Abstract

Using freshly isolated animal retinas, we have conducted a series of experiments to test fast intrinsic optical signals (IOSs) that have time courses comparable to electrophysiological kinetics. In this Letter, we demonstrate the feasibility of in vivo imaging of fast IOSs in intact frogs. A rapid line-scan confocal ophthalmoscope was constructed to achieve high-speed IOS recording. By rejecting out-of-focus background light, the line-scan confocal imager provided the resolution to differentiate individual photoreceptors in vivo. Rapid confocal imaging disclosed robust IOSs with time courses comparable to retinal electroretinogram kinetics. High-resolution IOS images revealed both positive (increasing) and negative (decreasing) light responses, with subcellular complexity.

© 2011 Optical Society of America

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X. C. Yao, L. Liu, and Y. G. Li, J. Innovative Opt. Health Sci. 2, 201 (2009).
[CrossRef]

X. C. Yao, Jpn. J. Ophthalmol. 53, 327 (2009).
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[CrossRef] [PubMed]

2008 (4)

D. Nagy, B. Schonfisch, E. Zrenner, and H. Jagle, Invest. Ophthalmol. Vis. Sci. 49, 4664 (2008).
[CrossRef] [PubMed]

B. Falsini, D. Marangoni, T. Salgarello, G. Stifano, L. Montrone, F. Campagna, S. Aliberti, E. Balestrazzi, and A. Colotto, Graefes Arch. Clin. Exp. Ophthalmol. 246, 1153 (2008).
[CrossRef] [PubMed]

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[CrossRef] [PubMed]

X. C. Yao and Y. B. Zhao, Opt. Express 16, 12446(2008).
[CrossRef] [PubMed]

2007 (3)

A. J. Foust and D. M. Rector, Neuroscience 145, 887(2007).
[CrossRef] [PubMed]

G. Hanazono, K. Tsunoda, K. Shinoda, K. Tsubota, Y. Miyake, and M. Tanifuji, Invest. Ophthalmol. Vis. Sci. 48, 2903 (2007).
[CrossRef] [PubMed]

R. S. Jonnal, J. Rha, Y. Zhang, B. Cense, W. H. Gao, and D. T. Miller, Opt. Express 15, 16141 (2007).
[CrossRef] [PubMed]

2006 (3)

L. M. Ventura, N. Sorokac, R. De Los Santos, W. J. Feuer, and V. Porciatti, Invest. Ophthalmol. Vis. Sci. 47, 3904 (2006).
[CrossRef] [PubMed]

V. J. Srinivasan, M. Wojtkowski, J. G. Fujimoto, and J. S. Duker, Opt. Lett. 31, 2308 (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, Proc. Natl. Acad. Sci. USA 103, 5066 (2006).
[CrossRef] [PubMed]

2005 (2)

2002 (1)

V. Y. Arshavsky, T. D. Lamb, and E. N. Pugh, Jr., Annu. Rev. Physiol. 64, 153 (2002).
[CrossRef] [PubMed]

2000 (4)

G. Li, H. Zwick, B. Stuck, and D. J. Lund, J. Biomed. Opt. 5, 307 (2000).
[CrossRef] [PubMed]

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[CrossRef] [PubMed]

D. C. Hood, Prog. Retin. Eye Res. 19, 607 (2000).
[CrossRef] [PubMed]

S. G. Jacobson, A. V. Cideciyan, A. Iannaccone, R. G. Weleber, G. A. Fishman, A. M. Maguire, L. M. Affatigato, J. Bennett, E. A. Pierce, M. Danciger, D. B. Farber, and E. M. Stone, Invest. Ophthalmol. Vis. Sci. 41, 1898 (2000).
[PubMed]

1996 (1)

C. A. Curcio, N. E. Medeiros, and C. L. Millican, Invest. Ophthalmol. Vis. Sci. 37, 1236 (1996).
[PubMed]

1982 (1)

H. A. Quigley, E. M. Addicks, and W. R. Green, Arch. Ophthalmol. 100, 135 (1982).
[CrossRef] [PubMed]

1981 (1)

H. Kuhn, N. Bennett, M. Michel-Villaz, and M. Chabre, Proc. Natl. Acad. Sci. USA 78, 6873 (1981).
[CrossRef] [PubMed]

1964 (1)

S. E. Nilsson, J. Ultrastruct. Res. 10, 390 (1964).
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Abramoff, M.

J. Schallek, H. Li, R. Kardon, Y. Kwon, M. Abramoff, P. Soliz, and D. Ts’o, Invest. Ophthalmol. Vis. Sci. 50, 4865(2009).
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H. A. Quigley, E. M. Addicks, and W. R. Green, Arch. Ophthalmol. 100, 135 (1982).
[CrossRef] [PubMed]

Affatigato, L. M.

S. G. Jacobson, A. V. Cideciyan, A. Iannaccone, R. G. Weleber, G. A. Fishman, A. M. Maguire, L. M. Affatigato, J. Bennett, E. A. Pierce, M. Danciger, D. B. Farber, and E. M. Stone, Invest. Ophthalmol. Vis. Sci. 41, 1898 (2000).
[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, Proc. Natl. Acad. Sci. USA 103, 5066 (2006).
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Amthor, F.

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, Proc. Natl. Acad. Sci. USA 103, 5066 (2006).
[CrossRef] [PubMed]

Arshavsky, V. Y.

V. Y. Arshavsky, T. D. Lamb, and E. N. Pugh, Jr., Annu. Rev. Physiol. 64, 153 (2002).
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Balestrazzi, E.

B. Falsini, D. Marangoni, T. Salgarello, G. Stifano, L. Montrone, F. Campagna, S. Aliberti, E. Balestrazzi, and A. Colotto, Graefes Arch. Clin. Exp. Ophthalmol. 246, 1153 (2008).
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Bennett, J.

S. G. Jacobson, A. V. Cideciyan, A. Iannaccone, R. G. Weleber, G. A. Fishman, A. M. Maguire, L. M. Affatigato, J. Bennett, E. A. Pierce, M. Danciger, D. B. Farber, and E. M. Stone, Invest. Ophthalmol. Vis. Sci. 41, 1898 (2000).
[PubMed]

Bennett, N.

H. Kuhn, N. Bennett, M. Michel-Villaz, and M. Chabre, Proc. Natl. Acad. Sci. USA 78, 6873 (1981).
[CrossRef] [PubMed]

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, Proc. Natl. Acad. Sci. USA 103, 5066 (2006).
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Cakir, Y.

Y. Cakir and S. M. Strauch, Pharmacol. Rep. PR 57, 467 (2005).

Campagna, F.

B. Falsini, D. Marangoni, T. Salgarello, G. Stifano, L. Montrone, F. Campagna, S. Aliberti, E. Balestrazzi, and A. Colotto, Graefes Arch. Clin. Exp. Ophthalmol. 246, 1153 (2008).
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Carroll, J.

Cense, B.

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H. Kuhn, N. Bennett, M. Michel-Villaz, and M. Chabre, Proc. Natl. Acad. Sci. USA 78, 6873 (1981).
[CrossRef] [PubMed]

Cideciyan, A. V.

S. G. Jacobson, A. V. Cideciyan, A. Iannaccone, R. G. Weleber, G. A. Fishman, A. M. Maguire, L. M. Affatigato, J. Bennett, E. A. Pierce, M. Danciger, D. B. Farber, and E. M. Stone, Invest. Ophthalmol. Vis. Sci. 41, 1898 (2000).
[PubMed]

Colotto, A.

B. Falsini, D. Marangoni, T. Salgarello, G. Stifano, L. Montrone, F. Campagna, S. Aliberti, E. Balestrazzi, and A. Colotto, Graefes Arch. Clin. Exp. Ophthalmol. 246, 1153 (2008).
[CrossRef] [PubMed]

Curcio, C. A.

C. A. Curcio, N. E. Medeiros, and C. L. Millican, Invest. Ophthalmol. Vis. Sci. 37, 1236 (1996).
[PubMed]

Danciger, M.

S. G. Jacobson, A. V. Cideciyan, A. Iannaccone, R. G. Weleber, G. A. Fishman, A. M. Maguire, L. M. Affatigato, J. Bennett, E. A. Pierce, M. Danciger, D. B. Farber, and E. M. Stone, Invest. Ophthalmol. Vis. Sci. 41, 1898 (2000).
[PubMed]

De Los Santos, R.

L. M. Ventura, N. Sorokac, R. De Los Santos, W. J. Feuer, and V. Porciatti, Invest. Ophthalmol. Vis. Sci. 47, 3904 (2006).
[CrossRef] [PubMed]

Drexler, W.

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, Proc. Natl. Acad. Sci. USA 103, 5066 (2006).
[CrossRef] [PubMed]

Duker, J. S.

Falsini, B.

B. Falsini, D. Marangoni, T. Salgarello, G. Stifano, L. Montrone, F. Campagna, S. Aliberti, E. Balestrazzi, and A. Colotto, Graefes Arch. Clin. Exp. Ophthalmol. 246, 1153 (2008).
[CrossRef] [PubMed]

Farber, D. B.

S. G. Jacobson, A. V. Cideciyan, A. Iannaccone, R. G. Weleber, G. A. Fishman, A. M. Maguire, L. M. Affatigato, J. Bennett, E. A. Pierce, M. Danciger, D. B. Farber, and E. M. Stone, Invest. Ophthalmol. Vis. Sci. 41, 1898 (2000).
[PubMed]

Feuer, W. J.

L. M. Ventura, N. Sorokac, R. De Los Santos, W. J. Feuer, and V. Porciatti, Invest. Ophthalmol. Vis. Sci. 47, 3904 (2006).
[CrossRef] [PubMed]

Fishman, G. A.

S. G. Jacobson, A. V. Cideciyan, A. Iannaccone, R. G. Weleber, G. A. Fishman, A. M. Maguire, L. M. Affatigato, J. Bennett, E. A. Pierce, M. Danciger, D. B. Farber, and E. M. Stone, Invest. Ophthalmol. Vis. Sci. 41, 1898 (2000).
[PubMed]

Foust, A. J.

A. J. Foust and D. M. Rector, Neuroscience 145, 887(2007).
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Fujimoto, J. G.

Gao, W. H.

George, J. S.

Godara, P.

Green, W. R.

H. A. Quigley, E. M. Addicks, and W. R. Green, Arch. Ophthalmol. 100, 135 (1982).
[CrossRef] [PubMed]

Grieve, K.

K. Grieve and A. Roorda, Invest. Ophthalmol. Vis. Sci. 49, 713 (2008).
[CrossRef] [PubMed]

Hanazono, G.

G. Hanazono, K. Tsunoda, K. Shinoda, K. Tsubota, Y. Miyake, and M. Tanifuji, Invest. Ophthalmol. Vis. Sci. 48, 2903 (2007).
[CrossRef] [PubMed]

Hermann, 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, Proc. Natl. Acad. Sci. USA 103, 5066 (2006).
[CrossRef] [PubMed]

Hood, D. C.

D. C. Hood, Prog. Retin. Eye Res. 19, 607 (2000).
[CrossRef] [PubMed]

Iannaccone, A.

S. G. Jacobson, A. V. Cideciyan, A. Iannaccone, R. G. Weleber, G. A. Fishman, A. M. Maguire, L. M. Affatigato, J. Bennett, E. A. Pierce, M. Danciger, D. B. Farber, and E. M. Stone, Invest. Ophthalmol. Vis. Sci. 41, 1898 (2000).
[PubMed]

Jacobson, S. G.

S. G. Jacobson, A. V. Cideciyan, A. Iannaccone, R. G. Weleber, G. A. Fishman, A. M. Maguire, L. M. Affatigato, J. Bennett, E. A. Pierce, M. Danciger, D. B. Farber, and E. M. Stone, Invest. Ophthalmol. Vis. Sci. 41, 1898 (2000).
[PubMed]

Jagle, H.

D. Nagy, B. Schonfisch, E. Zrenner, and H. Jagle, Invest. Ophthalmol. Vis. Sci. 49, 4664 (2008).
[CrossRef] [PubMed]

Jonnal, R. S.

Kardon, R.

J. Schallek, H. Li, R. Kardon, Y. Kwon, M. Abramoff, P. Soliz, and D. Ts’o, Invest. Ophthalmol. Vis. Sci. 50, 4865(2009).
[CrossRef] [PubMed]

Keyser, K.

Kuhn, H.

H. Kuhn, N. Bennett, M. Michel-Villaz, and M. Chabre, Proc. Natl. Acad. Sci. USA 78, 6873 (1981).
[CrossRef] [PubMed]

Kwon, Y.

J. Schallek, H. Li, R. Kardon, Y. Kwon, M. Abramoff, P. Soliz, and D. Ts’o, Invest. Ophthalmol. Vis. Sci. 50, 4865(2009).
[CrossRef] [PubMed]

Lamb, T. D.

V. Y. Arshavsky, T. D. Lamb, and E. N. Pugh, Jr., Annu. Rev. Physiol. 64, 153 (2002).
[CrossRef] [PubMed]

Li, G.

G. Li, H. Zwick, B. Stuck, and D. J. Lund, J. Biomed. Opt. 5, 307 (2000).
[CrossRef] [PubMed]

Li, H.

J. Schallek, H. Li, R. Kardon, Y. Kwon, M. Abramoff, P. Soliz, and D. Ts’o, Invest. Ophthalmol. Vis. Sci. 50, 4865(2009).
[CrossRef] [PubMed]

Li, Y. C.

Li, Y. G.

Liu, L.

Lund, D. J.

G. Li, H. Zwick, B. Stuck, and D. J. Lund, J. Biomed. Opt. 5, 307 (2000).
[CrossRef] [PubMed]

Maguire, A. M.

S. G. Jacobson, A. V. Cideciyan, A. Iannaccone, R. G. Weleber, G. A. Fishman, A. M. Maguire, L. M. Affatigato, J. Bennett, E. A. Pierce, M. Danciger, D. B. Farber, and E. M. Stone, Invest. Ophthalmol. Vis. Sci. 41, 1898 (2000).
[PubMed]

Marangoni, D.

B. Falsini, D. Marangoni, T. Salgarello, G. Stifano, L. Montrone, F. Campagna, S. Aliberti, E. Balestrazzi, and A. Colotto, Graefes Arch. Clin. Exp. Ophthalmol. 246, 1153 (2008).
[CrossRef] [PubMed]

Medeiros, N. E.

C. A. Curcio, N. E. Medeiros, and C. L. Millican, Invest. Ophthalmol. Vis. Sci. 37, 1236 (1996).
[PubMed]

Michel-Villaz, M.

H. Kuhn, N. Bennett, M. Michel-Villaz, and M. Chabre, Proc. Natl. Acad. Sci. USA 78, 6873 (1981).
[CrossRef] [PubMed]

Miller, D. T.

Millican, C. L.

C. A. Curcio, N. E. Medeiros, and C. L. Millican, Invest. Ophthalmol. Vis. Sci. 37, 1236 (1996).
[PubMed]

Miyake, Y.

G. Hanazono, K. Tsunoda, K. Shinoda, K. Tsubota, Y. Miyake, and M. Tanifuji, Invest. Ophthalmol. Vis. Sci. 48, 2903 (2007).
[CrossRef] [PubMed]

Montrone, L.

B. Falsini, D. Marangoni, T. Salgarello, G. Stifano, L. Montrone, F. Campagna, S. Aliberti, E. Balestrazzi, and A. Colotto, Graefes Arch. Clin. Exp. Ophthalmol. 246, 1153 (2008).
[CrossRef] [PubMed]

Nagy, D.

D. Nagy, B. Schonfisch, E. Zrenner, and H. Jagle, Invest. Ophthalmol. Vis. Sci. 49, 4664 (2008).
[CrossRef] [PubMed]

Nilsson, S. E.

S. E. Nilsson, J. Ultrastruct. Res. 10, 390 (1964).
[CrossRef] [PubMed]

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, Proc. Natl. Acad. Sci. USA 103, 5066 (2006).
[CrossRef] [PubMed]

Pierce, E. A.

S. G. Jacobson, A. V. Cideciyan, A. Iannaccone, R. G. Weleber, G. A. Fishman, A. M. Maguire, L. M. Affatigato, J. Bennett, E. A. Pierce, M. Danciger, D. B. Farber, and E. M. Stone, Invest. Ophthalmol. Vis. Sci. 41, 1898 (2000).
[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, Proc. Natl. Acad. Sci. USA 103, 5066 (2006).
[CrossRef] [PubMed]

Porciatti, V.

L. M. Ventura, N. Sorokac, R. De Los Santos, W. J. Feuer, and V. Porciatti, Invest. Ophthalmol. Vis. Sci. 47, 3904 (2006).
[CrossRef] [PubMed]

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, Proc. Natl. Acad. Sci. USA 103, 5066 (2006).
[CrossRef] [PubMed]

Pugh, E. N.

V. Y. Arshavsky, T. D. Lamb, and E. N. Pugh, Jr., Annu. Rev. Physiol. 64, 153 (2002).
[CrossRef] [PubMed]

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, Proc. Natl. Acad. Sci. USA 103, 5066 (2006).
[CrossRef] [PubMed]

Quigley, H. A.

H. A. Quigley, E. M. Addicks, and W. R. Green, Arch. Ophthalmol. 100, 135 (1982).
[CrossRef] [PubMed]

Rector, D. M.

A. J. Foust and D. M. Rector, Neuroscience 145, 887(2007).
[CrossRef] [PubMed]

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, Proc. Natl. Acad. Sci. USA 103, 5066 (2006).
[CrossRef] [PubMed]

Rha, J.

Roorda, A.

K. Grieve and A. Roorda, Invest. Ophthalmol. Vis. Sci. 49, 713 (2008).
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Figures (3)

Fig. 1
Fig. 1

Schematic diagram of line-scan confocal ophthalmoscope for reflected light IOS imaging: CO, collimator; CL, cylindrical lens; BS, beam splitter; SM, scanning mirror; DM, dichroic mirror; Lx, optical lenses. The NIR filter, in front of the linear CCD, was a long-pass filter that blocked visible stimulus light and transmitted NIR light reflected from the retina. The optical magnification of the system was estimated at 14 , corresponding to 1 μm / pixel in retinal image.

Fig. 2
Fig. 2

(a) Representative in vivo image ( 500 × 400 pixels) of frog retina. (b) Enlarged picture of the subimage ( 100 × 100 pixels) marked by the white square in (a). Individual blood vessels [white arrowheads in (a)] and photoreceptors [white arrowheads in (b)] were clearly observed.

Fig. 3
Fig. 3

(a) Representative spatial IOS image sequence. Each illustrated frame is an average over 100 ms interval (20 frames). The black arrowhead indicates the onset of the 10 ms green flash stimulus. 200 ms prestimulus baseline and 900 ms poststimulus IOS recordings are shown. (b) Representative IOS responses of individual pixels randomly selected from the image area. The gray bar indicates the stimulus onset and duration. (c) The top black trace shows the IOS magnitude (i.e., absolute value of the IOS) averaged over the whole image area, corresponding to the image sequence shown in (a). The gray trace shows one control experiment without stimulation. The black trace below shows concurrent frog ERG. The gray bar indicates the stimulus delivery.

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