupil when the entry pupil position is near its optimal location. The error bars show ±2 standard deviations of the estimate of the location of the peak. Each row represents a different subject. The leftmost plots are for foveally fixated measurement lights; the rightmost plots are locations 3 deg in the nasal retina. Similar results (not shown) were obtained for two other subjects.

Fig. 5
Fig. 5

Schematic diagram of the logic of the tests for photoreceptor disarray. The left column shows what should happen if we illuminate a group of photoreceptors from the left side of the pupil. If there were disarray, then the illumination light would be maximally coupled into the photoreceptors that point more to the left side of the pupil. These would return more light than photoreceptors that are pointing toward the right edge of the pupil. The resulting distribution of light in the plane of the pupil (top row) would therefore be skewed toward the left edge of the pupil. The center and right columns show the same logic for entry pupil positions near the center and right edges of the pupil, respectively. Thus, if there were significant photoreceptor disarray, the measured peak of the retinal light distribution in the would move toward the location of the illumination light in the pupil. If there were no photoreceptor disarray, then the directed portion of the exit distribution would be invariant in shape but would vary in amplitude in proportion to the coupling between the illumination and the photoreceptors.

Fig. 6
Fig. 6

Profile of the intensity distribution of light in the pupil (solid lines) for an optimal pupil entry location is compared with the estimates of the peak amplitude (the sum of the directed and the diffuse components of the light) obtained for different pupil entry positions. The distance between each entry pupil location and the optimum entry pupil location was measured. We then plotted the amplitude for each measurement at the proper distance from the peak of the optimum distribution (solid circles). Results are shown for one subject at 0 (top) and 3 deg retinal eccentricity (bottom). Similar results were obtained for two other subjects.

Fig. 7
Fig. 7

Comparison of the predicted ρ and the measured ρ’s (symbols) for diffraction-limited cones (solid line). The diffraction limit represents the narrowest possible directional tuning for cones with aperture sizes obtained from Curcio.21 We assumed that the cones were simple apertures illuminated from behind with a plane wave. This represents the limiting case, and for the center of the fovea the measured values of ρ approach this limit. Large plot: plot of the measured ρ for 1-deg (solid symbols) and 0.5-deg (open symbols) measurements averaged across five observers. Temporal and nasal retinal measurements are portrayed on the same axis. The retinal position for the centrally fixated stimuli were corrected for the size of the measurement fields by computing the average retinal position of the fields. Inset: measured ρ for the five subjects with use of a 0.5-deg measurement field compared with the diffraction limit. The retinal position was corrected for the average position of the measurement spot.

Equations (1)

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Lpupil=B+A*10-r*d2

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