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Flicker-induced changes in retinal blood flow assessed by Doppler optical coherence tomographyYimin Wang, Amani A. Fawzi, Ou Tan, Xinbo Zhang, and David Huang »View Author Affiliations
Yimin Wang,1
Amani A. Fawzi,2
Ou Tan,1
Xinbo Zhang,1
and David Huang1,*
1Casey Eye Institute and Department of Ophthalmology, Oregon Health & Science University, Portland, OR, USA 2Doheny Eye Institute and Department of Ophthalmology, University of Southern California, Los Angeles, CA, USA *Corresponding author: davidhuang@alum.mit.edu |
Biomedical Optics Express, Vol. 2, Issue 7, pp. 1852-1860 (2011)
http://dx.doi.org/10.1364/BOE.2.001852
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Abstract
We used Doppler Fourier-domain optical coherence tomography (OCT) to investigate flicker-induced changes of total retinal blood flow. Total retinal blood flow was measured by summing flows in veins imaged in double-circular scans around the optic disc. In 3 healthy volunteers, total retinal blood flow was measured before and 10-15 seconds after 30 seconds of flicker stimulation. The average blood flow increased 22.2% (p = 0.002). The total venous and arterial vessel cross-sectional area increased 11.3% (p < 0.001) and +2.7% (p = 0.28) respectively. The average venous and arterial flow velocity were calculated indirectly by dividing total retinal blood flow by total venous and arterial cross-sectional areas. They also increased by 8.8% (p = 0.046) and 18.3% (p = 0.004), respectively. These results show that human retinal blood flow increases after visible flicker stimulation, and this could be measured with OCT.
© 2011 OSA
OCIS Codes
(170.3880) Medical optics and biotechnology : Medical and biological imaging
(170.4470) Medical optics and biotechnology : Ophthalmology
(170.4500) Medical optics and biotechnology : Optical coherence tomography
(280.2490) Remote sensing and sensors : Flow diagnostics
ToC Category:
Ophthalmology Applications
History
Original Manuscript: March 8, 2011
Revised Manuscript: May 25, 2011
Manuscript Accepted: June 3, 2011
Published: June 6, 2011
Virtual Issues
In vivo Microcirculation Imaging
(2011) Biomedical Optics Express
Citation
Yimin Wang, Amani A. Fawzi, Ou Tan, Xinbo Zhang, and David Huang, "Flicker-induced changes in retinal blood flow assessed by Doppler optical coherence tomography," Biomed. Opt. Express 2, 1852-1860 (2011)
http://www.opticsinfobase.org/boe/abstract.cfm?URI=boe-2-7-1852
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References
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- W. Goebel, W. E. Lieb, A. Ho, R. C. Sergott, R. Farhoumand, and F. Grehn, “Color Doppler imaging: a new technique to assess orbital blood flow in patients with diabetic retinopathy,” Invest. Ophthalmol. Vis. Sci. 36(5), 864–870 (1995). [PubMed]
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- G. T. Feke, H. Tagawa, D. M. Deupree, D. G. Goger, J. Sebag, and J. J. Weiter, “Blood flow in the normal human retina,” Invest. Ophthalmol. Vis. Sci. 30(1), 58–65 (1989). [PubMed]
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- F. Formaz, C. E. Riva, and M. Geiser, “Diffuse luminance flicker increases retinal vessel diameter in humans,” Curr. Eye Res. 16(12), 1252–1257 (1997). [CrossRef] [PubMed]
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- M. R. Hee, J. A. Izatt, E. A. Swanson, D. Huang, J. S. Schuman, C. P. Lin, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography of the human retina,” Arch. Ophthalmol. 113(3), 325–332 (1995). [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,” Science 254(5035), 1178–1181 (1991). [CrossRef] [PubMed]
- A. E. Fung, G. A. Lalwani, P. J. Rosenfeld, S. R. Dubovy, S. Michels, W. J. Feuer, C. A. Puliafito, J. L. Davis, H. W. Flynn, and M. Esquiabro, “An optical coherence tomography-guided, variable dosing regimen with intravitreal ranibizumab (Lucentis) for neovascular age-related macular degeneration,” Am. J. Ophthalmol. 143(4), 566–583.e2 (2007). [CrossRef] [PubMed]
- C. E. Riva, T. Salgarello, E. Logean, A. Colotto, E. M. Galan, and B. Falsini, “Flicker-evoked response measured at the optic disc rim is reduced in ocular hypertension and early glaucoma,” Invest. Ophthalmol. Vis. Sci. 45(10), 3662–3668 (2004). [CrossRef] [PubMed]
- J. P. S. Garcia, P. T. Garcia, and R. B. Rosen, “Retinal blood flow in the normal human eye using the canon laser blood flowmeter,” Ophthalmic Res. 34(5), 295–299 (2002). [CrossRef] [PubMed]
- J. P. S. Garcia, P. T. Garcia, and R. B. Rosen, “Retinal blood flow in the normal human eye using the canon laser blood flowmeter,” Ophthalmic Res. 34(5), 295–299 (2002). [CrossRef] [PubMed]
- G. Garhöfer, C. Zawinka, H. Resch, K. H. Huemer, G. T. Dorner, and L. Schmetterer, “Diffuse luminance flicker increases blood flow in major retinal arteries and veins,” Vision Res. 44(8), 833–838 (2004). [CrossRef] [PubMed]
- F. Formaz, C. E. Riva, and M. Geiser, “Diffuse luminance flicker increases retinal vessel diameter in humans,” Curr. Eye Res. 16(12), 1252–1257 (1997). [CrossRef] [PubMed]
- Y. Wang, A. Lu, J. Gil-Flamer, O. Tan, J. A. Izatt, and D. Huang, “Measurement of total blood flow in the normal human retina using Doppler Fourier-domain optical coherence tomography,” Br. J. Ophthalmol. 93(5), 634–637 (2009). [CrossRef] [PubMed]
- W. Goebel, W. E. Lieb, A. Ho, R. C. Sergott, R. Farhoumand, and F. Grehn, “Color Doppler imaging: a new technique to assess orbital blood flow in patients with diabetic retinopathy,” Invest. Ophthalmol. Vis. Sci. 36(5), 864–870 (1995). [PubMed]
- G. T. Feke, H. Tagawa, D. M. Deupree, D. G. Goger, J. Sebag, and J. J. Weiter, “Blood flow in the normal human retina,” Invest. Ophthalmol. Vis. Sci. 30(1), 58–65 (1989). [PubMed]
- D. G. Buerk, B. M. Ances, J. H. Greenberg, and J. A. Detre, “Temporal dynamics of brain tissue nitric oxide during functional forepaw stimulation in rats,” Neuroimage 18(1), 1–9 (2003). [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,” Science 254(5035), 1178–1181 (1991). [CrossRef] [PubMed]
- W. Goebel, W. E. Lieb, A. Ho, R. C. Sergott, R. Farhoumand, and F. Grehn, “Color Doppler imaging: a new technique to assess orbital blood flow in patients with diabetic retinopathy,” Invest. Ophthalmol. Vis. Sci. 36(5), 864–870 (1995). [PubMed]
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- J. S. Schuman, T. Pedut-Kloizman, E. Hertzmark, M. R. Hee, J. R. Wilkins, J. G. Coker, C. A. Puliafito, J. G. Fujimoto, and E. A. Swanson, “Reproducibility of nerve fiber layer thickness measurements using optical coherence tomography,” Ophthalmology 103(11), 1889–1898 (1996). [PubMed]
- M. R. Hee, J. A. Izatt, E. A. Swanson, D. Huang, J. S. Schuman, C. P. Lin, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography of the human retina,” Arch. Ophthalmol. 113(3), 325–332 (1995). [PubMed]
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- G. T. Feke, H. Tagawa, D. M. Deupree, D. G. Goger, J. Sebag, and J. J. Weiter, “Blood flow in the normal human retina,” Invest. Ophthalmol. Vis. Sci. 30(1), 58–65 (1989). [PubMed]
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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]
- Y. Wang, A. Lu, J. Gil-Flamer, O. Tan, J. A. Izatt, and D. Huang, “Measurement of total blood flow in the normal human retina using Doppler Fourier-domain optical coherence tomography,” Br. J. Ophthalmol. 93(5), 634–637 (2009). [CrossRef] [PubMed]
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- G. T. Feke, H. Tagawa, D. M. Deupree, D. G. Goger, J. Sebag, and J. J. Weiter, “Blood flow in the normal human retina,” Invest. Ophthalmol. Vis. Sci. 30(1), 58–65 (1989). [PubMed]
- J. S. Schuman, T. Pedut-Kloizman, E. Hertzmark, M. R. Hee, J. R. Wilkins, J. G. Coker, C. A. Puliafito, J. G. Fujimoto, and E. A. Swanson, “Reproducibility of nerve fiber layer thickness measurements using optical coherence tomography,” Ophthalmology 103(11), 1889–1898 (1996). [PubMed]
- R. A. Leitgeb, L. Schmetterer, C. K. Hitzenberger, A. F. Fercher, F. Berisha, M. Wojtkowski, and T. Bajraszewski, “Real-time measurement of in vitro flow by Fourier-domain color Doppler optical coherence tomography,” Opt. Lett. 29(2), 171–173 (2004). [CrossRef] [PubMed]
- M. Wojtkowski, R. Leitgeb, A. Kowalczyk, T. Bajraszewski, and A. F. Fercher, “In vivo human retinal imaging by Fourier domain optical coherence tomography,” J. Biomed. Opt. 7(3), 457–463 (2002). [CrossRef] [PubMed]
- S. Yazdanfar, A. M. Rollins, and J. A. Izatt, “In vivo imaging of human retinal flow dynamics by color Doppler optical coherence tomography,” Arch. Ophthalmol. 121(2), 235–239 (2003). [PubMed]
- J. A. Izatt, M. D. Kulkarni, S. Yazdanfar, J. K. Barton, and A. J. Welch, “In vivo bidirectional color Doppler flow imaging of picoliter blood volumes using optical coherence tomography,” Opt. Lett. 22(18), 1439–1441 (1997). [CrossRef] [PubMed]
- G. Garhöfer, C. Zawinka, H. Resch, K. H. Huemer, G. T. Dorner, and L. Schmetterer, “Diffuse luminance flicker increases blood flow in major retinal arteries and veins,” Vision Res. 44(8), 833–838 (2004). [CrossRef] [PubMed]
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Acta Ophthalmol. Scand.
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Am. J. Ophthalmol.
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Arch. Ophthalmol.
- S. Yazdanfar, A. M. Rollins, and J. A. Izatt, “In vivo imaging of human retinal flow dynamics by color Doppler optical coherence tomography,” Arch. Ophthalmol. 121(2), 235–239 (2003). [PubMed]
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Cerebrovasc. Brain Metab. Rev.
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Curr. Eye Res.
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Eye (Lond.)
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Invest. Ophthalmol. Vis. Sci.
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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]
- C. E. Riva, T. Salgarello, E. Logean, A. Colotto, E. M. Galan, and B. Falsini, “Flicker-evoked response measured at the optic disc rim is reduced in ocular hypertension and early glaucoma,” Invest. Ophthalmol. Vis. Sci. 45(10), 3662–3668 (2004). [CrossRef] [PubMed]
- W. Goebel, W. E. Lieb, A. Ho, R. C. Sergott, R. Farhoumand, and F. Grehn, “Color Doppler imaging: a new technique to assess orbital blood flow in patients with diabetic retinopathy,” Invest. Ophthalmol. Vis. Sci. 36(5), 864–870 (1995). [PubMed]
- G. T. Feke, H. Tagawa, D. M. Deupree, D. G. Goger, J. Sebag, and J. J. Weiter, “Blood flow in the normal human retina,” Invest. Ophthalmol. Vis. Sci. 30(1), 58–65 (1989). [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]
- G. Donati, C. J. Pournaras, J. L. Munoz, S. Poitry, C. L. Poitry-Yamate, and M. Tsacopoulos, “Nitric oxide controls arteriolar tone in the retina of the miniature pig,” Invest. Ophthalmol. Vis. Sci. 36(11), 2228–2237 (1995). [PubMed]
J. Biomed. Opt.
- Y. Wang, B. A. Bower, J. A. Izatt, O. Tan, and D. Huang, “Retinal blood flow measurement by circumpapillary Fourier domain Doppler optical coherence tomography,” J. Biomed. Opt. 13(6), 064003 (2008). [CrossRef] [PubMed]
- M. Wojtkowski, R. Leitgeb, A. Kowalczyk, T. Bajraszewski, and A. F. Fercher, “In vivo human retinal imaging by Fourier domain optical coherence tomography,” J. Biomed. Opt. 7(3), 457–463 (2002). [CrossRef] [PubMed]
J. Cereb. Blood Flow Metab.
- H. Ito, K. Takahashi, J. Hatazawa, S. G. Kim, and I. Kanno, “Changes in human regional cerebral blood flow and cerebral blood volume during visual stimulation measured by positron emission tomography,” J. Cereb. Blood Flow Metab. 21(5), 608–612 (2001). [CrossRef] [PubMed]
J. Glaucoma
- M. T. Nicolela, P. Hnik, M. Schulzer, and S. M. Drance, “Reproducibility of retinal and optic nerve head blood flow measurements with scanning laser Doppler flowmetry,” J. Glaucoma 6(3), 157–164 (1997). [CrossRef] [PubMed]
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Neurosci. Lett.
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- C. E. Riva, S. Harino, R. D. Shonat, and B. L. Petrig, “Flicker evoked increase in optic nerve head blood flow in anesthetized cats,” Neurosci. Lett. 128(2), 291–296 (1991). [CrossRef] [PubMed]
Ophthalmic Res.
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Ophthalmology
- J. S. Schuman, T. Pedut-Kloizman, E. Hertzmark, M. R. Hee, J. R. Wilkins, J. G. Coker, C. A. Puliafito, J. G. Fujimoto, and E. A. Swanson, “Reproducibility of nerve fiber layer thickness measurements using optical coherence tomography,” Ophthalmology 103(11), 1889–1898 (1996). [PubMed]
- M. Bolz, K. Kriechbaum, C. Simader, G. Deak, J. Lammer, C. Treu, C. Scholda, C. Prünte, U. Schmidt-Erfurth, and Diabetic Retinopathy Research Group Vienna, “In vivo retinal morphology after grid laser treatment in diabetic macular edema,” Ophthalmology 117(3), 538–544 (2010). [CrossRef] [PubMed]
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Opt. Lett.
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Retina
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Science
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Vision Res.
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2011, Wang, Invest. Ophthalmol. Vis. Sci.
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- M. Bolz, K. Kriechbaum, C. Simader, G. Deak, J. Lammer, C. Treu, C. Scholda, C. Prünte, U. Schmidt-Erfurth, and Diabetic Retinopathy Research Group Vienna, “In vivo retinal morphology after grid laser treatment in diabetic macular edema,” Ophthalmology 117(3), 538–544 (2010). [CrossRef] [PubMed]
- Y. Wang, A. Lu, J. Gil-Flamer, O. Tan, J. A. Izatt, and D. Huang, “Measurement of total blood flow in the normal human retina using Doppler Fourier-domain optical coherence tomography,” Br. J. Ophthalmol. 93(5), 634–637 (2009). [CrossRef] [PubMed]
- Y. Wang, B. A. Bower, J. A. Izatt, O. Tan, and D. Huang, “Retinal blood flow measurement by circumpapillary Fourier domain Doppler optical coherence tomography,” J. Biomed. Opt. 13(6), 064003 (2008). [CrossRef] [PubMed]
- A. E. Fung, G. A. Lalwani, P. J. Rosenfeld, S. R. Dubovy, S. Michels, W. J. Feuer, C. A. Puliafito, J. L. Davis, H. W. Flynn, and M. Esquiabro, “An optical coherence tomography-guided, variable dosing regimen with intravitreal ranibizumab (Lucentis) for neovascular age-related macular degeneration,” Am. J. Ophthalmol. 143(4), 566–583.e2 (2007). [CrossRef] [PubMed]
- C. E. Riva, E. Logean, and B. Falsini, “Visually evoked hemodynamical response and assessment of neurovascular coupling in the optic nerve and retina,” Prog. Retin. Eye Res. 24(2), 183–215 (2005). [CrossRef] [PubMed]
- C. E. Riva, T. Salgarello, E. Logean, A. Colotto, E. M. Galan, and B. Falsini, “Flicker-evoked response measured at the optic disc rim is reduced in ocular hypertension and early glaucoma,” Invest. Ophthalmol. Vis. Sci. 45(10), 3662–3668 (2004). [CrossRef] [PubMed]
- G. Garhöfer, C. Zawinka, H. Resch, K. H. Huemer, G. T. Dorner, and L. Schmetterer, “Diffuse luminance flicker increases blood flow in major retinal arteries and veins,” Vision Res. 44(8), 833–838 (2004). [CrossRef] [PubMed]
- D. G. Buerk, B. M. Ances, J. H. Greenberg, and J. A. Detre, “Temporal dynamics of brain tissue nitric oxide during functional forepaw stimulation in rats,” Neuroimage 18(1), 1–9 (2003). [CrossRef] [PubMed]
- S. Yazdanfar, A. M. Rollins, and J. A. Izatt, “In vivo imaging of human retinal flow dynamics by color Doppler optical coherence tomography,” Arch. Ophthalmol. 121(2), 235–239 (2003). [PubMed]
- J. P. S. Garcia, P. T. Garcia, and R. B. Rosen, “Retinal blood flow in the normal human eye using the canon laser blood flowmeter,” Ophthalmic Res. 34(5), 295–299 (2002). [CrossRef] [PubMed]
- M. Wojtkowski, R. Leitgeb, A. Kowalczyk, T. Bajraszewski, and A. F. Fercher, “In vivo human retinal imaging by Fourier domain optical coherence tomography,” J. Biomed. Opt. 7(3), 457–463 (2002). [CrossRef] [PubMed]
- G. Michelson, A. Patzelt, and J. Harazny, “Flickering light increases retinal blood flow,” Retina 22(3), 336–343 (2002). [CrossRef] [PubMed]
- K. Polak, L. Schmetterer, and C. E. Riva, “Influence of flicker frequency on flicker-induced changes of retinal vessel diameter,” Invest. Ophthalmol. Vis. Sci. 43(8), 2721–2726 (2002). [PubMed]
- H. Ito, K. Takahashi, J. Hatazawa, S. G. Kim, and I. Kanno, “Changes in human regional cerebral blood flow and cerebral blood volume during visual stimulation measured by positron emission tomography,” J. Cereb. Blood Flow Metab. 21(5), 608–612 (2001). [CrossRef] [PubMed]
- M. T. Nicolela, P. Hnik, M. Schulzer, and S. M. Drance, “Reproducibility of retinal and optic nerve head blood flow measurements with scanning laser Doppler flowmetry,” J. Glaucoma 6(3), 157–164 (1997). [CrossRef] [PubMed]
- F. Formaz, C. E. Riva, and M. Geiser, “Diffuse luminance flicker increases retinal vessel diameter in humans,” Curr. Eye Res. 16(12), 1252–1257 (1997). [CrossRef] [PubMed]
- L. Wang and A. Bill, “Effects of constant and flickering light on retinal metabolism in rabbits,” Acta Ophthalmol. Scand. 75(3), 227–231 (1997). [CrossRef] [PubMed]
- J. S. Schuman, T. Pedut-Kloizman, E. Hertzmark, M. R. Hee, J. R. Wilkins, J. G. Coker, C. A. Puliafito, J. G. Fujimoto, and E. A. Swanson, “Reproducibility of nerve fiber layer thickness measurements using optical coherence tomography,” Ophthalmology 103(11), 1889–1898 (1996). [PubMed]
- M. R. Hee, J. A. Izatt, E. A. Swanson, D. Huang, J. S. Schuman, C. P. Lin, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography of the human retina,” Arch. Ophthalmol. 113(3), 325–332 (1995). [PubMed]
- A. Villringer and U. Dirnagl, “Coupling of brain activity and cerebral blood flow: basis of functional neuroimaging,” Cerebrovasc. Brain Metab. Rev. 7(3), 240–276 (1995). [PubMed]
- W. Goebel, W. E. Lieb, A. Ho, R. C. Sergott, R. Farhoumand, and F. Grehn, “Color Doppler imaging: a new technique to assess orbital blood flow in patients with diabetic retinopathy,” Invest. Ophthalmol. Vis. Sci. 36(5), 864–870 (1995). [PubMed]
- J. Kiryu, S. Asrani, M. Shahidi, M. Mori, and R. Zeimer, “Local response of the primate retinal microcirculation to increased metabolic demand induced by flicker,” Invest. Ophthalmol. Vis. Sci. 36(7), 1240–1246 (1995). [PubMed]
- G. Donati, C. J. Pournaras, J. L. Munoz, S. Poitry, C. L. Poitry-Yamate, and M. Tsacopoulos, “Nitric oxide controls arteriolar tone in the retina of the miniature pig,” Invest. Ophthalmol. Vis. Sci. 36(11), 2228–2237 (1995). [PubMed]
- A. J. Scheiner, C. E. Riva, K. Kazahaya, and B. L. Petrig, “Effect of flicker on macular blood flow assessed by the blue field simulation technique,” Invest. Ophthalmol. Vis. Sci. 35(9), 3436–3441 (1994). [PubMed]
- C. E. Riva, S. Harino, R. D. Shonat, and B. L. Petrig, “Flicker evoked increase in optic nerve head blood flow in anesthetized cats,” Neurosci. Lett. 128(2), 291–296 (1991). [CrossRef] [PubMed]
- C. E. Riva, S. Harino, R. D. Shonat, and B. L. Petrig, “Flicker evoked increase in optic nerve head blood flow in anesthetized cats,” Neurosci. Lett. 128(2), 291–296 (1991). [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,” Science 254(5035), 1178–1181 (1991). [CrossRef] [PubMed]
- A. Bill and G. O. Sperber, “Control of retinal and choroidal blood flow,” Eye (Lond.) 4(Pt 2), 319–325 (1990). [PubMed]
- G. T. Feke, H. Tagawa, D. M. Deupree, D. G. Goger, J. Sebag, and J. J. Weiter, “Blood flow in the normal human retina,” Invest. Ophthalmol. Vis. Sci. 30(1), 58–65 (1989). [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]
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