Abstract

Better understanding of stimulus-evoked intrinsic optical signals (IOSs) in the retina promises new methodology for study and diagnosis of retinal function. Using a flood-illumination near infrared (NIR) light microscope equipped with high-speed CCD (80 Hz) and CMOS (1000 Hz) cameras, we validated depth-resolved enface imaging of fast IOSs in isolated retina of leopard frog. Both positive (increasing) and negative (decreasing) IOSs were observed at the photoreceptor and inner layers of the retina. The distribution of IOSs with opposite polarities showed a center-surround pattern. At the photoreceptor layer, negative IOSs dominated the center area illuminated by the stimulus light spot, while positive signals dominated the surrounding area. In contrast, at inner retinal layers, positive IOSs dominated the center area covered by the stimulus light spot, and negative IOSs were mainly observed in the surrounding area. Fast CMOS imaging disclosed rapid IOSs within 5 ms after the stimulus onset, and both ON and OFF optical responses were observed associated with a step light stimulus.

© 2008 Optical Society of America

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    [Crossref] [PubMed]
  13. 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. Nati. Acad. Sci. USA 103, 5066–5071 (2006).
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  14. R. S. Jonnal, J. Rha, Y. Zhang, B. Cense, W. H. Gao, and D. T. Miller, “In vivo functional imaging of human cone photoreceptors,” Opt. Express 15, 16141–16160 (2007).
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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
  18. D. C. Hood, J. G. Odel, C. S. Chen, and B. J. Winn, “The multifocal electroretinogram,” J. Neuroophthalmol. 23, 225–235 (2003).
    [Crossref] [PubMed]
  19. D. C. Hood, “Assessing retinal function with the multifocal technique,” Prog. Retin. Eye. Res. 19, 607–646 (2000).
    [Crossref] [PubMed]
  20. Y. Okawa, T. Fujikado, T. Miyoshi, H. Sawai, S. Kusaka, T. Mihashi, Y. Hirohara, and Y. Tano, “Optical imaging to evaluate retinal activation by electrical currents using suprachoroidal-transretinal stimulation,” Invest. Ophthalmol. Vis. Sci. 48, 4777–4784 (2007).
    [Crossref] [PubMed]
  21. G. Hanazono, K. Tsunoda, K. Shinoda, K. Tsubota, Y. Miyake, and M. Tanifuji, “Intrinsic signal imaging in macaque retina reveals different types of flash-induced light reflectance changes of different origins,” Invest. Ophthalmol. Vis. Sci. 48, 2903–2912 (2007).
    [Crossref] [PubMed]
  22. M. D. Abramoff, Y. H. Kwon, D. Ts’o, P. Soliz, B. Zimmerman, J. Pokorny, and R. Kardon, “Visual stimulus-induced changes in human near-infrared fundus reflectance,” Invest. Ophthalmol. Vis. Sci 47, 715–721 (2006).
    [Crossref] [PubMed]
  23. V. J. Srinivasan, M. Wojtkowski, J. G. Fujimoto, and J. S. Duker, “In vivo measurement of retinal physiology with high-speed ultrahigh-resolution optical coherence tomography,” Opt. Lett. 31, 2308–2310 (2006).
    [Crossref] [PubMed]
  24. K. Grieve and A. Roorda, “Intrinsic signals from human cone photoreceptors,” Invest. Ophthalmol. Vis. Sci. 49, 713–719 (2008).
    [Crossref] [PubMed]
  25. X. C. Yao, Y. B. Zhao, and C. M. Gorga, “Optical visualization of stimulus-evoked fast neural activity and spreading waves in amphibian retina” Proc. SPIE 6864, 68640M (2008).
    [Crossref]
  26. P. A. Sieving, K. Murayama, and F. Naarendorp, “Push-pull model of the primate photopic electroretinogram: a role for hyperpolarizing neurons in shaping the b-wave,” Visual. Neurosci. 11, 519–532 (1994).
    [Crossref]
  27. 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, 6486–6501 (2008).
    [Crossref] [PubMed]
  28. A. Roorda and D. R. Williams, “Optical fiber properties of individual human cones,” J. Vis. 2, 404–412 (2002).
    [Crossref]
  29. K. Franze, J. Grosche, S. N. Skatchkov, S. Schinkinger, C. Foja, D. Schild, O. Uckermann, K. Travis, A. Reichenbach, and J. Guck, “Muller cells are living optical fibers in the vertebrate retina,” Proc. Nati. Acad. Sci. 104, 8287–8292 (2007).
    [Crossref]
  30. W. S. Stiles and B. H. Crawford, “The luminous efficiency of rays entering the eye pupil at different points,” Proc R Soc Lond B. 112, 428–450 (1933).
    [Crossref]
  31. H. Kuhn, 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. Nati. Acad. Sci. USA 78, 6873–6877 (1981).
    [Crossref]
  32. V. Y. Arshavsky, T. D. Lamb, and E. N. Pugh Jr., “G proteins and phototransduction,” Annu. Rev. Phys. 64, 153–187 (2002).
    [Crossref]
  33. S. Barnes, “Center-surround antagonism mediated by proton signaling at the cone photoreceptor synapse,” J Gen. Physiol. 122, 653–656 (2003).
    [Crossref] [PubMed]
  34. A. J. Foust and D. M. Rector, “Optically teasing apart neural swelling and depolarization,” Neuroscience 145, 887–899 (2007).
    [Crossref] [PubMed]
  35. B. M. Salzberg, A. L. Obaid, and H. Gainer, “Large and rapid changes in light scattering accompany secretion by nerve terminals in the mammalian neurohypophysis,” J. Gen. Physiol. 86, 395–411 (1985).
    [Crossref] [PubMed]
  36. D. Landowne, “Measuring nerve excitation with polarized light,” Jpn. J. Physiol. 43 Suppl 1, S7–11 (1993).
    [PubMed]
  37. R. A. Stepnoski, A. LaPorta, F. Raccuia-Behling, G. E. Blonder, R. E. Slusher, and D. Kleinfeld, “Noninvasive detection of changes in membrane potential in cultured neurons by light scattering,” Proc. Nati. Acad. Sci. USA 88, 9382–9386 (1991).
    [Crossref]
  38. X. C. Yao, D. M. Rector, and J. S. George, “Optical lever recording of displacements from activated lobster nerve bundles and Nitella internodes,” Appl. Opt. 42, 2972–2978 (2003).
    [Crossref] [PubMed]
  39. I. Tasaki and P. M. Byrne, “Rapid structural changes in nerve fibers evoked by electric current pulses,” Biochem. Biophys. Res. Commun. 188, 559–564 (1992).
    [Crossref] [PubMed]
  40. G. H. Kim, P. Kosterin, A. L. Obaid, and B. M. Salzberg, “A mechanical spike accompanies the action potential in Mammalian nerve terminals,” Biophys. J. 92, 3122–3129 (2007).
    [Crossref] [PubMed]
  41. L. B. Cohen, “Changes in neuron structure during action potential propagation and synaptic transmission,” Physiol. Rev. 53, 373–418 (1973).
    [PubMed]
  42. X. C. Yao, A. Foust, D. M. Rector, B. Barrowes, and J. S. George, “Cross-polarized reflected light measurement of fast optical responses associated with neural activation,” Biophys. J. 88, 4170–4177 (2005).
    [Crossref] [PubMed]

2008 (5)

J. L. Schei, M. D. McCluskey, A. J. Foust, X. C. Yao, and D. M. Rector, “Action potential propagation imaged with high temporal resolution near-infrared video microscopy and polarized light,” Neuroimage 40, 1034–1043 (2008).
[Crossref] [PubMed]

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

X. C. Yao, Y. B. Zhao, and C. M. Gorga, “Optical visualization of stimulus-evoked fast neural activity and spreading waves in amphibian retina” Proc. SPIE 6864, 68640M (2008).
[Crossref]

Y. B. Zhao and X. C. Yao, “Intrinsic optical imaging of stimulus-modulated physiological responses in amphibian retina,” Opt. Lett. 33, 342–344 (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, 6486–6501 (2008).
[Crossref] [PubMed]

2007 (6)

R. S. Jonnal, J. Rha, Y. Zhang, B. Cense, W. H. Gao, and D. T. Miller, “In vivo functional imaging of human cone photoreceptors,” Opt. Express 15, 16141–16160 (2007).
[Crossref] [PubMed]

Y. Okawa, T. Fujikado, T. Miyoshi, H. Sawai, S. Kusaka, T. Mihashi, Y. Hirohara, and Y. Tano, “Optical imaging to evaluate retinal activation by electrical currents using suprachoroidal-transretinal stimulation,” Invest. Ophthalmol. Vis. Sci. 48, 4777–4784 (2007).
[Crossref] [PubMed]

G. Hanazono, K. Tsunoda, K. Shinoda, K. Tsubota, Y. Miyake, and M. Tanifuji, “Intrinsic signal imaging in macaque retina reveals different types of flash-induced light reflectance changes of different origins,” Invest. Ophthalmol. Vis. Sci. 48, 2903–2912 (2007).
[Crossref] [PubMed]

K. Franze, J. Grosche, S. N. Skatchkov, S. Schinkinger, C. Foja, D. Schild, O. Uckermann, K. Travis, A. Reichenbach, and J. Guck, “Muller cells are living optical fibers in the vertebrate retina,” Proc. Nati. Acad. Sci. 104, 8287–8292 (2007).
[Crossref]

A. J. Foust and D. M. Rector, “Optically teasing apart neural swelling and depolarization,” Neuroscience 145, 887–899 (2007).
[Crossref] [PubMed]

G. H. Kim, P. Kosterin, A. L. Obaid, and B. M. Salzberg, “A mechanical spike accompanies the action potential in Mammalian nerve terminals,” Biophys. J. 92, 3122–3129 (2007).
[Crossref] [PubMed]

2006 (6)

M. D. Abramoff, Y. H. Kwon, D. Ts’o, P. Soliz, B. Zimmerman, J. Pokorny, and R. Kardon, “Visual stimulus-induced changes in human near-infrared fundus reflectance,” Invest. Ophthalmol. Vis. Sci 47, 715–721 (2006).
[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. Nati. Acad. Sci. USA 103, 5066–5071 (2006).
[Crossref]

C. Sekirnjak, P. Hottowy, A. Sher, W. Dabrowski, A. M. Litke, and E. J. Chichilnisky, “Electrical stimulation of mammalian retinal ganglion cells with multielectrode arrays,” J. Neurophysiol. 95, 3311–3327 (2006).
[Crossref] [PubMed]

X. C. Yao and J. S. George, “Dynamic neuroimaging of retinal light responses using fast intrinsic optical signals,” Neuroimage 33, 898–906 (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, 064030 (2006).
[Crossref]

V. J. Srinivasan, M. Wojtkowski, J. G. Fujimoto, and J. S. Duker, “In vivo measurement of retinal physiology with high-speed ultrahigh-resolution optical coherence tomography,” Opt. Lett. 31, 2308–2310 (2006).
[Crossref] [PubMed]

2005 (3)

X. C. Yao, A. Yamauchi, B. Perry, and J. S. George, “Rapid optical coherence tomography and recording functional scattering changes from activated frog retina,” Appl. Opt. 44, 2019–2023 (2005).
[Crossref] [PubMed]

X. C. Yao, A. Foust, D. M. Rector, B. Barrowes, and J. S. George, “Cross-polarized reflected light measurement of fast optical responses associated with neural activation,” Biophys. J. 88, 4170–4177 (2005).
[Crossref] [PubMed]

D. M. Rector, K. M. Carter, P. L. Volegov, and J. S. George, “Spatio-temporal mapping of rat whisker barrels with fast scattered light signals,” Neuroimage 26, 619–627 (2005).
[Crossref] [PubMed]

2003 (3)

X. C. Yao, D. M. Rector, and J. S. George, “Optical lever recording of displacements from activated lobster nerve bundles and Nitella internodes,” Appl. Opt. 42, 2972–2978 (2003).
[Crossref] [PubMed]

S. Barnes, “Center-surround antagonism mediated by proton signaling at the cone photoreceptor synapse,” J Gen. Physiol. 122, 653–656 (2003).
[Crossref] [PubMed]

D. C. Hood, J. G. Odel, C. S. Chen, and B. J. Winn, “The multifocal electroretinogram,” J. Neuroophthalmol. 23, 225–235 (2003).
[Crossref] [PubMed]

2002 (2)

A. Roorda and D. R. Williams, “Optical fiber properties of individual human cones,” J. Vis. 2, 404–412 (2002).
[Crossref]

V. Y. Arshavsky, T. D. Lamb, and E. N. Pugh Jr., “G proteins and phototransduction,” Annu. Rev. Phys. 64, 153–187 (2002).
[Crossref]

2000 (2)

D. C. Hood, “Assessing retinal function with the multifocal technique,” Prog. Retin. Eye. Res. 19, 607–646 (2000).
[Crossref] [PubMed]

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

1994 (1)

P. A. Sieving, K. Murayama, and F. Naarendorp, “Push-pull model of the primate photopic electroretinogram: a role for hyperpolarizing neurons in shaping the b-wave,” Visual. Neurosci. 11, 519–532 (1994).
[Crossref]

1993 (2)

S. M. Dawis and M. Rossetto, “Light-evoked changes in near-infrared transmission by the ON and OFF channels of the anuran retina,” Visual. Neurosci. 10, 687–692 (1993).
[Crossref]

D. Landowne, “Measuring nerve excitation with polarized light,” Jpn. J. Physiol. 43 Suppl 1, S7–11 (1993).
[PubMed]

1992 (1)

I. Tasaki and P. M. Byrne, “Rapid structural changes in nerve fibers evoked by electric current pulses,” Biochem. Biophys. Res. Commun. 188, 559–564 (1992).
[Crossref] [PubMed]

1991 (1)

R. A. Stepnoski, A. LaPorta, F. Raccuia-Behling, G. E. Blonder, R. E. Slusher, and D. Kleinfeld, “Noninvasive detection of changes in membrane potential in cultured neurons by light scattering,” Proc. Nati. Acad. Sci. USA 88, 9382–9386 (1991).
[Crossref]

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. Nati. Acad. Sci. USA 85, 5531–5535 (1988).
[Crossref]

1985 (1)

B. M. Salzberg, A. L. Obaid, and H. Gainer, “Large and rapid changes in light scattering accompany secretion by nerve terminals in the mammalian neurohypophysis,” J. Gen. Physiol. 86, 395–411 (1985).
[Crossref] [PubMed]

1981 (1)

H. Kuhn, 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. Nati. Acad. Sci. USA 78, 6873–6877 (1981).
[Crossref]

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, 1083–1085 (1978).
[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, 61–77 (1976).
[Crossref] [PubMed]

1973 (1)

L. B. Cohen, “Changes in neuron structure during action potential propagation and synaptic transmission,” Physiol. Rev. 53, 373–418 (1973).
[PubMed]

1968 (2)

L. B. Cohen, R. D. Keynes, and B. Hille, “Light scattering and birefringence changes during nerve activity,” Nature 218, 438–441 (1968).
[Crossref] [PubMed]

I. Tasaki, A. Watanabe, R. Sandlin, and L. Carnay, “Changes in fluorescence, turbidity, and birefringence associated with nerve excitation,” Proc. Nati. Acad. Sci. USA 61, 883–888 (1968).
[Crossref]

1933 (1)

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

Abramoff, M. D.

M. D. Abramoff, Y. H. Kwon, D. Ts’o, P. Soliz, B. Zimmerman, J. Pokorny, and R. Kardon, “Visual stimulus-induced changes in human near-infrared fundus reflectance,” Invest. Ophthalmol. Vis. Sci 47, 715–721 (2006).
[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. Nati. Acad. Sci. USA 103, 5066–5071 (2006).
[Crossref]

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. Nati. Acad. Sci. USA 103, 5066–5071 (2006).
[Crossref]

Arshavsky, V. Y.

V. Y. Arshavsky, T. D. Lamb, and E. N. Pugh Jr., “G proteins and phototransduction,” Annu. Rev. Phys. 64, 153–187 (2002).
[Crossref]

Barnes, S.

S. Barnes, “Center-surround antagonism mediated by proton signaling at the cone photoreceptor synapse,” J Gen. Physiol. 122, 653–656 (2003).
[Crossref] [PubMed]

Barrowes, B.

X. C. Yao, A. Foust, D. M. Rector, B. Barrowes, and J. S. George, “Cross-polarized reflected light measurement of fast optical responses associated with neural activation,” Biophys. J. 88, 4170–4177 (2005).
[Crossref] [PubMed]

Bennett, N.

H. Kuhn, 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. Nati. Acad. Sci. USA 78, 6873–6877 (1981).
[Crossref]

Bizheva, K.

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. Nati. Acad. Sci. USA 103, 5066–5071 (2006).
[Crossref]

Blonder, G. E.

R. A. Stepnoski, A. LaPorta, F. Raccuia-Behling, G. E. Blonder, R. E. Slusher, and D. Kleinfeld, “Noninvasive detection of changes in membrane potential in cultured neurons by light scattering,” Proc. Nati. Acad. Sci. USA 88, 9382–9386 (1991).
[Crossref]

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, 1083–1085 (1978).
[Crossref] [PubMed]

Byrne, P. M.

I. Tasaki and P. M. Byrne, “Rapid structural changes in nerve fibers evoked by electric current pulses,” Biochem. Biophys. Res. Commun. 188, 559–564 (1992).
[Crossref] [PubMed]

Carnay, L.

I. Tasaki, A. Watanabe, R. Sandlin, and L. Carnay, “Changes in fluorescence, turbidity, and birefringence associated with nerve excitation,” Proc. Nati. Acad. Sci. USA 61, 883–888 (1968).
[Crossref]

Carter, K. M.

D. M. Rector, K. M. Carter, P. L. Volegov, and J. S. George, “Spatio-temporal mapping of rat whisker barrels with fast scattered light signals,” Neuroimage 26, 619–627 (2005).
[Crossref] [PubMed]

Cense, B.

Chabre, M.

H. Kuhn, 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. Nati. Acad. Sci. USA 78, 6873–6877 (1981).
[Crossref]

Chen, C. S.

D. C. Hood, J. G. Odel, C. S. Chen, and B. J. Winn, “The multifocal electroretinogram,” J. Neuroophthalmol. 23, 225–235 (2003).
[Crossref] [PubMed]

Chichilnisky, E. J.

C. Sekirnjak, P. Hottowy, A. Sher, W. Dabrowski, A. M. Litke, and E. J. Chichilnisky, “Electrical stimulation of mammalian retinal ganglion cells with multielectrode arrays,” J. Neurophysiol. 95, 3311–3327 (2006).
[Crossref] [PubMed]

Cohen, L. B.

L. B. Cohen, “Changes in neuron structure during action potential propagation and synaptic transmission,” Physiol. Rev. 53, 373–418 (1973).
[PubMed]

L. B. Cohen, R. D. Keynes, and B. Hille, “Light scattering and birefringence changes during nerve activity,” Nature 218, 438–441 (1968).
[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 Lond B. 112, 428–450 (1933).
[Crossref]

Dabrowski, W.

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K. Franze, J. Grosche, S. N. Skatchkov, S. Schinkinger, C. Foja, D. Schild, O. Uckermann, K. Travis, A. Reichenbach, and J. Guck, “Muller cells are living optical fibers in the vertebrate retina,” Proc. Nati. Acad. Sci. 104, 8287–8292 (2007).
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J. L. Schei, M. D. McCluskey, A. J. Foust, X. C. Yao, and D. M. Rector, “Action potential propagation imaged with high temporal resolution near-infrared video microscopy and polarized light,” Neuroimage 40, 1034–1043 (2008).
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K. Franze, J. Grosche, S. N. Skatchkov, S. Schinkinger, C. Foja, D. Schild, O. Uckermann, K. Travis, A. Reichenbach, and J. Guck, “Muller cells are living optical fibers in the vertebrate retina,” Proc. Nati. Acad. Sci. 104, 8287–8292 (2007).
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Gainer, H.

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Gao, W. H.

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K. Franze, J. Grosche, S. N. Skatchkov, S. Schinkinger, C. Foja, D. Schild, O. Uckermann, K. Travis, A. Reichenbach, and J. Guck, “Muller cells are living optical fibers in the vertebrate retina,” Proc. Nati. Acad. Sci. 104, 8287–8292 (2007).
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K. Franze, J. Grosche, S. N. Skatchkov, S. Schinkinger, C. Foja, D. Schild, O. Uckermann, K. Travis, A. Reichenbach, and J. Guck, “Muller cells are living optical fibers in the vertebrate retina,” Proc. Nati. Acad. Sci. 104, 8287–8292 (2007).
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G. Hanazono, K. Tsunoda, K. Shinoda, K. Tsubota, Y. Miyake, and M. Tanifuji, “Intrinsic signal imaging in macaque retina reveals different types of flash-induced light reflectance changes of different origins,” Invest. Ophthalmol. Vis. Sci. 48, 2903–2912 (2007).
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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, 1083–1085 (1978).
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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. Nati. Acad. Sci. USA 103, 5066–5071 (2006).
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Y. Okawa, T. Fujikado, T. Miyoshi, H. Sawai, S. Kusaka, T. Mihashi, Y. Hirohara, and Y. Tano, “Optical imaging to evaluate retinal activation by electrical currents using suprachoroidal-transretinal stimulation,” Invest. Ophthalmol. Vis. Sci. 48, 4777–4784 (2007).
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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. Nati. Acad. Sci. USA 85, 5531–5535 (1988).
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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, 61–77 (1976).
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Kahlert, M.

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. Nati. Acad. Sci. USA 85, 5531–5535 (1988).
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M. D. Abramoff, Y. H. Kwon, D. Ts’o, P. Soliz, B. Zimmerman, J. Pokorny, and R. Kardon, “Visual stimulus-induced changes in human near-infrared fundus reflectance,” Invest. Ophthalmol. Vis. Sci 47, 715–721 (2006).
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L. B. Cohen, R. D. Keynes, and B. Hille, “Light scattering and birefringence changes during nerve activity,” Nature 218, 438–441 (1968).
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G. H. Kim, P. Kosterin, A. L. Obaid, and B. M. Salzberg, “A mechanical spike accompanies the action potential in Mammalian nerve terminals,” Biophys. J. 92, 3122–3129 (2007).
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H. Kolb, E. Fernandez, and R. Nelson, “Gross Anatomy of the Eye” (2003), http://webvision.med.utah.edu/anatomy.html.

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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. Nati. Acad. Sci. USA 85, 5531–5535 (1988).
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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, 61–77 (1976).
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H. Kuhn, 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. Nati. Acad. Sci. USA 78, 6873–6877 (1981).
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Y. Okawa, T. Fujikado, T. Miyoshi, H. Sawai, S. Kusaka, T. Mihashi, Y. Hirohara, and Y. Tano, “Optical imaging to evaluate retinal activation by electrical currents using suprachoroidal-transretinal stimulation,” Invest. Ophthalmol. Vis. Sci. 48, 4777–4784 (2007).
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M. D. Abramoff, Y. H. Kwon, D. Ts’o, P. Soliz, B. Zimmerman, J. Pokorny, and R. Kardon, “Visual stimulus-induced changes in human near-infrared fundus reflectance,” Invest. Ophthalmol. Vis. Sci 47, 715–721 (2006).
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V. Y. Arshavsky, T. D. Lamb, and E. N. Pugh Jr., “G proteins and phototransduction,” Annu. Rev. Phys. 64, 153–187 (2002).
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C. Sekirnjak, P. Hottowy, A. Sher, W. Dabrowski, A. M. Litke, and E. J. Chichilnisky, “Electrical stimulation of mammalian retinal ganglion cells with multielectrode arrays,” J. Neurophysiol. 95, 3311–3327 (2006).
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J. L. Schei, M. D. McCluskey, A. J. Foust, X. C. Yao, and D. M. Rector, “Action potential propagation imaged with high temporal resolution near-infrared video microscopy and polarized light,” Neuroimage 40, 1034–1043 (2008).
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H. Kuhn, 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. Nati. Acad. Sci. USA 78, 6873–6877 (1981).
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Y. Okawa, T. Fujikado, T. Miyoshi, H. Sawai, S. Kusaka, T. Mihashi, Y. Hirohara, and Y. Tano, “Optical imaging to evaluate retinal activation by electrical currents using suprachoroidal-transretinal stimulation,” Invest. Ophthalmol. Vis. Sci. 48, 4777–4784 (2007).
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Miller, D. T.

Miyake, Y.

G. Hanazono, K. Tsunoda, K. Shinoda, K. Tsubota, Y. Miyake, and M. Tanifuji, “Intrinsic signal imaging in macaque retina reveals different types of flash-induced light reflectance changes of different origins,” Invest. Ophthalmol. Vis. Sci. 48, 2903–2912 (2007).
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Miyoshi, T.

Y. Okawa, T. Fujikado, T. Miyoshi, H. Sawai, S. Kusaka, T. Mihashi, Y. Hirohara, and Y. Tano, “Optical imaging to evaluate retinal activation by electrical currents using suprachoroidal-transretinal stimulation,” Invest. Ophthalmol. Vis. Sci. 48, 4777–4784 (2007).
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P. A. Sieving, K. Murayama, and F. Naarendorp, “Push-pull model of the primate photopic electroretinogram: a role for hyperpolarizing neurons in shaping the b-wave,” Visual. Neurosci. 11, 519–532 (1994).
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G. H. Kim, P. Kosterin, A. L. Obaid, and B. M. Salzberg, “A mechanical spike accompanies the action potential in Mammalian nerve terminals,” Biophys. J. 92, 3122–3129 (2007).
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B. M. Salzberg, A. L. Obaid, and H. Gainer, “Large and rapid changes in light scattering accompany secretion by nerve terminals in the mammalian neurohypophysis,” J. Gen. Physiol. 86, 395–411 (1985).
[Crossref] [PubMed]

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D. C. Hood, J. G. Odel, C. S. Chen, and B. J. Winn, “The multifocal electroretinogram,” J. Neuroophthalmol. 23, 225–235 (2003).
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Y. Okawa, T. Fujikado, T. Miyoshi, H. Sawai, S. Kusaka, T. Mihashi, Y. Hirohara, and Y. Tano, “Optical imaging to evaluate retinal activation by electrical currents using suprachoroidal-transretinal stimulation,” Invest. Ophthalmol. Vis. Sci. 48, 4777–4784 (2007).
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Pepperberg, D. R.

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. Nati. Acad. Sci. USA 85, 5531–5535 (1988).
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Perry, B.

Pflug, R.

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. Nati. Acad. Sci. USA 103, 5066–5071 (2006).
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Pinto, L. H.

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, 1083–1085 (1978).
[Crossref] [PubMed]

Pokorny, J.

M. D. Abramoff, Y. H. Kwon, D. Ts’o, P. Soliz, B. Zimmerman, J. Pokorny, and R. Kardon, “Visual stimulus-induced changes in human near-infrared fundus reflectance,” Invest. Ophthalmol. Vis. Sci 47, 715–721 (2006).
[Crossref] [PubMed]

Popov, S.

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. Nati. Acad. Sci. USA 103, 5066–5071 (2006).
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Povazay, B.

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. Nati. Acad. Sci. USA 103, 5066–5071 (2006).
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Pugh Jr., E. N.

V. Y. Arshavsky, T. D. Lamb, and E. N. Pugh Jr., “G proteins and phototransduction,” Annu. Rev. Phys. 64, 153–187 (2002).
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Qiu, 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. Nati. Acad. Sci. USA 103, 5066–5071 (2006).
[Crossref]

Raccuia-Behling, F.

R. A. Stepnoski, A. LaPorta, F. Raccuia-Behling, G. E. Blonder, R. E. Slusher, and D. Kleinfeld, “Noninvasive detection of changes in membrane potential in cultured neurons by light scattering,” Proc. Nati. Acad. Sci. USA 88, 9382–9386 (1991).
[Crossref]

Rector, D. M.

J. L. Schei, M. D. McCluskey, A. J. Foust, X. C. Yao, and D. M. Rector, “Action potential propagation imaged with high temporal resolution near-infrared video microscopy and polarized light,” Neuroimage 40, 1034–1043 (2008).
[Crossref] [PubMed]

A. J. Foust and D. M. Rector, “Optically teasing apart neural swelling and depolarization,” Neuroscience 145, 887–899 (2007).
[Crossref] [PubMed]

X. C. Yao, A. Foust, D. M. Rector, B. Barrowes, and J. S. George, “Cross-polarized reflected light measurement of fast optical responses associated with neural activation,” Biophys. J. 88, 4170–4177 (2005).
[Crossref] [PubMed]

D. M. Rector, K. M. Carter, P. L. Volegov, and J. S. George, “Spatio-temporal mapping of rat whisker barrels with fast scattered light signals,” Neuroimage 26, 619–627 (2005).
[Crossref] [PubMed]

X. C. Yao, D. M. Rector, and J. S. George, “Optical lever recording of displacements from activated lobster nerve bundles and Nitella internodes,” Appl. Opt. 42, 2972–2978 (2003).
[Crossref] [PubMed]

Reichenbach, A.

K. Franze, J. Grosche, S. N. Skatchkov, S. Schinkinger, C. Foja, D. Schild, O. Uckermann, K. Travis, A. Reichenbach, and J. Guck, “Muller cells are living optical fibers in the vertebrate retina,” Proc. Nati. Acad. Sci. 104, 8287–8292 (2007).
[Crossref]

Reitsamer, H.

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. Nati. Acad. Sci. USA 103, 5066–5071 (2006).
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Rha, J.

Roorda, A.

K. Grieve and A. Roorda, “Intrinsic signals from human cone photoreceptors,” Invest. Ophthalmol. Vis. Sci. 49, 713–719 (2008).
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A. Roorda and D. R. Williams, “Optical fiber properties of individual human cones,” J. Vis. 2, 404–412 (2002).
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Rossetto, M.

S. M. Dawis and M. Rossetto, “Light-evoked changes in near-infrared transmission by the ON and OFF channels of the anuran retina,” Visual. Neurosci. 10, 687–692 (1993).
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Salzberg, B. M.

G. H. Kim, P. Kosterin, A. L. Obaid, and B. M. Salzberg, “A mechanical spike accompanies the action potential in Mammalian nerve terminals,” Biophys. J. 92, 3122–3129 (2007).
[Crossref] [PubMed]

B. M. Salzberg, A. L. Obaid, and H. Gainer, “Large and rapid changes in light scattering accompany secretion by nerve terminals in the mammalian neurohypophysis,” J. Gen. Physiol. 86, 395–411 (1985).
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Sandlin, R.

I. Tasaki, A. Watanabe, R. Sandlin, and L. Carnay, “Changes in fluorescence, turbidity, and birefringence associated with nerve excitation,” Proc. Nati. Acad. Sci. USA 61, 883–888 (1968).
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Sattmann, H.

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. Nati. Acad. Sci. USA 103, 5066–5071 (2006).
[Crossref]

Sawai, H.

Y. Okawa, T. Fujikado, T. Miyoshi, H. Sawai, S. Kusaka, T. Mihashi, Y. Hirohara, and Y. Tano, “Optical imaging to evaluate retinal activation by electrical currents using suprachoroidal-transretinal stimulation,” Invest. Ophthalmol. Vis. Sci. 48, 4777–4784 (2007).
[Crossref] [PubMed]

Schei, J. L.

J. L. Schei, M. D. McCluskey, A. J. Foust, X. C. Yao, and D. M. Rector, “Action potential propagation imaged with high temporal resolution near-infrared video microscopy and polarized light,” Neuroimage 40, 1034–1043 (2008).
[Crossref] [PubMed]

Schild, D.

K. Franze, J. Grosche, S. N. Skatchkov, S. Schinkinger, C. Foja, D. Schild, O. Uckermann, K. Travis, A. Reichenbach, and J. Guck, “Muller cells are living optical fibers in the vertebrate retina,” Proc. Nati. Acad. Sci. 104, 8287–8292 (2007).
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Schinkinger, S.

K. Franze, J. Grosche, S. N. Skatchkov, S. Schinkinger, C. Foja, D. Schild, O. Uckermann, K. Travis, A. Reichenbach, and J. Guck, “Muller cells are living optical fibers in the vertebrate retina,” Proc. Nati. Acad. Sci. 104, 8287–8292 (2007).
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H. P. Scholl and E. Zrenner, “Electrophysiology in the investigation of acquired retinal disorders,” Surv. Ophthalmol. 45, 29–47 (2000).
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C. Sekirnjak, P. Hottowy, A. Sher, W. Dabrowski, A. M. Litke, and E. J. Chichilnisky, “Electrical stimulation of mammalian retinal ganglion cells with multielectrode arrays,” J. Neurophysiol. 95, 3311–3327 (2006).
[Crossref] [PubMed]

Sher, A.

C. Sekirnjak, P. Hottowy, A. Sher, W. Dabrowski, A. M. Litke, and E. J. Chichilnisky, “Electrical stimulation of mammalian retinal ganglion cells with multielectrode arrays,” J. Neurophysiol. 95, 3311–3327 (2006).
[Crossref] [PubMed]

Shinoda, K.

G. Hanazono, K. Tsunoda, K. Shinoda, K. Tsubota, Y. Miyake, and M. Tanifuji, “Intrinsic signal imaging in macaque retina reveals different types of flash-induced light reflectance changes of different origins,” Invest. Ophthalmol. Vis. Sci. 48, 2903–2912 (2007).
[Crossref] [PubMed]

Sieving, P. A.

P. A. Sieving, K. Murayama, and F. Naarendorp, “Push-pull model of the primate photopic electroretinogram: a role for hyperpolarizing neurons in shaping the b-wave,” Visual. Neurosci. 11, 519–532 (1994).
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Supplementary Material (6)

» Media 1: MPG (2062 KB)     
» Media 2: MPG (2062 KB)     
» Media 3: MPG (2062 KB)     
» Media 4: MPG (2250 KB)     
» Media 5: MPG (2251 KB)     
» Media 6: MPG (2358 KB)     

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Figures (7)

Fig. 1.
Fig. 1.

Schematic diagram of the experimental setup. During the measurement, isolated frog retina was illuminated continuously by the NIR light for recording of stimulus-evoked IOSs. The visible light stimulator was used to produce a visible light flash for retinal stimulation. Concurrent ERG measurement was conducted to record electrophysiological responses associated with retinal activation. At the dichroic mirror (DM), visible stimulus light was reflected and NIR recording light was passed through. The eyepiece camera was used to adjust visible light stimulus aperture at the retina. In order to ensure light efficiency for intrinsic optical signal imaging, the beam splitter (BS) was removed from the optical path after we adjusted the visible light stimulator. The NIR filter was used to block visible stimulus light, and allow the NIR probe light to reach the CCD/CMOS camera.

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Fig. 2.
Fig. 2.

(a) Representative CCD image sequence of photoreceptor layer, without differential processing. The white spot in the second frame shows the visible stimulus pattern. At the photoreceptor layer, the diameter of the stimulus aperture was ~60 µm. (b) and (c) Intrinsic optical signals elicited by a 125 ms visible light flash. Each illustrated frame is an average over 100 ms interval (8 frames). 100 ms pre-stimulus and 500 ms after-stimulus images are shown in each imaging sequence. The imaging sequence c was recorded after the imaging sequence b, with a time interval of 2 minutes. (d) Temporal change of intrinsic optical responses. The numbered tracings 1–6 are corresponding to the arrows pointed retinal areas (average of 5×5 pixels) in sequence b. Vertical lines indicate the stimulus onset and offset. (e) (Media 1) video showing dynamic intrinsic optical signal patterns at the photoreceptor layer. This video is from the same image sequence shown in b. 0.5 s (40 frames) pre-stimulus baseline and 5 s (400 frames) after-stimulus images are shown.

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Fig. 3.
Fig. 3.

(a) Representative CCD image sequence of inner nuclear layer, without differential processing. The white spot in the second frame shows the visible stimulus pattern. At the photoreceptor layer, the diameter of the stimulus aperture was ~60 µm. (b) and (c) Intrinsic optical signals elicited by a 125 ms visible light flash. Each illustrated frame is an average over 100 ms interval (8 frames). 100 ms pre-stimulus and 500 ms after-stimulus images are shown in each imaging sequence. The imaging sequence c was recorded after the imaging sequence b, with a time interval of 2 minutes. (d) Temporal change of intrinsic optical responses. The numbered tracings 1–6 are corresponding to the arrows pointed retinal areas (average of 5×5 pixels) in sequence b. Vertical lines indicate the stimulus onset and offset. (e) (Media 2) video showing dynamic intrinsic optical patterns at the inner nuclear layer. This video is from the same image sequence shown in b. 0.5 s (40 frames) pre-stimulus baseline and 5 s (400 frames) after-stimulus images are shown.

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Fig. 4.
Fig. 4.

(a) Representative CCD image sequence of ganglion layer, without differential processing. The white spot in the second frame shows the visible stimulus pattern. At the photoreceptor layer, the diameter of the stimulus aperture was ~60 µm. (b) and (c) Intrinsic optical signals elicited by a 125 ms visible light flash. Each illustrated frame is an average over 100 ms interval (8 frames). 100 ms pre-stimulus and 500 ms after-stimulus images are shown in each imaging sequence. The imaging sequence c was recorded after the imaging sequence b, with a time interval of 2 minutes. (d) Temporal change of intrinsic optical responses. The numbered tracings 1–6 are corresponding to the arrows pointed retinal areas (average of 5×5 pixels) in sequence b. Vertical lines indicate the stimulus onset and offset. (e) (Media 3) video showing dynamic intrinsic optical patterns at the ganglion layer. This video is from the same image sequence shown in b. 0.5 s (40 frames) pre-stimulus baseline and 5 s (400 frames) afterstimulus images are shown.

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Fig. 5.
Fig. 5.

(a–c) Averaged intrinsic optical images of the photoreceptor (a), inner nuclear (b) and ganglion (c) layers. The white spot in the first frame of sequence (a) shows the stimulus pattern. At the photoreceptor layer, the diameter of the stimulus spot was ~60 µm. Each image sequence is an average of 12 experimental passes, and each illustrated frame is an average over 100 ms interval (8 frames). 100 ms pre-stimulus and 500 ms after-stimulus images are shown in each imaging sequence. (d–f) Statistics of positive and negative optical responses at the photoreceptor (d), inner nuclear (e), and ganglion (f) layers, corresponding to the areas marked by the square blocks shown in the third frames of sequences a–c.

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Fig. 6.
Fig. 6.

(a–c) Representative CMOS images of the photoreceptor (a), inner nuclear (b), and ganglion (c) layers of the retina before differential processing. Each CMOS frame consists of 160×120 pixels. The left-top and bottom right corners are Pixel (0, 0) and Pixel (159, 119), respectively. The white spot in (a) shows the stimulus pattern. At the photoreceptor layer, the diameter of the stimulus spot was ~60 µm. (d–f) (Media 4) Video clips of dynamic intrinsic optical changes recorded from the photoreceptor (d), middle (e) (Media 5), and ganglion (f) (Media 6) layers. The retina was activated by a 500 ms step light stimulus. The raw CMOS images were recorded with a speed of 1000 frame/s. Each illustrated frame of the videos is an average over 10 ms interval (10 frames). 200 ms pre-stimulus and 1000 ms after-stimulus images are shown in each video. The imaging sequences d, e, and f were recorded sequentially, with a time interval of 5 minutes. (g) Transient intrinsic optical changes of individual pixels. In each subpanel, Pixel (x, y) indicates the location of each representative pixel. Black, blue, and red tracings correspond to the intrinsic optical signal images recorded from photoreceptor layer (PRL), inner nuclear layer (INL), and ganglion layer (GL). Vertical lines indicate the stimulus onset and offset. Black arrows point to ON response of the IOSs corresponding to the stimulus onset. Green and purple arrows point to OFF response of the IOSs corresponding to the stimulus offset.

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Fig. 7.
Fig. 7.

Averaged intrinsic optical responses of the retinal area (40 µm×40 µm) covered by the white block shown in Fig. 6 (b). Black, blue, and red tracings correspond to the imaging sequences of the photoreceptor layer (PRL), inner nuclear layer (INL), and ganglion layer (GL) shown in Fig. 6 (d–f). Vertical lines indicate the stimulus onset and offset. Black arrows point to ON response of the IOSs corresponding to the stimulus onset. Green and purple arrows point to OFF response of the IOSs corresponding to the stimulus offset.

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