Abstract

Transient retinal phototropism (TRP) has been predominantly observed in rod photoreceptors activated by oblique visible light stimulation. Dynamic confocal microscopy and optical coherence tomography (OCT) have revealed rod outer segment (ROS) movement as the physical source of TRP. However, the physiological source of ROS movement is still not well understood. In this study, concurrent near-infrared imaging of TRP and electroretinogram (ERG) measurement of retinal electrophysiology revealed that ROS movement occurs before the onset of the ERG a-wave, which is known to reflect the hyperpolarization of retinal photoreceptors. Moreover, substitution of normal superfusing medium with low-sodium medium reversibly blocked the photoreceptor ERG a-wave, but largely preserved the stimulus-evoked ROS movements. Our experimental results and theoretical analysis indicate that early, disc-based stages of the phototransduction cascade, which occur before the hyperpolarization of retinal photoreceptors, contribute to the TRP associated ROS movement.

© 2016 Optical Society of America

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References

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2016 (1)

X. Zhao, D. Thapa, B. Wang, Y. Lu, S. Gai, and X. Yao, “Stimulus-evoked outer segment changes in rod photoreceptors,” J. Biomed. Opt. 21(6), 065006 (2016).
[Crossref] [PubMed]

2015 (4)

Q. Zhang, R. Lu, B. Wang, J. D. Messinger, C. A. Curcio, and X. Yao, “Functional optical coherence tomography enables in vivo physiological assessment of retinal rod and cone photoreceptors,” Sci. Rep. 5, 9595 (2015).
[Crossref] [PubMed]

X. Yao and B. Wang, “Intrinsic optical signal imaging of retinal physiology: a review,” J. Biomed. Opt. 20(9), 090901 (2015).
[Crossref] [PubMed]

Y. Zhi, B. Wang, and X. Yao, “Super-Resolution Scanning Laser Microscopy Based on Virtually Structured Detection,” Crit. Rev. Biomed. Eng. 43(4), 297–322 (2015).
[Crossref] [PubMed]

Y. Zhi, R. Lu, B. Wang, Q. Zhang, and X. Yao, “Rapid super-resolution line-scanning microscopy through virtually structured detection,” Opt. Lett. 40(8), 1683–1686 (2015).
[Crossref] [PubMed]

2014 (1)

2013 (3)

R. Lu, A. M. Levy, Q. Zhang, S. J. Pittler, and X. Yao, “Dynamic near-infrared imaging reveals transient phototropic change in retinal rod photoreceptors,” J. Biomed. Opt. 18(10), 106013 (2013).
[Crossref] [PubMed]

B. Wang, R. Lu, Q. Zhang, and X. Yao, “Breaking diffraction limit of lateral resolution in optical coherence tomography,” Quant. Imaging Med. Surg. 3(5), 243–248 (2013).
[PubMed]

N. Yagi, “Structural changes in rod outer segments of frog and mouse after illumination,” Exp. Eye Res. 116, 395–401 (2013).
[Crossref] [PubMed]

2012 (1)

Q. X. Zhang, R. W. Lu, C. A. Curcio, and X. C. Yao, “In vivo confocal intrinsic optical signal identification of localized retinal dysfunction,” Invest. Ophthalmol. Vis. Sci. 53(13), 8139–8145 (2012).
[Crossref] [PubMed]

2011 (1)

2010 (2)

2008 (1)

2006 (1)

T. D. Lamb and E. N. Pugh., “Phototransduction, dark adaptation, and rhodopsin regeneration the proctor lecture,” Invest. Ophthalmol. Vis. Sci. 47(12), 5137–5152 (2006).
[PubMed]

2001 (1)

M. E. Burns and D. A. Baylor, “Activation, deactivation, and adaptation in vertebrate photoreceptor cells,” Annu. Rev. Neurosci. 24(1), 779–805 (2001).
[Crossref] [PubMed]

2000 (3)

D. C. Mitchell and B. J. Litman, “Effect of ethanol and osmotic stress on receptor conformation. Reduced water activity amplifies the effect of ethanol on metarhodopsin II formation,” J. Biol. Chem. 275(8), 5355–5360 (2000).
[Crossref] [PubMed]

H. P. Scholl and E. Zrenner, “Electrophysiology in the investigation of acquired retinal disorders,” Surv. Ophthalmol. 45(1), 29–47 (2000).
[Crossref] [PubMed]

E. Hessel, A. Herrmann, P. Müller, P. P. Schnetkamp, and K. P. Hofmann, “The transbilayer distribution of phospholipids in disc membranes is a dynamic equilibrium evidence for rapid flip and flop movement,” Eur. J. Biochem. 267(5), 1473–1483 (2000).
[Crossref] [PubMed]

1990 (1)

M. Kahlert, D. R. Pepperberg, and K. P. Hofmann, “Effect of bleached rhodopsin on signal amplification in rod visual receptors,” Nature 345(6275), 537–539 (1990).
[Crossref] [PubMed]

1988 (1)

D. R. Pepperberg, M. Kahlert, A. Krause, and K. P. Hofmann, “Photic modulation of a highly sensitive, near-infrared light-scattering signal recorded from intact retinal photoreceptors,” Proc. Natl. Acad. Sci. U.S.A. 85(15), 5531–5535 (1988).
[Crossref] [PubMed]

1987 (1)

T. M. Vuong, C. Pfister, D. L. Worcester, and M. Chabre, “The transducin cascade is involved in the light-induced structural changes observed by neutron diffraction on retinal rod outer segments,” Biophys. J. 52(4), 587–594 (1987).
[Crossref] [PubMed]

1981 (2)

K. P. Hofmann, A. Schleicher, D. Emeis, and J. Reichert, “Light-induced axial and radial shrinkage effects and changes of the refractive index in isolated bovine rod outer segments and disc vesicles: physical analysis of near-infrared scattering changes,” Biophys. Struct. Mech. 8(1-2), 67–93 (1981).
[Crossref] [PubMed]

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]

1976 (1)

K. P. Hofmann, R. Uhl, W. Hoffmann, and W. Kreutz, “Measurements on fast light-induced light-scattering and -absorption changes in outer segments of vertebrate light sensitive rod cells,” Biophys. Struct. Mech. 2(1), 61–77 (1976).
[Crossref] [PubMed]

1975 (2)

H. Asai, T. Chiba, S. Kimura, and M. Takagi, “A light-induced conformational change in rod photoreceptor disc membrane,” Exp. Eye Res. 21(3), 259–267 (1975).
[Crossref] [PubMed]

N. Otsu, “A threshold selection method from gray-level histograms,” Automatica 11, 23–27 (1975).

1974 (1)

J. E. Brown and L. H. Pinto, “Ionic mechanism for the photoreceptor potential of the retina of Bufo marinus,” J. Physiol. 236(3), 575–591 (1974).
[Crossref] [PubMed]

1971 (1)

J. Heller, T. J. Ostwald, and D. Bok, “The osmotic behavior of rod photoreceptor outer segment discs,” J. Cell Biol. 48(3), 633–649 (1971).
[Crossref] [PubMed]

1970 (1)

J. Heller, T. J. Ostwald, and D. Bok, “Effect of illumination on the membrane permeability of rod photoreceptor discs,” Biochemistry 9(25), 4884–4889 (1970).
[Crossref] [PubMed]

1933 (1)

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

Amthor, F.

Asai, H.

H. Asai, T. Chiba, S. Kimura, and M. Takagi, “A light-induced conformational change in rod photoreceptor disc membrane,” Exp. Eye Res. 21(3), 259–267 (1975).
[Crossref] [PubMed]

Baylor, D. A.

M. E. Burns and D. A. Baylor, “Activation, deactivation, and adaptation in vertebrate photoreceptor cells,” Annu. Rev. Neurosci. 24(1), 779–805 (2001).
[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]

Bok, D.

J. Heller, T. J. Ostwald, and D. Bok, “The osmotic behavior of rod photoreceptor outer segment discs,” J. Cell Biol. 48(3), 633–649 (1971).
[Crossref] [PubMed]

J. Heller, T. J. Ostwald, and D. Bok, “Effect of illumination on the membrane permeability of rod photoreceptor discs,” Biochemistry 9(25), 4884–4889 (1970).
[Crossref] [PubMed]

Brown, J. E.

J. E. Brown and L. H. Pinto, “Ionic mechanism for the photoreceptor potential of the retina of Bufo marinus,” J. Physiol. 236(3), 575–591 (1974).
[Crossref] [PubMed]

Burns, M. E.

M. E. Burns and D. A. Baylor, “Activation, deactivation, and adaptation in vertebrate photoreceptor cells,” Annu. Rev. Neurosci. 24(1), 779–805 (2001).
[Crossref] [PubMed]

Chabre, M.

T. M. Vuong, C. Pfister, D. L. Worcester, and M. Chabre, “The transducin cascade is involved in the light-induced structural changes observed by neutron diffraction on retinal rod outer segments,” Biophys. J. 52(4), 587–594 (1987).
[Crossref] [PubMed]

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]

Chiba, T.

H. Asai, T. Chiba, S. Kimura, and M. Takagi, “A light-induced conformational change in rod photoreceptor disc membrane,” Exp. Eye Res. 21(3), 259–267 (1975).
[Crossref] [PubMed]

Crawford, B.

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

Curcio, C. A.

Q. Zhang, R. Lu, B. Wang, J. D. Messinger, C. A. Curcio, and X. Yao, “Functional optical coherence tomography enables in vivo physiological assessment of retinal rod and cone photoreceptors,” Sci. Rep. 5, 9595 (2015).
[Crossref] [PubMed]

Q. X. Zhang, R. W. Lu, C. A. Curcio, and X. C. Yao, “In vivo confocal intrinsic optical signal identification of localized retinal dysfunction,” Invest. Ophthalmol. Vis. Sci. 53(13), 8139–8145 (2012).
[Crossref] [PubMed]

Emeis, D.

K. P. Hofmann, A. Schleicher, D. Emeis, and J. Reichert, “Light-induced axial and radial shrinkage effects and changes of the refractive index in isolated bovine rod outer segments and disc vesicles: physical analysis of near-infrared scattering changes,” Biophys. Struct. Mech. 8(1-2), 67–93 (1981).
[Crossref] [PubMed]

Gai, S.

X. Zhao, D. Thapa, B. Wang, Y. Lu, S. Gai, and X. Yao, “Stimulus-evoked outer segment changes in rod photoreceptors,” J. Biomed. Opt. 21(6), 065006 (2016).
[Crossref] [PubMed]

Heller, J.

J. Heller, T. J. Ostwald, and D. Bok, “The osmotic behavior of rod photoreceptor outer segment discs,” J. Cell Biol. 48(3), 633–649 (1971).
[Crossref] [PubMed]

J. Heller, T. J. Ostwald, and D. Bok, “Effect of illumination on the membrane permeability of rod photoreceptor discs,” Biochemistry 9(25), 4884–4889 (1970).
[Crossref] [PubMed]

Herrmann, A.

E. Hessel, A. Herrmann, P. Müller, P. P. Schnetkamp, and K. P. Hofmann, “The transbilayer distribution of phospholipids in disc membranes is a dynamic equilibrium evidence for rapid flip and flop movement,” Eur. J. Biochem. 267(5), 1473–1483 (2000).
[Crossref] [PubMed]

Hessel, E.

E. Hessel, A. Herrmann, P. Müller, P. P. Schnetkamp, and K. P. Hofmann, “The transbilayer distribution of phospholipids in disc membranes is a dynamic equilibrium evidence for rapid flip and flop movement,” Eur. J. Biochem. 267(5), 1473–1483 (2000).
[Crossref] [PubMed]

Hoffmann, W.

K. P. Hofmann, R. Uhl, W. Hoffmann, and W. Kreutz, “Measurements on fast light-induced light-scattering and -absorption changes in outer segments of vertebrate light sensitive rod cells,” Biophys. Struct. Mech. 2(1), 61–77 (1976).
[Crossref] [PubMed]

Hofmann, K. P.

E. Hessel, A. Herrmann, P. Müller, P. P. Schnetkamp, and K. P. Hofmann, “The transbilayer distribution of phospholipids in disc membranes is a dynamic equilibrium evidence for rapid flip and flop movement,” Eur. J. Biochem. 267(5), 1473–1483 (2000).
[Crossref] [PubMed]

M. Kahlert, D. R. Pepperberg, and K. P. Hofmann, “Effect of bleached rhodopsin on signal amplification in rod visual receptors,” Nature 345(6275), 537–539 (1990).
[Crossref] [PubMed]

D. R. Pepperberg, M. Kahlert, A. Krause, and K. P. Hofmann, “Photic modulation of a highly sensitive, near-infrared light-scattering signal recorded from intact retinal photoreceptors,” Proc. Natl. Acad. Sci. U.S.A. 85(15), 5531–5535 (1988).
[Crossref] [PubMed]

K. P. Hofmann, A. Schleicher, D. Emeis, and J. Reichert, “Light-induced axial and radial shrinkage effects and changes of the refractive index in isolated bovine rod outer segments and disc vesicles: physical analysis of near-infrared scattering changes,” Biophys. Struct. Mech. 8(1-2), 67–93 (1981).
[Crossref] [PubMed]

K. P. Hofmann, R. Uhl, W. Hoffmann, and W. Kreutz, “Measurements on fast light-induced light-scattering and -absorption changes in outer segments of vertebrate light sensitive rod cells,” Biophys. Struct. Mech. 2(1), 61–77 (1976).
[Crossref] [PubMed]

Kahlert, M.

M. Kahlert, D. R. Pepperberg, and K. P. Hofmann, “Effect of bleached rhodopsin on signal amplification in rod visual receptors,” Nature 345(6275), 537–539 (1990).
[Crossref] [PubMed]

D. R. Pepperberg, M. Kahlert, A. Krause, and K. P. Hofmann, “Photic modulation of a highly sensitive, near-infrared light-scattering signal recorded from intact retinal photoreceptors,” Proc. Natl. Acad. Sci. U.S.A. 85(15), 5531–5535 (1988).
[Crossref] [PubMed]

Kimura, S.

H. Asai, T. Chiba, S. Kimura, and M. Takagi, “A light-induced conformational change in rod photoreceptor disc membrane,” Exp. Eye Res. 21(3), 259–267 (1975).
[Crossref] [PubMed]

Krause, A.

D. R. Pepperberg, M. Kahlert, A. Krause, and K. P. Hofmann, “Photic modulation of a highly sensitive, near-infrared light-scattering signal recorded from intact retinal photoreceptors,” Proc. Natl. Acad. Sci. U.S.A. 85(15), 5531–5535 (1988).
[Crossref] [PubMed]

Kreutz, W.

K. P. Hofmann, R. Uhl, W. Hoffmann, and W. Kreutz, “Measurements on fast light-induced light-scattering and -absorption changes in outer segments of vertebrate light sensitive rod cells,” Biophys. Struct. Mech. 2(1), 61–77 (1976).
[Crossref] [PubMed]

Kühn, H.

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]

Lamb, T. D.

T. D. Lamb and E. N. Pugh., “Phototransduction, dark adaptation, and rhodopsin regeneration the proctor lecture,” Invest. Ophthalmol. Vis. Sci. 47(12), 5137–5152 (2006).
[PubMed]

Levy, A. M.

R. Lu, A. M. Levy, Q. Zhang, S. J. Pittler, and X. Yao, “Dynamic near-infrared imaging reveals transient phototropic change in retinal rod photoreceptors,” J. Biomed. Opt. 18(10), 106013 (2013).
[Crossref] [PubMed]

Li, Y. G.

Litman, B. J.

D. C. Mitchell and B. J. Litman, “Effect of ethanol and osmotic stress on receptor conformation. Reduced water activity amplifies the effect of ethanol on metarhodopsin II formation,” J. Biol. Chem. 275(8), 5355–5360 (2000).
[Crossref] [PubMed]

Liu, L.

Lu, R.

Y. Zhi, R. Lu, B. Wang, Q. Zhang, and X. Yao, “Rapid super-resolution line-scanning microscopy through virtually structured detection,” Opt. Lett. 40(8), 1683–1686 (2015).
[Crossref] [PubMed]

Q. Zhang, R. Lu, B. Wang, J. D. Messinger, C. A. Curcio, and X. Yao, “Functional optical coherence tomography enables in vivo physiological assessment of retinal rod and cone photoreceptors,” Sci. Rep. 5, 9595 (2015).
[Crossref] [PubMed]

B. Wang, Q. Zhang, R. Lu, Y. Zhi, and X. Yao, “Functional optical coherence tomography reveals transient phototropic change of photoreceptor outer segments,” Opt. Lett. 39(24), 6923–6926 (2014).
[Crossref] [PubMed]

B. Wang, R. Lu, Q. Zhang, and X. Yao, “Breaking diffraction limit of lateral resolution in optical coherence tomography,” Quant. Imaging Med. Surg. 3(5), 243–248 (2013).
[PubMed]

R. Lu, A. M. Levy, Q. Zhang, S. J. Pittler, and X. Yao, “Dynamic near-infrared imaging reveals transient phototropic change in retinal rod photoreceptors,” J. Biomed. Opt. 18(10), 106013 (2013).
[Crossref] [PubMed]

Lu, R. W.

Q. X. Zhang, R. W. Lu, C. A. Curcio, and X. C. Yao, “In vivo confocal intrinsic optical signal identification of localized retinal dysfunction,” Invest. Ophthalmol. Vis. Sci. 53(13), 8139–8145 (2012).
[Crossref] [PubMed]

Q. X. Zhang, R. W. Lu, Y. G. Li, and X. C. Yao, “In vivo confocal imaging of fast intrinsic optical signals correlated with frog retinal activation,” Opt. Lett. 36(23), 4692–4694 (2011).
[Crossref] [PubMed]

Lu, Y.

X. Zhao, D. Thapa, B. Wang, Y. Lu, S. Gai, and X. Yao, “Stimulus-evoked outer segment changes in rod photoreceptors,” J. Biomed. Opt. 21(6), 065006 (2016).
[Crossref] [PubMed]

Messinger, J. D.

Q. Zhang, R. Lu, B. Wang, J. D. Messinger, C. A. Curcio, and X. Yao, “Functional optical coherence tomography enables in vivo physiological assessment of retinal rod and cone photoreceptors,” Sci. Rep. 5, 9595 (2015).
[Crossref] [PubMed]

Michel-Villaz, 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]

Mitchell, D. C.

D. C. Mitchell and B. J. Litman, “Effect of ethanol and osmotic stress on receptor conformation. Reduced water activity amplifies the effect of ethanol on metarhodopsin II formation,” J. Biol. Chem. 275(8), 5355–5360 (2000).
[Crossref] [PubMed]

Müller, P.

E. Hessel, A. Herrmann, P. Müller, P. P. Schnetkamp, and K. P. Hofmann, “The transbilayer distribution of phospholipids in disc membranes is a dynamic equilibrium evidence for rapid flip and flop movement,” Eur. J. Biochem. 267(5), 1473–1483 (2000).
[Crossref] [PubMed]

Ostwald, T. J.

J. Heller, T. J. Ostwald, and D. Bok, “The osmotic behavior of rod photoreceptor outer segment discs,” J. Cell Biol. 48(3), 633–649 (1971).
[Crossref] [PubMed]

J. Heller, T. J. Ostwald, and D. Bok, “Effect of illumination on the membrane permeability of rod photoreceptor discs,” Biochemistry 9(25), 4884–4889 (1970).
[Crossref] [PubMed]

Otsu, N.

N. Otsu, “A threshold selection method from gray-level histograms,” Automatica 11, 23–27 (1975).

Pepperberg, D. R.

M. Kahlert, D. R. Pepperberg, and K. P. Hofmann, “Effect of bleached rhodopsin on signal amplification in rod visual receptors,” Nature 345(6275), 537–539 (1990).
[Crossref] [PubMed]

D. R. Pepperberg, M. Kahlert, A. Krause, and K. P. Hofmann, “Photic modulation of a highly sensitive, near-infrared light-scattering signal recorded from intact retinal photoreceptors,” Proc. Natl. Acad. Sci. U.S.A. 85(15), 5531–5535 (1988).
[Crossref] [PubMed]

Pfister, C.

T. M. Vuong, C. Pfister, D. L. Worcester, and M. Chabre, “The transducin cascade is involved in the light-induced structural changes observed by neutron diffraction on retinal rod outer segments,” Biophys. J. 52(4), 587–594 (1987).
[Crossref] [PubMed]

Pinto, L. H.

J. E. Brown and L. H. Pinto, “Ionic mechanism for the photoreceptor potential of the retina of Bufo marinus,” J. Physiol. 236(3), 575–591 (1974).
[Crossref] [PubMed]

Pittler, S. J.

R. Lu, A. M. Levy, Q. Zhang, S. J. Pittler, and X. Yao, “Dynamic near-infrared imaging reveals transient phototropic change in retinal rod photoreceptors,” J. Biomed. Opt. 18(10), 106013 (2013).
[Crossref] [PubMed]

Pugh, E. N.

T. D. Lamb and E. N. Pugh., “Phototransduction, dark adaptation, and rhodopsin regeneration the proctor lecture,” Invest. Ophthalmol. Vis. Sci. 47(12), 5137–5152 (2006).
[PubMed]

Reichert, J.

K. P. Hofmann, A. Schleicher, D. Emeis, and J. Reichert, “Light-induced axial and radial shrinkage effects and changes of the refractive index in isolated bovine rod outer segments and disc vesicles: physical analysis of near-infrared scattering changes,” Biophys. Struct. Mech. 8(1-2), 67–93 (1981).
[Crossref] [PubMed]

Schleicher, A.

K. P. Hofmann, A. Schleicher, D. Emeis, and J. Reichert, “Light-induced axial and radial shrinkage effects and changes of the refractive index in isolated bovine rod outer segments and disc vesicles: physical analysis of near-infrared scattering changes,” Biophys. Struct. Mech. 8(1-2), 67–93 (1981).
[Crossref] [PubMed]

Schnetkamp, P. P.

E. Hessel, A. Herrmann, P. Müller, P. P. Schnetkamp, and K. P. Hofmann, “The transbilayer distribution of phospholipids in disc membranes is a dynamic equilibrium evidence for rapid flip and flop movement,” Eur. J. Biochem. 267(5), 1473–1483 (2000).
[Crossref] [PubMed]

Scholl, H. P.

H. P. Scholl and E. Zrenner, “Electrophysiology in the investigation of acquired retinal disorders,” Surv. Ophthalmol. 45(1), 29–47 (2000).
[Crossref] [PubMed]

Stiles, W.

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

Takagi, M.

H. Asai, T. Chiba, S. Kimura, and M. Takagi, “A light-induced conformational change in rod photoreceptor disc membrane,” Exp. Eye Res. 21(3), 259–267 (1975).
[Crossref] [PubMed]

Thapa, D.

X. Zhao, D. Thapa, B. Wang, Y. Lu, S. Gai, and X. Yao, “Stimulus-evoked outer segment changes in rod photoreceptors,” J. Biomed. Opt. 21(6), 065006 (2016).
[Crossref] [PubMed]

Uhl, R.

K. P. Hofmann, R. Uhl, W. Hoffmann, and W. Kreutz, “Measurements on fast light-induced light-scattering and -absorption changes in outer segments of vertebrate light sensitive rod cells,” Biophys. Struct. Mech. 2(1), 61–77 (1976).
[Crossref] [PubMed]

Vuong, T. M.

T. M. Vuong, C. Pfister, D. L. Worcester, and M. Chabre, “The transducin cascade is involved in the light-induced structural changes observed by neutron diffraction on retinal rod outer segments,” Biophys. J. 52(4), 587–594 (1987).
[Crossref] [PubMed]

Wang, B.

X. Zhao, D. Thapa, B. Wang, Y. Lu, S. Gai, and X. Yao, “Stimulus-evoked outer segment changes in rod photoreceptors,” J. Biomed. Opt. 21(6), 065006 (2016).
[Crossref] [PubMed]

X. Yao and B. Wang, “Intrinsic optical signal imaging of retinal physiology: a review,” J. Biomed. Opt. 20(9), 090901 (2015).
[Crossref] [PubMed]

Q. Zhang, R. Lu, B. Wang, J. D. Messinger, C. A. Curcio, and X. Yao, “Functional optical coherence tomography enables in vivo physiological assessment of retinal rod and cone photoreceptors,” Sci. Rep. 5, 9595 (2015).
[Crossref] [PubMed]

Y. Zhi, R. Lu, B. Wang, Q. Zhang, and X. Yao, “Rapid super-resolution line-scanning microscopy through virtually structured detection,” Opt. Lett. 40(8), 1683–1686 (2015).
[Crossref] [PubMed]

Y. Zhi, B. Wang, and X. Yao, “Super-Resolution Scanning Laser Microscopy Based on Virtually Structured Detection,” Crit. Rev. Biomed. Eng. 43(4), 297–322 (2015).
[Crossref] [PubMed]

B. Wang, Q. Zhang, R. Lu, Y. Zhi, and X. Yao, “Functional optical coherence tomography reveals transient phototropic change of photoreceptor outer segments,” Opt. Lett. 39(24), 6923–6926 (2014).
[Crossref] [PubMed]

B. Wang, R. Lu, Q. Zhang, and X. Yao, “Breaking diffraction limit of lateral resolution in optical coherence tomography,” Quant. Imaging Med. Surg. 3(5), 243–248 (2013).
[PubMed]

Wang, J. Y.

Worcester, D. L.

T. M. Vuong, C. Pfister, D. L. Worcester, and M. Chabre, “The transducin cascade is involved in the light-induced structural changes observed by neutron diffraction on retinal rod outer segments,” Biophys. J. 52(4), 587–594 (1987).
[Crossref] [PubMed]

Yagi, N.

N. Yagi, “Structural changes in rod outer segments of frog and mouse after illumination,” Exp. Eye Res. 116, 395–401 (2013).
[Crossref] [PubMed]

Yao, X.

X. Zhao, D. Thapa, B. Wang, Y. Lu, S. Gai, and X. Yao, “Stimulus-evoked outer segment changes in rod photoreceptors,” J. Biomed. Opt. 21(6), 065006 (2016).
[Crossref] [PubMed]

Q. Zhang, R. Lu, B. Wang, J. D. Messinger, C. A. Curcio, and X. Yao, “Functional optical coherence tomography enables in vivo physiological assessment of retinal rod and cone photoreceptors,” Sci. Rep. 5, 9595 (2015).
[Crossref] [PubMed]

X. Yao and B. Wang, “Intrinsic optical signal imaging of retinal physiology: a review,” J. Biomed. Opt. 20(9), 090901 (2015).
[Crossref] [PubMed]

Y. Zhi, B. Wang, and X. Yao, “Super-Resolution Scanning Laser Microscopy Based on Virtually Structured Detection,” Crit. Rev. Biomed. Eng. 43(4), 297–322 (2015).
[Crossref] [PubMed]

Y. Zhi, R. Lu, B. Wang, Q. Zhang, and X. Yao, “Rapid super-resolution line-scanning microscopy through virtually structured detection,” Opt. Lett. 40(8), 1683–1686 (2015).
[Crossref] [PubMed]

B. Wang, Q. Zhang, R. Lu, Y. Zhi, and X. Yao, “Functional optical coherence tomography reveals transient phototropic change of photoreceptor outer segments,” Opt. Lett. 39(24), 6923–6926 (2014).
[Crossref] [PubMed]

B. Wang, R. Lu, Q. Zhang, and X. Yao, “Breaking diffraction limit of lateral resolution in optical coherence tomography,” Quant. Imaging Med. Surg. 3(5), 243–248 (2013).
[PubMed]

R. Lu, A. M. Levy, Q. Zhang, S. J. Pittler, and X. Yao, “Dynamic near-infrared imaging reveals transient phototropic change in retinal rod photoreceptors,” J. Biomed. Opt. 18(10), 106013 (2013).
[Crossref] [PubMed]

Yao, X. C.

Zhang, Q.

Y. Zhi, R. Lu, B. Wang, Q. Zhang, and X. Yao, “Rapid super-resolution line-scanning microscopy through virtually structured detection,” Opt. Lett. 40(8), 1683–1686 (2015).
[Crossref] [PubMed]

Q. Zhang, R. Lu, B. Wang, J. D. Messinger, C. A. Curcio, and X. Yao, “Functional optical coherence tomography enables in vivo physiological assessment of retinal rod and cone photoreceptors,” Sci. Rep. 5, 9595 (2015).
[Crossref] [PubMed]

B. Wang, Q. Zhang, R. Lu, Y. Zhi, and X. Yao, “Functional optical coherence tomography reveals transient phototropic change of photoreceptor outer segments,” Opt. Lett. 39(24), 6923–6926 (2014).
[Crossref] [PubMed]

B. Wang, R. Lu, Q. Zhang, and X. Yao, “Breaking diffraction limit of lateral resolution in optical coherence tomography,” Quant. Imaging Med. Surg. 3(5), 243–248 (2013).
[PubMed]

R. Lu, A. M. Levy, Q. Zhang, S. J. Pittler, and X. Yao, “Dynamic near-infrared imaging reveals transient phototropic change in retinal rod photoreceptors,” J. Biomed. Opt. 18(10), 106013 (2013).
[Crossref] [PubMed]

Zhang, Q. X.

Zhao, X.

X. Zhao, D. Thapa, B. Wang, Y. Lu, S. Gai, and X. Yao, “Stimulus-evoked outer segment changes in rod photoreceptors,” J. Biomed. Opt. 21(6), 065006 (2016).
[Crossref] [PubMed]

Zhao, Y. B.

Zhi, Y.

Zrenner, E.

H. P. Scholl and E. Zrenner, “Electrophysiology in the investigation of acquired retinal disorders,” Surv. Ophthalmol. 45(1), 29–47 (2000).
[Crossref] [PubMed]

Annu. Rev. Neurosci. (1)

M. E. Burns and D. A. Baylor, “Activation, deactivation, and adaptation in vertebrate photoreceptor cells,” Annu. Rev. Neurosci. 24(1), 779–805 (2001).
[Crossref] [PubMed]

Automatica (1)

N. Otsu, “A threshold selection method from gray-level histograms,” Automatica 11, 23–27 (1975).

Biochemistry (1)

J. Heller, T. J. Ostwald, and D. Bok, “Effect of illumination on the membrane permeability of rod photoreceptor discs,” Biochemistry 9(25), 4884–4889 (1970).
[Crossref] [PubMed]

Biophys. J. (1)

T. M. Vuong, C. Pfister, D. L. Worcester, and M. Chabre, “The transducin cascade is involved in the light-induced structural changes observed by neutron diffraction on retinal rod outer segments,” Biophys. J. 52(4), 587–594 (1987).
[Crossref] [PubMed]

Biophys. Struct. Mech. (2)

K. P. Hofmann, R. Uhl, W. Hoffmann, and W. Kreutz, “Measurements on fast light-induced light-scattering and -absorption changes in outer segments of vertebrate light sensitive rod cells,” Biophys. Struct. Mech. 2(1), 61–77 (1976).
[Crossref] [PubMed]

K. P. Hofmann, A. Schleicher, D. Emeis, and J. Reichert, “Light-induced axial and radial shrinkage effects and changes of the refractive index in isolated bovine rod outer segments and disc vesicles: physical analysis of near-infrared scattering changes,” Biophys. Struct. Mech. 8(1-2), 67–93 (1981).
[Crossref] [PubMed]

Crit. Rev. Biomed. Eng. (1)

Y. Zhi, B. Wang, and X. Yao, “Super-Resolution Scanning Laser Microscopy Based on Virtually Structured Detection,” Crit. Rev. Biomed. Eng. 43(4), 297–322 (2015).
[Crossref] [PubMed]

Eur. J. Biochem. (1)

E. Hessel, A. Herrmann, P. Müller, P. P. Schnetkamp, and K. P. Hofmann, “The transbilayer distribution of phospholipids in disc membranes is a dynamic equilibrium evidence for rapid flip and flop movement,” Eur. J. Biochem. 267(5), 1473–1483 (2000).
[Crossref] [PubMed]

Exp. Eye Res. (2)

H. Asai, T. Chiba, S. Kimura, and M. Takagi, “A light-induced conformational change in rod photoreceptor disc membrane,” Exp. Eye Res. 21(3), 259–267 (1975).
[Crossref] [PubMed]

N. Yagi, “Structural changes in rod outer segments of frog and mouse after illumination,” Exp. Eye Res. 116, 395–401 (2013).
[Crossref] [PubMed]

Invest. Ophthalmol. Vis. Sci. (2)

Q. X. Zhang, R. W. Lu, C. A. Curcio, and X. C. Yao, “In vivo confocal intrinsic optical signal identification of localized retinal dysfunction,” Invest. Ophthalmol. Vis. Sci. 53(13), 8139–8145 (2012).
[Crossref] [PubMed]

T. D. Lamb and E. N. Pugh., “Phototransduction, dark adaptation, and rhodopsin regeneration the proctor lecture,” Invest. Ophthalmol. Vis. Sci. 47(12), 5137–5152 (2006).
[PubMed]

J. Biol. Chem. (1)

D. C. Mitchell and B. J. Litman, “Effect of ethanol and osmotic stress on receptor conformation. Reduced water activity amplifies the effect of ethanol on metarhodopsin II formation,” J. Biol. Chem. 275(8), 5355–5360 (2000).
[Crossref] [PubMed]

J. Biomed. Opt. (3)

X. Yao and B. Wang, “Intrinsic optical signal imaging of retinal physiology: a review,” J. Biomed. Opt. 20(9), 090901 (2015).
[Crossref] [PubMed]

R. Lu, A. M. Levy, Q. Zhang, S. J. Pittler, and X. Yao, “Dynamic near-infrared imaging reveals transient phototropic change in retinal rod photoreceptors,” J. Biomed. Opt. 18(10), 106013 (2013).
[Crossref] [PubMed]

X. Zhao, D. Thapa, B. Wang, Y. Lu, S. Gai, and X. Yao, “Stimulus-evoked outer segment changes in rod photoreceptors,” J. Biomed. Opt. 21(6), 065006 (2016).
[Crossref] [PubMed]

J. Cell Biol. (1)

J. Heller, T. J. Ostwald, and D. Bok, “The osmotic behavior of rod photoreceptor outer segment discs,” J. Cell Biol. 48(3), 633–649 (1971).
[Crossref] [PubMed]

J. Physiol. (1)

J. E. Brown and L. H. Pinto, “Ionic mechanism for the photoreceptor potential of the retina of Bufo marinus,” J. Physiol. 236(3), 575–591 (1974).
[Crossref] [PubMed]

Nature (1)

M. Kahlert, D. R. Pepperberg, and K. P. Hofmann, “Effect of bleached rhodopsin on signal amplification in rod visual receptors,” Nature 345(6275), 537–539 (1990).
[Crossref] [PubMed]

Opt. Express (1)

Opt. Lett. (5)

Proc. Natl. Acad. Sci. U.S.A. (2)

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]

D. R. Pepperberg, M. Kahlert, A. Krause, and K. P. Hofmann, “Photic modulation of a highly sensitive, near-infrared light-scattering signal recorded from intact retinal photoreceptors,” Proc. Natl. Acad. Sci. U.S.A. 85(15), 5531–5535 (1988).
[Crossref] [PubMed]

Proc. R. Soc. Lond., B (1)

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

Quant. Imaging Med. Surg. (1)

B. Wang, R. Lu, Q. Zhang, and X. Yao, “Breaking diffraction limit of lateral resolution in optical coherence tomography,” Quant. Imaging Med. Surg. 3(5), 243–248 (2013).
[PubMed]

Sci. Rep. (1)

Q. Zhang, R. Lu, B. Wang, J. D. Messinger, C. A. Curcio, and X. Yao, “Functional optical coherence tomography enables in vivo physiological assessment of retinal rod and cone photoreceptors,” Sci. Rep. 5, 9595 (2015).
[Crossref] [PubMed]

Surv. Ophthalmol. (1)

H. P. Scholl and E. Zrenner, “Electrophysiology in the investigation of acquired retinal disorders,” Surv. Ophthalmol. 45(1), 29–47 (2000).
[Crossref] [PubMed]

Other (2)

D. Sun, S. Roth, and M. J. Black, “Secrets of optical flow estimation and their principles,” in Computer Vision and Pattern Recognition (CVPR),2010IEEE Conference on, (IEEE, 2010), 2432–2439.
[Crossref]

X. C. Yao, R. W. Lu, and B. Q. Wang, “Super-resolution scanning through virtully structured detection,” USA Provisional Patent, PCT# 61933987 (2014).

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Figures (5)

Fig. 1
Fig. 1 (A) Schematic diagram of the experiment setup. Left: A custom modified microscope with a 40X water immersion microscope and a CCD (100 fps) or a CMOS (500 fps) camera was employed for imaging. Right: The ERG recoding was achieved by placing electrodes on the retina in a glass chamber (dashed square). The isolated retina was continuously superfused with physiological medium during the experiment. (B) The retina was placed with photoreceptor layer on the top and was obliquely (~20°) stimulated by visible light from the top [2]. The coordinate axes shown at the bottom were used to define the direction of ROS movement. The 90° direction represents ROS movement toward the incident stimulation.
Fig. 2
Fig. 2 (A) Top: Representative microscopy images of ROSs acquired in intervals of 0.2 s. The white regions in the panels represent the stimulus pattern presentations. Bottom: The imaging period (5 s) had three phases: pre-stimulus (1 s), stimulus (1 s), and post-stimulus (3 s) phases. (B) Dynamic magnitude changes of ROS movements corresponding to the retinal images in A. Enlarged microscopy image of ROSs acquired at time 0.4 s (C) and the corresponding movement magnitude (D) and direction (E) maps. (F) Time course of the mean magnitude of ROS movements. (G) Full-field ERG recorded from the isolated retina. The shaded areas in F and G indicate the stimulus duration.
Fig. 3
Fig. 3 (A) Representative ROS image acquired at a frame speed of 500 fps. Time course of the averaged mean movement magnitudes of ROSs (B1), and averaged ERGs (C1) acquired from ten different retinal locations. (B2) Enlarged picture of the dashed square in B1. (C2) Enlarged picture of the dashed square in C1. The red triangles in B2 and C2 indicate the onset times determined by the 3-δ threshold of ROS movement and ERG a-wave, respectively. Each data point shown in C2 (sampling rate of the original data: 10 kHz) represents the value exhibited at the end of a given 2-ms interval. Gray areas in B1 and C1 show standard deviations. Shaded areas in B1, B2, C1, and C2 represent stimulation periods.
Fig. 4
Fig. 4 Comparison of ROS movements and ERGs between control groups (superfusion with Ringer’s medium) and the low-sodium group (superfusion with low-sodium medium). The retina superfusion followed a sequence of Ringer’s medium superfusion (control group), low-sodium medium superfusion (low Na+ group), and Ringer’s medium superfusion (control group). Representative ROS images acquired from the same area of the retina before (A1), during (B1) and after (C1) superfusion with the low-sodium medium. Representative movement magnitude maps and movement direction maps, before (A2, A3, respectively), during (B2, B3, respectively) and after (C2, C3, respectively) superfusion with the low-sodium medium. Time course of the mean movement magnitude of ROSs and ERGs acquired before (A4, A5, respectively), during (B4, B5, respectively) and after (C4, C5, respectively) the low-sodium superfusion. The magnitude maps (A2, B2 and C2) and direction maps (A3, B3 and C3) were calculated from the retinal images acquired at 0.4 s after the onset of the stimulus in the different groups.
Fig. 5
Fig. 5 Averaged ROS movements (A) and ERGs (B) of control (A1, B1), low-sodium (A2, B2), and recovery (A3, B3) groups. Each trace is the average of data obtained from 6 frog retinas. The gray area that accompanies each trace illustrates standard deviation. Vertical solid and dashed lines show stimulus onset and offset, respectively.

Equations (1)

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I k ( x p , y p )> I ¯ pre ( x p , y p )+3 δ pre ( x p , y p )

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