Abstract

In this paper, we demonstrate the use of optical coherence tomography/optical microangiography (OCT/OMAG) to image and measure the effects of acute intraocular pressure (IOP) elevation on retinal, choroidal and optic nerve head (ONH) perfusion in the rat eye. In the experiments, IOP was elevated from 10 to 100 mmHg in 10 mmHg increments. At each IOP level, three-dimensional data volumes were captured using an ultrahigh sensitive (UHS) OMAG scanning protocol for 3D volumetric perfusion imaging, followed by repeated B-scans for Doppler OMAG analysis to determine blood flow velocity. Velocity and vessel diameter measurements were used to calculate blood flow in selected retinal blood vessels. Choroidal perfusion was calculated by determining the peripapillary choroidal filling at each pressure level and calculating this as a percentage of area filling at baseline (10 mmHg). ONH blood perfusion was calculated as the percentage of blood flow area over a segmented ONH area to a depth 150 microns posterior to the choroidal opening. We show that volumetric blood flow reconstructions revealed detailed 3D maps, to the capillary level, of the retinal, choroidal and ONH microvasculature, revealing retinal arterioles, capillaries and veins, the choroidal opening and a consistent presence of the central retinal artery inferior to the ONH. While OCT structural images revealed a reversible compression of the ONH and vasculature with elevated IOP, OMAG successfully documented changes in retinal, choroidal and ONH blood perfusion and allowed quantitative measurements of these changes. Starting from 30 mm Hg, retinal blood flow (RBF) diminished linearly with increasing IOP and was nearly extinguished at 100 mm Hg, with full recovery after return of IOP to baseline. Choroidal filling was unaffected until IOP reached 60 mmHg, then decreased to 20% of baseline at IOP 100 mmHg, and normalized when IOP returned to baseline. A reduction in ONH blood perfusion at higher IOP’s was also observed, but shadow from overlying retinal vessels at lower IOP’s limited precise measurements of changes in ONH capillary perfusion compared to baseline. Therefore, OCT/OMAG can be a useful tool to image and measure blood flow in the retina, choroidal and ONH of the rat eye as well as document the effects of elevated IOP on blood flow in these vascular beds.

© 2012 OSA

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    [CrossRef] [PubMed]

2012

Z. He, C. T. Nguyen, J. A. Armitage, A. J. Vingrys, and B. V. Bui, “Blood pressure modifies retinal susceptibility to intraocular pressure elevation,” PLoS ONE7(2), e31104 (2012).
[CrossRef] [PubMed]

C. Dai, P. T. Khaw, Z. Q. Yin, D. Li, G. Raisman, and Y. Li, “Structural basis of glaucoma: the fortified astrocytes of the optic nerve head are the target of raised intraocular pressure,” Glia60(1), 13–28 (2012).
[CrossRef] [PubMed]

2011

Y. Wang, A. A. Fawzi, R. Varma, A. A. Sadun, X. Zhang, O. Tan, J. A. Izatt, and D. Huang, “Pilot study of optical coherence tomography measurement of retinal blood flow in retinal and optic nerve diseases,” Invest. Ophthalmol. Vis. Sci.52(2), 840–845 (2011).
[CrossRef] [PubMed]

B. Fortune, T. E. Choe, J. Reynaud, C. Hardin, G. A. Cull, C. F. Burgoyne, and L. Wang, “Deformation of the rodent optic nerve head and peripapillary structures during acute intraocular pressure elevation,” Invest. Ophthalmol. Vis. Sci.52(9), 6651–6661 (2011).
[CrossRef] [PubMed]

J. C. Morrison, W. O. Cepurna, Y. Guo, and E. C. Johnson, “Pathophysiology of human glaucomatous optic nerve damage: insights from rodent models of glaucoma,” Exp. Eye Res.93(2), 156–164 (2011).
[CrossRef] [PubMed]

Y. Guo, E. C. Johnson, W. O. Cepurna, J. A. Dyck, T. Doser, and J. C. Morrison, “Early gene expression changes in the retinal ganglion cell layer of a rat glaucoma model,” Invest. Ophthalmol. Vis. Sci.52(3), 1460–1473 (2011).
[CrossRef] [PubMed]

E. C. Johnson, T. A. Doser, W. O. Cepurna, J. A. Dyck, L. Jia, Y. Guo, W. S. Lambert, and J. C. Morrison, “Cell proliferation and interleukin-6-type cytokine signaling are implicated by gene expression responses in early optic nerve head injury in rat glaucoma,” Invest. Ophthalmol. Vis. Sci.52(1), 504–518 (2011).
[CrossRef] [PubMed]

Z. He, A. J. Vingrys, J. A. Armitage, and B. V. Bui, “The role of blood pressure in glaucoma,” Clin. Exp. Optom.94(2), 133–149 (2011).
[CrossRef] [PubMed]

Y. Jia, P. Li, and R. K. Wang, “Optical microangiography provides an ability to monitor responses of cerebral microcirculation to hypoxia and hyperoxia in mice,” J. Biomed. Opt.16(9), 096019 (2011).
[CrossRef] [PubMed]

Y. Jia, P. Li, S. Dziennis, and R. K. Wang, “Responses of peripheral blood flow to acute hypoxia and hyperoxia as measured by optical microangiography,” PLoS ONE6(10), e26802 (2011).
[CrossRef] [PubMed]

R. Varma, P. P. Lee, I. Goldberg, and S. Kotak, “An assessment of the health and economic burdens of glaucoma,” Am. J. Ophthalmol.152(4), 515–522 (2011).
[CrossRef] [PubMed]

R. F. Leoni, F. F. Paiva, E. C. Henning, G. C. Nascimento, A. Tannús, D. B. de Araujo, and A. C. Silva, “Magnetic resonance imaging quantification of regional cerebral blood flow and cerebrovascular reactivity to carbon dioxide in normotensive and hypertensive rats,” Neuroimage58(1), 75–81 (2011).
[CrossRef] [PubMed]

Z. Zhi, W. Cepurna, E. Johnson, T. Shen, J. Morrison, and R. K. Wang, “Volumetric and quantitative imaging of retinal blood flow in rats with optical microangiography,” Biomed. Opt. Express2(3), 579–591 (2011).
[CrossRef] [PubMed]

Z. Zhi, Y. Jung, Y. Jia, L. An, and R. K. Wang, “Highly sensitive imaging of renal microcirculation in vivo using ultrahigh sensitive optical microangiography,” Biomed. Opt. Express2(5), 1059–1068 (2011).
[CrossRef] [PubMed]

2010

V. J. Srinivasan, J. Y. Jiang, M. A. Yaseen, H. Radhakrishnan, W. Wu, S. Barry, A. E. Cable, and D. A. Boas, “Rapid volumetric angiography of cortical microvasculature with optical coherence tomography,” Opt. Lett.35(1), 43–45 (2010).
[CrossRef] [PubMed]

L. An, J. Qin, and R. K. Wang, “Ultrahigh sensitive optical microangiography for in vivo imaging of microcirculations within human skin tissue beds,” Opt. Express18(8), 8220–8228 (2010).
[CrossRef] [PubMed]

R. K. Wang, L. An, P. Francis, and D. J. Wilson, “Depth-resolved imaging of capillary networks in retina and choroid using ultrahigh sensitive optical microangiography,” Opt. Lett.35(9), 1467–1469 (2010).
[CrossRef] [PubMed]

M. D. Roberts, I. A. Sigal, Y. Liang, C. F. Burgoyne, and J. C. Downs, “Changes in the biomechanical response of the optic nerve head in early experimental glaucoma,” Invest. Ophthalmol. Vis. Sci.51(11), 5675–5684 (2010).
[CrossRef] [PubMed]

M. Pazos, S. Gardiner, J. G. J. Reynaud, W. O. Cepurna, E. C. Johnson, J. C. Morrison, C. F. Burgoyne, and H. Yang, “Radial optic nerve expansion within the expanding scleral canal in the hypertonic saline rat early experimental glaucoma (EEG) model,” Invest. Ophthalmol. Vis. Sci.51, 4806 (2010).

2009

Y. Liang, J. C. Downs, B. Fortune, G. Cull, G. A. Cioffi, and L. Wang, “Impact of systemic blood pressure on the relationship between intraocular pressure and blood flow in the optic nerve head of nonhuman primates,” Invest. Ophthalmol. Vis. Sci.50(5), 2154–2160 (2009).
[CrossRef] [PubMed]

R. K. Wang and L. An, “Doppler optical micro-angiography for volumetric imaging of vascular perfusion in vivo,” Opt. Express17(11), 8926–8940 (2009).
[CrossRef] [PubMed]

2008

J. C. Morrison, E. Johnson, and W. O. Cepurna, “Rat models for glaucoma research,” Prog. Brain Res.173, 285–301 (2008).
[CrossRef] [PubMed]

2007

I. H. Pang and A. F. Clark, “Rodent models for glaucoma retinopathy and optic neuropathy,” J. Glaucoma16(5), 483–505 (2007).
[CrossRef] [PubMed]

M. E. van Velthoven, D. J. Faber, F. D. Verbraak, T. G. van Leeuwen, and M. D. de Smet, “Recent developments in optical coherence tomography for imaging the retina,” Prog. Retin. Eye Res.26(1), 57–77 (2007).
[CrossRef] [PubMed]

R. K. Wang, S. L. Jacques, Z. Ma, S. Hurst, S. R. Hanson, and A. Gruber, “Three dimensional optical angiography,” Opt. Express15(7), 4083–4097 (2007).
[CrossRef] [PubMed]

E. Polska, C. Simader, G. Weigert, A. Doelemeyer, J. Kolodjaschna, O. Scharmann, and L. Schmetterer, “Regulation of choroidal blood flow during combined changes in intraocular pressure and arterial blood pressure,” Invest. Ophthalmol. Vis. Sci.48(8), 3768–3774 (2007).
[CrossRef] [PubMed]

2005

G. Weigert, O. Findl, A. Luksch, G. Rainer, B. Kiss, C. Vass, and L. Schmetterer, “Effects of moderate changes in intraocular pressure on ocular hemodynamics in patients with primary open-angle glaucoma and healthy controls,” Ophthalmology112(8), 1337–1342 (2005).
[CrossRef] [PubMed]

M. C. Grieshaber and J. Flammer, “Blood flow in glaucoma,” Curr. Opin. Ophthalmol.16(2), 79–83 (2005).
[CrossRef] [PubMed]

B. V. Bui, B. Edmunds, G. A. Cioffi, and B. Fortune, “The gradient of retinal functional changes during acute intraocular pressure elevation,” Invest. Ophthalmol. Vis. Sci.46(1), 202–213 (2005).
[CrossRef] [PubMed]

2003

2002

J. Flammer, S. Orgül, V. P. Costa, N. Orzalesi, G. K. Krieglstein, L. M. Serra, J. P. Renard, and E. Stefánsson, “The impact of ocular blood flow in glaucoma,” Prog. Retin. Eye Res.21(4), 359–393 (2002).
[CrossRef] [PubMed]

2001

C. E. Riva, “Basic principles of laser Doppler flowmetry and application to the ocular circulation,” Int. Ophthalmol.23(4/6), 183–189 (2001).
[CrossRef] [PubMed]

T. Fukuchi, K. Takahashi, and K. Shou, “Optical coherence tomography (OCT) findings in normal retina and laser-induced choroidal neovascularization in rats,” Graefes Arch. Clin. Exp. Ophthalmol.239(1), 41–46 (2001).
[CrossRef] [PubMed]

2000

K. Yaoeda, M. Shirakashi, S. Funaki, H. Funaki, T. Nakatsue, and H. Abe, “Measurement of microcirculation in the optic nerve head by laser speckle flowgraphy and scanning laser Doppler flowmetry,” Am. J. Ophthalmol.129(6), 734–739 (2000).
[CrossRef] [PubMed]

Y. Zhao, Z. Chen, C. Saxer, S. Xiang, J. F. de Boer, and J. S. Nelson, “Phase-resolved optical coherence tomography and optical Doppler tomography for imaging blood flow in human skin with fast scanning speed and high velocity sensitivity,” Opt. Lett.25(2), 114–116 (2000).
[CrossRef] [PubMed]

1999

J. C. Morrison, E. C. Johnson, W. O. Cepurna, and R. H. Funk, “Microvasculature of the rat optic nerve head,” Invest. Ophthalmol. Vis. Sci.40(8), 1702–1709 (1999).
[PubMed]

B. L. Petrig, C. E. Riva, and S. S. Hayreh, “Laser Doppler flowmetry and optic nerve head blood flow,” Am. J. Ophthalmol.127(4), 413–425 (1999).
[CrossRef] [PubMed]

D. S. Chauhan and J. Marshall, “The interpretation of optical coherence tomography images of the retina,” Invest. Ophthalmol. Vis. Sci.40(10), 2332–2342 (1999).
[PubMed]

1998

J. E. Grunwald, J. Piltz, S. M. Hariprasad, and J. DuPont, “Optic nerve and choroidal circulation in glaucoma,” Invest. Ophthalmol. Vis. Sci.39(12), 2329–2336 (1998).
[PubMed]

1997

J. C. Morrison, C. G. Moore, L. M. Deppmeier, B. G. Gold, C. K. Meshul, and E. C. Johnson, “A rat model of chronic pressure-induced optic nerve damage,” Exp. Eye Res.64(1), 85–96 (1997).
[CrossRef] [PubMed]

L. E. Pillunat, D. R. Anderson, R. W. Knighton, K. M. Joos, and W. J. Feuer, “Autoregulation of human optic nerve head circulation in response to increased intraocular pressure,” Exp. Eye Res.64(5), 737–744 (1997).
[CrossRef] [PubMed]

1996

C. E. Riva, S. D. Cranstoun, and B. L. Petrig, “Effect of decreased ocular perfusion pressure on blood flow and the flicker-induced flow response in the cat optic nerve head,” Microvasc. Res.52(3), 258–269 (1996).
[CrossRef] [PubMed]

A. Harris, D. R. Anderson, L. Pillunat, K. Joos, R. W. Knighton, L. Kagemann, and B. J. Martin, “Laser Doppler flowmetry measurement of changes in human optic nerve head blood flow in response to blood gas perturbations,” J. Glaucoma5(4), 258–265 (1996).
[CrossRef] [PubMed]

1992

C. E. Riva, S. Harino, B. L. Petrig, and R. D. Shonat, “Laser Doppler flowmetry in the optic nerve,” Exp. Eye Res.55(3), 499–506 (1992).
[CrossRef] [PubMed]

J. W. Kiel and A. P. Shepherd, “Autoregulation of choroidal blood flow in the rabbit,” Invest. Ophthalmol. Vis. Sci.33(8), 2399–2410 (1992).
[PubMed]

1991

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography,” Science254(5035), 1178–1181 (1991).
[CrossRef] [PubMed]

1988

F. Binaghi, F. Cannas, and F. Pitzus, “La flussimetria Doppler laser. Principi ed applicazioni cliniche nelle acrosindromi vascolari [Laser Doppler flowmetry. principles and clinical applications in vascular acro-syndromes],” Minerva Med.79(10), 831–838 (1988).
[PubMed]

1986

C. E. Riva, J. E. Grunwald, and B. L. Petrig, “Autoregulation of human retinal blood flow. An investigation with laser Doppler velocimetry,” Invest. Ophthalmol. Vis. Sci.27(12), 1706–1712 (1986).
[PubMed]

W. C. Seyde and D. E. Longnecker, “Cerebral oxygen tension in rats during deliberate hypotension with sodium nitroprusside, 2-chloroadenosine, or deep isoflurane anesthesia,” Anesthesiology64(4), 480–485 (1986).
[CrossRef] [PubMed]

1985

C. E. Riva, J. E. Grunwald, S. H. Sinclair, and B. L. Petrig, “Blood velocity and volumetric flow rate in human retinal vessels,” Invest. Ophthalmol. Vis. Sci.26(8), 1124–1132 (1985).
[PubMed]

1983

N. Sossi and D. R. Anderson, “Effect of elevated intraocular pressure on blood flow. Occurrence in cat optic nerve head studied with iodoantipyrine I 125,” Arch. Ophthalmol.101(1), 98–101 (1983).
[CrossRef] [PubMed]

1982

K. R. Brein and C. E. Riva, “Laser Doppler velocimetry measurement of pulsatile blood flow in capillary tubes,” Microvasc. Res.24(1), 114–118 (1982).
[CrossRef] [PubMed]

1979

C. Geijer and A. Bill, “Effects of raised intraocular pressure on retinal, prelaminar, laminar, and retrolaminar optic nerve blood flow in monkeys,” Invest. Ophthalmol. Vis. Sci.18(10), 1030–1042 (1979).
[PubMed]

1972

A. Alm and A. Bill, “The oxygen supply to the retina. II. Effects of high intraocular pressure and of increased arterial carbon dioxide tension on uveal and retinal blood flow in cats. A study with radioactively labelled microspheres including flow determinations in brain and some other tissues,” Acta Physiol. Scand.84(3), 306–319 (1972).
[CrossRef] [PubMed]

Abe, H.

K. Yaoeda, M. Shirakashi, S. Funaki, H. Funaki, T. Nakatsue, and H. Abe, “Measurement of microcirculation in the optic nerve head by laser speckle flowgraphy and scanning laser Doppler flowmetry,” Am. J. Ophthalmol.129(6), 734–739 (2000).
[CrossRef] [PubMed]

Alm, A.

A. Alm and A. Bill, “The oxygen supply to the retina. II. Effects of high intraocular pressure and of increased arterial carbon dioxide tension on uveal and retinal blood flow in cats. A study with radioactively labelled microspheres including flow determinations in brain and some other tissues,” Acta Physiol. Scand.84(3), 306–319 (1972).
[CrossRef] [PubMed]

An, L.

Anderson, D. R.

L. E. Pillunat, D. R. Anderson, R. W. Knighton, K. M. Joos, and W. J. Feuer, “Autoregulation of human optic nerve head circulation in response to increased intraocular pressure,” Exp. Eye Res.64(5), 737–744 (1997).
[CrossRef] [PubMed]

A. Harris, D. R. Anderson, L. Pillunat, K. Joos, R. W. Knighton, L. Kagemann, and B. J. Martin, “Laser Doppler flowmetry measurement of changes in human optic nerve head blood flow in response to blood gas perturbations,” J. Glaucoma5(4), 258–265 (1996).
[CrossRef] [PubMed]

N. Sossi and D. R. Anderson, “Effect of elevated intraocular pressure on blood flow. Occurrence in cat optic nerve head studied with iodoantipyrine I 125,” Arch. Ophthalmol.101(1), 98–101 (1983).
[CrossRef] [PubMed]

Armitage, J. A.

Z. He, C. T. Nguyen, J. A. Armitage, A. J. Vingrys, and B. V. Bui, “Blood pressure modifies retinal susceptibility to intraocular pressure elevation,” PLoS ONE7(2), e31104 (2012).
[CrossRef] [PubMed]

Z. He, A. J. Vingrys, J. A. Armitage, and B. V. Bui, “The role of blood pressure in glaucoma,” Clin. Exp. Optom.94(2), 133–149 (2011).
[CrossRef] [PubMed]

Bajraszewski, T.

Barry, S.

Bill, A.

C. Geijer and A. Bill, “Effects of raised intraocular pressure on retinal, prelaminar, laminar, and retrolaminar optic nerve blood flow in monkeys,” Invest. Ophthalmol. Vis. Sci.18(10), 1030–1042 (1979).
[PubMed]

A. Alm and A. Bill, “The oxygen supply to the retina. II. Effects of high intraocular pressure and of increased arterial carbon dioxide tension on uveal and retinal blood flow in cats. A study with radioactively labelled microspheres including flow determinations in brain and some other tissues,” Acta Physiol. Scand.84(3), 306–319 (1972).
[CrossRef] [PubMed]

Binaghi, F.

F. Binaghi, F. Cannas, and F. Pitzus, “La flussimetria Doppler laser. Principi ed applicazioni cliniche nelle acrosindromi vascolari [Laser Doppler flowmetry. principles and clinical applications in vascular acro-syndromes],” Minerva Med.79(10), 831–838 (1988).
[PubMed]

Boas, D. A.

Bouma, B.

Brein, K. R.

K. R. Brein and C. E. Riva, “Laser Doppler velocimetry measurement of pulsatile blood flow in capillary tubes,” Microvasc. Res.24(1), 114–118 (1982).
[CrossRef] [PubMed]

Bui, B. V.

Z. He, C. T. Nguyen, J. A. Armitage, A. J. Vingrys, and B. V. Bui, “Blood pressure modifies retinal susceptibility to intraocular pressure elevation,” PLoS ONE7(2), e31104 (2012).
[CrossRef] [PubMed]

Z. He, A. J. Vingrys, J. A. Armitage, and B. V. Bui, “The role of blood pressure in glaucoma,” Clin. Exp. Optom.94(2), 133–149 (2011).
[CrossRef] [PubMed]

B. V. Bui, B. Edmunds, G. A. Cioffi, and B. Fortune, “The gradient of retinal functional changes during acute intraocular pressure elevation,” Invest. Ophthalmol. Vis. Sci.46(1), 202–213 (2005).
[CrossRef] [PubMed]

Burgoyne, C. F.

B. Fortune, T. E. Choe, J. Reynaud, C. Hardin, G. A. Cull, C. F. Burgoyne, and L. Wang, “Deformation of the rodent optic nerve head and peripapillary structures during acute intraocular pressure elevation,” Invest. Ophthalmol. Vis. Sci.52(9), 6651–6661 (2011).
[CrossRef] [PubMed]

M. D. Roberts, I. A. Sigal, Y. Liang, C. F. Burgoyne, and J. C. Downs, “Changes in the biomechanical response of the optic nerve head in early experimental glaucoma,” Invest. Ophthalmol. Vis. Sci.51(11), 5675–5684 (2010).
[CrossRef] [PubMed]

M. Pazos, S. Gardiner, J. G. J. Reynaud, W. O. Cepurna, E. C. Johnson, J. C. Morrison, C. F. Burgoyne, and H. Yang, “Radial optic nerve expansion within the expanding scleral canal in the hypertonic saline rat early experimental glaucoma (EEG) model,” Invest. Ophthalmol. Vis. Sci.51, 4806 (2010).

Cable, A. E.

Cannas, F.

F. Binaghi, F. Cannas, and F. Pitzus, “La flussimetria Doppler laser. Principi ed applicazioni cliniche nelle acrosindromi vascolari [Laser Doppler flowmetry. principles and clinical applications in vascular acro-syndromes],” Minerva Med.79(10), 831–838 (1988).
[PubMed]

Cense, B.

Cepurna, W.

Cepurna, W. O.

Y. Guo, E. C. Johnson, W. O. Cepurna, J. A. Dyck, T. Doser, and J. C. Morrison, “Early gene expression changes in the retinal ganglion cell layer of a rat glaucoma model,” Invest. Ophthalmol. Vis. Sci.52(3), 1460–1473 (2011).
[CrossRef] [PubMed]

E. C. Johnson, T. A. Doser, W. O. Cepurna, J. A. Dyck, L. Jia, Y. Guo, W. S. Lambert, and J. C. Morrison, “Cell proliferation and interleukin-6-type cytokine signaling are implicated by gene expression responses in early optic nerve head injury in rat glaucoma,” Invest. Ophthalmol. Vis. Sci.52(1), 504–518 (2011).
[CrossRef] [PubMed]

J. C. Morrison, W. O. Cepurna, Y. Guo, and E. C. Johnson, “Pathophysiology of human glaucomatous optic nerve damage: insights from rodent models of glaucoma,” Exp. Eye Res.93(2), 156–164 (2011).
[CrossRef] [PubMed]

M. Pazos, S. Gardiner, J. G. J. Reynaud, W. O. Cepurna, E. C. Johnson, J. C. Morrison, C. F. Burgoyne, and H. Yang, “Radial optic nerve expansion within the expanding scleral canal in the hypertonic saline rat early experimental glaucoma (EEG) model,” Invest. Ophthalmol. Vis. Sci.51, 4806 (2010).

J. C. Morrison, E. Johnson, and W. O. Cepurna, “Rat models for glaucoma research,” Prog. Brain Res.173, 285–301 (2008).
[CrossRef] [PubMed]

J. C. Morrison, E. C. Johnson, W. O. Cepurna, and R. H. Funk, “Microvasculature of the rat optic nerve head,” Invest. Ophthalmol. Vis. Sci.40(8), 1702–1709 (1999).
[PubMed]

Chang, W.

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography,” Science254(5035), 1178–1181 (1991).
[CrossRef] [PubMed]

Chauhan, D. S.

D. S. Chauhan and J. Marshall, “The interpretation of optical coherence tomography images of the retina,” Invest. Ophthalmol. Vis. Sci.40(10), 2332–2342 (1999).
[PubMed]

Chen, T.

Chen, Z.

Choe, T. E.

B. Fortune, T. E. Choe, J. Reynaud, C. Hardin, G. A. Cull, C. F. Burgoyne, and L. Wang, “Deformation of the rodent optic nerve head and peripapillary structures during acute intraocular pressure elevation,” Invest. Ophthalmol. Vis. Sci.52(9), 6651–6661 (2011).
[CrossRef] [PubMed]

Cioffi, G. A.

Y. Liang, J. C. Downs, B. Fortune, G. Cull, G. A. Cioffi, and L. Wang, “Impact of systemic blood pressure on the relationship between intraocular pressure and blood flow in the optic nerve head of nonhuman primates,” Invest. Ophthalmol. Vis. Sci.50(5), 2154–2160 (2009).
[CrossRef] [PubMed]

B. V. Bui, B. Edmunds, G. A. Cioffi, and B. Fortune, “The gradient of retinal functional changes during acute intraocular pressure elevation,” Invest. Ophthalmol. Vis. Sci.46(1), 202–213 (2005).
[CrossRef] [PubMed]

Clark, A. F.

I. H. Pang and A. F. Clark, “Rodent models for glaucoma retinopathy and optic neuropathy,” J. Glaucoma16(5), 483–505 (2007).
[CrossRef] [PubMed]

Costa, V. P.

J. Flammer, S. Orgül, V. P. Costa, N. Orzalesi, G. K. Krieglstein, L. M. Serra, J. P. Renard, and E. Stefánsson, “The impact of ocular blood flow in glaucoma,” Prog. Retin. Eye Res.21(4), 359–393 (2002).
[CrossRef] [PubMed]

Cranstoun, S. D.

C. E. Riva, S. D. Cranstoun, and B. L. Petrig, “Effect of decreased ocular perfusion pressure on blood flow and the flicker-induced flow response in the cat optic nerve head,” Microvasc. Res.52(3), 258–269 (1996).
[CrossRef] [PubMed]

Cull, G.

Y. Liang, J. C. Downs, B. Fortune, G. Cull, G. A. Cioffi, and L. Wang, “Impact of systemic blood pressure on the relationship between intraocular pressure and blood flow in the optic nerve head of nonhuman primates,” Invest. Ophthalmol. Vis. Sci.50(5), 2154–2160 (2009).
[CrossRef] [PubMed]

Cull, G. A.

B. Fortune, T. E. Choe, J. Reynaud, C. Hardin, G. A. Cull, C. F. Burgoyne, and L. Wang, “Deformation of the rodent optic nerve head and peripapillary structures during acute intraocular pressure elevation,” Invest. Ophthalmol. Vis. Sci.52(9), 6651–6661 (2011).
[CrossRef] [PubMed]

Dai, C.

C. Dai, P. T. Khaw, Z. Q. Yin, D. Li, G. Raisman, and Y. Li, “Structural basis of glaucoma: the fortified astrocytes of the optic nerve head are the target of raised intraocular pressure,” Glia60(1), 13–28 (2012).
[CrossRef] [PubMed]

de Araujo, D. B.

R. F. Leoni, F. F. Paiva, E. C. Henning, G. C. Nascimento, A. Tannús, D. B. de Araujo, and A. C. Silva, “Magnetic resonance imaging quantification of regional cerebral blood flow and cerebrovascular reactivity to carbon dioxide in normotensive and hypertensive rats,” Neuroimage58(1), 75–81 (2011).
[CrossRef] [PubMed]

de Boer, J.

de Boer, J. F.

de Smet, M. D.

M. E. van Velthoven, D. J. Faber, F. D. Verbraak, T. G. van Leeuwen, and M. D. de Smet, “Recent developments in optical coherence tomography for imaging the retina,” Prog. Retin. Eye Res.26(1), 57–77 (2007).
[CrossRef] [PubMed]

Deppmeier, L. M.

J. C. Morrison, C. G. Moore, L. M. Deppmeier, B. G. Gold, C. K. Meshul, and E. C. Johnson, “A rat model of chronic pressure-induced optic nerve damage,” Exp. Eye Res.64(1), 85–96 (1997).
[CrossRef] [PubMed]

Doelemeyer, A.

E. Polska, C. Simader, G. Weigert, A. Doelemeyer, J. Kolodjaschna, O. Scharmann, and L. Schmetterer, “Regulation of choroidal blood flow during combined changes in intraocular pressure and arterial blood pressure,” Invest. Ophthalmol. Vis. Sci.48(8), 3768–3774 (2007).
[CrossRef] [PubMed]

Doser, T.

Y. Guo, E. C. Johnson, W. O. Cepurna, J. A. Dyck, T. Doser, and J. C. Morrison, “Early gene expression changes in the retinal ganglion cell layer of a rat glaucoma model,” Invest. Ophthalmol. Vis. Sci.52(3), 1460–1473 (2011).
[CrossRef] [PubMed]

Doser, T. A.

E. C. Johnson, T. A. Doser, W. O. Cepurna, J. A. Dyck, L. Jia, Y. Guo, W. S. Lambert, and J. C. Morrison, “Cell proliferation and interleukin-6-type cytokine signaling are implicated by gene expression responses in early optic nerve head injury in rat glaucoma,” Invest. Ophthalmol. Vis. Sci.52(1), 504–518 (2011).
[CrossRef] [PubMed]

Downs, J. C.

M. D. Roberts, I. A. Sigal, Y. Liang, C. F. Burgoyne, and J. C. Downs, “Changes in the biomechanical response of the optic nerve head in early experimental glaucoma,” Invest. Ophthalmol. Vis. Sci.51(11), 5675–5684 (2010).
[CrossRef] [PubMed]

Y. Liang, J. C. Downs, B. Fortune, G. Cull, G. A. Cioffi, and L. Wang, “Impact of systemic blood pressure on the relationship between intraocular pressure and blood flow in the optic nerve head of nonhuman primates,” Invest. Ophthalmol. Vis. Sci.50(5), 2154–2160 (2009).
[CrossRef] [PubMed]

Drexler, W.

DuPont, J.

J. E. Grunwald, J. Piltz, S. M. Hariprasad, and J. DuPont, “Optic nerve and choroidal circulation in glaucoma,” Invest. Ophthalmol. Vis. Sci.39(12), 2329–2336 (1998).
[PubMed]

Dyck, J. A.

Y. Guo, E. C. Johnson, W. O. Cepurna, J. A. Dyck, T. Doser, and J. C. Morrison, “Early gene expression changes in the retinal ganglion cell layer of a rat glaucoma model,” Invest. Ophthalmol. Vis. Sci.52(3), 1460–1473 (2011).
[CrossRef] [PubMed]

E. C. Johnson, T. A. Doser, W. O. Cepurna, J. A. Dyck, L. Jia, Y. Guo, W. S. Lambert, and J. C. Morrison, “Cell proliferation and interleukin-6-type cytokine signaling are implicated by gene expression responses in early optic nerve head injury in rat glaucoma,” Invest. Ophthalmol. Vis. Sci.52(1), 504–518 (2011).
[CrossRef] [PubMed]

Dziennis, S.

Y. Jia, P. Li, S. Dziennis, and R. K. Wang, “Responses of peripheral blood flow to acute hypoxia and hyperoxia as measured by optical microangiography,” PLoS ONE6(10), e26802 (2011).
[CrossRef] [PubMed]

Edmunds, B.

B. V. Bui, B. Edmunds, G. A. Cioffi, and B. Fortune, “The gradient of retinal functional changes during acute intraocular pressure elevation,” Invest. Ophthalmol. Vis. Sci.46(1), 202–213 (2005).
[CrossRef] [PubMed]

Faber, D. J.

M. E. van Velthoven, D. J. Faber, F. D. Verbraak, T. G. van Leeuwen, and M. D. de Smet, “Recent developments in optical coherence tomography for imaging the retina,” Prog. Retin. Eye Res.26(1), 57–77 (2007).
[CrossRef] [PubMed]

Fawzi, A. A.

Y. Wang, A. A. Fawzi, R. Varma, A. A. Sadun, X. Zhang, O. Tan, J. A. Izatt, and D. Huang, “Pilot study of optical coherence tomography measurement of retinal blood flow in retinal and optic nerve diseases,” Invest. Ophthalmol. Vis. Sci.52(2), 840–845 (2011).
[CrossRef] [PubMed]

Fercher, A.

Feuer, W. J.

L. E. Pillunat, D. R. Anderson, R. W. Knighton, K. M. Joos, and W. J. Feuer, “Autoregulation of human optic nerve head circulation in response to increased intraocular pressure,” Exp. Eye Res.64(5), 737–744 (1997).
[CrossRef] [PubMed]

Findl, O.

G. Weigert, O. Findl, A. Luksch, G. Rainer, B. Kiss, C. Vass, and L. Schmetterer, “Effects of moderate changes in intraocular pressure on ocular hemodynamics in patients with primary open-angle glaucoma and healthy controls,” Ophthalmology112(8), 1337–1342 (2005).
[CrossRef] [PubMed]

Fizanne, L.

L. Fizanne, B. Fromy, M. P. Preckel, D. Sigaudo-Roussel, and J. L. Saumet, “Effect of isoflurane on skin-pressure-induced vasodilation,” J. Vasc. Res.40(4), 416–422 (2003).
[CrossRef] [PubMed]

Flammer, J.

M. C. Grieshaber and J. Flammer, “Blood flow in glaucoma,” Curr. Opin. Ophthalmol.16(2), 79–83 (2005).
[CrossRef] [PubMed]

J. Flammer, S. Orgül, V. P. Costa, N. Orzalesi, G. K. Krieglstein, L. M. Serra, J. P. Renard, and E. Stefánsson, “The impact of ocular blood flow in glaucoma,” Prog. Retin. Eye Res.21(4), 359–393 (2002).
[CrossRef] [PubMed]

Flotte, T.

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography,” Science254(5035), 1178–1181 (1991).
[CrossRef] [PubMed]

Fortune, B.

B. Fortune, T. E. Choe, J. Reynaud, C. Hardin, G. A. Cull, C. F. Burgoyne, and L. Wang, “Deformation of the rodent optic nerve head and peripapillary structures during acute intraocular pressure elevation,” Invest. Ophthalmol. Vis. Sci.52(9), 6651–6661 (2011).
[CrossRef] [PubMed]

Y. Liang, J. C. Downs, B. Fortune, G. Cull, G. A. Cioffi, and L. Wang, “Impact of systemic blood pressure on the relationship between intraocular pressure and blood flow in the optic nerve head of nonhuman primates,” Invest. Ophthalmol. Vis. Sci.50(5), 2154–2160 (2009).
[CrossRef] [PubMed]

B. V. Bui, B. Edmunds, G. A. Cioffi, and B. Fortune, “The gradient of retinal functional changes during acute intraocular pressure elevation,” Invest. Ophthalmol. Vis. Sci.46(1), 202–213 (2005).
[CrossRef] [PubMed]

Francis, P.

Fromy, B.

L. Fizanne, B. Fromy, M. P. Preckel, D. Sigaudo-Roussel, and J. L. Saumet, “Effect of isoflurane on skin-pressure-induced vasodilation,” J. Vasc. Res.40(4), 416–422 (2003).
[CrossRef] [PubMed]

Fujimoto, J. G.

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography,” Science254(5035), 1178–1181 (1991).
[CrossRef] [PubMed]

Fukuchi, T.

T. Fukuchi, K. Takahashi, and K. Shou, “Optical coherence tomography (OCT) findings in normal retina and laser-induced choroidal neovascularization in rats,” Graefes Arch. Clin. Exp. Ophthalmol.239(1), 41–46 (2001).
[CrossRef] [PubMed]

Funaki, H.

K. Yaoeda, M. Shirakashi, S. Funaki, H. Funaki, T. Nakatsue, and H. Abe, “Measurement of microcirculation in the optic nerve head by laser speckle flowgraphy and scanning laser Doppler flowmetry,” Am. J. Ophthalmol.129(6), 734–739 (2000).
[CrossRef] [PubMed]

Funaki, S.

K. Yaoeda, M. Shirakashi, S. Funaki, H. Funaki, T. Nakatsue, and H. Abe, “Measurement of microcirculation in the optic nerve head by laser speckle flowgraphy and scanning laser Doppler flowmetry,” Am. J. Ophthalmol.129(6), 734–739 (2000).
[CrossRef] [PubMed]

Funk, R. H.

J. C. Morrison, E. C. Johnson, W. O. Cepurna, and R. H. Funk, “Microvasculature of the rat optic nerve head,” Invest. Ophthalmol. Vis. Sci.40(8), 1702–1709 (1999).
[PubMed]

Gardiner, S.

M. Pazos, S. Gardiner, J. G. J. Reynaud, W. O. Cepurna, E. C. Johnson, J. C. Morrison, C. F. Burgoyne, and H. Yang, “Radial optic nerve expansion within the expanding scleral canal in the hypertonic saline rat early experimental glaucoma (EEG) model,” Invest. Ophthalmol. Vis. Sci.51, 4806 (2010).

Geijer, C.

C. Geijer and A. Bill, “Effects of raised intraocular pressure on retinal, prelaminar, laminar, and retrolaminar optic nerve blood flow in monkeys,” Invest. Ophthalmol. Vis. Sci.18(10), 1030–1042 (1979).
[PubMed]

Gold, B. G.

J. C. Morrison, C. G. Moore, L. M. Deppmeier, B. G. Gold, C. K. Meshul, and E. C. Johnson, “A rat model of chronic pressure-induced optic nerve damage,” Exp. Eye Res.64(1), 85–96 (1997).
[CrossRef] [PubMed]

Goldberg, I.

R. Varma, P. P. Lee, I. Goldberg, and S. Kotak, “An assessment of the health and economic burdens of glaucoma,” Am. J. Ophthalmol.152(4), 515–522 (2011).
[CrossRef] [PubMed]

Gregory, K.

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography,” Science254(5035), 1178–1181 (1991).
[CrossRef] [PubMed]

Grieshaber, M. C.

M. C. Grieshaber and J. Flammer, “Blood flow in glaucoma,” Curr. Opin. Ophthalmol.16(2), 79–83 (2005).
[CrossRef] [PubMed]

Gruber, A.

Grunwald, J. E.

J. E. Grunwald, J. Piltz, S. M. Hariprasad, and J. DuPont, “Optic nerve and choroidal circulation in glaucoma,” Invest. Ophthalmol. Vis. Sci.39(12), 2329–2336 (1998).
[PubMed]

C. E. Riva, J. E. Grunwald, and B. L. Petrig, “Autoregulation of human retinal blood flow. An investigation with laser Doppler velocimetry,” Invest. Ophthalmol. Vis. Sci.27(12), 1706–1712 (1986).
[PubMed]

C. E. Riva, J. E. Grunwald, S. H. Sinclair, and B. L. Petrig, “Blood velocity and volumetric flow rate in human retinal vessels,” Invest. Ophthalmol. Vis. Sci.26(8), 1124–1132 (1985).
[PubMed]

Guo, Y.

Y. Guo, E. C. Johnson, W. O. Cepurna, J. A. Dyck, T. Doser, and J. C. Morrison, “Early gene expression changes in the retinal ganglion cell layer of a rat glaucoma model,” Invest. Ophthalmol. Vis. Sci.52(3), 1460–1473 (2011).
[CrossRef] [PubMed]

E. C. Johnson, T. A. Doser, W. O. Cepurna, J. A. Dyck, L. Jia, Y. Guo, W. S. Lambert, and J. C. Morrison, “Cell proliferation and interleukin-6-type cytokine signaling are implicated by gene expression responses in early optic nerve head injury in rat glaucoma,” Invest. Ophthalmol. Vis. Sci.52(1), 504–518 (2011).
[CrossRef] [PubMed]

J. C. Morrison, W. O. Cepurna, Y. Guo, and E. C. Johnson, “Pathophysiology of human glaucomatous optic nerve damage: insights from rodent models of glaucoma,” Exp. Eye Res.93(2), 156–164 (2011).
[CrossRef] [PubMed]

Hanson, S. R.

Hardin, C.

B. Fortune, T. E. Choe, J. Reynaud, C. Hardin, G. A. Cull, C. F. Burgoyne, and L. Wang, “Deformation of the rodent optic nerve head and peripapillary structures during acute intraocular pressure elevation,” Invest. Ophthalmol. Vis. Sci.52(9), 6651–6661 (2011).
[CrossRef] [PubMed]

Harino, S.

C. E. Riva, S. Harino, B. L. Petrig, and R. D. Shonat, “Laser Doppler flowmetry in the optic nerve,” Exp. Eye Res.55(3), 499–506 (1992).
[CrossRef] [PubMed]

Hariprasad, S. M.

J. E. Grunwald, J. Piltz, S. M. Hariprasad, and J. DuPont, “Optic nerve and choroidal circulation in glaucoma,” Invest. Ophthalmol. Vis. Sci.39(12), 2329–2336 (1998).
[PubMed]

Harris, A.

A. Harris, D. R. Anderson, L. Pillunat, K. Joos, R. W. Knighton, L. Kagemann, and B. J. Martin, “Laser Doppler flowmetry measurement of changes in human optic nerve head blood flow in response to blood gas perturbations,” J. Glaucoma5(4), 258–265 (1996).
[CrossRef] [PubMed]

Hayreh, S. S.

B. L. Petrig, C. E. Riva, and S. S. Hayreh, “Laser Doppler flowmetry and optic nerve head blood flow,” Am. J. Ophthalmol.127(4), 413–425 (1999).
[CrossRef] [PubMed]

He, Z.

Z. He, C. T. Nguyen, J. A. Armitage, A. J. Vingrys, and B. V. Bui, “Blood pressure modifies retinal susceptibility to intraocular pressure elevation,” PLoS ONE7(2), e31104 (2012).
[CrossRef] [PubMed]

Z. He, A. J. Vingrys, J. A. Armitage, and B. V. Bui, “The role of blood pressure in glaucoma,” Clin. Exp. Optom.94(2), 133–149 (2011).
[CrossRef] [PubMed]

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D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography,” Science254(5035), 1178–1181 (1991).
[CrossRef] [PubMed]

Henning, E. C.

R. F. Leoni, F. F. Paiva, E. C. Henning, G. C. Nascimento, A. Tannús, D. B. de Araujo, and A. C. Silva, “Magnetic resonance imaging quantification of regional cerebral blood flow and cerebrovascular reactivity to carbon dioxide in normotensive and hypertensive rats,” Neuroimage58(1), 75–81 (2011).
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Y. Wang, A. A. Fawzi, R. Varma, A. A. Sadun, X. Zhang, O. Tan, J. A. Izatt, and D. Huang, “Pilot study of optical coherence tomography measurement of retinal blood flow in retinal and optic nerve diseases,” Invest. Ophthalmol. Vis. Sci.52(2), 840–845 (2011).
[CrossRef] [PubMed]

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography,” Science254(5035), 1178–1181 (1991).
[CrossRef] [PubMed]

Hurst, S.

Izatt, J. A.

Y. Wang, A. A. Fawzi, R. Varma, A. A. Sadun, X. Zhang, O. Tan, J. A. Izatt, and D. Huang, “Pilot study of optical coherence tomography measurement of retinal blood flow in retinal and optic nerve diseases,” Invest. Ophthalmol. Vis. Sci.52(2), 840–845 (2011).
[CrossRef] [PubMed]

Jacques, S. L.

Jia, L.

E. C. Johnson, T. A. Doser, W. O. Cepurna, J. A. Dyck, L. Jia, Y. Guo, W. S. Lambert, and J. C. Morrison, “Cell proliferation and interleukin-6-type cytokine signaling are implicated by gene expression responses in early optic nerve head injury in rat glaucoma,” Invest. Ophthalmol. Vis. Sci.52(1), 504–518 (2011).
[CrossRef] [PubMed]

Jia, Y.

Y. Jia, P. Li, and R. K. Wang, “Optical microangiography provides an ability to monitor responses of cerebral microcirculation to hypoxia and hyperoxia in mice,” J. Biomed. Opt.16(9), 096019 (2011).
[CrossRef] [PubMed]

Z. Zhi, Y. Jung, Y. Jia, L. An, and R. K. Wang, “Highly sensitive imaging of renal microcirculation in vivo using ultrahigh sensitive optical microangiography,” Biomed. Opt. Express2(5), 1059–1068 (2011).
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Y. Jia, P. Li, S. Dziennis, and R. K. Wang, “Responses of peripheral blood flow to acute hypoxia and hyperoxia as measured by optical microangiography,” PLoS ONE6(10), e26802 (2011).
[CrossRef] [PubMed]

Jiang, J. Y.

Johnson, E.

Johnson, E. C.

E. C. Johnson, T. A. Doser, W. O. Cepurna, J. A. Dyck, L. Jia, Y. Guo, W. S. Lambert, and J. C. Morrison, “Cell proliferation and interleukin-6-type cytokine signaling are implicated by gene expression responses in early optic nerve head injury in rat glaucoma,” Invest. Ophthalmol. Vis. Sci.52(1), 504–518 (2011).
[CrossRef] [PubMed]

Y. Guo, E. C. Johnson, W. O. Cepurna, J. A. Dyck, T. Doser, and J. C. Morrison, “Early gene expression changes in the retinal ganglion cell layer of a rat glaucoma model,” Invest. Ophthalmol. Vis. Sci.52(3), 1460–1473 (2011).
[CrossRef] [PubMed]

J. C. Morrison, W. O. Cepurna, Y. Guo, and E. C. Johnson, “Pathophysiology of human glaucomatous optic nerve damage: insights from rodent models of glaucoma,” Exp. Eye Res.93(2), 156–164 (2011).
[CrossRef] [PubMed]

M. Pazos, S. Gardiner, J. G. J. Reynaud, W. O. Cepurna, E. C. Johnson, J. C. Morrison, C. F. Burgoyne, and H. Yang, “Radial optic nerve expansion within the expanding scleral canal in the hypertonic saline rat early experimental glaucoma (EEG) model,” Invest. Ophthalmol. Vis. Sci.51, 4806 (2010).

J. C. Morrison, E. C. Johnson, W. O. Cepurna, and R. H. Funk, “Microvasculature of the rat optic nerve head,” Invest. Ophthalmol. Vis. Sci.40(8), 1702–1709 (1999).
[PubMed]

J. C. Morrison, C. G. Moore, L. M. Deppmeier, B. G. Gold, C. K. Meshul, and E. C. Johnson, “A rat model of chronic pressure-induced optic nerve damage,” Exp. Eye Res.64(1), 85–96 (1997).
[CrossRef] [PubMed]

Joos, K.

A. Harris, D. R. Anderson, L. Pillunat, K. Joos, R. W. Knighton, L. Kagemann, and B. J. Martin, “Laser Doppler flowmetry measurement of changes in human optic nerve head blood flow in response to blood gas perturbations,” J. Glaucoma5(4), 258–265 (1996).
[CrossRef] [PubMed]

Joos, K. M.

L. E. Pillunat, D. R. Anderson, R. W. Knighton, K. M. Joos, and W. J. Feuer, “Autoregulation of human optic nerve head circulation in response to increased intraocular pressure,” Exp. Eye Res.64(5), 737–744 (1997).
[CrossRef] [PubMed]

Jung, Y.

Kagemann, L.

A. Harris, D. R. Anderson, L. Pillunat, K. Joos, R. W. Knighton, L. Kagemann, and B. J. Martin, “Laser Doppler flowmetry measurement of changes in human optic nerve head blood flow in response to blood gas perturbations,” J. Glaucoma5(4), 258–265 (1996).
[CrossRef] [PubMed]

Khaw, P. T.

C. Dai, P. T. Khaw, Z. Q. Yin, D. Li, G. Raisman, and Y. Li, “Structural basis of glaucoma: the fortified astrocytes of the optic nerve head are the target of raised intraocular pressure,” Glia60(1), 13–28 (2012).
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J. W. Kiel and A. P. Shepherd, “Autoregulation of choroidal blood flow in the rabbit,” Invest. Ophthalmol. Vis. Sci.33(8), 2399–2410 (1992).
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G. Weigert, O. Findl, A. Luksch, G. Rainer, B. Kiss, C. Vass, and L. Schmetterer, “Effects of moderate changes in intraocular pressure on ocular hemodynamics in patients with primary open-angle glaucoma and healthy controls,” Ophthalmology112(8), 1337–1342 (2005).
[CrossRef] [PubMed]

Knighton, R. W.

L. E. Pillunat, D. R. Anderson, R. W. Knighton, K. M. Joos, and W. J. Feuer, “Autoregulation of human optic nerve head circulation in response to increased intraocular pressure,” Exp. Eye Res.64(5), 737–744 (1997).
[CrossRef] [PubMed]

A. Harris, D. R. Anderson, L. Pillunat, K. Joos, R. W. Knighton, L. Kagemann, and B. J. Martin, “Laser Doppler flowmetry measurement of changes in human optic nerve head blood flow in response to blood gas perturbations,” J. Glaucoma5(4), 258–265 (1996).
[CrossRef] [PubMed]

Kolodjaschna, J.

E. Polska, C. Simader, G. Weigert, A. Doelemeyer, J. Kolodjaschna, O. Scharmann, and L. Schmetterer, “Regulation of choroidal blood flow during combined changes in intraocular pressure and arterial blood pressure,” Invest. Ophthalmol. Vis. Sci.48(8), 3768–3774 (2007).
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Kotak, S.

R. Varma, P. P. Lee, I. Goldberg, and S. Kotak, “An assessment of the health and economic burdens of glaucoma,” Am. J. Ophthalmol.152(4), 515–522 (2011).
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Krieglstein, G. K.

J. Flammer, S. Orgül, V. P. Costa, N. Orzalesi, G. K. Krieglstein, L. M. Serra, J. P. Renard, and E. Stefánsson, “The impact of ocular blood flow in glaucoma,” Prog. Retin. Eye Res.21(4), 359–393 (2002).
[CrossRef] [PubMed]

Lambert, W. S.

E. C. Johnson, T. A. Doser, W. O. Cepurna, J. A. Dyck, L. Jia, Y. Guo, W. S. Lambert, and J. C. Morrison, “Cell proliferation and interleukin-6-type cytokine signaling are implicated by gene expression responses in early optic nerve head injury in rat glaucoma,” Invest. Ophthalmol. Vis. Sci.52(1), 504–518 (2011).
[CrossRef] [PubMed]

Lee, P. P.

R. Varma, P. P. Lee, I. Goldberg, and S. Kotak, “An assessment of the health and economic burdens of glaucoma,” Am. J. Ophthalmol.152(4), 515–522 (2011).
[CrossRef] [PubMed]

Leitgeb, R.

Leoni, R. F.

R. F. Leoni, F. F. Paiva, E. C. Henning, G. C. Nascimento, A. Tannús, D. B. de Araujo, and A. C. Silva, “Magnetic resonance imaging quantification of regional cerebral blood flow and cerebrovascular reactivity to carbon dioxide in normotensive and hypertensive rats,” Neuroimage58(1), 75–81 (2011).
[CrossRef] [PubMed]

Li, D.

C. Dai, P. T. Khaw, Z. Q. Yin, D. Li, G. Raisman, and Y. Li, “Structural basis of glaucoma: the fortified astrocytes of the optic nerve head are the target of raised intraocular pressure,” Glia60(1), 13–28 (2012).
[CrossRef] [PubMed]

Li, P.

Y. Jia, P. Li, and R. K. Wang, “Optical microangiography provides an ability to monitor responses of cerebral microcirculation to hypoxia and hyperoxia in mice,” J. Biomed. Opt.16(9), 096019 (2011).
[CrossRef] [PubMed]

Y. Jia, P. Li, S. Dziennis, and R. K. Wang, “Responses of peripheral blood flow to acute hypoxia and hyperoxia as measured by optical microangiography,” PLoS ONE6(10), e26802 (2011).
[CrossRef] [PubMed]

Li, Y.

C. Dai, P. T. Khaw, Z. Q. Yin, D. Li, G. Raisman, and Y. Li, “Structural basis of glaucoma: the fortified astrocytes of the optic nerve head are the target of raised intraocular pressure,” Glia60(1), 13–28 (2012).
[CrossRef] [PubMed]

Liang, Y.

M. D. Roberts, I. A. Sigal, Y. Liang, C. F. Burgoyne, and J. C. Downs, “Changes in the biomechanical response of the optic nerve head in early experimental glaucoma,” Invest. Ophthalmol. Vis. Sci.51(11), 5675–5684 (2010).
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Y. Liang, J. C. Downs, B. Fortune, G. Cull, G. A. Cioffi, and L. Wang, “Impact of systemic blood pressure on the relationship between intraocular pressure and blood flow in the optic nerve head of nonhuman primates,” Invest. Ophthalmol. Vis. Sci.50(5), 2154–2160 (2009).
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D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography,” Science254(5035), 1178–1181 (1991).
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W. C. Seyde and D. E. Longnecker, “Cerebral oxygen tension in rats during deliberate hypotension with sodium nitroprusside, 2-chloroadenosine, or deep isoflurane anesthesia,” Anesthesiology64(4), 480–485 (1986).
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Luksch, A.

G. Weigert, O. Findl, A. Luksch, G. Rainer, B. Kiss, C. Vass, and L. Schmetterer, “Effects of moderate changes in intraocular pressure on ocular hemodynamics in patients with primary open-angle glaucoma and healthy controls,” Ophthalmology112(8), 1337–1342 (2005).
[CrossRef] [PubMed]

Ma, Z.

Marshall, J.

D. S. Chauhan and J. Marshall, “The interpretation of optical coherence tomography images of the retina,” Invest. Ophthalmol. Vis. Sci.40(10), 2332–2342 (1999).
[PubMed]

Martin, B. J.

A. Harris, D. R. Anderson, L. Pillunat, K. Joos, R. W. Knighton, L. Kagemann, and B. J. Martin, “Laser Doppler flowmetry measurement of changes in human optic nerve head blood flow in response to blood gas perturbations,” J. Glaucoma5(4), 258–265 (1996).
[CrossRef] [PubMed]

Meshul, C. K.

J. C. Morrison, C. G. Moore, L. M. Deppmeier, B. G. Gold, C. K. Meshul, and E. C. Johnson, “A rat model of chronic pressure-induced optic nerve damage,” Exp. Eye Res.64(1), 85–96 (1997).
[CrossRef] [PubMed]

Moore, C. G.

J. C. Morrison, C. G. Moore, L. M. Deppmeier, B. G. Gold, C. K. Meshul, and E. C. Johnson, “A rat model of chronic pressure-induced optic nerve damage,” Exp. Eye Res.64(1), 85–96 (1997).
[CrossRef] [PubMed]

Morrison, J.

Morrison, J. C.

E. C. Johnson, T. A. Doser, W. O. Cepurna, J. A. Dyck, L. Jia, Y. Guo, W. S. Lambert, and J. C. Morrison, “Cell proliferation and interleukin-6-type cytokine signaling are implicated by gene expression responses in early optic nerve head injury in rat glaucoma,” Invest. Ophthalmol. Vis. Sci.52(1), 504–518 (2011).
[CrossRef] [PubMed]

Y. Guo, E. C. Johnson, W. O. Cepurna, J. A. Dyck, T. Doser, and J. C. Morrison, “Early gene expression changes in the retinal ganglion cell layer of a rat glaucoma model,” Invest. Ophthalmol. Vis. Sci.52(3), 1460–1473 (2011).
[CrossRef] [PubMed]

J. C. Morrison, W. O. Cepurna, Y. Guo, and E. C. Johnson, “Pathophysiology of human glaucomatous optic nerve damage: insights from rodent models of glaucoma,” Exp. Eye Res.93(2), 156–164 (2011).
[CrossRef] [PubMed]

M. Pazos, S. Gardiner, J. G. J. Reynaud, W. O. Cepurna, E. C. Johnson, J. C. Morrison, C. F. Burgoyne, and H. Yang, “Radial optic nerve expansion within the expanding scleral canal in the hypertonic saline rat early experimental glaucoma (EEG) model,” Invest. Ophthalmol. Vis. Sci.51, 4806 (2010).

J. C. Morrison, E. Johnson, and W. O. Cepurna, “Rat models for glaucoma research,” Prog. Brain Res.173, 285–301 (2008).
[CrossRef] [PubMed]

J. C. Morrison, E. C. Johnson, W. O. Cepurna, and R. H. Funk, “Microvasculature of the rat optic nerve head,” Invest. Ophthalmol. Vis. Sci.40(8), 1702–1709 (1999).
[PubMed]

J. C. Morrison, C. G. Moore, L. M. Deppmeier, B. G. Gold, C. K. Meshul, and E. C. Johnson, “A rat model of chronic pressure-induced optic nerve damage,” Exp. Eye Res.64(1), 85–96 (1997).
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Nakatsue, T.

K. Yaoeda, M. Shirakashi, S. Funaki, H. Funaki, T. Nakatsue, and H. Abe, “Measurement of microcirculation in the optic nerve head by laser speckle flowgraphy and scanning laser Doppler flowmetry,” Am. J. Ophthalmol.129(6), 734–739 (2000).
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Nascimento, G. C.

R. F. Leoni, F. F. Paiva, E. C. Henning, G. C. Nascimento, A. Tannús, D. B. de Araujo, and A. C. Silva, “Magnetic resonance imaging quantification of regional cerebral blood flow and cerebrovascular reactivity to carbon dioxide in normotensive and hypertensive rats,” Neuroimage58(1), 75–81 (2011).
[CrossRef] [PubMed]

Nassif, N.

Nelson, J. S.

Nguyen, C. T.

Z. He, C. T. Nguyen, J. A. Armitage, A. J. Vingrys, and B. V. Bui, “Blood pressure modifies retinal susceptibility to intraocular pressure elevation,” PLoS ONE7(2), e31104 (2012).
[CrossRef] [PubMed]

Orgül, S.

J. Flammer, S. Orgül, V. P. Costa, N. Orzalesi, G. K. Krieglstein, L. M. Serra, J. P. Renard, and E. Stefánsson, “The impact of ocular blood flow in glaucoma,” Prog. Retin. Eye Res.21(4), 359–393 (2002).
[CrossRef] [PubMed]

Orzalesi, N.

J. Flammer, S. Orgül, V. P. Costa, N. Orzalesi, G. K. Krieglstein, L. M. Serra, J. P. Renard, and E. Stefánsson, “The impact of ocular blood flow in glaucoma,” Prog. Retin. Eye Res.21(4), 359–393 (2002).
[CrossRef] [PubMed]

Paiva, F. F.

R. F. Leoni, F. F. Paiva, E. C. Henning, G. C. Nascimento, A. Tannús, D. B. de Araujo, and A. C. Silva, “Magnetic resonance imaging quantification of regional cerebral blood flow and cerebrovascular reactivity to carbon dioxide in normotensive and hypertensive rats,” Neuroimage58(1), 75–81 (2011).
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I. H. Pang and A. F. Clark, “Rodent models for glaucoma retinopathy and optic neuropathy,” J. Glaucoma16(5), 483–505 (2007).
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Park, B.

Pazos, M.

M. Pazos, S. Gardiner, J. G. J. Reynaud, W. O. Cepurna, E. C. Johnson, J. C. Morrison, C. F. Burgoyne, and H. Yang, “Radial optic nerve expansion within the expanding scleral canal in the hypertonic saline rat early experimental glaucoma (EEG) model,” Invest. Ophthalmol. Vis. Sci.51, 4806 (2010).

Petrig, B. L.

B. L. Petrig, C. E. Riva, and S. S. Hayreh, “Laser Doppler flowmetry and optic nerve head blood flow,” Am. J. Ophthalmol.127(4), 413–425 (1999).
[CrossRef] [PubMed]

C. E. Riva, S. D. Cranstoun, and B. L. Petrig, “Effect of decreased ocular perfusion pressure on blood flow and the flicker-induced flow response in the cat optic nerve head,” Microvasc. Res.52(3), 258–269 (1996).
[CrossRef] [PubMed]

C. E. Riva, S. Harino, B. L. Petrig, and R. D. Shonat, “Laser Doppler flowmetry in the optic nerve,” Exp. Eye Res.55(3), 499–506 (1992).
[CrossRef] [PubMed]

C. E. Riva, J. E. Grunwald, and B. L. Petrig, “Autoregulation of human retinal blood flow. An investigation with laser Doppler velocimetry,” Invest. Ophthalmol. Vis. Sci.27(12), 1706–1712 (1986).
[PubMed]

C. E. Riva, J. E. Grunwald, S. H. Sinclair, and B. L. Petrig, “Blood velocity and volumetric flow rate in human retinal vessels,” Invest. Ophthalmol. Vis. Sci.26(8), 1124–1132 (1985).
[PubMed]

Pierce, M.

Pillunat, L.

A. Harris, D. R. Anderson, L. Pillunat, K. Joos, R. W. Knighton, L. Kagemann, and B. J. Martin, “Laser Doppler flowmetry measurement of changes in human optic nerve head blood flow in response to blood gas perturbations,” J. Glaucoma5(4), 258–265 (1996).
[CrossRef] [PubMed]

Pillunat, L. E.

L. E. Pillunat, D. R. Anderson, R. W. Knighton, K. M. Joos, and W. J. Feuer, “Autoregulation of human optic nerve head circulation in response to increased intraocular pressure,” Exp. Eye Res.64(5), 737–744 (1997).
[CrossRef] [PubMed]

Piltz, J.

J. E. Grunwald, J. Piltz, S. M. Hariprasad, and J. DuPont, “Optic nerve and choroidal circulation in glaucoma,” Invest. Ophthalmol. Vis. Sci.39(12), 2329–2336 (1998).
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F. Binaghi, F. Cannas, and F. Pitzus, “La flussimetria Doppler laser. Principi ed applicazioni cliniche nelle acrosindromi vascolari [Laser Doppler flowmetry. principles and clinical applications in vascular acro-syndromes],” Minerva Med.79(10), 831–838 (1988).
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E. Polska, C. Simader, G. Weigert, A. Doelemeyer, J. Kolodjaschna, O. Scharmann, and L. Schmetterer, “Regulation of choroidal blood flow during combined changes in intraocular pressure and arterial blood pressure,” Invest. Ophthalmol. Vis. Sci.48(8), 3768–3774 (2007).
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L. Fizanne, B. Fromy, M. P. Preckel, D. Sigaudo-Roussel, and J. L. Saumet, “Effect of isoflurane on skin-pressure-induced vasodilation,” J. Vasc. Res.40(4), 416–422 (2003).
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D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography,” Science254(5035), 1178–1181 (1991).
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Qin, J.

Radhakrishnan, H.

Rainer, G.

G. Weigert, O. Findl, A. Luksch, G. Rainer, B. Kiss, C. Vass, and L. Schmetterer, “Effects of moderate changes in intraocular pressure on ocular hemodynamics in patients with primary open-angle glaucoma and healthy controls,” Ophthalmology112(8), 1337–1342 (2005).
[CrossRef] [PubMed]

Raisman, G.

C. Dai, P. T. Khaw, Z. Q. Yin, D. Li, G. Raisman, and Y. Li, “Structural basis of glaucoma: the fortified astrocytes of the optic nerve head are the target of raised intraocular pressure,” Glia60(1), 13–28 (2012).
[CrossRef] [PubMed]

Renard, J. P.

J. Flammer, S. Orgül, V. P. Costa, N. Orzalesi, G. K. Krieglstein, L. M. Serra, J. P. Renard, and E. Stefánsson, “The impact of ocular blood flow in glaucoma,” Prog. Retin. Eye Res.21(4), 359–393 (2002).
[CrossRef] [PubMed]

Reynaud, J.

B. Fortune, T. E. Choe, J. Reynaud, C. Hardin, G. A. Cull, C. F. Burgoyne, and L. Wang, “Deformation of the rodent optic nerve head and peripapillary structures during acute intraocular pressure elevation,” Invest. Ophthalmol. Vis. Sci.52(9), 6651–6661 (2011).
[CrossRef] [PubMed]

Reynaud, J. G. J.

M. Pazos, S. Gardiner, J. G. J. Reynaud, W. O. Cepurna, E. C. Johnson, J. C. Morrison, C. F. Burgoyne, and H. Yang, “Radial optic nerve expansion within the expanding scleral canal in the hypertonic saline rat early experimental glaucoma (EEG) model,” Invest. Ophthalmol. Vis. Sci.51, 4806 (2010).

Riva, C. E.

C. E. Riva, “Basic principles of laser Doppler flowmetry and application to the ocular circulation,” Int. Ophthalmol.23(4/6), 183–189 (2001).
[CrossRef] [PubMed]

B. L. Petrig, C. E. Riva, and S. S. Hayreh, “Laser Doppler flowmetry and optic nerve head blood flow,” Am. J. Ophthalmol.127(4), 413–425 (1999).
[CrossRef] [PubMed]

C. E. Riva, S. D. Cranstoun, and B. L. Petrig, “Effect of decreased ocular perfusion pressure on blood flow and the flicker-induced flow response in the cat optic nerve head,” Microvasc. Res.52(3), 258–269 (1996).
[CrossRef] [PubMed]

C. E. Riva, S. Harino, B. L. Petrig, and R. D. Shonat, “Laser Doppler flowmetry in the optic nerve,” Exp. Eye Res.55(3), 499–506 (1992).
[CrossRef] [PubMed]

C. E. Riva, J. E. Grunwald, and B. L. Petrig, “Autoregulation of human retinal blood flow. An investigation with laser Doppler velocimetry,” Invest. Ophthalmol. Vis. Sci.27(12), 1706–1712 (1986).
[PubMed]

C. E. Riva, J. E. Grunwald, S. H. Sinclair, and B. L. Petrig, “Blood velocity and volumetric flow rate in human retinal vessels,” Invest. Ophthalmol. Vis. Sci.26(8), 1124–1132 (1985).
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K. R. Brein and C. E. Riva, “Laser Doppler velocimetry measurement of pulsatile blood flow in capillary tubes,” Microvasc. Res.24(1), 114–118 (1982).
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Figures (7)

Fig. 1
Fig. 1

(A) Cross-sectional OCT structural image showing the layers and ONH anatomy of rat eye. See text for abbreviation definitions. (B) 3-dimensional rendering of OMAG images, showing the microvasculature of the retina (R), choroid (CH) and sclera (SC). (C) Posterior view of UHS-OMAG image approximately 150µm posterior to the opening of the choroicapillaris, showing that the rat central retinal artery (CRA) enters the globe inferior to the ONH. (D–G) Maximal projection maps of the 3-D microvasculature viewed anteriorly as: (D) a combined projection of the retinal and choroidal microvasculature; (E) a reduced view of the retinal vessels to illustrate their relationship to the choroidal opening at the ONH; (F) the choroid and choroicapillaris after removal of retinal vessels, with arrow pointing to the CRA in the inferior aspect of the opening; and (G) retinal microvasculature alone. White bar = 250 µm.

Fig. 2
Fig. 2

Compared to a histologic section (Left), vertical longitudinal OCT structure image views of the ONH (right) demonstrate that the central retinal artery (CRA) is located inferior to the optic nerve head (ONH), and separated from it by a band of sclera (*). (Right) Sequential images show posterior displacement of the retina (R) and choroid (C) and compression of the CRA with ONH contour change at increasingly higher IOPs. I = inferior; S = superior. White bar = 200 µm.

Fig. 3
Fig. 3

Horizontal views at higher IOPs show posterior bowing of the retina and choroid around the ONH and the posterior displacement of the central retinal vessels (*) into the ONH with the dashed lines as reference. White bar = 200 µm.

Fig. 4
Fig. 4

(A) UHS-OMAG microangiogram maps of the rat RBF at different IOPs. (B) Quantitative RBF data (Mean ± SEM) from 6 eyes (15 vessels) show the relative change of RBF under increased IOPs. (C) The corresponding vessel diameter change. The values in B and C are normalized to the percentage of baseline value (10mmHg).

Fig. 5
Fig. 5

UHS-OMAG microangiogram of choroidal and ONH capillary beds at increasing IOP from 10 mmHg to 100 mmHg and back to 10 mmHg, viewed after removal of the retinal vessels. Arrows indicate ONH capillary flow signals (also see Fig. 7D), visible up to 70 mmHg. Asterisks indicate appearance of filling voids with increasing IOP.

Fig. 6
Fig. 6

Quantitative measurement of the IOP effect on the choroidal perfusion illustrated by the percent of perfused choroidal area compared to baseline value at 10 mmHg (Mean ± SEM, n = 5).

Fig. 7
Fig. 7

Top: (A) Typical cross-section OCT structure image (at 20 mmHg) across the CRA where the dashed circle shows the shadowed region, and (B) corresponding flow image of (A). (C) Typical cross-section OCT structure (at 60 mmHg) showing the dimension (between the two lines) for ONH perfusion analysis, and (D) corresponding flow image of (C). Middle: Steps in quantitation of ONH blood perfusion, including removal of retinal vasculature from anterior view 3-D vasculature maps (E to F), generating the blood flow signal pixel map (G) and the ONH volume (H). Image size: 0.5x0.5 mm2. Bottom: Graph of ONH blood perfusion (Mean ± SEM) change of 5 animals at increasing IOPs. Up to 50 mmHg, blood perfusion appears to increase, possibly as a result of improved signal detection due to a gradual decrease in the shadowing effect as blood flow in overlying retinal vessels is reduced. Above 50 mmHg, reduction in ONH blood perfusion overcomes this effect and becomes clearly evident, reducing to near 0 at 100 mmHg and returning to baseline when IOP is lowered to 10 mmHg.

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V Z = Δφ λ 0 4πnΔ t A

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