Wavefront sensorless adaptive optics ophthalmoscopy in the human eye

doi:10.1364/OE.19.014160

Wavefront sensorless adaptive optics ophthalmoscopy in the human eye

Heidi Hofer, Nripun Sredar, Hope Queener, Chaohong Li, and Jason Porter »View Author Affiliations

Optics Express, Vol. 19, Issue 15, pp. 14160-14171 (2011)
http://dx.doi.org/10.1364/OE.19.014160

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Abstract

Wavefront sensor noise and fidelity place a fundamental limit on achievable image quality in current adaptive optics ophthalmoscopes. Additionally, the wavefront sensor ‘beacon’ can interfere with visual experiments. We demonstrate real-time (25 Hz), wavefront sensorless adaptive optics imaging in the living human eye with image quality rivaling that of wavefront sensor based control in the same system. A stochastic parallel gradient descent algorithm directly optimized the mean intensity in retinal image frames acquired with a confocal adaptive optics scanning laser ophthalmoscope (AOSLO). When imaging through natural, undilated pupils, both control methods resulted in comparable mean image intensities. However, when imaging through dilated pupils, image intensity was generally higher following wavefront sensor-based control. Despite the typically reduced intensity, image contrast was higher, on average, with sensorless control. Wavefront sensorless control is a viable option for imaging the living human eye and future refinements of this technique may result in even greater optical gains.

OCIS Codes
(000.3860) General : Mathematical methods in physics
(330.4460) Vision, color, and visual optics : Ophthalmic optics and devices
(110.1080) Imaging systems : Active or adaptive optics

ToC Category:
Vision, Color, and Visual Optics

History
Original Manuscript: April 14, 2011
Revised Manuscript: June 26, 2011
Manuscript Accepted: June 27, 2011
Published: July 11, 2011

Virtual Issues
Vol. 6, Iss. 8 Virtual Journal for Biomedical Optics

Citation
Heidi Hofer, Nripun Sredar, Hope Queener, Chaohong Li, and Jason Porter, "Wavefront sensorless adaptive optics ophthalmoscopy in the human eye," Opt. Express 19, 14160-14171 (2011)
http://www.opticsinfobase.org/oe/abstract.cfm?URI=oe-19-15-14160

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References

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(11), 2884–2892 (1997). [CrossRef] [PubMed]
A. Roorda and D. R. Williams, “The arrangement of the three cone classes in the living human eye,” Nature 397(6719), 520–522 (1999). [CrossRef] [PubMed]
H. Hofer, B. Singer, and D. R. Williams, “Different sensations from cones with the same photopigment,” J. Vis. 5(5), 444–454 (2005). [CrossRef] [PubMed]
W. Makous, J. Carroll, J. I. Wolfing, J. Lin, N. Christie, and D. R. Williams, “Retinal microscotomas revealed with adaptive-optics microflashes,” Invest. Ophthalmol. Vis. Sci. 47(9), 4160–4167 (2006). [CrossRef] [PubMed]
L. C. Sincich, Y. Zhang, P. Tiruveedhula, J. C. Horton, and A. Roorda, “Resolving single cone inputs to visual receptive fields,” Nat. Neurosci. 12(8), 967–969 (2009). [CrossRef] [PubMed]
E. A. Rossi and A. Roorda, “The relationship between visual resolution and cone spacing in the human fovea,” Nat. Neurosci. 13(2), 156–157 (2010). [CrossRef] [PubMed]
R. S. Jonnal, J. R. Besecker, J. C. Derby, O. P. Kocaoglu, B. Cense, W. Gao, Q. Wang, and D. T. Miller, “Imaging outer segment renewal in living human cone photoreceptors,” Opt. Express 18(5), 5257–5270 (2010). [CrossRef] [PubMed]
A. Roorda, F. Romero-Borja, W. Donnelly Iii, H. Queener, T. Hebert, and M. Campbell, “Adaptive optics scanning laser ophthalmoscopy,” Opt. Express 10(9), 405–412 (2002). [PubMed]
B. Hermann, E. J. Fernández, A. Unterhuber, H. Sattmann, A. F. Fercher, W. Drexler, P. M. Prieto, and P. Artal, “Adaptive-optics ultrahigh-resolution optical coherence tomography,” Opt. Lett. 29(18), 2142–2144 (2004). [CrossRef] [PubMed]
Y. Zhang, B. Cense, J. Rha, R. S. Jonnal, W. Gao, R. J. Zawadzki, J. S. Werner, S. Jones, S. Olivier, and D. T. Miller, “High-speed volumetric imaging of cone photoreceptors with adaptive optics spectral-domain optical coherence tomography,” Opt. Express 14(10), 4380–4394 (2006). [CrossRef] [PubMed]
D. C. Gray, W. Merigan, J. I. Wolfing, B. P. Gee, J. Porter, A. Dubra, T. H. Twietmeyer, K. Ahamd, R. Tumbar, F. Reinholz, and D. R. Williams, “In vivo fluorescence imaging of primate retinal ganglion cells and retinal pigment epithelial cells,” Opt. Express 14(16), 7144–7158 (2006). [CrossRef] [PubMed]
J. J. Hunter, B. Masella, A. Dubra, R. Sharma, L. Yin, W. H. Merigan, G. Palczewska, K. Palczewski, and D. R. Williams, “Images of photoreceptors in living primate eyes using adaptive optics two-photon ophthalmoscopy,” Biomed. Opt. Express 2(1), 139–148 (2011). [CrossRef] [PubMed]
J. Carroll, M. Neitz, H. Hofer, J. Neitz, and D. R. Williams, “Functional photoreceptor loss revealed with adaptive optics: an alternate cause of color blindness,” Proc. Natl. Acad. Sci. U.S.A. 101(22), 8461–8466 (2004). [CrossRef] [PubMed]
J. I. Wolfing, M. Chung, J. Carroll, A. Roorda, and D. R. Williams, “High-resolution retinal imaging of cone-rod dystrophy,” Ophthalmology 113(6), 1014–1019 (2006). [CrossRef] [PubMed]
K. E. Talcott, K. Ratnam, S. M. Sunquist, A. S. Lucero, B. J. Lujan, W. Tao, T. C. Porco, A. Roorda, and J. L. Duncan, “Longitudinal study of cone photoreceptors during retinal degeneration and in response to ciliary neurotrophic growth factor,” Invest. Ophthalmol. Vis. Sci. 52(5), 2219–2226 (2011). [CrossRef]
S. Ooto, M. Hangai, A. Sakamoto, A. Tsujikawa, K. Yamashiro, Y. Ojima, Y. Yamada, H. Mukai, S. Oshima, T. Inoue, and N. Yoshimura, “High-resolution imaging of resolved central serous chorioretinopathy using adaptive optics scanning laser ophthalmoscopy,” Ophthalmology 117(9), 1800.e1–1809.e2 (2010). [CrossRef] [PubMed]
Y. Kitaguchi, S. Kusaka, T. Yamaguchi, T. Mihashi, and T. Fujikado, “Detection of photoreceptor disruption by adaptive optics fundus imaging and Fourier-domain optical coherence tomography in eyes with occult macular dystrophy,” Clin. Ophthalmol. 5, 345–351 (2011). [CrossRef] [PubMed]
N. Doble, “High-resolution, in vivo retinal imaging using adaptive optics and its future role in ophthalmology,” Expert Rev. Med. Devices 2(2), 205–216 (2005). [CrossRef] [PubMed]
M. J. Booth, “Adaptive optics in microscopy,” Philos. Transact. A Math. Phys. Eng. Sci. 365(1861), 2829–2843 (2007). [CrossRef] [PubMed]
D. P. Biss, R. H. Webb, Z. Yaopeng, T. G. Bifano, P. Zamiri, and C. P. Lin, “An adaptive optics biomicroscope for mouse retinal imaging,” Proc. SPIE 6467, 646703, 646708 (2007). [CrossRef]
S. Zommer, E. N. Ribak, S. G. Lipson, and J. Adler, “Simulated annealing in ocular adaptive optics,” Opt. Lett. 31(7), 939–941 (2006). [CrossRef] [PubMed]
M. A. Vorontsov, “Decoupled stochastic parallel gradient descent optimization for adaptive optics: integrated approach for wave-front sensor information fusion,” J. Opt. Soc. Am. A 19(2), 356–368 (2002). [CrossRef] [PubMed]
J. R. Fienup and J. J. Miller, “Aberration correction by maximizing generalized sharpness metrics,” J. Opt. Soc. Am. A 20(4), 609–620 (2003). [CrossRef] [PubMed]
D. Débarre, E. J. Botcherby, T. Watanabe, S. Srinivas, M. J. Booth, and T. Wilson, “Image-based adaptive optics for two-photon microscopy,” Opt. Lett. 34(16), 2495–2497 (2009). [CrossRef] [PubMed]
C. Li, N. Sredar, K. M. Ivers, H. Queener, and J. Porter, “A correction algorithm to simultaneously control dual deformable mirrors in a woofer-tweeter adaptive optics system,” Opt. Express 18(16), 16671–16684 (2010). [CrossRef] [PubMed]
T. Wilson, “The role of the pinhole in confocal imaging systems,” in Handbook of Biological Confocal Microscopy. Pawley, J. B., ed. (Plenum Press, New York, 1995).
N. Doble, D. T. Miller, G. Yoon, and D. R. Williams, “Requirements for discrete actuator and segmented wavefront correctors for aberration compensation in two large populations of human eyes,” Appl. Opt. 46(20), 4501–4514 (2007). [CrossRef] [PubMed]
W. Zou, X. Qi, and S. A. Burns, “Woofer-tweeter adaptive optics scanning laser ophthalmoscopic imaging based on Lagrange-multiplier damped least-squares algorithm,” Biomed. Opt. Express 2(7), 1986–2004 (2011). [CrossRef] [PubMed]
W. Jiang and H. Li, “Hartmann-Shack Wavefront Sensing and Control Algorithm,” in Adaptive Optics and Optical Structures. Proceedings of the SPIE, Schulte-in-den-Baeumen, J.J., Tyson, R. K., eds. (SPIE 1990) 1271: 82–93.
H. Hofer, P. Artal, B. Singer, J. L. Aragón, and D. R. Williams, “Dynamics of the eye’s wave aberration,” J. Opt. Soc. Am. A 18(3), 497–506 (2001). [CrossRef] [PubMed]
J. Porter, H. Queener, J. Lin, K. Thorne, and A. Awwal, eds., Adaptive Optics for Vision Science: Principles, Practices, Design, and Applications Ch. 5 (John Wiley and Sons, Inc., New Jersey, 2006).
A. V. Cideciyan, S. G. Jacobson, T. S. Aleman, D. Gu, S. E. Pearce-Kelling, A. Sumaroka, G. M. Acland, and G. D. Aguirre, “In vivo dynamics of retinal injury and repair in the rhodopsin mutant dog model of human retinitis pigmentosa,” Proc. Natl. Acad. Sci. U.S.A. 102(14), 5233–5238 (2005). [CrossRef] [PubMed]

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[1] 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(11), 2884–2892 (1997). [CrossRef] [PubMed]

[2] A. Roorda and D. R. Williams, “The arrangement of the three cone classes in the living human eye,” Nature 397(6719), 520–522 (1999). [CrossRef] [PubMed]

[3] H. Hofer, B. Singer, and D. R. Williams, “Different sensations from cones with the same photopigment,” J. Vis. 5(5), 444–454 (2005). [CrossRef] [PubMed]

[4] W. Makous, J. Carroll, J. I. Wolfing, J. Lin, N. Christie, and D. R. Williams, “Retinal microscotomas revealed with adaptive-optics microflashes,” Invest. Ophthalmol. Vis. Sci. 47(9), 4160–4167 (2006). [CrossRef] [PubMed]

[5] L. C. Sincich, Y. Zhang, P. Tiruveedhula, J. C. Horton, and A. Roorda, “Resolving single cone inputs to visual receptive fields,” Nat. Neurosci. 12(8), 967–969 (2009). [CrossRef] [PubMed]

[6] E. A. Rossi and A. Roorda, “The relationship between visual resolution and cone spacing in the human fovea,” Nat. Neurosci. 13(2), 156–157 (2010). [CrossRef] [PubMed]

[7] R. S. Jonnal, J. R. Besecker, J. C. Derby, O. P. Kocaoglu, B. Cense, W. Gao, Q. Wang, and D. T. Miller, “Imaging outer segment renewal in living human cone photoreceptors,” Opt. Express 18(5), 5257–5270 (2010). [CrossRef] [PubMed]

[8] A. Roorda, F. Romero-Borja, W. Donnelly Iii, H. Queener, T. Hebert, and M. Campbell, “Adaptive optics scanning laser ophthalmoscopy,” Opt. Express 10(9), 405–412 (2002). [PubMed]

[9] B. Hermann, E. J. Fernández, A. Unterhuber, H. Sattmann, A. F. Fercher, W. Drexler, P. M. Prieto, and P. Artal, “Adaptive-optics ultrahigh-resolution optical coherence tomography,” Opt. Lett. 29(18), 2142–2144 (2004). [CrossRef] [PubMed]

[10] Y. Zhang, B. Cense, J. Rha, R. S. Jonnal, W. Gao, R. J. Zawadzki, J. S. Werner, S. Jones, S. Olivier, and D. T. Miller, “High-speed volumetric imaging of cone photoreceptors with adaptive optics spectral-domain optical coherence tomography,” Opt. Express 14(10), 4380–4394 (2006). [CrossRef] [PubMed]

[11] D. C. Gray, W. Merigan, J. I. Wolfing, B. P. Gee, J. Porter, A. Dubra, T. H. Twietmeyer, K. Ahamd, R. Tumbar, F. Reinholz, and D. R. Williams, “In vivo fluorescence imaging of primate retinal ganglion cells and retinal pigment epithelial cells,” Opt. Express 14(16), 7144–7158 (2006). [CrossRef] [PubMed]

[12] J. J. Hunter, B. Masella, A. Dubra, R. Sharma, L. Yin, W. H. Merigan, G. Palczewska, K. Palczewski, and D. R. Williams, “Images of photoreceptors in living primate eyes using adaptive optics two-photon ophthalmoscopy,” Biomed. Opt. Express 2(1), 139–148 (2011). [CrossRef] [PubMed]

[13] J. Carroll, M. Neitz, H. Hofer, J. Neitz, and D. R. Williams, “Functional photoreceptor loss revealed with adaptive optics: an alternate cause of color blindness,” Proc. Natl. Acad. Sci. U.S.A. 101(22), 8461–8466 (2004). [CrossRef] [PubMed]

[14] J. I. Wolfing, M. Chung, J. Carroll, A. Roorda, and D. R. Williams, “High-resolution retinal imaging of cone-rod dystrophy,” Ophthalmology 113(6), 1014–1019 (2006). [CrossRef] [PubMed]

[15] K. E. Talcott, K. Ratnam, S. M. Sunquist, A. S. Lucero, B. J. Lujan, W. Tao, T. C. Porco, A. Roorda, and J. L. Duncan, “Longitudinal study of cone photoreceptors during retinal degeneration and in response to ciliary neurotrophic growth factor,” Invest. Ophthalmol. Vis. Sci. 52(5), 2219–2226 (2011). [CrossRef]

[16] S. Ooto, M. Hangai, A. Sakamoto, A. Tsujikawa, K. Yamashiro, Y. Ojima, Y. Yamada, H. Mukai, S. Oshima, T. Inoue, and N. Yoshimura, “High-resolution imaging of resolved central serous chorioretinopathy using adaptive optics scanning laser ophthalmoscopy,” Ophthalmology 117(9), 1800.e1–1809.e2 (2010). [CrossRef] [PubMed]

[17] Y. Kitaguchi, S. Kusaka, T. Yamaguchi, T. Mihashi, and T. Fujikado, “Detection of photoreceptor disruption by adaptive optics fundus imaging and Fourier-domain optical coherence tomography in eyes with occult macular dystrophy,” Clin. Ophthalmol. 5, 345–351 (2011). [CrossRef] [PubMed]

[18] N. Doble, “High-resolution, in vivo retinal imaging using adaptive optics and its future role in ophthalmology,” Expert Rev. Med. Devices 2(2), 205–216 (2005). [CrossRef] [PubMed]

[19] M. J. Booth, “Adaptive optics in microscopy,” Philos. Transact. A Math. Phys. Eng. Sci. 365(1861), 2829–2843 (2007). [CrossRef] [PubMed]

[20] D. P. Biss, R. H. Webb, Z. Yaopeng, T. G. Bifano, P. Zamiri, and C. P. Lin, “An adaptive optics biomicroscope for mouse retinal imaging,” Proc. SPIE 6467, 646703, 646708 (2007). [CrossRef]

[21] S. Zommer, E. N. Ribak, S. G. Lipson, and J. Adler, “Simulated annealing in ocular adaptive optics,” Opt. Lett. 31(7), 939–941 (2006). [CrossRef] [PubMed]

[22] M. A. Vorontsov, “Decoupled stochastic parallel gradient descent optimization for adaptive optics: integrated approach for wave-front sensor information fusion,” J. Opt. Soc. Am. A 19(2), 356–368 (2002). [CrossRef] [PubMed]

[23] J. R. Fienup and J. J. Miller, “Aberration correction by maximizing generalized sharpness metrics,” J. Opt. Soc. Am. A 20(4), 609–620 (2003). [CrossRef] [PubMed]

[24] D. Débarre, E. J. Botcherby, T. Watanabe, S. Srinivas, M. J. Booth, and T. Wilson, “Image-based adaptive optics for two-photon microscopy,” Opt. Lett. 34(16), 2495–2497 (2009). [CrossRef] [PubMed]

[25] C. Li, N. Sredar, K. M. Ivers, H. Queener, and J. Porter, “A correction algorithm to simultaneously control dual deformable mirrors in a woofer-tweeter adaptive optics system,” Opt. Express 18(16), 16671–16684 (2010). [CrossRef] [PubMed]

[26] T. Wilson, “The role of the pinhole in confocal imaging systems,” in Handbook of Biological Confocal Microscopy. Pawley, J. B., ed. (Plenum Press, New York, 1995).

[27] N. Doble, D. T. Miller, G. Yoon, and D. R. Williams, “Requirements for discrete actuator and segmented wavefront correctors for aberration compensation in two large populations of human eyes,” Appl. Opt. 46(20), 4501–4514 (2007). [CrossRef] [PubMed]

[28] W. Zou, X. Qi, and S. A. Burns, “Woofer-tweeter adaptive optics scanning laser ophthalmoscopic imaging based on Lagrange-multiplier damped least-squares algorithm,” Biomed. Opt. Express 2(7), 1986–2004 (2011). [CrossRef] [PubMed]

[29] W. Jiang and H. Li, “Hartmann-Shack Wavefront Sensing and Control Algorithm,” in Adaptive Optics and Optical Structures. Proceedings of the SPIE, Schulte-in-den-Baeumen, J.J., Tyson, R. K., eds. (SPIE 1990) 1271: 82–93.

[30] H. Hofer, P. Artal, B. Singer, J. L. Aragón, and D. R. Williams, “Dynamics of the eye’s wave aberration,” J. Opt. Soc. Am. A 18(3), 497–506 (2001). [CrossRef] [PubMed]

[31] J. Porter, H. Queener, J. Lin, K. Thorne, and A. Awwal, eds., Adaptive Optics for Vision Science: Principles, Practices, Design, and Applications Ch. 5 (John Wiley and Sons, Inc., New Jersey, 2006).

[32] A. V. Cideciyan, S. G. Jacobson, T. S. Aleman, D. Gu, S. E. Pearce-Kelling, A. Sumaroka, G. M. Acland, and G. D. Aguirre, “In vivo dynamics of retinal injury and repair in the rhodopsin mutant dog model of human retinitis pigmentosa,” Proc. Natl. Acad. Sci. U.S.A. 102(14), 5233–5238 (2005). [CrossRef] [PubMed]

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Wavefront sensorless adaptive optics ophthalmoscopy in the human eye