Adaptive-optics imaging of human cone photoreceptor distribution

doi:10.1364/JOSAA.25.003021

Adaptive-optics imaging of human cone photoreceptor distribution

Toco Yuen Chui, HongXin Song, and Stephen A. Burns »View Author Affiliations

JOSA A, Vol. 25, Issue 12, pp. 3021-3029 (2008)
http://dx.doi.org/10.1364/JOSAA.25.003021

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References (43)
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Abstract

We have used an adaptive-optics scanning laser ophthalmoscope to image the cone photoreceptor mosaic throughout the central 10°–12° of the retina for four normal subjects. We then constructed montages of the images and processed the montages to determine cone locations. Cone densities range from approximately $10,000 cones ∕ {mm}^{2}$ at 7° to $40,000 cones ∕ {mm}^{2}$ at 1°. The smallest cones were not resolved in the center of the fovea. From the locations of the cones we also analyzed the packing properties of the cone mosaic, finding that all four subjects had a slight cone streak of increased cone density and that, in agreement with previous studies using different approaches, the packing geometry decreased in regularity from the fovea toward the periphery. We also found variations in packing density between subjects and in local anisotropy across retinal locations. The complete montages are presented for download, as well as the estimated cone locations.

OCIS Codes
(010.1080) Atmospheric and oceanic optics : Active or adaptive optics
(180.1790) Microscopy : Confocal microscopy
(330.5310) Vision, color, and visual optics : Vision - photoreceptors

ToC Category:
Vision, Color, and Visual Optics

History
Original Manuscript: July 29, 2008
Revised Manuscript: October 8, 2008
Manuscript Accepted: October 14, 2008
Published: November 19, 2008

Virtual Issues
Vol. 4, Iss. 2 Virtual Journal for Biomedical Optics
Interactive Science Publishing (2008) Optics Express

Citation
Toco Yuen Chui, HongXin Song, and Stephen A. Burns, "Adaptive-optics imaging of human cone photoreceptor distribution," J. Opt. Soc. Am. A 25, 3021-3029 (2008)
http://www.opticsinfobase.org/josaa/abstract.cfm?URI=josaa-25-12-3021

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References

D. R. Williams, “Seeing through the photoreceptor mosaic,” Trends Neurosci. 9, 193-198 (1986). [CrossRef]
D. R. Williams and R. Collier, “Consequences of spatial sampling by a human photoreceptor mosaic,” Science 221, 385-387 (1983). [CrossRef] [PubMed]
J. Hirsch and C. A. Curcio, “The spatial resolution capacity of human fovea,” Vision Res. 29, 1095-1101 (1989). [CrossRef] [PubMed]
D. R. Williams and N. J. Coletta, “Cone spacing and the visual resolution limit,” J. Opt. Soc. Am. A 4, 1514-1523 (1987). [CrossRef] [PubMed]
D. R. Williams, “Aliasing in human foveal vision,” Vision Res. 25, 195-205 (1985). [CrossRef] [PubMed]
F. W. Campbell and D. G. Green, “Optical and retinal factors affecting visual resolution,” J. Physiol. (London) 181, 576-593 (1965).
S. J. Anderson and R. F. Hess, “Post-receptoral undersampling in normal human peripheral-vision,” Vision Res. 30, 1507-1515 (1990). [CrossRef] [PubMed]
L. N. Thibos, D. L. Still, and A. Bradley, “Characterization of spatial aliasing and contrast sensitivity in peripheral vision,” Vision Res. 36, 249-258 (1996). [CrossRef] [PubMed]
L. N. Thibos, F. E. Cheney, and D. J. Walsh, “Retinal limits to the detection and resolution of gratings,” J. Opt. Soc. Am. A 4, 1524-1529 (1987). [CrossRef] [PubMed]
N. J. Coletta and T. Watson, “Effect of myopia on visual acuity measured with laser interference fringes,” Vision Res. 46, 636-651 (2006). [CrossRef]
S. J. Anderson, K. T. Mullen, and R. F. Hess, “Human peripheral spatial resolution for achromatic and chromatic stimuli: limits imposed by optical and retinal factors,” J. Physiol. (London) 442, 47-64 (1991).
S. L. Polyak, The Retina (U. Chicago Press, 1941).
C. A. Curcio, K. R. Sloan, Jr., O. Packer, A. E. Hendrickson, and R. E. Kalina, “Distribution of cones in human and monkey retina: individual variability and radial asymmetry,” Science 236, 579-582 (1987). [CrossRef] [PubMed]
C. A. Curcio and K. R. Sloan, “Packing geometry of human cone photoreceptors: variation with eccentricity and evidence for local anistropy,” Vision Res. 9, 169-180 (1992).
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. Liang, D. R. Williams, and D. T. Miller, “Supernormal vision and high-resolution retinal imaging through adaptive optics,” J. Opt. Soc. Am. A 14, 2884-2892 (1997). [CrossRef]
A. Roorda, “Adaptive optics ophthalmoscopy,” J. Refract. Surg. 16, S602-S607 (2000). [PubMed]
A. Roorda, F. Romero-Borja, W. J. Donnelly, H. Queener, T. J. Hebert, and M. C. W. Campbell, “Adaptive optics scanning laser ophthalmoscopy,” Opt. Express 10, 405-412 (2002). [PubMed]
P. Bedggood, M. Daaboul, R. Ashman, G. Smith, and A. Metha, “Characteristics of the human isoplanatic patch and implications for adaptive optics retinal imaging,” J. Biomed. Opt. 13, 024008 (2008). [CrossRef] [PubMed]
S. A. Burns, R. Tumbar, A. E. Elsner, D. Ferguson, and D. X. Hammer, “Large-field-of-view, modular, stabilized, adaptive-optics-based scanning laser ophthalmoscope,” J. Opt. Soc. Am. A 24, 1313-1326 (2007). [CrossRef]
S. B. Stevenson and A. Roorda, “Correcting for miniature eye movements in high resolution scanning laser ophthalmoscopy,” Proc. SPIE 5288, 145-151 (2005). [CrossRef]
K. Y. Li and A. Roorda, “Automated identification of cone photoreceptors in adaptive optics retinal images,” J. Opt. Soc. Am. A 24, 1358-1363 (2007). [CrossRef]
D. H. Wojtas, B. Wu, P. K. Ahnelt, P. J. Bones, and R. P. Millane, “Automated analysis of differential interference contrast microscopy images of the foveal cone mosaic,” J. Opt. Soc. Am. A 25, 1181-1189 (2008). [CrossRef]
R. Montes-Mico, A. Caliz, and J. L. Alio, “Wavefront analysis of higher order aberrations in dry eye patients,” J. Refract. Surg. 20, 243-247 (2004). [PubMed]
S. Koh, N. Maeda, T. Kuroda, Y. Hori, H. Watanabe, T. Fujikado, Y. Tano, Y. Hirohara, and T. Mihashi, “Effect of tear film break-up on higher-order aberrations measured with wavefront sensor,” Am. J. Ophthalmol. 134, 115-117 (2002). [CrossRef] [PubMed]
S. Koh and N. Maeda, “Wavefront sensing and the dynamics of tear film,” Cornea 26, S41-S45 (2007). [CrossRef] [PubMed]
N. J. Coletta and D. R. Williams, “Psychophysical estimation of extrafoveal cone spacing,” J. Opt. Soc. Am. A 4, 1503-1513 (1987). [CrossRef] [PubMed]
J. Liang, B. Grimm, S. Goetz, and J. F. Bille, “Objective measurements of wave aberrations of the human eye with the use of a Hartmann-Shack wave-front sensor.,” J. Opt. Soc. Am. A 11, 1949-1957 (1994). [CrossRef]
L. N. Thibos, X. Hong, A. Bradley, and R. A. Applegate, “Accuracy and precision of objective refraction from wavefront aberrations,” J. Vision 4, 329-351 (2004). [CrossRef]
R. Navarro, “Measurement, modeling and improvement of optical image quality in human eyes,” Acta Phys. Pol. A 101, 147-158 (2002).
T. Y. Chui, H. Song, and S. A. Burns, “Individual variations in human cone photoreceptor packing density: variations with refractive error,” Invest. Ophthalmol. Visual Sci. 49, 4679-4687 (2008). [CrossRef]
P. K. Ahnelt, H. Kolb, and R. Pflug, “Identification of a subtype of cone photoreceptor, likely to be blue sensitive, in the human retina,” J. Comp. Neurol. 255, 18-34 (1987). [CrossRef] [PubMed]
C. Yuodelis and A. Hendrickson, “A qualitative and quantitative analysis of the human fovea during development,” Vision Res. 26, 847-855 (1986). [CrossRef] [PubMed]
G. A. Osterberg, “Topography of the layer of rods and cones in the human retina,” Acta Ophthalmol. 13 Suppl 6, 1-97 (1935).
J. Hirsch and R. Hylton, “Quality of the primate photoreceptor lattice and limits of spatial vision,” Vision Res. 24, 347-356 (1984). [CrossRef] [PubMed]
J. I. Yellott, “Spectral consequences of photoreceptor sampling in the rhesus retina,” Science 221, 382-385 (1983). [CrossRef] [PubMed]
J. Rovamo, V. Virsu, P. Laurinen, and L. Hyvarinen, “Resolution of gratings oriented along and across meridians in peripheral vision,” Invest. Ophthalmol. Visual Sci. 23, 666-670 (1982).
M. A. Berkley, F. Kitterle, and D. W. Watkins, “Grating visibility as a function of orientation and retinal eccentricity,” Vision Res. 15, 239-244 (1975). [CrossRef] [PubMed]
F. W. Campbell, J. J. Kulikowski, and J. Levinson, “The effect of orientation on the visual resolution of gratings,” J. Physiol. (London) 187, 427-436 (1966).
S. Appelle, “Perception and discrimination as a function of stimulus orientation: the 'oblique effect' in man and animals,” Psychol. Bull. 78, 266-278 (1972). [CrossRef] [PubMed]
L. Maffei and F. W. Campbell, “Neurophysiological localization of the vertical and horizontal visual coordinates in man,” Science 167, 386-387 (1970). [CrossRef] [PubMed]
F. W. Campbell and J. J. Kulikowski, “Orientational selectivity of the human visual system,” J. Physiol. (London) 187, 437-445 (1966).
R. S. Anderson, M. O. Wilkinson, and L. N. Thibos, “Psychophysical localization of the human visual streak,” Optom. Vision Sci. 69, 171-174 (1992). [CrossRef]

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[1] D. R. Williams, “Seeing through the photoreceptor mosaic,” Trends Neurosci. 9, 193-198 (1986). [CrossRef]

[2] D. R. Williams and R. Collier, “Consequences of spatial sampling by a human photoreceptor mosaic,” Science 221, 385-387 (1983). [CrossRef] [PubMed]

[3] J. Hirsch and C. A. Curcio, “The spatial resolution capacity of human fovea,” Vision Res. 29, 1095-1101 (1989). [CrossRef] [PubMed]

[4] D. R. Williams and N. J. Coletta, “Cone spacing and the visual resolution limit,” J. Opt. Soc. Am. A 4, 1514-1523 (1987). [CrossRef] [PubMed]

[5] D. R. Williams, “Aliasing in human foveal vision,” Vision Res. 25, 195-205 (1985). [CrossRef] [PubMed]

[6] F. W. Campbell and D. G. Green, “Optical and retinal factors affecting visual resolution,” J. Physiol. (London) 181, 576-593 (1965).

[7] S. J. Anderson and R. F. Hess, “Post-receptoral undersampling in normal human peripheral-vision,” Vision Res. 30, 1507-1515 (1990). [CrossRef] [PubMed]

[8] L. N. Thibos, D. L. Still, and A. Bradley, “Characterization of spatial aliasing and contrast sensitivity in peripheral vision,” Vision Res. 36, 249-258 (1996). [CrossRef] [PubMed]

[9] L. N. Thibos, F. E. Cheney, and D. J. Walsh, “Retinal limits to the detection and resolution of gratings,” J. Opt. Soc. Am. A 4, 1524-1529 (1987). [CrossRef] [PubMed]

[10] N. J. Coletta and T. Watson, “Effect of myopia on visual acuity measured with laser interference fringes,” Vision Res. 46, 636-651 (2006). [CrossRef]

[11] S. J. Anderson, K. T. Mullen, and R. F. Hess, “Human peripheral spatial resolution for achromatic and chromatic stimuli: limits imposed by optical and retinal factors,” J. Physiol. (London) 442, 47-64 (1991).

[12] S. L. Polyak, The Retina (U. Chicago Press, 1941).

[13] C. A. Curcio, K. R. Sloan, Jr., O. Packer, A. E. Hendrickson, and R. E. Kalina, “Distribution of cones in human and monkey retina: individual variability and radial asymmetry,” Science 236, 579-582 (1987). [CrossRef] [PubMed]

[14] C. A. Curcio and K. R. Sloan, “Packing geometry of human cone photoreceptors: variation with eccentricity and evidence for local anistropy,” Vision Res. 9, 169-180 (1992).

[15] 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]

[16] J. Liang, D. R. Williams, and D. T. Miller, “Supernormal vision and high-resolution retinal imaging through adaptive optics,” J. Opt. Soc. Am. A 14, 2884-2892 (1997). [CrossRef]

[17] A. Roorda, “Adaptive optics ophthalmoscopy,” J. Refract. Surg. 16, S602-S607 (2000). [PubMed]

[18] A. Roorda, F. Romero-Borja, W. J. Donnelly, H. Queener, T. J. Hebert, and M. C. W. Campbell, “Adaptive optics scanning laser ophthalmoscopy,” Opt. Express 10, 405-412 (2002). [PubMed]

[19] P. Bedggood, M. Daaboul, R. Ashman, G. Smith, and A. Metha, “Characteristics of the human isoplanatic patch and implications for adaptive optics retinal imaging,” J. Biomed. Opt. 13, 024008 (2008). [CrossRef] [PubMed]

[20] S. A. Burns, R. Tumbar, A. E. Elsner, D. Ferguson, and D. X. Hammer, “Large-field-of-view, modular, stabilized, adaptive-optics-based scanning laser ophthalmoscope,” J. Opt. Soc. Am. A 24, 1313-1326 (2007). [CrossRef]

[21] S. B. Stevenson and A. Roorda, “Correcting for miniature eye movements in high resolution scanning laser ophthalmoscopy,” Proc. SPIE 5288, 145-151 (2005). [CrossRef]

[22] K. Y. Li and A. Roorda, “Automated identification of cone photoreceptors in adaptive optics retinal images,” J. Opt. Soc. Am. A 24, 1358-1363 (2007). [CrossRef]

[23] D. H. Wojtas, B. Wu, P. K. Ahnelt, P. J. Bones, and R. P. Millane, “Automated analysis of differential interference contrast microscopy images of the foveal cone mosaic,” J. Opt. Soc. Am. A 25, 1181-1189 (2008). [CrossRef]

[24] R. Montes-Mico, A. Caliz, and J. L. Alio, “Wavefront analysis of higher order aberrations in dry eye patients,” J. Refract. Surg. 20, 243-247 (2004). [PubMed]

[25] S. Koh, N. Maeda, T. Kuroda, Y. Hori, H. Watanabe, T. Fujikado, Y. Tano, Y. Hirohara, and T. Mihashi, “Effect of tear film break-up on higher-order aberrations measured with wavefront sensor,” Am. J. Ophthalmol. 134, 115-117 (2002). [CrossRef] [PubMed]

[26] S. Koh and N. Maeda, “Wavefront sensing and the dynamics of tear film,” Cornea 26, S41-S45 (2007). [CrossRef] [PubMed]

[27] N. J. Coletta and D. R. Williams, “Psychophysical estimation of extrafoveal cone spacing,” J. Opt. Soc. Am. A 4, 1503-1513 (1987). [CrossRef] [PubMed]

[28] J. Liang, B. Grimm, S. Goetz, and J. F. Bille, “Objective measurements of wave aberrations of the human eye with the use of a Hartmann-Shack wave-front sensor.,” J. Opt. Soc. Am. A 11, 1949-1957 (1994). [CrossRef]

[29] L. N. Thibos, X. Hong, A. Bradley, and R. A. Applegate, “Accuracy and precision of objective refraction from wavefront aberrations,” J. Vision 4, 329-351 (2004). [CrossRef]

[30] R. Navarro, “Measurement, modeling and improvement of optical image quality in human eyes,” Acta Phys. Pol. A 101, 147-158 (2002).

[31] T. Y. Chui, H. Song, and S. A. Burns, “Individual variations in human cone photoreceptor packing density: variations with refractive error,” Invest. Ophthalmol. Visual Sci. 49, 4679-4687 (2008). [CrossRef]

[32] P. K. Ahnelt, H. Kolb, and R. Pflug, “Identification of a subtype of cone photoreceptor, likely to be blue sensitive, in the human retina,” J. Comp. Neurol. 255, 18-34 (1987). [CrossRef] [PubMed]

[33] C. Yuodelis and A. Hendrickson, “A qualitative and quantitative analysis of the human fovea during development,” Vision Res. 26, 847-855 (1986). [CrossRef] [PubMed]

[34] G. A. Osterberg, “Topography of the layer of rods and cones in the human retina,” Acta Ophthalmol. 13 Suppl 6, 1-97 (1935).

[35] J. Hirsch and R. Hylton, “Quality of the primate photoreceptor lattice and limits of spatial vision,” Vision Res. 24, 347-356 (1984). [CrossRef] [PubMed]

[36] J. I. Yellott, “Spectral consequences of photoreceptor sampling in the rhesus retina,” Science 221, 382-385 (1983). [CrossRef] [PubMed]

[37] J. Rovamo, V. Virsu, P. Laurinen, and L. Hyvarinen, “Resolution of gratings oriented along and across meridians in peripheral vision,” Invest. Ophthalmol. Visual Sci. 23, 666-670 (1982).

[38] M. A. Berkley, F. Kitterle, and D. W. Watkins, “Grating visibility as a function of orientation and retinal eccentricity,” Vision Res. 15, 239-244 (1975). [CrossRef] [PubMed]

[39] F. W. Campbell, J. J. Kulikowski, and J. Levinson, “The effect of orientation on the visual resolution of gratings,” J. Physiol. (London) 187, 427-436 (1966).

[40] S. Appelle, “Perception and discrimination as a function of stimulus orientation: the 'oblique effect' in man and animals,” Psychol. Bull. 78, 266-278 (1972). [CrossRef] [PubMed]

[41] L. Maffei and F. W. Campbell, “Neurophysiological localization of the vertical and horizontal visual coordinates in man,” Science 167, 386-387 (1970). [CrossRef] [PubMed]

[42] F. W. Campbell and J. J. Kulikowski, “Orientational selectivity of the human visual system,” J. Physiol. (London) 187, 437-445 (1966).

[43] R. S. Anderson, M. O. Wilkinson, and L. N. Thibos, “Psychophysical localization of the human visual streak,” Optom. Vision Sci. 69, 171-174 (1992). [CrossRef]

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Adaptive-optics imaging of human cone photoreceptor distribution