Abstract

A growing body of evidence suggests that phototransduction can be studied in the human eye in vivo by imaging of fast intrinsic optical signals (IOS). There is consensus concerning the limiting influence of motion-associated imaging noise on the reproducibility of IOS-measurements, especially in those employing spectral-domain optical coherence tomography (SD-OCT). However, no study to date has conducted a comprehensive analysis of this noise in the context of IOS-imaging. In this study, we discuss biophysical correlates of IOS, and we address motion-associated imaging noise by providing correctional post-processing methods. In order to avoid cross-talk of adjacent IOS of opposite signal polarity, cellular resolution and stability of imaging to the level of individual cones is likely needed. The optical Stiles-Crawford effect can be a source of significant IOS-imaging noise if alignment with the peak of the Stiles-Crawford function cannot be maintained. Therefore, complete head stabilization by implementation of a bite-bar may be critical to maintain a constant pupil entry position of the OCT beam. Due to depth-dependent sensitivity fall-off, heartbeat and breathing associated axial movements can cause tissue reflectivity to vary by 29% over time, although known methods can be implemented to null these effects. Substantial variations in reflectivity can be caused by variable illumination due to changes in the beam pupil entry position and angle, which can be reduced by an adaptive algorithm based on slope-fitting of optical attenuation in the choriocapillary lamina.

© 2015 Optical Society of America

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2014 (1)

2013 (7)

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. Express 4(1), 51–65 (2013).
[Crossref] [PubMed]

T. Klein, W. Wieser, L. Reznicek, A. Neubauer, A. Kampik, and R. Huber, “Multi-MHz retinal OCT,” Biomed. Opt. Express 4(10), 1890–1908 (2013).
[Crossref] [PubMed]

B. Wang, R. Lu, Q. Zhang, Y. Jiang, and X. Yao, “En face optical coherence tomography of transient light response at photoreceptor outer segments in living frog eyecup,” Opt. Lett. 38(22), 4526–4529 (2013).
[Crossref] [PubMed]

L. Thaler, A. C. Schütz, M. A. Goodale, and K. R. Gegenfurtner, “What is the best fixation target? The effect of target shape on stability of fixational eye movements,” Vision Res. 76, 31–42 (2013).
[Crossref] [PubMed]

H. Radhakrishnan and V. J. Srinivasan, “Compartment-resolved imaging of cortical functional hyperemia with OCT angiography,” Biomed. Opt. Express 4(8), 1255–1268 (2013).
[Crossref] [PubMed]

P. Bedggood and A. Metha, “Optical imaging of human cone photoreceptors directly following the capture of light,” PLoS ONE 8(11), e79251 (2013).
[Crossref] [PubMed]

K. A. Vermeer, J. Mo, J. J. Weda, H. G. Lemij, and J. F. de Boer, “Depth-resolved model-based reconstruction of attenuation coefficients in optical coherence tomography,” Biomed. Opt. Express 5(1), 322–337 (2013).
[Crossref] [PubMed]

2012 (5)

I. Grulkowski, J. J. Liu, B. Potsaid, V. Jayaraman, C. D. Lu, J. Jiang, A. E. Cable, J. S. Duker, and J. G. Fujimoto, “Retinal, anterior segment and full eye imaging using ultrahigh speed swept source OCT with vertical-cavity surface emitting lasers,” Biomed. Opt. Express 3(11), 2733–2751 (2012).
[Crossref] [PubMed]

Q. Q. Zhang, X. J. Wu, T. Tang, S. W. Zhu, Q. Yao, B. Z. Gao, and X. C. Yuan, “Quantitative analysis of rectal cancer by spectral domain optical coherence tomography,” Phys. Med. Biol. 57(16), 5235–5244 (2012).
[Crossref] [PubMed]

P. Bedggood and A. Metha, “Variability in bleach kinetics and amount of photopigment between individual foveal cones,” Invest. Ophthalmol. Vis. Sci. 53(7), 3673–3681 (2012).
[Crossref] [PubMed]

R. S. Jonnal, O. P. Kocaoglu, Q. Wang, S. Lee, and D. T. Miller, “Phase-sensitive imaging of the outer retina using optical coherence tomography and adaptive optics,” Biomed. Opt. Express 3(1), 104–124 (2012).
[Crossref] [PubMed]

J. I. Korenbrot, “Speed, sensitivity, and stability of the light response in rod and cone photoreceptors: facts and models,” Prog. Retin. Eye Res. 31(5), 442–466 (2012).
[Crossref] [PubMed]

2011 (4)

A. A. Moayed, S. Hariri, V. Choh, and K. Bizheva, “In vivo imaging of intrinsic optical signals in chicken retina with functional optical coherence tomography,” Opt. Lett. 36(23), 4575–4577 (2011).
[Crossref] [PubMed]

O. P. Kocaoglu, S. Lee, R. S. Jonnal, Q. Wang, A. E. Herde, J. C. Derby, W. Gao, and D. T. Miller, “Imaging cone photoreceptors in three dimensions and in time using ultrahigh resolution optical coherence tomography with adaptive optics,” Biomed. Opt. Express 2(4), 748–763 (2011).
[Crossref] [PubMed]

R. de Kinkelder, J. Kalkman, D. J. Faber, O. Schraa, P. H. Kok, F. D. Verbraak, and T. G. van Leeuwen, “Heartbeat-induced axial motion artifacts in optical coherence tomography measurements of the retina,” Invest. Ophthalmol. Vis. Sci. 52(6), 3908–3913 (2011).
[Crossref] [PubMed]

Y. Y. Shih, B. H. De la Garza, E. R. Muir, W. E. Rogers, J. M. Harrison, J. W. Kiel, and T. Q. Duong, “Lamina-specific functional MRI of retinal and choroidal responses to visual stimuli,” Invest. Ophthalmol. Vis. Sci. 52(8), 5303–5310 (2011).
[Crossref] [PubMed]

2010 (1)

T. Schmoll, C. Kolbitsch, and R. A. Leitgeb, “In vivo functional retinal optical coherence tomography,” J. Biomed. Opt. 15(4), 041513 (2010).
[Crossref] [PubMed]

2009 (6)

V. J. Srinivasan, Y. Chen, J. S. Duker, and J. G. Fujimoto, “In vivo functional imaging of intrinsic scattering changes in the human retina with high-speed ultrahigh resolution OCT,” Opt. Express 17(5), 3861–3877 (2009).
[PubMed]

J. Rha, B. Schroeder, P. Godara, and J. Carroll, “Variable optical activation of human cone photoreceptors visualized using a short coherence light source,” Opt. Lett. 34(24), 3782–3784 (2009).
[Crossref] [PubMed]

A. R. Tumlinson, B. Hermann, B. Hofer, B. Povazay, T. H. Margrain, A. M. Binns, and W. Drexler, “Techniques for extraction of depth-resolved in vivo human retinal intrinsic optical signals with optical coherence tomography,” Jpn. J. Ophthalmol. 53(4), 315–326 (2009).
[Crossref] [PubMed]

X. C. Yao, “Intrinsic optical signal imaging of retinal activation,” Jpn. J. Ophthalmol. 53(4), 327–333 (2009).
[Crossref] [PubMed]

S. Ricco, M. Chen, H. Ishikawa, G. Wollstein, and J. Schuman, “Correcting motion artifacts in retinal spectral domain optical coherence tomography via image registration,” Med. Image Comput. Assist. Interv. 12(Pt 1), 100–107 (2009).
[PubMed]

D. Ts’o, J. Schallek, Y. Kwon, R. Kardon, M. Abramoff, and P. Soliz, “Noninvasive functional imaging of the retina reveals outer retinal and hemodynamic intrinsic optical signal origins,” Jpn. J. Ophthalmol. 53(4), 334–344 (2009).
[Crossref] [PubMed]

2008 (5)

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(2), 024008 (2008).
[Crossref] [PubMed]

B. Potsaid, I. Gorczynska, V. J. Srinivasan, Y. Chen, J. Jiang, A. Cable, and J. G. Fujimoto, “Ultrahigh speed spectral / Fourier domain OCT ophthalmic imaging at 70,000 to 312,500 axial scans per second,” Opt. Express 16(19), 15149–15169 (2008).
[Crossref] [PubMed]

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(9), 6486–6501 (2008).
[Crossref] [PubMed]

D. Nagy, B. Schönfisch, E. Zrenner, and H. Jägle, “Long-term follow-up of retinitis pigmentosa patients with multifocal electroretinography,” Invest. Ophthalmol. Vis. Sci. 49(10), 4664–4671 (2008).
[Crossref] [PubMed]

K. Grieve and A. Roorda, “Intrinsic signals from human cone photoreceptors,” Invest. Ophthalmol. Vis. Sci. 49(2), 713–719 (2008).
[Crossref] [PubMed]

2007 (1)

2006 (2)

K. Bizheva, R. Pflug, B. Hermann, B. Povazay, H. Sattmann, P. Qiu, E. Anger, H. Reitsamer, S. Popov, J. R. Taylor, A. Unterhuber, P. Ahnelt, and W. Drexler, “Optophysiology: Depth-resolved probing of retinal physiology with functional ultrahigh-resolution optical coherence tomography,” Proc. Natl. Acad. Sci. U.S.A. 103(13), 5066–5071 (2006).
[Crossref] [PubMed]

X. C. Yao and J. S. George, “Near-infrared imaging of fast intrinsic optical responses in visible light-activated amphibian retina,” J. Biomed. Opt. 11(6), 064030 (2006).
[Crossref] [PubMed]

2005 (3)

2004 (7)

C. Friedburg, C. P. Allen, P. J. Mason, and T. D. Lamb, “Contribution of cone photoreceptors and post-receptoral mechanisms to the human photopic electroretinogram,” J. Physiol. 556(3), 819–834 (2004).
[Crossref] [PubMed]

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]

A. Podoleanu, I. Charalambous, L. Plesea, A. Dogariu, and R. Rosen, “Correction of distortions in optical coherence tomography imaging of the eye,” Phys. Med. Biol. 49(7), 1277–1294 (2004).
[Crossref] [PubMed]

S. H. Yun, G. Tearney, J. de Boer, and B. Bouma, “Motion artifacts in optical coherence tomography with frequency-domain ranging,” Opt. Express 12(13), 2977–2998 (2004).
[Crossref] [PubMed]

N. Nassif, B. Cense, B. Park, M. Pierce, S. Yun, B. Bouma, G. Tearney, T. Chen, and J. de Boer, “In vivo high-resolution video-rate spectral-domain optical coherence tomography of the human retina and optic nerve,” Opt. Express 12(3), 367–376 (2004).
[Crossref] [PubMed]

D. Faber, F. van der Meer, M. Aalders, and T. van Leeuwen, “Quantitative measurement of attenuation coefficients of weakly scattering media using optical coherence tomography,” Opt. Express 12(19), 4353–4365 (2004).
[Crossref] [PubMed]

D. K. Sardar, F. S. Salinas, J. J. Perez, and A. T. Tsin, “Optical characterization of bovine retinal tissues,” J. Biomed. Opt. 9(3), 624–631 (2004).
[Crossref] [PubMed]

2003 (3)

2002 (1)

F. Møller, M. L. Laursen, J. Tygesen, and A. K. Sjølie, “Binocular quantification and characterization of microsaccades,” Graefes Arch. Clin. Exp. Ophthalmol. 240(9), 765–770 (2002).
[Crossref] [PubMed]

2001 (1)

A. Kusnetzow, A. Dukkipati, K. R. Babu, D. Singh, B. W. Vought, B. E. Knox, and R. R. Birge, “The photobleaching sequence of a short-wavelength visual pigment,” Biochemistry 40(26), 7832–7844 (2001).
[Crossref] [PubMed]

2000 (3)

I. B. Leskov, V. A. Klenchin, J. W. Handy, G. G. Whitlock, V. I. Govardovskii, M. D. Bownds, T. D. Lamb, E. N. Pugh, and V. Y. Arshavsky, “The gain of rod phototransduction: reconciliation of biochemical and electrophysiological measurements,” Neuron 27(3), 525–537 (2000).
[Crossref] [PubMed]

M. Heck, A. Pulvermüller, and K. P. Hofmann, “Light scattering methods to monitor interactions between rhodopsin-containing membranes and soluble proteins,” Methods Enzymol. 315, 329–347 (2000).
[Crossref] [PubMed]

P. J. DeLint, T. T. Berendschot, J. van de Kraats, and D. van Norren, “Slow optical changes in human photoreceptors induced by light,” Invest. Ophthalmol. Vis. Sci. 41(1), 282–289 (2000).
[PubMed]

1999 (1)

B. W. Vought, A. Dukkipatti, M. Max, B. E. Knox, and R. R. Birge, “Photochemistry of the primary event in short-wavelength visual opsins at low temperature,” Biochemistry 38(35), 11287–11297 (1999).
[Crossref] [PubMed]

1997 (2)

H. Imai, A. Terakita, S. Tachibanaki, Y. Imamoto, T. Yoshizawa, and Y. Shichida, “Photochemical and biochemical properties of chicken blue-sensitive cone visual pigment,” Biochemistry 36(42), 12773–12779 (1997).
[Crossref] [PubMed]

P. J. Delint, T. T. Berendschot, and D. van Norren, “Local photoreceptor alignment measured with a scanning laser ophthalmoscope,” Vision Res. 37(2), 243–248 (1997).
[Crossref] [PubMed]

1996 (4)

J. van de Kraats, T. T. Berendschot, and D. van Norren, “The pathways of light measured in fundus reflectometry,” Vision Res. 36(15), 2229–2247 (1996).
[Crossref] [PubMed]

D. T. Miller, D. R. Williams, G. M. Morris, and J. Liang, “Images of cone photoreceptors in the living human eye,” Vision Res. 36(8), 1067–1079 (1996).
[Crossref] [PubMed]

F. Møller, A. K. Sjølie, and T. Bek, “Quantitative assessment of fixational eye movements by scanning laser ophthalmoscopy,” Acta Ophthalmol. Scand. 74(6), 578–583 (1996).
[Crossref] [PubMed]

C. A. Curcio, N. E. Medeiros, and C. L. Millican, “Photoreceptor loss in age-related macular degeneration,” Invest. Ophthalmol. Vis. Sci. 37(7), 1236–1249 (1996).
[PubMed]

1995 (4)

D. C. Hood and D. G. Birch, “Phototransduction in human cones measured using the alpha-wave of the ERG,” Vision Res. 35(20), 2801–2810 (1995).
[Crossref] [PubMed]

H. Imai, Y. Imamoto, T. Yoshizawa, and Y. Shichida, “Difference in molecular properties between chicken green and rhodopsin as related to the functional difference between cone and rod photoreceptor cells,” Biochemistry 34(33), 10525–10531 (1995).
[Crossref] [PubMed]

D. M. Schneeweis and J. L. Schnapf, “Photovoltage of rods and cones in the macaque retina,” Science 268(5213), 1053–1056 (1995).
[Crossref] [PubMed]

S. A. Burns, S. Wu, F. Delori, and A. E. Elsner, “Direct measurement of human-cone-photoreceptor alignment,” J. Opt. Soc. Am. A 12(10), 2329–2338 (1995).
[Crossref] [PubMed]

1994 (1)

T. Yoshizawa, “Molecular basis for color vision,” Biophys. Chem. 50(1-2), 17–24 (1994).
[Crossref] [PubMed]

1993 (1)

1990 (2)

D. Y. Ts’o, R. D. Frostig, E. E. Lieke, and A. Grinvald, “Functional organization of primate visual cortex revealed by high resolution optical imaging,” Science 249(4967), 417–420 (1990).
[Crossref] [PubMed]

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

1989 (1)

J. S. Sunness, R. W. Massof, M. A. Johnson, N. M. Bressler, S. B. Bressler, and S. L. Fine, “Diminished foveal sensitivity may predict the development of advanced age-related macular degeneration,” Ophthalmology 96(3), 375–381 (1989).
[Crossref] [PubMed]

1987 (1)

I. Tasaki and P. M. Byrne, “Rapid mechanical changes in the amphibian retina evoked by brief light pulses,” Biochem. Biophys. Res. Commun. 143(1), 93–97 (1987).
[Crossref] [PubMed]

1984 (1)

I. Tasaki and T. Nakaye, “Rapid mechanical responses of the dark-adapted squid retina to light pulses,” Science 223(4634), 411–413 (1984).
[Crossref] [PubMed]

1981 (1)

H. Kühn, N. Bennett, M. Michel-Villaz, and M. Chabre, “Interactions between photoexcited rhodopsin and GTP-binding protein: kinetic and stoichiometric analyses from light-scattering changes,” Proc. Natl. Acad. Sci. U.S.A. 78(11), 6873–6877 (1981).
[Crossref] [PubMed]

1978 (1)

H. H. Harary, J. E. Brown, and L. H. Pinto, “Rapid light-induced changes in near infrared transmission of rods in Bufo marinus,” Science 202(4372), 1083–1085 (1978).
[Crossref] [PubMed]

1977 (2)

B. C. Hill, E. D. Schubert, M. A. Nokes, and R. P. Michelson, “Laser interferometer measurement of changes in crayfish axon diameter concurrent with action potential,” Science 196(4288), 426–428 (1977).
[Crossref] [PubMed]

A. L. Hodgkin and P. M. Obryan, “Internal recording of the early receptor potential in turtle cones,” J. Physiol. 267(3), 737–766 (1977).
[Crossref] [PubMed]

1975 (1)

H. Collewijn, F. van der Mark, and T. C. Jansen, “Precise recording of human eye movements,” Vision Res. 15(3), 447–450 (1975).
[Crossref] [PubMed]

1971 (1)

A. M. Laties and J. M. Enoch, “An analysis of retinal receptor orientation. I. Angular relationship of neighboring photoreceptors,” Invest. Ophthalmol. 10(1), 69–77 (1971).
[PubMed]

1967 (1)

G. Westheimer, “Dependence of the magnitude of the Stiles-Crawford effect on retinal location,” J. Physiol. 192(2), 309–315 (1967).
[Crossref] [PubMed]

1933 (1)

W. S. Stiles and B. H. Crawford, “The luminous efficiency of rays entering the eye pupil at different points,” Proc. R. Soc. London B. 112(778), 428–450 (1933).
[Crossref]

Aalders, M.

Abramoff, M.

D. Ts’o, J. Schallek, Y. Kwon, R. Kardon, M. Abramoff, and P. Soliz, “Noninvasive functional imaging of the retina reveals outer retinal and hemodynamic intrinsic optical signal origins,” Jpn. J. Ophthalmol. 53(4), 334–344 (2009).
[Crossref] [PubMed]

Ahnelt, P.

K. Bizheva, R. Pflug, B. Hermann, B. Povazay, H. Sattmann, P. Qiu, E. Anger, H. Reitsamer, S. Popov, J. R. Taylor, A. Unterhuber, P. Ahnelt, and W. Drexler, “Optophysiology: Depth-resolved probing of retinal physiology with functional ultrahigh-resolution optical coherence tomography,” Proc. Natl. Acad. Sci. U.S.A. 103(13), 5066–5071 (2006).
[Crossref] [PubMed]

K. Bizheva, R. Pflug, S. Gasparoni, B. Hermann, H. Sattmann, E. Anger, S. Popov, H. Reitsamer, P. Ahnelt, and W. Drexler, “Optophysiology - Spatially resolved optical probing of retinal physiology with functional ultrahigh resolution optical coherence tomography,” Invest. Ophthalmol. Vis. Sci. 46(13), 5066–5071 (2005).

Allen, C. P.

C. Friedburg, C. P. Allen, P. J. Mason, and T. D. Lamb, “Contribution of cone photoreceptors and post-receptoral mechanisms to the human photopic electroretinogram,” J. Physiol. 556(3), 819–834 (2004).
[Crossref] [PubMed]

Anger, E.

K. Bizheva, R. Pflug, B. Hermann, B. Povazay, H. Sattmann, P. Qiu, E. Anger, H. Reitsamer, S. Popov, J. R. Taylor, A. Unterhuber, P. Ahnelt, and W. Drexler, “Optophysiology: Depth-resolved probing of retinal physiology with functional ultrahigh-resolution optical coherence tomography,” Proc. Natl. Acad. Sci. U.S.A. 103(13), 5066–5071 (2006).
[Crossref] [PubMed]

K. Bizheva, R. Pflug, S. Gasparoni, B. Hermann, H. Sattmann, E. Anger, S. Popov, H. Reitsamer, P. Ahnelt, and W. Drexler, “Optophysiology - Spatially resolved optical probing of retinal physiology with functional ultrahigh resolution optical coherence tomography,” Invest. Ophthalmol. Vis. Sci. 46(13), 5066–5071 (2005).

Arathorn, D. W.

Arsanjani, R.

R. L. Brown, L. L. Lynch, T. L. Haley, and R. Arsanjani, “Pseudechetoxin binds to the pore turret of cyclic nucleotide-gated ion channels,” J. Gen. Physiol. 122(6), 749–760 (2003).
[Crossref] [PubMed]

Arshavsky, V. Y.

I. B. Leskov, V. A. Klenchin, J. W. Handy, G. G. Whitlock, V. I. Govardovskii, M. D. Bownds, T. D. Lamb, E. N. Pugh, and V. Y. Arshavsky, “The gain of rod phototransduction: reconciliation of biochemical and electrophysiological measurements,” Neuron 27(3), 525–537 (2000).
[Crossref] [PubMed]

Ashman, R.

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(2), 024008 (2008).
[Crossref] [PubMed]

Babu, K. R.

A. Kusnetzow, A. Dukkipati, K. R. Babu, D. Singh, B. W. Vought, B. E. Knox, and R. R. Birge, “The photobleaching sequence of a short-wavelength visual pigment,” Biochemistry 40(26), 7832–7844 (2001).
[Crossref] [PubMed]

Bedggood, P.

P. Bedggood and A. Metha, “Optical imaging of human cone photoreceptors directly following the capture of light,” PLoS ONE 8(11), e79251 (2013).
[Crossref] [PubMed]

P. Bedggood and A. Metha, “Variability in bleach kinetics and amount of photopigment between individual foveal cones,” Invest. Ophthalmol. Vis. Sci. 53(7), 3673–3681 (2012).
[Crossref] [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(2), 024008 (2008).
[Crossref] [PubMed]

Bek, T.

F. Møller, A. K. Sjølie, and T. Bek, “Quantitative assessment of fixational eye movements by scanning laser ophthalmoscopy,” Acta Ophthalmol. Scand. 74(6), 578–583 (1996).
[Crossref] [PubMed]

Bennett, N.

H. Kühn, N. Bennett, M. Michel-Villaz, and M. Chabre, “Interactions between photoexcited rhodopsin and GTP-binding protein: kinetic and stoichiometric analyses from light-scattering changes,” Proc. Natl. Acad. Sci. U.S.A. 78(11), 6873–6877 (1981).
[Crossref] [PubMed]

Berendschot, T. T.

N. P. Zagers, T. T. Berendschot, and D. van Norren, “Wavelength dependence of reflectometric cone photoreceptor directionality,” J. Opt. Soc. Am. A 20(1), 18–23 (2003).
[Crossref] [PubMed]

P. J. DeLint, T. T. Berendschot, J. van de Kraats, and D. van Norren, “Slow optical changes in human photoreceptors induced by light,” Invest. Ophthalmol. Vis. Sci. 41(1), 282–289 (2000).
[PubMed]

P. J. Delint, T. T. Berendschot, and D. van Norren, “Local photoreceptor alignment measured with a scanning laser ophthalmoscope,” Vision Res. 37(2), 243–248 (1997).
[Crossref] [PubMed]

J. van de Kraats, T. T. Berendschot, and D. van Norren, “The pathways of light measured in fundus reflectometry,” Vision Res. 36(15), 2229–2247 (1996).
[Crossref] [PubMed]

Binns, A. M.

A. R. Tumlinson, B. Hermann, B. Hofer, B. Povazay, T. H. Margrain, A. M. Binns, and W. Drexler, “Techniques for extraction of depth-resolved in vivo human retinal intrinsic optical signals with optical coherence tomography,” Jpn. J. Ophthalmol. 53(4), 315–326 (2009).
[Crossref] [PubMed]

Birch, D. G.

D. C. Hood and D. G. Birch, “Phototransduction in human cones measured using the alpha-wave of the ERG,” Vision Res. 35(20), 2801–2810 (1995).
[Crossref] [PubMed]

Birge, R. R.

A. Kusnetzow, A. Dukkipati, K. R. Babu, D. Singh, B. W. Vought, B. E. Knox, and R. R. Birge, “The photobleaching sequence of a short-wavelength visual pigment,” Biochemistry 40(26), 7832–7844 (2001).
[Crossref] [PubMed]

B. W. Vought, A. Dukkipatti, M. Max, B. E. Knox, and R. R. Birge, “Photochemistry of the primary event in short-wavelength visual opsins at low temperature,” Biochemistry 38(35), 11287–11297 (1999).
[Crossref] [PubMed]

Bizheva, K.

A. A. Moayed, S. Hariri, V. Choh, and K. Bizheva, “In vivo imaging of intrinsic optical signals in chicken retina with functional optical coherence tomography,” Opt. Lett. 36(23), 4575–4577 (2011).
[Crossref] [PubMed]

K. Bizheva, R. Pflug, B. Hermann, B. Povazay, H. Sattmann, P. Qiu, E. Anger, H. Reitsamer, S. Popov, J. R. Taylor, A. Unterhuber, P. Ahnelt, and W. Drexler, “Optophysiology: Depth-resolved probing of retinal physiology with functional ultrahigh-resolution optical coherence tomography,” Proc. Natl. Acad. Sci. U.S.A. 103(13), 5066–5071 (2006).
[Crossref] [PubMed]

K. Bizheva, R. Pflug, S. Gasparoni, B. Hermann, H. Sattmann, E. Anger, S. Popov, H. Reitsamer, P. Ahnelt, and W. Drexler, “Optophysiology - Spatially resolved optical probing of retinal physiology with functional ultrahigh resolution optical coherence tomography,” Invest. Ophthalmol. Vis. Sci. 46(13), 5066–5071 (2005).

Bouma, B.

Bower, B. A.

Bownds, M. D.

I. B. Leskov, V. A. Klenchin, J. W. Handy, G. G. Whitlock, V. I. Govardovskii, M. D. Bownds, T. D. Lamb, E. N. Pugh, and V. Y. Arshavsky, “The gain of rod phototransduction: reconciliation of biochemical and electrophysiological measurements,” Neuron 27(3), 525–537 (2000).
[Crossref] [PubMed]

Braaf, B.

Bressler, N. M.

J. S. Sunness, R. W. Massof, M. A. Johnson, N. M. Bressler, S. B. Bressler, and S. L. Fine, “Diminished foveal sensitivity may predict the development of advanced age-related macular degeneration,” Ophthalmology 96(3), 375–381 (1989).
[Crossref] [PubMed]

Bressler, S. B.

J. S. Sunness, R. W. Massof, M. A. Johnson, N. M. Bressler, S. B. Bressler, and S. L. Fine, “Diminished foveal sensitivity may predict the development of advanced age-related macular degeneration,” Ophthalmology 96(3), 375–381 (1989).
[Crossref] [PubMed]

Brown, J. E.

H. H. Harary, J. E. Brown, and L. H. Pinto, “Rapid light-induced changes in near infrared transmission of rods in Bufo marinus,” Science 202(4372), 1083–1085 (1978).
[Crossref] [PubMed]

Brown, R. L.

R. L. Brown, L. L. Lynch, T. L. Haley, and R. Arsanjani, “Pseudechetoxin binds to the pore turret of cyclic nucleotide-gated ion channels,” J. Gen. Physiol. 122(6), 749–760 (2003).
[Crossref] [PubMed]

Burns, S. A.

Byrne, P. M.

I. Tasaki and P. M. Byrne, “Rapid mechanical changes in the amphibian retina evoked by brief light pulses,” Biochem. Biophys. Res. Commun. 143(1), 93–97 (1987).
[Crossref] [PubMed]

Cable, A.

Cable, A. E.

Carroll, J.

Cense, B.

Chabre, M.

H. Kühn, N. Bennett, M. Michel-Villaz, and M. Chabre, “Interactions between photoexcited rhodopsin and GTP-binding protein: kinetic and stoichiometric analyses from light-scattering changes,” Proc. Natl. Acad. Sci. U.S.A. 78(11), 6873–6877 (1981).
[Crossref] [PubMed]

Charalambous, I.

A. Podoleanu, I. Charalambous, L. Plesea, A. Dogariu, and R. Rosen, “Correction of distortions in optical coherence tomography imaging of the eye,” Phys. Med. Biol. 49(7), 1277–1294 (2004).
[Crossref] [PubMed]

Chen, M.

S. Ricco, M. Chen, H. Ishikawa, G. Wollstein, and J. Schuman, “Correcting motion artifacts in retinal spectral domain optical coherence tomography via image registration,” Med. Image Comput. Assist. Interv. 12(Pt 1), 100–107 (2009).
[PubMed]

Chen, T.

Chen, Y.

Choh, V.

Choi, S.

Collewijn, H.

H. Collewijn, F. van der Mark, and T. C. Jansen, “Precise recording of human eye movements,” Vision Res. 15(3), 447–450 (1975).
[Crossref] [PubMed]

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 B. 112(778), 428–450 (1933).
[Crossref]

Curcio, C. A.

C. A. Curcio, N. E. Medeiros, and C. L. Millican, “Photoreceptor loss in age-related macular degeneration,” Invest. Ophthalmol. Vis. Sci. 37(7), 1236–1249 (1996).
[PubMed]

Daaboul, M.

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(2), 024008 (2008).
[Crossref] [PubMed]

de Boer, J.

de Boer, J. F.

de Kinkelder, R.

R. de Kinkelder, J. Kalkman, D. J. Faber, O. Schraa, P. H. Kok, F. D. Verbraak, and T. G. van Leeuwen, “Heartbeat-induced axial motion artifacts in optical coherence tomography measurements of the retina,” Invest. Ophthalmol. Vis. Sci. 52(6), 3908–3913 (2011).
[Crossref] [PubMed]

De la Garza, B. H.

Y. Y. Shih, B. H. De la Garza, E. R. Muir, W. E. Rogers, J. M. Harrison, J. W. Kiel, and T. Q. Duong, “Lamina-specific functional MRI of retinal and choroidal responses to visual stimuli,” Invest. Ophthalmol. Vis. Sci. 52(8), 5303–5310 (2011).
[Crossref] [PubMed]

DeLint, P. J.

P. J. DeLint, T. T. Berendschot, J. van de Kraats, and D. van Norren, “Slow optical changes in human photoreceptors induced by light,” Invest. Ophthalmol. Vis. Sci. 41(1), 282–289 (2000).
[PubMed]

P. J. Delint, T. T. Berendschot, and D. van Norren, “Local photoreceptor alignment measured with a scanning laser ophthalmoscope,” Vision Res. 37(2), 243–248 (1997).
[Crossref] [PubMed]

Delori, F.

S. A. Burns, S. Wu, F. Delori, and A. E. Elsner, “Direct measurement of human-cone-photoreceptor alignment,” J. Opt. Soc. Am. A 12(10), 2329–2338 (1995).
[Crossref] [PubMed]

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

Derby, J. C.

Dogariu, A.

A. Podoleanu, I. Charalambous, L. Plesea, A. Dogariu, and R. Rosen, “Correction of distortions in optical coherence tomography imaging of the eye,” Phys. Med. Biol. 49(7), 1277–1294 (2004).
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Drexler, W.

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Acta Ophthalmol. Scand. (1)

F. Møller, A. K. Sjølie, and T. Bek, “Quantitative assessment of fixational eye movements by scanning laser ophthalmoscopy,” Acta Ophthalmol. Scand. 74(6), 578–583 (1996).
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Appl. Opt. (1)

Biochem. Biophys. Res. Commun. (1)

I. Tasaki and P. M. Byrne, “Rapid mechanical changes in the amphibian retina evoked by brief light pulses,” Biochem. Biophys. Res. Commun. 143(1), 93–97 (1987).
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Biochemistry (4)

H. Imai, Y. Imamoto, T. Yoshizawa, and Y. Shichida, “Difference in molecular properties between chicken green and rhodopsin as related to the functional difference between cone and rod photoreceptor cells,” Biochemistry 34(33), 10525–10531 (1995).
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[Crossref] [PubMed]

B. W. Vought, A. Dukkipatti, M. Max, B. E. Knox, and R. R. Birge, “Photochemistry of the primary event in short-wavelength visual opsins at low temperature,” Biochemistry 38(35), 11287–11297 (1999).
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A. Kusnetzow, A. Dukkipati, K. R. Babu, D. Singh, B. W. Vought, B. E. Knox, and R. R. Birge, “The photobleaching sequence of a short-wavelength visual pigment,” Biochemistry 40(26), 7832–7844 (2001).
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Biomed. Opt. Express (8)

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R. S. Jonnal, O. P. Kocaoglu, Q. Wang, S. Lee, and D. T. Miller, “Phase-sensitive imaging of the outer retina using optical coherence tomography and adaptive optics,” Biomed. Opt. Express 3(1), 104–124 (2012).
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Figures (5)

Fig. 1
Fig. 1 (a) Simplified scheme of key processes involved in phototransduction (modified from Leskov et al., 2000) [32]. Upon absorption of visible photons by visual pigment, consisting of rhodopsin and an opsin chromophore (R) (step 1), rhodopsin undergoes conformational changes until Metarhodopsin II is formed (RMII). Consequently, the G-protein transducin (Gt) is bound from solution and is enzymatically activated by RMII by phosphorylation (step 2). Activated Gt (Gt*) then dissociates from RMII (step 3). Next, two molecules of Gt* bind and activate the enzyme phosphodiesterase (PDE*) (step 4). PDE* catalyzes the hydrolysis of cyclic guanosine monophosphate (cGMP), which is responsible for holding open cyclic nucleotide gated (CNG) channels to allow for the influx of Na+ and Ca2+. As a consequence of cGMP-hydrolysis after visual stimulation, CNG-channel bound cGMP dissociates, leading to channel closure and membrane hyperpolarization (step 5). Consequently, voltage-sensitive calcium channels close, leading to cessation of the photoreceptor’s dark current and inhibition of the release of the neurotransmitter glutamate. (b) The hypothesized involvement of PDE-activity in the generation of the fluctuation-type of fast IOS described earlier [7]. In the dark (left image), light rays impinging on the photoreceptor outer segment (black lines) reflect principally off the inner-outer segment junction (IS/OS-junction) and the OS outer tips (blue lines), with the optical path length between these structures Λ 1 = n 1 L 1 . Upon stimulation (right image), osmotic swelling may cause changes in the optical path length ( Λ 2 ) , as well as light scatter caused by localized PDE-activity ( Λ 3 ) . This PDE-activity has a higher probability of occurring in basal disks close to the IS/OS-junction as a consequence of self-screening (see text for details).
Fig. 2
Fig. 2 Fast IOS-pattern in frog retina observed with line-scanning en face OCT after the application of a circular stimulus. The IOS in this image have similar amplitudes across the image in a random arrangement. Adapted from [42] with permission.
Fig. 3
Fig. 3 Effect of sensitivity fall-off on time-resolved SD-OCT imaging. (a) Measured (blue dots) sensitivity fall-off versus distance from zero optical path length delay and a Gaussian-fit (line) by using Eq. (2). (b) Mean image (n = 900) of motion-tracked B-scans after axial flattening to the IS/OS-junction. Red box: region of interest (ROI) of the IS/OS-junction, used to plot intensity data in (c) and (d). (c) Mean intensity versus retinal depth. Data is plotted before correction of sensitivity fall-off (red) and fitted with a model of the intensity decay with depth, which was calculated from sensitivity measurements shown in (a). The corrected intensity (blue) was fitted with the expected linear curve (dotted line). (d) Comparison of original (red line) and corrected (blue line) mean intensity of the ROI over time, plotted together with retinal depth (grey line), showing reduced variation with retinal depth after fall-off compensation. However, substantial variability in reflectivity remains. See text for details.
Fig. 4
Fig. 4 Influence of variable illumination on OCT reflectivity. Epiretinal specular reflections are prominent in mean intensity projections of scans at t0 – 2s (a), but less so at t6-8s (b), together with increased reflectivity in deeper layers. (c) The fractional reflectivity changes of a layer of interest, such as the OS (blue dots) and a reference layer, the OS/RPE-complex (red dots) do not show a highly linear correspondence. The axial positions of these layers (inset in the top right of (c)) were identical for each B-scan. We tested if normalization to the OS/RPE complex band is sufficient to suppress noise caused by variable illumination, as proposed previously [16]. The median value of the linear amplitude reflectance of these bands was determined for each A-scan (excluding vessel shadows). A random set of these values was averaged per B-scan, and the fractional reflectance relative to the first B-scan was determined. (d) The linear amplitude reflectance of the OS-band (blue dots) still shows the change in reflectance after normalization (green dots), although a partial compensation effect is evident
Fig. 5
Fig. 5 Compensation for variation in background illumination in timelapse OCT-recordings. (a) Mean image of axially flattened B-scans (n = 400). 125 A-scans per choriocapillary bed, indicated in yellow, were averaged and used to estimate the illumination parameters (see text). Vessel shadows were blotted out (b) Example curve fit of reflectivity with depth using Eq. (3). Shown in blue is the intensity with depth after noise suppression by A-scan averaging. The fitted curve is shown in green. (c) Effect of compensation. The mean intensity of a region-of-interest, comprising the IS/OS-junction, OS/RPE and RPE bands of the same A-scans used for averaging in (a), was used as an indication of general reflectivity changes over time (light blue: left side, orange: right side). After normalization using Eq. (4) of the same regions of interest on the left side (blue) and the right side (red), the large-scale intensity variations caused by misalignments of the optical axes of OCT and the eye have been reduced. (d) Direct comparison of normalization for reflectivity in the RPE/OS layer (blue line) and of normalization by the proposed technique (red line).

Equations (4)

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Δ I x,z,t / I ¯ x,z,baseline = I x,z,t I ¯ x,z,baseline I ¯ x,z,baseline .
S(z)=exp( z 2 / σ 2 ),
I(z)= A 0 exp(2μz)+ A 1 ,
I (normalized) x,z,t =( I x,z,t A 1,t A 0,t A ¯ 1 )+ A ¯ 0 ,

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