Abstract

Eye motion is a major impediment to the efficient acquisition of high resolution retinal images with the adaptive optics (AO) scanning light ophthalmoscope (AOSLO). Here we demonstrate a solution to this problem by implementing both optical stabilization and digital image registration in an AOSLO. We replaced the slow scanning mirror with a two-axis tip/tilt mirror for the dual functions of slow scanning and optical stabilization. Closed-loop optical stabilization reduced the amplitude of eye-movement related-image motion by a factor of 10–15. The residual RMS error after optical stabilization alone was on the order of the size of foveal cones: ~1.66–2.56 μm or ~0.34–0.53 arcmin with typical fixational eye motion for normal observers. The full implementation, with real-time digital image registration, corrected the residual eye motion after optical stabilization with an accuracy of ~0.20–0.25 μm or ~0.04–0.05 arcmin RMS, which to our knowledge is more accurate than any method previously reported.

© 2014 Optical Society of America

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2014 (1)

W. M. Harmening, W. S. Tuten, A. Roorda, and L. C. Sincich, “Mapping the Perceptual Grain of the Human Retina,” J. Neurosci.34(16), 5667–5677 (2014).
[CrossRef] [PubMed]

2013 (4)

2012 (2)

2011 (3)

D. R. Williams, “Imaging single cells in the living retina,” Vision Res.51(13), 1379–1396 (2011).
[CrossRef] [PubMed]

E. A. Rossi, M. Chung, A. Dubra, J. J. Hunter, W. H. Merigan, and D. R. Williams, “Imaging retinal mosaics in the living eye,” Eye (Lond.)25(3), 301–308 (2011).
[CrossRef] [PubMed]

A. Dubra and Y. Sulai, “Reflective afocal broadband adaptive optics scanning ophthalmoscope,” Biomed. Opt. Express2(6), 1757–1768 (2011).
[CrossRef] [PubMed]

2010 (2)

2009 (2)

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]

M. Rolfs, “Microsaccades: Small steps on a long way,” Vision Res.49(20), 2415–2441 (2009).
[CrossRef] [PubMed]

2008 (1)

2007 (4)

2006 (2)

2004 (1)

S. Martinez-Conde, S. L. Macknik, and D. H. Hubel, “The role of fixational eye movements in visual perception,” Nat. Rev. Neurosci.5(3), 229–240 (2004).
[CrossRef] [PubMed]

2002 (1)

1997 (4)

J. Liang, D. R. Williams, and D. T. Miller, “Supernormal vision and high-resolution retinal imaging through adaptive optics,” J. Opt. Soc. Am. A14(11), 2884–2892 (1997).
[CrossRef] [PubMed]

D. G. Pelli, “The VideoToolbox software for visual psychophysics: Transforming numbers into movies,” Spat. Vis.10(4), 437–442 (1997).
[CrossRef] [PubMed]

D. H. Brainard, “The psychophysics toolbox,” Spat. Vis.10(4), 433–436 (1997).
[CrossRef] [PubMed]

J. B. Mulligan, “Image processing for improved eye-tracking accuracy,” Behav. Res. Methods Instrum. Comput.29(1), 54–65 (1997).
[CrossRef] [PubMed]

1996 (1)

M. Stetter, R. A. Sendtner, and G. T. Timberlake, “A novel method for measuring saccade profiles using the scanning laser ophthalmoscope,” Vision Res.36(13), 1987–1994 (1996).
[CrossRef] [PubMed]

1992 (1)

D. Ott and W. J. Daunicht, “Eye-Movement Measurement with the scanning laser ophthalmoscope,” Clin. Vis. Sci.7, 551–556 (1992).

1990 (1)

D. Ott and M. Lades, “Measurement of eye rotations in three dimensions and the retinal stimulus projection using scanning laser ophthalmoscopy,” Ophthalmic Physiol. Opt.10(1), 67–71 (1990).
[CrossRef] [PubMed]

1989 (1)

D. Ott and R. Eckmiller, “Ocular torsion measured by TV- and scanning laser ophthalmoscopy during horizontal pursuit in humans and monkeys,” Invest. Ophthalmol. Vis. Sci.30(12), 2512–2520 (1989).
[PubMed]

1985 (1)

1975 (1)

R. M. Jones and T. Tulunay-Keesey, “Accuracy of image stabilization by an optical-electronic feedback system,” Vision Res.15(1), 57–61 (1975).
[CrossRef] [PubMed]

1973 (1)

1968 (1)

L. A. Riggs and A. M. Schick, “Accuracy of retinal image stabilization achieved with a plane mirror on a tightly fitting contact lens,” Vision Res.8(2), 159–169 (1968).
[CrossRef] [PubMed]

1959 (1)

1954 (1)

1953 (1)

1901 (1)

R. Dodge and T. S. Cline, “The angle velocity of eye movements,” Psychol. Rev.8(2), 145–157 (1901).
[CrossRef]

1804 (1)

D. (I.P.V.) Troxler, “Über das Verschwinden gegebener Gegenstände innerhalb unseres Gesichtskreises. [On the disappearance of given objects from our visual field],” Ophthalmol. Bibl. Ger.2, 1–53 (1804).

Achtman, R. L.

E. A. Rossi, R. L. Achtman, A. Guidon, D. R. Williams, A. Roorda, D. Bavelier, and J. Carroll, “Visual Function and Cortical Organization in Carriers of Blue Cone Monochromacy,” PLoS ONE8(2), e57956 (2013).
[CrossRef] [PubMed]

Arathorn, D. W.

D. W. Arathorn, S. B. Stevenson, Q. Yang, P. Tiruveedhula, and A. Roorda, “How the unstable eye sees a stable and moving world,” J. Vis.13(10), 22 (2013).
[CrossRef] [PubMed]

B. Braaf, K. V. Vienola, C. K. Sheehy, Q. Yang, K. A. Vermeer, P. Tiruveedhula, D. W. Arathorn, A. Roorda, and J. F. de Boer, “Real-time eye motion correction in phase-resolved OCT angiography with tracking SLO,” Biomed. Opt. Express4(1), 51–65 (2013).
[CrossRef] [PubMed]

K. V. Vienola, B. Braaf, C. K. Sheehy, Q. Yang, P. Tiruveedhula, D. W. Arathorn, J. F. de Boer, and A. Roorda, “Real-time eye motion compensation for OCT imaging with tracking SLO,” Biomed. Opt. Express3(11), 2950–2963 (2012).
[CrossRef] [PubMed]

C. K. Sheehy, Q. Yang, D. W. Arathorn, P. Tiruveedhula, J. F. de Boer, and A. Roorda, “High-speed, image-based eye tracking with a scanning laser ophthalmoscope,” Biomed. Opt. Express3(10), 2611–2622 (2012).
[CrossRef] [PubMed]

Q. Yang, D. W. Arathorn, P. Tiruveedhula, C. R. Vogel, and A. Roorda, “Design of an integrated hardware interface for AOSLO image capture and cone-targeted stimulus delivery,” Opt. Express18(17), 17841–17858 (2010).
[CrossRef] [PubMed]

D. W. Arathorn, Q. Yang, C. R. Vogel, Y. Zhang, P. Tiruveedhula, and A. Roorda, “Retinally stabilized cone-targeted stimulus delivery,” Opt. Express15(21), 13731–13744 (2007).
[CrossRef] [PubMed]

C. R. Vogel, D. W. Arathorn, A. Roorda, and A. Parker, “Retinal motion estimation in adaptive optics scanning laser ophthalmoscopy,” Opt. Express14(2), 487–497 (2006).
[CrossRef] [PubMed]

Armington, J. C.

Bavelier, D.

E. A. Rossi, R. L. Achtman, A. Guidon, D. R. Williams, A. Roorda, D. Bavelier, and J. Carroll, “Visual Function and Cortical Organization in Carriers of Blue Cone Monochromacy,” PLoS ONE8(2), e57956 (2013).
[CrossRef] [PubMed]

Bigelow, C. E.

Braaf, B.

Brainard, D.

M. Kleiner, D. Brainard, and D. G. Pelli, “What’s new in Psychtoolbox-3?” Perception36, 1 (2007).

Brainard, D. H.

D. H. Brainard, “The psychophysics toolbox,” Spat. Vis.10(4), 433–436 (1997).
[CrossRef] [PubMed]

Burns, S. A.

Campbell, M.

Carroll, J.

E. A. Rossi, R. L. Achtman, A. Guidon, D. R. Williams, A. Roorda, D. Bavelier, and J. Carroll, “Visual Function and Cortical Organization in Carriers of Blue Cone Monochromacy,” PLoS ONE8(2), e57956 (2013).
[CrossRef] [PubMed]

Chung, M.

E. A. Rossi, M. Chung, A. Dubra, J. J. Hunter, W. H. Merigan, and D. R. Williams, “Imaging retinal mosaics in the living eye,” Eye (Lond.)25(3), 301–308 (2011).
[CrossRef] [PubMed]

Chung, M. M.

Cline, T. S.

R. Dodge and T. S. Cline, “The angle velocity of eye movements,” Psychol. Rev.8(2), 145–157 (1901).
[CrossRef]

Cornsweet, J. C.

Cornsweet, T. N.

Crane, H. D.

Daunicht, W. J.

D. Ott and W. J. Daunicht, “Eye-Movement Measurement with the scanning laser ophthalmoscope,” Clin. Vis. Sci.7, 551–556 (1992).

de Boer, J. F.

Deng, C.

Dodge, R.

R. Dodge and T. S. Cline, “The angle velocity of eye movements,” Psychol. Rev.8(2), 145–157 (1901).
[CrossRef]

Donnelly Iii, W.

Dubra, A.

Eckmiller, R.

D. Ott and R. Eckmiller, “Ocular torsion measured by TV- and scanning laser ophthalmoscopy during horizontal pursuit in humans and monkeys,” Invest. Ophthalmol. Vis. Sci.30(12), 2512–2520 (1989).
[PubMed]

Elsner, A. E.

Ferguson, D.

Ferguson, R. D.

Fienup, J. R.

Fischer, W.

Folwell, M. A.

Guidon, A.

E. A. Rossi, R. L. Achtman, A. Guidon, D. R. Williams, A. Roorda, D. Bavelier, and J. Carroll, “Visual Function and Cortical Organization in Carriers of Blue Cone Monochromacy,” PLoS ONE8(2), e57956 (2013).
[CrossRef] [PubMed]

Guizar-Sicairos, M.

Hammer, D. X.

Harmening, W. M.

W. M. Harmening, W. S. Tuten, A. Roorda, and L. C. Sincich, “Mapping the Perceptual Grain of the Human Retina,” J. Neurosci.34(16), 5667–5677 (2014).
[CrossRef] [PubMed]

Hebert, T.

Horton, J. C.

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]

Hubel, D. H.

S. Martinez-Conde, S. L. Macknik, and D. H. Hubel, “The role of fixational eye movements in visual perception,” Nat. Rev. Neurosci.5(3), 229–240 (2004).
[CrossRef] [PubMed]

Hunter, J. J.

E. A. Rossi, M. Chung, A. Dubra, J. J. Hunter, W. H. Merigan, and D. R. Williams, “Imaging retinal mosaics in the living eye,” Eye (Lond.)25(3), 301–308 (2011).
[CrossRef] [PubMed]

Iftimia, N. V.

Iovin, R.

F. Santini, G. Redner, R. Iovin, and M. Rucci, “EyeRIS: a general-purpose system for eye-movement-contingent display control,” Behav. Res. Methods39(3), 350–364 (2007).
[CrossRef] [PubMed]

Jones, R. M.

R. M. Jones and T. Tulunay-Keesey, “Accuracy of image stabilization by an optical-electronic feedback system,” Vision Res.15(1), 57–61 (1975).
[CrossRef] [PubMed]

Kleiner, M.

M. Kleiner, D. Brainard, and D. G. Pelli, “What’s new in Psychtoolbox-3?” Perception36, 1 (2007).

Lades, M.

D. Ott and M. Lades, “Measurement of eye rotations in three dimensions and the retinal stimulus projection using scanning laser ophthalmoscopy,” Ophthalmic Physiol. Opt.10(1), 67–71 (1990).
[CrossRef] [PubMed]

Latchney, L. R.

Liang, J.

Macknik, S. L.

S. Martinez-Conde, S. L. Macknik, and D. H. Hubel, “The role of fixational eye movements in visual perception,” Nat. Rev. Neurosci.5(3), 229–240 (2004).
[CrossRef] [PubMed]

Martinez-Conde, S.

S. Martinez-Conde, S. L. Macknik, and D. H. Hubel, “The role of fixational eye movements in visual perception,” Nat. Rev. Neurosci.5(3), 229–240 (2004).
[CrossRef] [PubMed]

Merigan, W. H.

E. A. Rossi, M. Chung, A. Dubra, J. J. Hunter, W. H. Merigan, and D. R. Williams, “Imaging retinal mosaics in the living eye,” Eye (Lond.)25(3), 301–308 (2011).
[CrossRef] [PubMed]

Miller, D. T.

Mujat, M.

Mulligan, J. B.

J. B. Mulligan, “Image processing for improved eye-tracking accuracy,” Behav. Res. Methods Instrum. Comput.29(1), 54–65 (1997).
[CrossRef] [PubMed]

Nachmias, J.

Ott, D.

D. Ott and W. J. Daunicht, “Eye-Movement Measurement with the scanning laser ophthalmoscope,” Clin. Vis. Sci.7, 551–556 (1992).

D. Ott and M. Lades, “Measurement of eye rotations in three dimensions and the retinal stimulus projection using scanning laser ophthalmoscopy,” Ophthalmic Physiol. Opt.10(1), 67–71 (1990).
[CrossRef] [PubMed]

D. Ott and R. Eckmiller, “Ocular torsion measured by TV- and scanning laser ophthalmoscopy during horizontal pursuit in humans and monkeys,” Invest. Ophthalmol. Vis. Sci.30(12), 2512–2520 (1989).
[PubMed]

Parker, A.

Parkins, K.

Patel, A. H.

Pelli, D. G.

M. Kleiner, D. Brainard, and D. G. Pelli, “What’s new in Psychtoolbox-3?” Perception36, 1 (2007).

D. G. Pelli, “The VideoToolbox software for visual psychophysics: Transforming numbers into movies,” Spat. Vis.10(4), 437–442 (1997).
[CrossRef] [PubMed]

Queener, H.

Rangel-Fonseca, P.

Ratliff, F.

Redner, G.

F. Santini, G. Redner, R. Iovin, and M. Rucci, “EyeRIS: a general-purpose system for eye-movement-contingent display control,” Behav. Res. Methods39(3), 350–364 (2007).
[CrossRef] [PubMed]

Riggs, L. A.

Rolfs, M.

M. Rolfs, “Microsaccades: Small steps on a long way,” Vision Res.49(20), 2415–2441 (2009).
[CrossRef] [PubMed]

Romero-Borja, F.

Roorda, A.

W. M. Harmening, W. S. Tuten, A. Roorda, and L. C. Sincich, “Mapping the Perceptual Grain of the Human Retina,” J. Neurosci.34(16), 5667–5677 (2014).
[CrossRef] [PubMed]

D. W. Arathorn, S. B. Stevenson, Q. Yang, P. Tiruveedhula, and A. Roorda, “How the unstable eye sees a stable and moving world,” J. Vis.13(10), 22 (2013).
[CrossRef] [PubMed]

B. Braaf, K. V. Vienola, C. K. Sheehy, Q. Yang, K. A. Vermeer, P. Tiruveedhula, D. W. Arathorn, A. Roorda, and J. F. de Boer, “Real-time eye motion correction in phase-resolved OCT angiography with tracking SLO,” Biomed. Opt. Express4(1), 51–65 (2013).
[CrossRef] [PubMed]

E. A. Rossi, R. L. Achtman, A. Guidon, D. R. Williams, A. Roorda, D. Bavelier, and J. Carroll, “Visual Function and Cortical Organization in Carriers of Blue Cone Monochromacy,” PLoS ONE8(2), e57956 (2013).
[CrossRef] [PubMed]

K. V. Vienola, B. Braaf, C. K. Sheehy, Q. Yang, P. Tiruveedhula, D. W. Arathorn, J. F. de Boer, and A. Roorda, “Real-time eye motion compensation for OCT imaging with tracking SLO,” Biomed. Opt. Express3(11), 2950–2963 (2012).
[CrossRef] [PubMed]

C. K. Sheehy, Q. Yang, D. W. Arathorn, P. Tiruveedhula, J. F. de Boer, and A. Roorda, “High-speed, image-based eye tracking with a scanning laser ophthalmoscope,” Biomed. Opt. Express3(10), 2611–2622 (2012).
[CrossRef] [PubMed]

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[CrossRef] [PubMed]

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[CrossRef] [PubMed]

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[CrossRef] [PubMed]

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[CrossRef] [PubMed]

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Supplementary Material (3)

» Media 1: MPEG (1120 KB)     
» Media 2: MPEG (2482 KB)     
» Media 3: MPEG (580 KB)     

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Figures (9)

Fig. 1
Fig. 1

Two axes of the PI TTM (dark shaded square) showing its full range of motion (lightly shaded diamond). The dashed rectangle encloses the area of the stabilization range that can be utilized in the optical system. The small dark square shows the size of a 1.5° × 1.5° AOSLO imaging field. Scale bar is one degree.

Fig. 2
Fig. 2

Flow chart of optical stabilization system

Fig. 3
Fig. 3

Strip-level data acquisition, buffering, and eye motion detection. The duration of the longest latencies (T1,T3,T4 & T5) are denoted by the brackets; arrows denote the end of each latency. Note that T2 and T6 are extremely short; their durations are denoted by the thickness of the labeled arrows.

Fig. 4
Fig. 4

Human imaging locations. Subjects NOR011a, NOR025a, NOR037a, were imaged using the pattern of locations shown in (a), while subject NOR047a was imaged with the pattern shown in (b). The gray circle denotes the foveal center imaging location, while the gray squares denote eccentric imaging locations.

Fig. 5
Fig. 5

Eye motion trace computed from the image sequence shown in Media 2, showing vertical (y) component of eye motion before (red) and after optical stabilization alone (blue) and optical stabilization combined with digital registration (green). Inset shows zoomed in trace for the region denoted by the dashed rectangle. Asterisks denote spurious motion measurements during blinks or large amplitude motion (see Appendix for details).

Fig. 6
Fig. 6

Small amplitude motion is calculated by comparing strips of data between consecutive frames. This works well when the motion between frames is small (such as between frame Fr and Fn. However, this fails when the between frame motion is large (such as between frame Fr and frame Fn + 1).

Fig. 7
Fig. 7

A frame offset (Xn,c,Yn,c) is applied before calculating strip motion to increase the probability that strips on the current frame will be compared with the appropriate overlapping strips on the reference frame (Fr)

Fig. 8
Fig. 8

The computational cost of the frame offset (Xn,c,Yn,c) calculation is reduced by using only the central portion of the frame (denoted by the shaded region).

Fig. 9
Fig. 9

Large amplitude motion and blink detection computes motion between consecutive frames using strips from the same frame position (denoted by the darker shading).

Tables (3)

Tables Icon

Table 1 Electronic latencies of the optical stabilization system

Tables Icon

Table 2 Optical stabilization system performance for each participant

Tables Icon

Table 3 Comparison to other stabilization and registration methods

Equations (11)

Equations on this page are rendered with MathJax. Learn more.

| r 1 |=1
| r 2 |=1
r =a r 1 +b r 2 ,
R (t+1)= R (t)+ g Δ R (t)
S +Θ{ R (t+1)}
RMS= i=1 N ( r i r ¯ ) 2 N1
R( u,v )=FF T R2C ( r( x,y ) )
T( u,v )=FF T R2C ( t( x,y ) )
A( u,v )=R( u,v )conj( T( u,v ) )
b( x,y )=FF T C2R 1 ( A(u,v) )
( x,y ) max =argmax( b(x,y) ),

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