Abstract

Understanding of visual signal processing can benefit from simultaneous measurement of different types of retinal neurons working together. In this Letter, we demonstrate that intrinsic optical signal (IOS) imaging of frog retina slices allows simultaneous observation of stimulus-evoked responses propagating from the photoreceptors to the inner neurons. High-resolution imaging revealed robust IOSs at the photoreceptor, the inner plexiform, and the ganglion cell layers. While IOSs of the photoreceptor layer were mainly confined to the area directly stimulated by the visible light, IOSs of the inner retinal layers spread from the stimulus site into relatively large areas with a characteristic near-to-far time course.

© 2010 Optical Society of America

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2010 (1)

2009 (2)

V. J. Srinivasan, Y. Chen, J. S. Duker, and J. G. Fujimoto, Opt. Express 17, 3861 (2009).
[CrossRef] [PubMed]

M. Wittmann, G. Queisser, A. Eder, J. S. Wiegert, C. P. Bengtson, A. Hellwig, G. Wittum, and H. Bading, J. Neurosci. 29, 14687 (2009).
[CrossRef] [PubMed]

2008 (1)

2006 (3)

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]

X. C. Yao and J. S. George, NeuroImage 33, 898 (2006).
[CrossRef] [PubMed]

C. Sekirnjak, P. Hottowy, A. Sher, W. Dabrowski, A. M. Litke, and E. J. Chichilnisky, J. Neurophysiol. 95, 3311(2006).
[CrossRef] [PubMed]

2005 (1)

2003 (1)

1993 (1)

S. M. Dawis and M. Rossetto, Visual Neurosci. 10, 687 (1993).
[CrossRef]

1992 (1)

I. Tasaki and P. M. Byrne, Biochem. Biophys. Res. Commun. 188, 559 (1992).
[CrossRef] [PubMed]

1988 (1)

D. R. Pepperberg, M. Kahlert, A. Krause, and K. P. Hofmann, Proc. Natl. Acad. Sci. USA 85, 5531 (1988).
[CrossRef] [PubMed]

1985 (1)

B. M. Salzberg, A. L. Obaid, and H. Gainer, J. Gen. Physiol. 86, 395 (1985).
[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, Proc. Natl. Acad. Sci. USA 103, 5066 (2006).
[CrossRef] [PubMed]

Amthor, F. R.

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]

Bading, H.

M. Wittmann, G. Queisser, A. Eder, J. S. Wiegert, C. P. Bengtson, A. Hellwig, G. Wittum, and H. Bading, J. Neurosci. 29, 14687 (2009).
[CrossRef] [PubMed]

Bengtson, C. P.

M. Wittmann, G. Queisser, A. Eder, J. S. Wiegert, C. P. Bengtson, A. Hellwig, G. Wittum, and H. Bading, J. Neurosci. 29, 14687 (2009).
[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).
[CrossRef] [PubMed]

Byrne, P. M.

I. Tasaki and P. M. Byrne, Biochem. Biophys. Res. Commun. 188, 559 (1992).
[CrossRef] [PubMed]

Chen, Y.

Chichilnisky, E. J.

C. Sekirnjak, P. Hottowy, A. Sher, W. Dabrowski, A. M. Litke, and E. J. Chichilnisky, J. Neurophysiol. 95, 3311(2006).
[CrossRef] [PubMed]

Dabrowski, W.

C. Sekirnjak, P. Hottowy, A. Sher, W. Dabrowski, A. M. Litke, and E. J. Chichilnisky, J. Neurophysiol. 95, 3311(2006).
[CrossRef] [PubMed]

Dawis, S. M.

S. M. Dawis and M. Rossetto, Visual Neurosci. 10, 687 (1993).
[CrossRef]

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.

Eder, A.

M. Wittmann, G. Queisser, A. Eder, J. S. Wiegert, C. P. Bengtson, A. Hellwig, G. Wittum, and H. Bading, J. Neurosci. 29, 14687 (2009).
[CrossRef] [PubMed]

Fujimoto, J. G.

Gainer, H.

B. M. Salzberg, A. L. Obaid, and H. Gainer, J. Gen. Physiol. 86, 395 (1985).
[CrossRef] [PubMed]

George, J. S.

Hellwig, A.

M. Wittmann, G. Queisser, A. Eder, J. S. Wiegert, C. P. Bengtson, A. Hellwig, G. Wittum, and H. Bading, J. Neurosci. 29, 14687 (2009).
[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]

Hofmann, K. P.

D. R. Pepperberg, M. Kahlert, A. Krause, and K. P. Hofmann, Proc. Natl. Acad. Sci. USA 85, 5531 (1988).
[CrossRef] [PubMed]

Hottowy, P.

C. Sekirnjak, P. Hottowy, A. Sher, W. Dabrowski, A. M. Litke, and E. J. Chichilnisky, J. Neurophysiol. 95, 3311(2006).
[CrossRef] [PubMed]

Kahlert, M.

D. R. Pepperberg, M. Kahlert, A. Krause, and K. P. Hofmann, Proc. Natl. Acad. Sci. USA 85, 5531 (1988).
[CrossRef] [PubMed]

Krause, A.

D. R. Pepperberg, M. Kahlert, A. Krause, and K. P. Hofmann, Proc. Natl. Acad. Sci. USA 85, 5531 (1988).
[CrossRef] [PubMed]

Li, Y. G.

Litke, A. M.

C. Sekirnjak, P. Hottowy, A. Sher, W. Dabrowski, A. M. Litke, and E. J. Chichilnisky, J. Neurophysiol. 95, 3311(2006).
[CrossRef] [PubMed]

Liu, L.

Obaid, A. L.

B. M. Salzberg, A. L. Obaid, and H. Gainer, J. Gen. Physiol. 86, 395 (1985).
[CrossRef] [PubMed]

Pepperberg, D. R.

D. R. Pepperberg, M. Kahlert, A. Krause, and K. P. Hofmann, Proc. Natl. Acad. Sci. USA 85, 5531 (1988).
[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]

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]

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]

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]

Queisser, G.

M. Wittmann, G. Queisser, A. Eder, J. S. Wiegert, C. P. Bengtson, A. Hellwig, G. Wittum, and H. Bading, J. Neurosci. 29, 14687 (2009).
[CrossRef] [PubMed]

Rector, D. M.

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]

Rossetto, M.

S. M. Dawis and M. Rossetto, Visual Neurosci. 10, 687 (1993).
[CrossRef]

Salzberg, B. M.

B. M. Salzberg, A. L. Obaid, and H. Gainer, J. Gen. Physiol. 86, 395 (1985).
[CrossRef] [PubMed]

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

Sekirnjak, C.

C. Sekirnjak, P. Hottowy, A. Sher, W. Dabrowski, A. M. Litke, and E. J. Chichilnisky, J. Neurophysiol. 95, 3311(2006).
[CrossRef] [PubMed]

Sher, A.

C. Sekirnjak, P. Hottowy, A. Sher, W. Dabrowski, A. M. Litke, and E. J. Chichilnisky, J. Neurophysiol. 95, 3311(2006).
[CrossRef] [PubMed]

Srinivasan, V. J.

Tasaki, I.

I. Tasaki and P. M. Byrne, Biochem. Biophys. Res. Commun. 188, 559 (1992).
[CrossRef] [PubMed]

Taylor, J. 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]

Unterhuber, A.

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]

Wiegert, J. S.

M. Wittmann, G. Queisser, A. Eder, J. S. Wiegert, C. P. Bengtson, A. Hellwig, G. Wittum, and H. Bading, J. Neurosci. 29, 14687 (2009).
[CrossRef] [PubMed]

Wittmann, M.

M. Wittmann, G. Queisser, A. Eder, J. S. Wiegert, C. P. Bengtson, A. Hellwig, G. Wittum, and H. Bading, J. Neurosci. 29, 14687 (2009).
[CrossRef] [PubMed]

Wittum, G.

M. Wittmann, G. Queisser, A. Eder, J. S. Wiegert, C. P. Bengtson, A. Hellwig, G. Wittum, and H. Bading, J. Neurosci. 29, 14687 (2009).
[CrossRef] [PubMed]

Yamauchi, A.

Yao, X. C.

Zhang, Q. X.

Zhao, Y. B.

Appl. Opt. (2)

Biochem. Biophys. Res. Commun. (1)

I. Tasaki and P. M. Byrne, Biochem. Biophys. Res. Commun. 188, 559 (1992).
[CrossRef] [PubMed]

J. Gen. Physiol. (1)

B. M. Salzberg, A. L. Obaid, and H. Gainer, J. Gen. Physiol. 86, 395 (1985).
[CrossRef] [PubMed]

J. Neurophysiol. (1)

C. Sekirnjak, P. Hottowy, A. Sher, W. Dabrowski, A. M. Litke, and E. J. Chichilnisky, J. Neurophysiol. 95, 3311(2006).
[CrossRef] [PubMed]

J. Neurosci. (1)

M. Wittmann, G. Queisser, A. Eder, J. S. Wiegert, C. P. Bengtson, A. Hellwig, G. Wittum, and H. Bading, J. Neurosci. 29, 14687 (2009).
[CrossRef] [PubMed]

NeuroImage (1)

X. C. Yao and J. S. George, NeuroImage 33, 898 (2006).
[CrossRef] [PubMed]

Opt. Express (3)

Proc. Natl. Acad. Sci. USA (2)

K. Bizheva, R. Pflug, B. Hermann, B. Povazay, H. Sattmann, P. Qiu, E. Anger, H. Reitsamer, S. Popov, J. R. Taylor, A. Unterhuber, P. Ahnelt, and W. Drexler, Proc. Natl. Acad. Sci. USA 103, 5066 (2006).
[CrossRef] [PubMed]

D. R. Pepperberg, M. Kahlert, A. Krause, and K. P. Hofmann, Proc. Natl. Acad. Sci. USA 85, 5531 (1988).
[CrossRef] [PubMed]

Visual Neurosci. (1)

S. M. Dawis and M. Rossetto, Visual Neurosci. 10, 687 (1993).
[CrossRef]

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Figures (3)

Fig. 1
Fig. 1

Schematic diagram of experimental setup. During the measurement, the retinal slice was continuously illuminated by the NIR light for recording of stimulus-evoked IOSs, while the collimated visible light stimulator with a square aperture was used for retinal stimulation. At the dichroic mirror (DM), visible stimulus light was reflected and NIR recording light was passed through. The NIR filter was used to block visible stimulus light and allow the NIR probe light to reach the CMOS camera. A 10 × system magnification, from the retina to the camera, was used for this study.

Fig. 2
Fig. 2

A, representative raw image sequence of the retinal slice before differential processing. B, IOS image sequence. The raw CMOS images were recorded with a speed of 500 frame / s . Each illustrated frame is an average over a 200 ms interval (100 frames). The IOS images were reconstructed by processing the raw images as follows: (1) the prestimulus baseline images were averaged, pixel by pixel, and was taken as the background light intensity, I, of each pixel; (2) the background light intensity was subtracted from each recorded frame sequentially, pixel by pixel, to get the dynamic optical response, Δ I , of each pixel of the images; and (3) the image sequence of Δ I / I was constructed to show the dynamic intrinsic optical changes of the retina activated by a visible light stimulus. C, enlarged image of the fifth frame in A. D, enlarged image of the fifth frame in B. The white square indicates the visible light stimulus aperture. The two lower arrowheads point to the somas of two ganglion cells (GC1 and GC2) The two upper arrowheads point to the IOSs between the photoreceptor and the IPL.

Fig. 3
Fig. 3

A and B show enlarged raw and IOS images of the area marked by the white square in Fig. 2C. C, statistics of positive and negative signals over the retinal slice shown in B. D and E are spatiotemporal images of the line areas 1 and 2 in B. F, averaged spatiotemporal image of the retinal slice shown in B. At each time point (i.e., each frame), the IOSs were averaged in the lateral direction and, thus, a two- dimensional IOS image, such as B, was condensed to a one- dimensional vertical line in the spatiotemporal image of F. In D, E, and F, the vertical solid and dashed lines indicate the onset and offset of the visible light stimulus.

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