Abstract

Functional measurement is important for retinal study and disease diagnosis. Transient intrinsic optical signal (IOS) response, tightly correlated with functional stimulation, has been previously detected in normal retinas. In this paper, comparative IOS imaging of wild-type (WT) and rod-degenerated mutant mouse retinas is reported. Both 2-month and 1-year-old mice were measured. In 2-month-old mutant mice, time course and peak value of the stimulus-evoked IOS were significantly delayed (relative to stimulus onset) and reduced, respectively, compared to age matched WT mice. In 1-year-old mutant mice, stimulus-evoked IOS was totally absent. However, enhanced spontaneous IOS responses, which might reflect inner neural remodeling in diseased retina, were observed in both 2-month and 1-year-old mutant retinas. Our experiments demonstrate the potential of using IOS imaging for noninvasive and high resolution identification of disease-associated retinal dysfunctions. Moreover, high spatiotemporal resolution IOS imaging may also lead to advanced understanding of disease-associated neural remodeling in the retina.

© 2012 OSA

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    [CrossRef] [PubMed]
  26. K. P. Hofmann, R. Uhl, W. Hoffmann, 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]
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    [CrossRef] [PubMed]
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    [CrossRef] [PubMed]
  29. X. C. Yao, D. M. Rector, J. S. George, “Optical lever recording of displacements from activated lobster nerve bundles and Nitella internodes,” Appl. Opt. 42(16), 2972–2978 (2003).
    [CrossRef] [PubMed]
  30. I. Tasaki, P. M. Byrne, “Rapid structural changes in nerve fibers evoked by electric current pulses,” Biochem. Biophys. Res. Commun. 188(2), 559–564 (1992).
    [CrossRef] [PubMed]
  31. G. H. Kim, P. Kosterin, A. L. Obaid, B. M. Salzberg, “A mechanical spike accompanies the action potential in Mammalian nerve terminals,” Biophys. J. 92(9), 3122–3129 (2007).
    [CrossRef] [PubMed]
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    [PubMed]
  33. R. E. Marc, B. W. Jones, C. B. Watt, E. Strettoi, “Neural remodeling in retinal degeneration,” Prog. Retin. Eye Res. 22(5), 607–655 (2003).
    [CrossRef] [PubMed]
  34. S. F. Stasheff, “Emergence of sustained spontaneous hyperactivity and temporary preservation of OFF responses in ganglion cells of the retinal degeneration (rd1) mouse,” J. Neurophysiol. 99(3), 1408–1421 (2008).
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    [CrossRef] [PubMed]

2011

X. Huang, W. Kong, Y. Zhou, G. Gregori, “Distortion of axonal cytoskeleton: an early sign of glaucomatous damage,” Invest. Ophthalmol. Vis. Sci. 52(6), 2879–2888 (2011).
[CrossRef] [PubMed]

J. Borowska, S. Trenholm, G. B. Awatramani, “An intrinsic neural oscillator in the degenerating mouse retina,” J. Neurosci. 31(13), 5000–5012 (2011).
[CrossRef] [PubMed]

T. Theelen, C. B. Hoyng, B. J. Klevering, and C. B, “Functional imaging of inherited retinal disease with a commercial optical coherence tomography,” Proc. SPIE 8091, 8009110–8009118 (2011).

Y. C. Li, W. X. Cui, X. J. Wang, F. Amthor, R. W. Lu, A. Thompson, X. C. Yao, “Intrinsic optical signal imaging of glucose-stimulated insulin secreting β-cells,” Opt. Express 19(1), 99–106 (2011).
[CrossRef] [PubMed]

Q.-X. Zhang, R.-W. Lu, Y.-G. Li, 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]

2010

2009

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

Y. Zhang, L. L. Molday, R. S. Molday, S. S. Sarfare, M. L. Woodruff, G. L. Fain, T. W. Kraft, S. J. Pittler, “Knockout of GARPs and the β-subunit of the rod cGMP-gated channel disrupts disk morphogenesis and rod outer segment structural integrity,” J. Cell Sci. 122(8), 1192–1200 (2009).
[CrossRef] [PubMed]

X. C. Yao, L. Liu, Y. G. Li, “Intrinsic optical signal imaging of retinal activity in frog eye,” J Innov Opt Health Sci 2(02), 201–208 (2009).
[CrossRef]

J. Schallek, H. Li, R. Kardon, Y. Kwon, M. Abramoff, P. Soliz, D. Ts’o, “Stimulus-evoked intrinsic optical signals in the retina: spatial and temporal characteristics,” Invest. Ophthalmol. Vis. Sci. 50(10), 4865–4872 (2009).
[CrossRef] [PubMed]

2008

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

S. F. Stasheff, “Emergence of sustained spontaneous hyperactivity and temporary preservation of OFF responses in ganglion cells of the retinal degeneration (rd1) mouse,” J. Neurophysiol. 99(3), 1408–1421 (2008).
[CrossRef] [PubMed]

X. C. Yao, Y. B. Zhao, “Optical dissection of stimulus-evoked retinal activation,” Opt. Express 16(17), 12446–12459 (2008).
[CrossRef] [PubMed]

2007

R. S. Jonnal, J. Rha, Y. Zhang, B. Cense, W. H. Gao, D. T. Miller, “In vivo functional imaging of human cone photoreceptors,” Opt. Express 15(24), 16141–16160 (2007).
[CrossRef] [PubMed]

G. H. Kim, P. Kosterin, A. L. Obaid, B. M. Salzberg, “A mechanical spike accompanies the action potential in Mammalian nerve terminals,” Biophys. J. 92(9), 3122–3129 (2007).
[CrossRef] [PubMed]

C. Gargini, E. Terzibasi, F. Mazzoni, E. Strettoi, “Retinal organization in the retinal degeneration 10 (rd10) mutant mouse: a morphological and ERG study,” J. Comp. Neurol. 500(2), 222–238 (2007).
[CrossRef] [PubMed]

2006

Y. W. Qin, G. Z. Xu, W. J. Wang, “Dendritic abnormalities in retinal ganglion cells of three-month diabetic rats,” Curr. Eye Res. 31(11), 967–974 (2006).
[CrossRef] [PubMed]

X. C. Yao, J. S. George, “Dynamic neuroimaging of retinal light responses using fast intrinsic optical signals,” Neuroimage 33(3), 898–906 (2006).
[CrossRef] [PubMed]

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

2005

2003

2002

V. Y. Arshavsky, T. D. Lamb, E. N. Pugh., “G proteins and phototransduction,” Annu. Rev. Physiol. 64(1), 153–187 (2002).
[CrossRef] [PubMed]

2001

M. Haller, S. L. Mironov, D. W. Richter, “Intrinsic optical signals in respiratory brain stem regions of mice: neurotransmitters, neuromodulators, and metabolic stress,” J. Neurophysiol. 86(1), 412–421 (2001).
[PubMed]

2000

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

D. C. Hood, “Assessing retinal function with the multifocal technique,” Prog. Retin. Eye Res. 19(5), 607–646 (2000).
[CrossRef] [PubMed]

1999

R. D. Andrew, C. R. Jarvis, A. S. Obeidat, “Potential sources of intrinsic optical signals imaged in live brain slices,” Methods 18(2), 185–196, 179 (1999).
[CrossRef] [PubMed]

1998

K. Holthoff, O. W. Witte, “Intrinsic optical signals in vitro: a tool to measure alterations in extracellular space with two-dimensional resolution,” Brain Res. Bull. 47(6), 649–655 (1998).
[CrossRef] [PubMed]

1996

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

1992

I. Tasaki, P. M. Byrne, “Rapid structural changes in nerve fibers evoked by electric current pulses,” Biochem. Biophys. Res. Commun. 188(2), 559–564 (1992).
[CrossRef] [PubMed]

1981

H. Kühn, N. Bennett, M. Michel-Villaz, 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

K. P. Hofmann, R. Uhl, W. Hoffmann, 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]

1973

L. B. Cohen, “Changes in neuron structure during action potential propagation and synaptic transmission,” Physiol. Rev. 53(2), 373–418 (1973).
[PubMed]

1946

G. L. Kesteven, “The coefficient of variation,” Nature 158(4015), 520–521 (1946).
[CrossRef] [PubMed]

Abramoff, M.

J. Schallek, H. Li, R. Kardon, Y. Kwon, M. Abramoff, P. Soliz, D. Ts’o, “Stimulus-evoked intrinsic optical signals in the retina: spatial and temporal characteristics,” Invest. Ophthalmol. Vis. Sci. 50(10), 4865–4872 (2009).
[CrossRef] [PubMed]

Amthor, F.

Amthor, F. R.

Andrew, R. D.

R. D. Andrew, C. R. Jarvis, A. S. Obeidat, “Potential sources of intrinsic optical signals imaged in live brain slices,” Methods 18(2), 185–196, 179 (1999).
[CrossRef] [PubMed]

Arshavsky, V. Y.

V. Y. Arshavsky, T. D. Lamb, E. N. Pugh., “G proteins and phototransduction,” Annu. Rev. Physiol. 64(1), 153–187 (2002).
[CrossRef] [PubMed]

Awatramani, G. B.

J. Borowska, S. Trenholm, G. B. Awatramani, “An intrinsic neural oscillator in the degenerating mouse retina,” J. Neurosci. 31(13), 5000–5012 (2011).
[CrossRef] [PubMed]

Bennett, N.

H. Kühn, N. Bennett, M. Michel-Villaz, 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]

Borowska, J.

J. Borowska, S. Trenholm, G. B. Awatramani, “An intrinsic neural oscillator in the degenerating mouse retina,” J. Neurosci. 31(13), 5000–5012 (2011).
[CrossRef] [PubMed]

Byrne, P. M.

I. Tasaki, P. M. Byrne, “Rapid structural changes in nerve fibers evoked by electric current pulses,” Biochem. Biophys. Res. Commun. 188(2), 559–564 (1992).
[CrossRef] [PubMed]

Cense, B.

Chabre, M.

H. Kühn, N. Bennett, M. Michel-Villaz, 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]

Chen, Y.

Cohen, L. B.

L. B. Cohen, “Changes in neuron structure during action potential propagation and synaptic transmission,” Physiol. Rev. 53(2), 373–418 (1973).
[PubMed]

Cui, W. X.

Curcio, C. A.

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

Duker, J. S.

Fain, G. L.

Y. Zhang, L. L. Molday, R. S. Molday, S. S. Sarfare, M. L. Woodruff, G. L. Fain, T. W. Kraft, S. J. Pittler, “Knockout of GARPs and the β-subunit of the rod cGMP-gated channel disrupts disk morphogenesis and rod outer segment structural integrity,” J. Cell Sci. 122(8), 1192–1200 (2009).
[CrossRef] [PubMed]

Fujimoto, J. G.

Gao, W. H.

Gargini, C.

C. Gargini, E. Terzibasi, F. Mazzoni, E. Strettoi, “Retinal organization in the retinal degeneration 10 (rd10) mutant mouse: a morphological and ERG study,” J. Comp. Neurol. 500(2), 222–238 (2007).
[CrossRef] [PubMed]

George, J. S.

X. C. Yao, J. S. George, “Dynamic neuroimaging of retinal light responses using fast intrinsic optical signals,” Neuroimage 33(3), 898–906 (2006).
[CrossRef] [PubMed]

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

X. C. Yao, A. Yamauchi, B. Perry, J. S. George, “Rapid optical coherence tomography and recording functional scattering changes from activated frog retina,” Appl. Opt. 44(11), 2019–2023 (2005).
[CrossRef] [PubMed]

X. C. Yao, D. M. Rector, J. S. George, “Optical lever recording of displacements from activated lobster nerve bundles and Nitella internodes,” Appl. Opt. 42(16), 2972–2978 (2003).
[CrossRef] [PubMed]

Gregori, G.

X. Huang, W. Kong, Y. Zhou, G. Gregori, “Distortion of axonal cytoskeleton: an early sign of glaucomatous damage,” Invest. Ophthalmol. Vis. Sci. 52(6), 2879–2888 (2011).
[CrossRef] [PubMed]

Haller, M.

M. Haller, S. L. Mironov, D. W. Richter, “Intrinsic optical signals in respiratory brain stem regions of mice: neurotransmitters, neuromodulators, and metabolic stress,” J. Neurophysiol. 86(1), 412–421 (2001).
[PubMed]

Hoffmann, W.

K. P. Hofmann, R. Uhl, W. Hoffmann, 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.

K. P. Hofmann, R. Uhl, W. Hoffmann, 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]

Holthoff, K.

K. Holthoff, O. W. Witte, “Intrinsic optical signals in vitro: a tool to measure alterations in extracellular space with two-dimensional resolution,” Brain Res. Bull. 47(6), 649–655 (1998).
[CrossRef] [PubMed]

Hood, D. C.

D. C. Hood, “Assessing retinal function with the multifocal technique,” Prog. Retin. Eye Res. 19(5), 607–646 (2000).
[CrossRef] [PubMed]

Hoyng, C. B.

T. Theelen, C. B. Hoyng, B. J. Klevering, and C. B, “Functional imaging of inherited retinal disease with a commercial optical coherence tomography,” Proc. SPIE 8091, 8009110–8009118 (2011).

Huang, X.

X. Huang, W. Kong, Y. Zhou, G. Gregori, “Distortion of axonal cytoskeleton: an early sign of glaucomatous damage,” Invest. Ophthalmol. Vis. Sci. 52(6), 2879–2888 (2011).
[CrossRef] [PubMed]

Jägle, H.

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

Jarvis, C. R.

R. D. Andrew, C. R. Jarvis, A. S. Obeidat, “Potential sources of intrinsic optical signals imaged in live brain slices,” Methods 18(2), 185–196, 179 (1999).
[CrossRef] [PubMed]

Jones, B. W.

R. E. Marc, B. W. Jones, C. B. Watt, E. Strettoi, “Neural remodeling in retinal degeneration,” Prog. Retin. Eye Res. 22(5), 607–655 (2003).
[CrossRef] [PubMed]

Jonnal, R. S.

Kardon, R.

J. Schallek, H. Li, R. Kardon, Y. Kwon, M. Abramoff, P. Soliz, D. Ts’o, “Stimulus-evoked intrinsic optical signals in the retina: spatial and temporal characteristics,” Invest. Ophthalmol. Vis. Sci. 50(10), 4865–4872 (2009).
[CrossRef] [PubMed]

Kesteven, G. L.

G. L. Kesteven, “The coefficient of variation,” Nature 158(4015), 520–521 (1946).
[CrossRef] [PubMed]

Kim, G. H.

G. H. Kim, P. Kosterin, A. L. Obaid, B. M. Salzberg, “A mechanical spike accompanies the action potential in Mammalian nerve terminals,” Biophys. J. 92(9), 3122–3129 (2007).
[CrossRef] [PubMed]

Klevering, B. J.

T. Theelen, C. B. Hoyng, B. J. Klevering, and C. B, “Functional imaging of inherited retinal disease with a commercial optical coherence tomography,” Proc. SPIE 8091, 8009110–8009118 (2011).

Kong, W.

X. Huang, W. Kong, Y. Zhou, G. Gregori, “Distortion of axonal cytoskeleton: an early sign of glaucomatous damage,” Invest. Ophthalmol. Vis. Sci. 52(6), 2879–2888 (2011).
[CrossRef] [PubMed]

Kosterin, P.

G. H. Kim, P. Kosterin, A. L. Obaid, B. M. Salzberg, “A mechanical spike accompanies the action potential in Mammalian nerve terminals,” Biophys. J. 92(9), 3122–3129 (2007).
[CrossRef] [PubMed]

Kraft, T. W.

Y. Zhang, L. L. Molday, R. S. Molday, S. S. Sarfare, M. L. Woodruff, G. L. Fain, T. W. Kraft, S. J. Pittler, “Knockout of GARPs and the β-subunit of the rod cGMP-gated channel disrupts disk morphogenesis and rod outer segment structural integrity,” J. Cell Sci. 122(8), 1192–1200 (2009).
[CrossRef] [PubMed]

Kreutz, W.

K. P. Hofmann, R. Uhl, W. Hoffmann, 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, 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]

Kwon, Y.

J. Schallek, H. Li, R. Kardon, Y. Kwon, M. Abramoff, P. Soliz, D. Ts’o, “Stimulus-evoked intrinsic optical signals in the retina: spatial and temporal characteristics,” Invest. Ophthalmol. Vis. Sci. 50(10), 4865–4872 (2009).
[CrossRef] [PubMed]

Lamb, T. D.

V. Y. Arshavsky, T. D. Lamb, E. N. Pugh., “G proteins and phototransduction,” Annu. Rev. Physiol. 64(1), 153–187 (2002).
[CrossRef] [PubMed]

Li, H.

J. Schallek, H. Li, R. Kardon, Y. Kwon, M. Abramoff, P. Soliz, D. Ts’o, “Stimulus-evoked intrinsic optical signals in the retina: spatial and temporal characteristics,” Invest. Ophthalmol. Vis. Sci. 50(10), 4865–4872 (2009).
[CrossRef] [PubMed]

Li, Y. C.

Li, Y. G.

Li, Y.-G.

Liu, L.

Lu, R. W.

Lu, R.-W.

Marc, R. E.

R. E. Marc, B. W. Jones, C. B. Watt, E. Strettoi, “Neural remodeling in retinal degeneration,” Prog. Retin. Eye Res. 22(5), 607–655 (2003).
[CrossRef] [PubMed]

Mazzoni, F.

C. Gargini, E. Terzibasi, F. Mazzoni, E. Strettoi, “Retinal organization in the retinal degeneration 10 (rd10) mutant mouse: a morphological and ERG study,” J. Comp. Neurol. 500(2), 222–238 (2007).
[CrossRef] [PubMed]

Medeiros, N. E.

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

Michel-Villaz, M.

H. Kühn, N. Bennett, M. Michel-Villaz, 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]

Miller, D. T.

Millican, C. L.

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

Mironov, S. L.

M. Haller, S. L. Mironov, D. W. Richter, “Intrinsic optical signals in respiratory brain stem regions of mice: neurotransmitters, neuromodulators, and metabolic stress,” J. Neurophysiol. 86(1), 412–421 (2001).
[PubMed]

Molday, L. L.

Y. Zhang, L. L. Molday, R. S. Molday, S. S. Sarfare, M. L. Woodruff, G. L. Fain, T. W. Kraft, S. J. Pittler, “Knockout of GARPs and the β-subunit of the rod cGMP-gated channel disrupts disk morphogenesis and rod outer segment structural integrity,” J. Cell Sci. 122(8), 1192–1200 (2009).
[CrossRef] [PubMed]

Molday, R. S.

Y. Zhang, L. L. Molday, R. S. Molday, S. S. Sarfare, M. L. Woodruff, G. L. Fain, T. W. Kraft, S. J. Pittler, “Knockout of GARPs and the β-subunit of the rod cGMP-gated channel disrupts disk morphogenesis and rod outer segment structural integrity,” J. Cell Sci. 122(8), 1192–1200 (2009).
[CrossRef] [PubMed]

Nagy, D.

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

Obaid, A. L.

G. H. Kim, P. Kosterin, A. L. Obaid, B. M. Salzberg, “A mechanical spike accompanies the action potential in Mammalian nerve terminals,” Biophys. J. 92(9), 3122–3129 (2007).
[CrossRef] [PubMed]

Obeidat, A. S.

R. D. Andrew, C. R. Jarvis, A. S. Obeidat, “Potential sources of intrinsic optical signals imaged in live brain slices,” Methods 18(2), 185–196, 179 (1999).
[CrossRef] [PubMed]

Perry, B.

Pittler, S. J.

Y. Zhang, L. L. Molday, R. S. Molday, S. S. Sarfare, M. L. Woodruff, G. L. Fain, T. W. Kraft, S. J. Pittler, “Knockout of GARPs and the β-subunit of the rod cGMP-gated channel disrupts disk morphogenesis and rod outer segment structural integrity,” J. Cell Sci. 122(8), 1192–1200 (2009).
[CrossRef] [PubMed]

Pugh, E. N.

V. Y. Arshavsky, T. D. Lamb, E. N. Pugh., “G proteins and phototransduction,” Annu. Rev. Physiol. 64(1), 153–187 (2002).
[CrossRef] [PubMed]

Qin, Y. W.

Y. W. Qin, G. Z. Xu, W. J. Wang, “Dendritic abnormalities in retinal ganglion cells of three-month diabetic rats,” Curr. Eye Res. 31(11), 967–974 (2006).
[CrossRef] [PubMed]

Rector, D. M.

Rha, J.

Richter, D. W.

M. Haller, S. L. Mironov, D. W. Richter, “Intrinsic optical signals in respiratory brain stem regions of mice: neurotransmitters, neuromodulators, and metabolic stress,” J. Neurophysiol. 86(1), 412–421 (2001).
[PubMed]

Salzberg, B. M.

G. H. Kim, P. Kosterin, A. L. Obaid, B. M. Salzberg, “A mechanical spike accompanies the action potential in Mammalian nerve terminals,” Biophys. J. 92(9), 3122–3129 (2007).
[CrossRef] [PubMed]

Sarfare, S. S.

Y. Zhang, L. L. Molday, R. S. Molday, S. S. Sarfare, M. L. Woodruff, G. L. Fain, T. W. Kraft, S. J. Pittler, “Knockout of GARPs and the β-subunit of the rod cGMP-gated channel disrupts disk morphogenesis and rod outer segment structural integrity,” J. Cell Sci. 122(8), 1192–1200 (2009).
[CrossRef] [PubMed]

Schallek, J.

J. Schallek, H. Li, R. Kardon, Y. Kwon, M. Abramoff, P. Soliz, D. Ts’o, “Stimulus-evoked intrinsic optical signals in the retina: spatial and temporal characteristics,” Invest. Ophthalmol. Vis. Sci. 50(10), 4865–4872 (2009).
[CrossRef] [PubMed]

Scholl, H. P.

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

Schönfisch, B.

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

Soliz, P.

J. Schallek, H. Li, R. Kardon, Y. Kwon, M. Abramoff, P. Soliz, D. Ts’o, “Stimulus-evoked intrinsic optical signals in the retina: spatial and temporal characteristics,” Invest. Ophthalmol. Vis. Sci. 50(10), 4865–4872 (2009).
[CrossRef] [PubMed]

Srinivasan, V. J.

Stasheff, S. F.

S. F. Stasheff, “Emergence of sustained spontaneous hyperactivity and temporary preservation of OFF responses in ganglion cells of the retinal degeneration (rd1) mouse,” J. Neurophysiol. 99(3), 1408–1421 (2008).
[CrossRef] [PubMed]

Strettoi, E.

C. Gargini, E. Terzibasi, F. Mazzoni, E. Strettoi, “Retinal organization in the retinal degeneration 10 (rd10) mutant mouse: a morphological and ERG study,” J. Comp. Neurol. 500(2), 222–238 (2007).
[CrossRef] [PubMed]

R. E. Marc, B. W. Jones, C. B. Watt, E. Strettoi, “Neural remodeling in retinal degeneration,” Prog. Retin. Eye Res. 22(5), 607–655 (2003).
[CrossRef] [PubMed]

Tasaki, I.

I. Tasaki, P. M. Byrne, “Rapid structural changes in nerve fibers evoked by electric current pulses,” Biochem. Biophys. Res. Commun. 188(2), 559–564 (1992).
[CrossRef] [PubMed]

Terzibasi, E.

C. Gargini, E. Terzibasi, F. Mazzoni, E. Strettoi, “Retinal organization in the retinal degeneration 10 (rd10) mutant mouse: a morphological and ERG study,” J. Comp. Neurol. 500(2), 222–238 (2007).
[CrossRef] [PubMed]

Theelen, T.

T. Theelen, C. B. Hoyng, B. J. Klevering, and C. B, “Functional imaging of inherited retinal disease with a commercial optical coherence tomography,” Proc. SPIE 8091, 8009110–8009118 (2011).

Thompson, A.

Trenholm, S.

J. Borowska, S. Trenholm, G. B. Awatramani, “An intrinsic neural oscillator in the degenerating mouse retina,” J. Neurosci. 31(13), 5000–5012 (2011).
[CrossRef] [PubMed]

Ts’o, D.

J. Schallek, H. Li, R. Kardon, Y. Kwon, M. Abramoff, P. Soliz, D. Ts’o, “Stimulus-evoked intrinsic optical signals in the retina: spatial and temporal characteristics,” Invest. Ophthalmol. Vis. Sci. 50(10), 4865–4872 (2009).
[CrossRef] [PubMed]

Uhl, R.

K. P. Hofmann, R. Uhl, W. Hoffmann, 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]

Wang, J. Y.

Wang, W. J.

Y. W. Qin, G. Z. Xu, W. J. Wang, “Dendritic abnormalities in retinal ganglion cells of three-month diabetic rats,” Curr. Eye Res. 31(11), 967–974 (2006).
[CrossRef] [PubMed]

Wang, X. J.

Watt, C. B.

R. E. Marc, B. W. Jones, C. B. Watt, E. Strettoi, “Neural remodeling in retinal degeneration,” Prog. Retin. Eye Res. 22(5), 607–655 (2003).
[CrossRef] [PubMed]

Witte, O. W.

K. Holthoff, O. W. Witte, “Intrinsic optical signals in vitro: a tool to measure alterations in extracellular space with two-dimensional resolution,” Brain Res. Bull. 47(6), 649–655 (1998).
[CrossRef] [PubMed]

Woodruff, M. L.

Y. Zhang, L. L. Molday, R. S. Molday, S. S. Sarfare, M. L. Woodruff, G. L. Fain, T. W. Kraft, S. J. Pittler, “Knockout of GARPs and the β-subunit of the rod cGMP-gated channel disrupts disk morphogenesis and rod outer segment structural integrity,” J. Cell Sci. 122(8), 1192–1200 (2009).
[CrossRef] [PubMed]

Xu, G. Z.

Y. W. Qin, G. Z. Xu, W. J. Wang, “Dendritic abnormalities in retinal ganglion cells of three-month diabetic rats,” Curr. Eye Res. 31(11), 967–974 (2006).
[CrossRef] [PubMed]

Yamauchi, A.

Yao, X. C.

Y. C. Li, W. X. Cui, X. J. Wang, F. Amthor, R. W. Lu, A. Thompson, X. C. Yao, “Intrinsic optical signal imaging of glucose-stimulated insulin secreting β-cells,” Opt. Express 19(1), 99–106 (2011).
[CrossRef] [PubMed]

Q. X. Zhang, J. Y. Wang, L. Liu, X. C. Yao, “Microlens array recording of localized retinal responses,” Opt. Lett. 35(22), 3838–3840 (2010).
[CrossRef] [PubMed]

Y. G. Li, Q. X. Zhang, L. Liu, F. R. Amthor, X. C. Yao, “High spatiotemporal resolution imaging of fast intrinsic optical signals activated by retinal flicker stimulation,” Opt. Express 18(7), 7210–7218 (2010).
[CrossRef] [PubMed]

X. C. Yao, L. Liu, Y. G. Li, “Intrinsic optical signal imaging of retinal activity in frog eye,” J Innov Opt Health Sci 2(02), 201–208 (2009).
[CrossRef]

X. C. Yao, Y. B. Zhao, “Optical dissection of stimulus-evoked retinal activation,” Opt. Express 16(17), 12446–12459 (2008).
[CrossRef] [PubMed]

X. C. Yao, J. S. George, “Dynamic neuroimaging of retinal light responses using fast intrinsic optical signals,” Neuroimage 33(3), 898–906 (2006).
[CrossRef] [PubMed]

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

X. C. Yao, A. Yamauchi, B. Perry, J. S. George, “Rapid optical coherence tomography and recording functional scattering changes from activated frog retina,” Appl. Opt. 44(11), 2019–2023 (2005).
[CrossRef] [PubMed]

X. C. Yao, D. M. Rector, J. S. George, “Optical lever recording of displacements from activated lobster nerve bundles and Nitella internodes,” Appl. Opt. 42(16), 2972–2978 (2003).
[CrossRef] [PubMed]

Yao, X.-C.

Zhang, Q. X.

Zhang, Q.-X.

Zhang, Y.

Y. Zhang, L. L. Molday, R. S. Molday, S. S. Sarfare, M. L. Woodruff, G. L. Fain, T. W. Kraft, S. J. Pittler, “Knockout of GARPs and the β-subunit of the rod cGMP-gated channel disrupts disk morphogenesis and rod outer segment structural integrity,” J. Cell Sci. 122(8), 1192–1200 (2009).
[CrossRef] [PubMed]

R. S. Jonnal, J. Rha, Y. Zhang, B. Cense, W. H. Gao, D. T. Miller, “In vivo functional imaging of human cone photoreceptors,” Opt. Express 15(24), 16141–16160 (2007).
[CrossRef] [PubMed]

Zhao, Y. B.

Zhou, Y.

X. Huang, W. Kong, Y. Zhou, G. Gregori, “Distortion of axonal cytoskeleton: an early sign of glaucomatous damage,” Invest. Ophthalmol. Vis. Sci. 52(6), 2879–2888 (2011).
[CrossRef] [PubMed]

Zrenner, E.

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

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

Annu. Rev. Physiol.

V. Y. Arshavsky, T. D. Lamb, E. N. Pugh., “G proteins and phototransduction,” Annu. Rev. Physiol. 64(1), 153–187 (2002).
[CrossRef] [PubMed]

Appl. Opt.

Biochem. Biophys. Res. Commun.

I. Tasaki, P. M. Byrne, “Rapid structural changes in nerve fibers evoked by electric current pulses,” Biochem. Biophys. Res. Commun. 188(2), 559–564 (1992).
[CrossRef] [PubMed]

Biophys. J.

G. H. Kim, P. Kosterin, A. L. Obaid, B. M. Salzberg, “A mechanical spike accompanies the action potential in Mammalian nerve terminals,” Biophys. J. 92(9), 3122–3129 (2007).
[CrossRef] [PubMed]

Biophys. Struct. Mech.

K. P. Hofmann, R. Uhl, W. Hoffmann, 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]

Brain Res. Bull.

K. Holthoff, O. W. Witte, “Intrinsic optical signals in vitro: a tool to measure alterations in extracellular space with two-dimensional resolution,” Brain Res. Bull. 47(6), 649–655 (1998).
[CrossRef] [PubMed]

Curr. Eye Res.

Y. W. Qin, G. Z. Xu, W. J. Wang, “Dendritic abnormalities in retinal ganglion cells of three-month diabetic rats,” Curr. Eye Res. 31(11), 967–974 (2006).
[CrossRef] [PubMed]

Invest. Ophthalmol. Vis. Sci.

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

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

X. Huang, W. Kong, Y. Zhou, G. Gregori, “Distortion of axonal cytoskeleton: an early sign of glaucomatous damage,” Invest. Ophthalmol. Vis. Sci. 52(6), 2879–2888 (2011).
[CrossRef] [PubMed]

J. Schallek, H. Li, R. Kardon, Y. Kwon, M. Abramoff, P. Soliz, D. Ts’o, “Stimulus-evoked intrinsic optical signals in the retina: spatial and temporal characteristics,” Invest. Ophthalmol. Vis. Sci. 50(10), 4865–4872 (2009).
[CrossRef] [PubMed]

J Innov Opt Health Sci

X. C. Yao, L. Liu, Y. G. Li, “Intrinsic optical signal imaging of retinal activity in frog eye,” J Innov Opt Health Sci 2(02), 201–208 (2009).
[CrossRef]

J. Biomed. Opt.

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

J. Cell Sci.

Y. Zhang, L. L. Molday, R. S. Molday, S. S. Sarfare, M. L. Woodruff, G. L. Fain, T. W. Kraft, S. J. Pittler, “Knockout of GARPs and the β-subunit of the rod cGMP-gated channel disrupts disk morphogenesis and rod outer segment structural integrity,” J. Cell Sci. 122(8), 1192–1200 (2009).
[CrossRef] [PubMed]

J. Comp. Neurol.

C. Gargini, E. Terzibasi, F. Mazzoni, E. Strettoi, “Retinal organization in the retinal degeneration 10 (rd10) mutant mouse: a morphological and ERG study,” J. Comp. Neurol. 500(2), 222–238 (2007).
[CrossRef] [PubMed]

J. Neurophysiol.

M. Haller, S. L. Mironov, D. W. Richter, “Intrinsic optical signals in respiratory brain stem regions of mice: neurotransmitters, neuromodulators, and metabolic stress,” J. Neurophysiol. 86(1), 412–421 (2001).
[PubMed]

S. F. Stasheff, “Emergence of sustained spontaneous hyperactivity and temporary preservation of OFF responses in ganglion cells of the retinal degeneration (rd1) mouse,” J. Neurophysiol. 99(3), 1408–1421 (2008).
[CrossRef] [PubMed]

J. Neurosci.

J. Borowska, S. Trenholm, G. B. Awatramani, “An intrinsic neural oscillator in the degenerating mouse retina,” J. Neurosci. 31(13), 5000–5012 (2011).
[CrossRef] [PubMed]

Methods

R. D. Andrew, C. R. Jarvis, A. S. Obeidat, “Potential sources of intrinsic optical signals imaged in live brain slices,” Methods 18(2), 185–196, 179 (1999).
[CrossRef] [PubMed]

Nature

G. L. Kesteven, “The coefficient of variation,” Nature 158(4015), 520–521 (1946).
[CrossRef] [PubMed]

Neuroimage

X. C. Yao, J. S. George, “Dynamic neuroimaging of retinal light responses using fast intrinsic optical signals,” Neuroimage 33(3), 898–906 (2006).
[CrossRef] [PubMed]

Opt. Express

Opt. Lett.

Physiol. Rev.

L. B. Cohen, “Changes in neuron structure during action potential propagation and synaptic transmission,” Physiol. Rev. 53(2), 373–418 (1973).
[PubMed]

Proc. Natl. Acad. Sci. U.S.A.

H. Kühn, N. Bennett, M. Michel-Villaz, 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]

Proc. SPIE

T. Theelen, C. B. Hoyng, B. J. Klevering, and C. B, “Functional imaging of inherited retinal disease with a commercial optical coherence tomography,” Proc. SPIE 8091, 8009110–8009118 (2011).

Prog. Retin. Eye Res.

R. E. Marc, B. W. Jones, C. B. Watt, E. Strettoi, “Neural remodeling in retinal degeneration,” Prog. Retin. Eye Res. 22(5), 607–655 (2003).
[CrossRef] [PubMed]

D. C. Hood, “Assessing retinal function with the multifocal technique,” Prog. Retin. Eye Res. 19(5), 607–646 (2000).
[CrossRef] [PubMed]

Surv. Ophthalmol.

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

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Figures (4)

Fig. 1
Fig. 1

Schematic diagram of experiment setup. A custom modified microscope, with 20x objective and high speed CMOS camera (10 bits depth and 1000 frames/s), was used for this study. During the measurement, the mouse retina was continuously illuminated by the NIR light for IOS recording; a 10 ms visible light flash was used for retinal stimulation.

Fig. 2
Fig. 2

(a) Representative images of a mouse retina. The white rectangle in the third frame showed the visible stimulus pattern. The black arrow indicated the delivery of stimulus light. (b) Dynamic differential IOS images of two-month-old WT mouse retina. (c) Dynamic differential IOS images of two-month-old mutant mouse retina. (d) Dynamic differential IOS images of 1-year-old mutant retina. Scale bars (in black) represent 50 µm.

Fig. 3
Fig. 3

(a) Spatiotemporal patterns of positive and negative IOS signals, corresponding to Fig. 2(b). The top panel is the image of positive pixel numbers and the bottom is negative signal pixel numbers. The unit of the color bar is pixel number. Scale bars (in black) represent 50 µm. The vertical axis (x) corresponds to the horizontal axis (x) in Fig. 2(b). The method to reconstruct spatiotemporal images was described in the section of data processing. (b) Dynamic IOS magnitude changes of the three retinas shown in Fig. 2(b)-2(d). (c) Statistical analysis of IOS magnitude of 7 two-month-old WT and 11 two-month-old mutant mouse retinas (p<0.0001). (d) Statistical analysis of corresponding IOS onset time (p<0.0004) and peak time (p<0.002).

Fig. 4
Fig. 4

(a) Raw structure images of 2-month-old WT (left) and mutant (right) mouse retinas; (b) Texture images of WT (top) and mutant (bottom) mouse retina. The texture images represent the strength of spontaneous activity over the pre-stimulus time. (c) Statistical analysis of background smoothness of 21 WT and 19 mutant mouse retinas (p<0.0001). (d) Statistical analysis of background uniformity (p = 0.002). Scale bars represent 50 µm.

Equations (5)

Equations on this page are rendered with MathJax. Learn more.

I O S t i ( x , y ) > I O S ¯ ( x , y ) + 3 σ ( x , y )
I O S t i ( x , y ) < I O S ¯ ( x , y ) 3 σ ( x , y )
I O S ¯ ( x , y ) = 1 n j = 1 j = n I O S t j ( x , y )
σ ( x , y ) = 1 n j = 1 j = n ( I O S t j ( x , y ) I O S ¯ ( x , y ) ) 2
C V ( x , y ) = σ ( x , y ) I O S ¯ ( x , y )

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