Abstract

A method of measuring cortical oxygen metabolism in the mouse brain that uses independent quantitative measurements of three key parameters: cerebral blood flow (CBF), arteriovenous oxygen extraction (OE), and hemoglobin concentration ([HbT]) is presented. Measurements were performed using a single visible light spectral/Fourier domain OCT microscope, with Doppler and spectroscopic capabilities, through a thinned-skull cranial window in the mouse brain. Baseline metabolic measurements in mice are shown to be consistent with literature values. Oxygen consumption, as measured by this method, did not change substantially during minor changes either in the fraction of inspired oxygen (FiO2) or in the fraction of inspired carbon dioxide (FiCO2), in spite of larger variations in oxygen saturations. This set of experiments supports, but does not prove, the validity of the proposed method of measuring brain oxygen metabolism.

© 2015 Optical Society of America

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2015 (3)

2014 (4)

W. Song, Q. Wei, W. Liu, T. Liu, J. Yi, N. Sheibani, A. A. Fawzi, R. A. Linsenmeier, S. Jiao, and H. F. Zhang, “A combined method to quantify the retinal metabolic rate of oxygen using photoacoustic ophthalmoscopy and optical coherence tomography,” Sci. Rep. 4, 6525 (2014).
[Crossref] [PubMed]

A. Torricelli, D. Contini, A. Pifferi, M. Caffini, R. Re, L. Zucchelli, and L. Spinelli, “Time domain functional NIRS imaging for human brain mapping,” Neuroimage 85(Pt 1), 28–50 (2014).
[Crossref] [PubMed]

T. Durduran and A. G. Yodh, “Diffuse correlation spectroscopy for non-invasive, micro-vascular cerebral blood flow measurement,” Neuroimage 85(Pt 1), 51–63 (2014).
[Crossref] [PubMed]

L. Østergaard, T. S. Engedal, R. Aamand, R. Mikkelsen, N. K. Iversen, M. Anzabi, E. T. Næss-Schmidt, K. R. Drasbek, V. Bay, J. U. Blicher, A. Tietze, I. K. Mikkelsen, B. Hansen, S. N. Jespersen, N. Juul, J. C. Sørensen, and M. Rasmussen, “Capillary transit time heterogeneity and flow-metabolism coupling after traumatic brain injury,” J. Cereb. Blood Flow Metab. 34(10), 1585–1598 (2014).
[Crossref] [PubMed]

2013 (8)

A. Parpaleix, Y. Houssen, and S. Charpak, “Imaging local neuronal activity by monitoring PO₂ transients in capillaries,” Nat. Med. 19(2), 241–246 (2013).
[Crossref] [PubMed]

L. Wang, K. Maslov, and L. V. Wang, “Single-cell label-free photoacoustic flowoxigraphy in vivo,” Proc. Natl. Acad. Sci. U.S.A. 110(15), 5759–5764 (2013).
[Crossref] [PubMed]

W. Cui, X. H. Zhu, M. L. Vollmers, E. T. Colonna, G. Adriany, B. Tramm, J. M. Dubinsky, and G. Öz, “Non-invasive measurement of cerebral oxygen metabolism in the mouse brain by ultra-high field (17)O MR spectroscopy,” J. Cereb. Blood Flow Metab. 33(12), 1846–1849 (2013).
[Crossref] [PubMed]

J. Wanek, P. Y. Teng, N. P. Blair, and M. Shahidi, “Inner retinal oxygen delivery and metabolism under normoxia and hypoxia in rat,” Invest. Ophthalmol. Vis. Sci. 54(7), 5012–5019 (2013).
[Crossref] [PubMed]

J. Yi, Q. Wei, W. Liu, V. Backman, and H. F. Zhang, “Visible-light optical coherence tomography for retinal oximetry,” Opt. Lett. 38(11), 1796–1798 (2013).
[Crossref] [PubMed]

P. Blinder, P. S. Tsai, J. P. Kaufhold, P. M. Knutsen, H. Suhl, and D. Kleinfeld, “The cortical angiome: an interconnected vascular network with noncolumnar patterns of blood flow,” Nat. Neurosci. 16(7), 889–897 (2013).
[Crossref] [PubMed]

X. H. Zhu, J. M. Chen, T. W. Tu, W. Chen, and S. K. Song, “Simultaneous and noninvasive imaging of cerebral oxygen metabolic rate, blood flow and oxygen extraction fraction in stroke mice,” Neuroimage 64, 437–447 (2013).
[Crossref] [PubMed]

V. J. Srinivasan, E. T. Mandeville, A. Can, F. Blasi, M. Climov, A. Daneshmand, J. H. Lee, E. Yu, H. Radhakrishnan, E. H. Lo, S. Sakadžić, K. Eikermann-Haerter, and C. Ayata, “Multiparametric, longitudinal optical coherence tomography imaging reveals acute injury and chronic recovery in experimental ischemic stroke,” PLoS One 8(8), e71478 (2013).
[Crossref] [PubMed]

2012 (3)

A. K. Dunn, “Laser speckle contrast imaging of cerebral blood flow,” Ann. Biomed. Eng. 40(2), 367–377 (2012).
[Crossref] [PubMed]

C. N. Hall, M. C. Klein-Flügge, C. Howarth, and D. Attwell, “Oxidative phosphorylation, not glycolysis, powers presynaptic and postsynaptic mechanisms underlying brain information processing,” J. Neurosci. 32(26), 8940–8951 (2012).
[Crossref] [PubMed]

D. A. Antonetti, R. Klein, and T. W. Gardner, “Diabetic retinopathy,” N. Engl. J. Med. 366(13), 1227–1239 (2012).
[Crossref] [PubMed]

2011 (4)

J. Yao, K. I. Maslov, Y. Zhang, Y. Xia, and L. V. Wang, “Label-free oxygen-metabolic photoacoustic microscopy in vivo,” J. Biomed. Opt. 16(7), 076003 (2011).
[Crossref] [PubMed]

B. M. Raabe, J. E. Artwohl, J. E. Purcell, J. Lovaglio, and J. D. Fortman, “Effects of weekly blood collection in C57BL/6 mice,” J. Am. Assoc. Lab. Anim. Sci. 50(5), 680–685 (2011).
[PubMed]

K. A. Kasischke, E. M. Lambert, B. Panepento, A. Sun, H. A. Gelbard, R. W. Burgess, T. H. Foster, and M. Nedergaard, “Two-photon NADH imaging exposes boundaries of oxygen diffusion in cortical vascular supply regions,” J. Cereb. Blood Flow Metab. 31(1), 68–81 (2011).
[Crossref] [PubMed]

F. E. Robles, C. Wilson, G. Grant, and A. Wax, “Molecular imaging true-colour spectroscopic optical coherence tomography,” Nat. Photonics 5(12), 744–747 (2011).
[Crossref] [PubMed]

2010 (2)

P. J. Drew, A. Y. Shih, J. D. Driscoll, P. M. Knutsen, P. Blinder, D. Davalos, K. Akassoglou, P. S. Tsai, and D. Kleinfeld, “Chronic optical access through a polished and reinforced thinned skull,” Nat. Methods 7(12), 981–984 (2010).
[Crossref] [PubMed]

K. A. Williams, M. Magnuson, W. Majeed, S. M. LaConte, S. J. Peltier, X. Hu, and S. D. Keilholz, “Comparison of alpha-chloralose, medetomidine and isoflurane anesthesia for functional connectivity mapping in the rat,” Magn. Reson. Imaging 28(7), 995–1003 (2010).
[Crossref] [PubMed]

2008 (3)

A. L. Vazquez, K. Masamoto, and S. G. Kim, “Dynamics of oxygen delivery and consumption during evoked neural stimulation using a compartment model and CBF and tissue P(O2) measurements,” Neuroimage 42(1), 49–59 (2008).
[Crossref] [PubMed]

A. D. Estrada, A. Ponticorvo, T. N. Ford, and A. K. Dunn, “Microvascular oxygen quantification using two-photon microscopy,” Opt. Lett. 33(10), 1038–1040 (2008).
[Crossref] [PubMed]

M. Mozaffarieh, M. C. Grieshaber, and J. Flammer, “Oxygen and blood flow: players in the pathogenesis of glaucoma,” Mol. Vis. 14, 224–233 (2008).
[PubMed]

2007 (2)

J. Karbowski, “Global and regional brain metabolic scaling and its functional consequences,” BMC Biol. 5(1), 18 (2007).
[Crossref] [PubMed]

Y. Wang, B. A. Bower, J. A. Izatt, O. Tan, and D. Huang, “In vivo total retinal blood flow measurement by Fourier domain Doppler optical coherence tomography,” J. Biomed. Opt. 12(4), 041215 (2007).
[Crossref] [PubMed]

2006 (1)

S. H. Yee, K. Lee, P. A. Jerabek, and P. T. Fox, “Quantitative measurement of oxygen metabolic rate in the rat brain using microPET imaging of briefly inhaled 15O-labelled oxygen gas,” Nucl. Med. Commun. 27(7), 573–581 (2006).
[Crossref] [PubMed]

2005 (1)

A. K. Dunn, A. Devor, A. M. Dale, and D. A. Boas, “Spatial extent of oxygen metabolism and hemodynamic changes during functional activation of the rat somatosensory cortex,” Neuroimage 27(2), 279–290 (2005).
[Crossref] [PubMed]

2004 (1)

C. Iadecola, “Neurovascular regulation in the normal brain and in Alzheimer’s disease,” Nat. Rev. Neurosci. 5(5), 347–360 (2004).
[Crossref] [PubMed]

2003 (1)

J. P. Culver, T. Durduran, D. Furuya, C. Cheung, J. H. Greenberg, and A. G. Yodh, “Diffuse optical tomography of cerebral blood flow, oxygenation, and metabolism in rat during focal ischemia,” J. Cereb. Blood Flow Metab. 23(8), 911–924 (2003).
[Crossref] [PubMed]

2001 (1)

M. E. Raichle, A. M. MacLeod, A. Z. Snyder, W. J. Powers, D. A. Gusnard, and G. L. Shulman, “A default mode of brain function,” Proc. Natl. Acad. Sci. U.S.A. 98(2), 676–682 (2001).
[Crossref] [PubMed]

2000 (1)

B. J. Tromberg, N. Shah, R. Lanning, A. Cerussi, J. Espinoza, T. Pham, L. Svaasand, and J. Butler, “Non-invasive in vivo characterization of breast tumors using photon migration spectroscopy,” Neoplasia 2(1-2), 26–40 (2000).
[Crossref] [PubMed]

1999 (2)

U. Dirnagl, C. Iadecola, and M. A. Moskowitz, “Pathobiology of ischaemic stroke: an integrated view,” Trends Neurosci. 22(9), 391–397 (1999).
[Crossref] [PubMed]

J. A. Ulatowski, J. M. E. Oja, J. I. Suarez, R. A. Kauppinen, R. J. Traystman, and P. C. M. van Zijl, “In vivo determination of absolute cerebral blood volume using hemoglobin as a natural contrast agent: An MRI study using altered arterial carbon dioxide tension,” J. Cereb. Blood Flow Metab. 19(7), 809–817 (1999).
[Crossref] [PubMed]

1998 (2)

T. L. Davis, K. K. Kwong, R. M. Weisskoff, and B. R. Rosen, “Calibrated functional MRI: mapping the dynamics of oxidative metabolism,” Proc. Natl. Acad. Sci. U.S.A. 95(4), 1834–1839 (1998).
[Crossref] [PubMed]

J. B. Mandeville, J. J. A. Marota, B. E. Kosofsky, J. R. Keltner, R. Weissleder, B. R. Rosen, and R. M. Weisskoff, “Dynamic functional imaging of relative cerebral blood volume during rat forepaw stimulation,” Magn. Reson. Med. 39(4), 615–624 (1998).
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1997 (2)

1995 (1)

1993 (2)

A. Villringer, J. Planck, C. Hock, L. Schleinkofer, and U. Dirnagl, “Near infrared spectroscopy (NIRS): a new tool to study hemodynamic changes during activation of brain function in human adults,” Neurosci. Lett. 154(1-2), 101–104 (1993).
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S. Ogawa, R. S. Menon, D. W. Tank, S. G. Kim, H. Merkle, J. M. Ellermann, and K. Ugurbil, “Functional brain mapping by blood oxygenation level-dependent contrast magnetic resonance imaging. A comparison of signal characteristics with a biophysical model,” Biophys. J. 64(3), 803–812 (1993).
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1990 (3)

S. Ogawa, T. M. Lee, A. R. Kay, and D. W. Tank, “Brain magnetic resonance imaging with contrast dependent on blood oxygenation,” Proc. Natl. Acad. Sci. U.S.A. 87(24), 9868–9872 (1990).
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E. Stefansson, “Oxygen and diabetic eye disease,” Graefes Arch. Clin. Exp. Ophthalmol. 228(2), 120–123 (1990).
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1989 (3)

M. S. Patterson, B. Chance, and B. C. Wilson, “Time resolved reflectance and transmittance for the non-invasive measurement of tissue optical properties,” Appl. Opt. 28(12), 2331–2336 (1989).
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U. Dirnagl, B. Kaplan, M. Jacewicz, and W. Pulsinelli, “Continuous measurement of cerebral cortical blood flow by laser-Doppler flowmetry in a rat stroke model,” J. Cereb. Blood Flow Metab. 9(5), 589–596 (1989).
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1986 (1)

H. J. Kretschmann, G. Kammradt, I. Krauthausen, B. Sauer, and F. Wingert, “Brain growth in man,” Bibl. Anat. 28, 1–26 (1986).
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1985 (1)

M. C. Ingvar, P. Maeder, L. Sokoloff, and C. B. Smith, “Effects of ageing on local rates of cerebral protein synthesis in Sprague-Dawley rats,” Brain 108(1), 155–170 (1985).
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1984 (1)

M. A. Mintun, M. E. Raichle, W. R. Martin, and P. Herscovitch, “Brain oxygen utilization measured with O-15 radiotracers and positron emission tomography,” J. Nucl. Med. 25(2), 177–187 (1984).
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1980 (1)

C. B. Smith, C. Goochee, S. I. Rapoport, and L. Sokoloff, “Effects of ageing on local rates of cerebral glucose utilization in the rat,” Brain 103(2), 351–365 (1980).
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Aamand, R.

L. Østergaard, T. S. Engedal, R. Aamand, R. Mikkelsen, N. K. Iversen, M. Anzabi, E. T. Næss-Schmidt, K. R. Drasbek, V. Bay, J. U. Blicher, A. Tietze, I. K. Mikkelsen, B. Hansen, S. N. Jespersen, N. Juul, J. C. Sørensen, and M. Rasmussen, “Capillary transit time heterogeneity and flow-metabolism coupling after traumatic brain injury,” J. Cereb. Blood Flow Metab. 34(10), 1585–1598 (2014).
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Adriany, G.

W. Cui, X. H. Zhu, M. L. Vollmers, E. T. Colonna, G. Adriany, B. Tramm, J. M. Dubinsky, and G. Öz, “Non-invasive measurement of cerebral oxygen metabolism in the mouse brain by ultra-high field (17)O MR spectroscopy,” J. Cereb. Blood Flow Metab. 33(12), 1846–1849 (2013).
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Akassoglou, K.

P. J. Drew, A. Y. Shih, J. D. Driscoll, P. M. Knutsen, P. Blinder, D. Davalos, K. Akassoglou, P. S. Tsai, and D. Kleinfeld, “Chronic optical access through a polished and reinforced thinned skull,” Nat. Methods 7(12), 981–984 (2010).
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D. A. Antonetti, R. Klein, and T. W. Gardner, “Diabetic retinopathy,” N. Engl. J. Med. 366(13), 1227–1239 (2012).
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Anzabi, M.

L. Østergaard, T. S. Engedal, R. Aamand, R. Mikkelsen, N. K. Iversen, M. Anzabi, E. T. Næss-Schmidt, K. R. Drasbek, V. Bay, J. U. Blicher, A. Tietze, I. K. Mikkelsen, B. Hansen, S. N. Jespersen, N. Juul, J. C. Sørensen, and M. Rasmussen, “Capillary transit time heterogeneity and flow-metabolism coupling after traumatic brain injury,” J. Cereb. Blood Flow Metab. 34(10), 1585–1598 (2014).
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Arridge, S. R.

D. T. Delpy, S. R. Arridge, M. Cope, D. Edwards, E. O. Reynolds, C. E. Richardson, S. Wray, J. Wyatt, and P. van der Zee, “Quantitation of pathlength in optical spectroscopy,” Adv. Exp. Med. Biol. 248, 41–46 (1989).
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Artwohl, J. E.

B. M. Raabe, J. E. Artwohl, J. E. Purcell, J. Lovaglio, and J. D. Fortman, “Effects of weekly blood collection in C57BL/6 mice,” J. Am. Assoc. Lab. Anim. Sci. 50(5), 680–685 (2011).
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Ashkanian, M.

L. Østergaard, S. N. Jespersen, T. Engedahl, E. Gutiérrez Jiménez, M. Ashkanian, M. B. Hansen, S. Eskildsen, and K. Mouridsen, “Capillary dysfunction: its detection and causative role in dementias and stroke,” Curr. Neurol. Neurosci. Rep. 15(6), 37 (2015).
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Attwell, D.

C. N. Hall, M. C. Klein-Flügge, C. Howarth, and D. Attwell, “Oxidative phosphorylation, not glycolysis, powers presynaptic and postsynaptic mechanisms underlying brain information processing,” J. Neurosci. 32(26), 8940–8951 (2012).
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V. J. Srinivasan, E. T. Mandeville, A. Can, F. Blasi, M. Climov, A. Daneshmand, J. H. Lee, E. Yu, H. Radhakrishnan, E. H. Lo, S. Sakadžić, K. Eikermann-Haerter, and C. Ayata, “Multiparametric, longitudinal optical coherence tomography imaging reveals acute injury and chronic recovery in experimental ischemic stroke,” PLoS One 8(8), e71478 (2013).
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Backman, V.

Barton, J. K.

Bay, V.

L. Østergaard, T. S. Engedal, R. Aamand, R. Mikkelsen, N. K. Iversen, M. Anzabi, E. T. Næss-Schmidt, K. R. Drasbek, V. Bay, J. U. Blicher, A. Tietze, I. K. Mikkelsen, B. Hansen, S. N. Jespersen, N. Juul, J. C. Sørensen, and M. Rasmussen, “Capillary transit time heterogeneity and flow-metabolism coupling after traumatic brain injury,” J. Cereb. Blood Flow Metab. 34(10), 1585–1598 (2014).
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Blair, N. P.

J. Wanek, P. Y. Teng, N. P. Blair, and M. Shahidi, “Inner retinal oxygen delivery and metabolism under normoxia and hypoxia in rat,” Invest. Ophthalmol. Vis. Sci. 54(7), 5012–5019 (2013).
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Blasi, F.

V. J. Srinivasan, E. T. Mandeville, A. Can, F. Blasi, M. Climov, A. Daneshmand, J. H. Lee, E. Yu, H. Radhakrishnan, E. H. Lo, S. Sakadžić, K. Eikermann-Haerter, and C. Ayata, “Multiparametric, longitudinal optical coherence tomography imaging reveals acute injury and chronic recovery in experimental ischemic stroke,” PLoS One 8(8), e71478 (2013).
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Blicher, J. U.

L. Østergaard, T. S. Engedal, R. Aamand, R. Mikkelsen, N. K. Iversen, M. Anzabi, E. T. Næss-Schmidt, K. R. Drasbek, V. Bay, J. U. Blicher, A. Tietze, I. K. Mikkelsen, B. Hansen, S. N. Jespersen, N. Juul, J. C. Sørensen, and M. Rasmussen, “Capillary transit time heterogeneity and flow-metabolism coupling after traumatic brain injury,” J. Cereb. Blood Flow Metab. 34(10), 1585–1598 (2014).
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Blinder, P.

P. Blinder, P. S. Tsai, J. P. Kaufhold, P. M. Knutsen, H. Suhl, and D. Kleinfeld, “The cortical angiome: an interconnected vascular network with noncolumnar patterns of blood flow,” Nat. Neurosci. 16(7), 889–897 (2013).
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P. J. Drew, A. Y. Shih, J. D. Driscoll, P. M. Knutsen, P. Blinder, D. Davalos, K. Akassoglou, P. S. Tsai, and D. Kleinfeld, “Chronic optical access through a polished and reinforced thinned skull,” Nat. Methods 7(12), 981–984 (2010).
[Crossref] [PubMed]

Boas, D. A.

A. K. Dunn, A. Devor, A. M. Dale, and D. A. Boas, “Spatial extent of oxygen metabolism and hemodynamic changes during functional activation of the rat somatosensory cortex,” Neuroimage 27(2), 279–290 (2005).
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Bower, B. A.

Y. Wang, B. A. Bower, J. A. Izatt, O. Tan, and D. Huang, “In vivo total retinal blood flow measurement by Fourier domain Doppler optical coherence tomography,” J. Biomed. Opt. 12(4), 041215 (2007).
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Burgess, R. W.

K. A. Kasischke, E. M. Lambert, B. Panepento, A. Sun, H. A. Gelbard, R. W. Burgess, T. H. Foster, and M. Nedergaard, “Two-photon NADH imaging exposes boundaries of oxygen diffusion in cortical vascular supply regions,” J. Cereb. Blood Flow Metab. 31(1), 68–81 (2011).
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Butler, J.

B. J. Tromberg, N. Shah, R. Lanning, A. Cerussi, J. Espinoza, T. Pham, L. Svaasand, and J. Butler, “Non-invasive in vivo characterization of breast tumors using photon migration spectroscopy,” Neoplasia 2(1-2), 26–40 (2000).
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Caffini, M.

A. Torricelli, D. Contini, A. Pifferi, M. Caffini, R. Re, L. Zucchelli, and L. Spinelli, “Time domain functional NIRS imaging for human brain mapping,” Neuroimage 85(Pt 1), 28–50 (2014).
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Can, A.

V. J. Srinivasan, E. T. Mandeville, A. Can, F. Blasi, M. Climov, A. Daneshmand, J. H. Lee, E. Yu, H. Radhakrishnan, E. H. Lo, S. Sakadžić, K. Eikermann-Haerter, and C. Ayata, “Multiparametric, longitudinal optical coherence tomography imaging reveals acute injury and chronic recovery in experimental ischemic stroke,” PLoS One 8(8), e71478 (2013).
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Cerussi, A.

B. J. Tromberg, N. Shah, R. Lanning, A. Cerussi, J. Espinoza, T. Pham, L. Svaasand, and J. Butler, “Non-invasive in vivo characterization of breast tumors using photon migration spectroscopy,” Neoplasia 2(1-2), 26–40 (2000).
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Cerussi, A. E.

Chance, B.

Charpak, S.

A. Parpaleix, Y. Houssen, and S. Charpak, “Imaging local neuronal activity by monitoring PO₂ transients in capillaries,” Nat. Med. 19(2), 241–246 (2013).
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Chen, J. M.

X. H. Zhu, J. M. Chen, T. W. Tu, W. Chen, and S. K. Song, “Simultaneous and noninvasive imaging of cerebral oxygen metabolic rate, blood flow and oxygen extraction fraction in stroke mice,” Neuroimage 64, 437–447 (2013).
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Chen, W.

X. H. Zhu, J. M. Chen, T. W. Tu, W. Chen, and S. K. Song, “Simultaneous and noninvasive imaging of cerebral oxygen metabolic rate, blood flow and oxygen extraction fraction in stroke mice,” Neuroimage 64, 437–447 (2013).
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Chen, Z.

Cheung, C.

J. P. Culver, T. Durduran, D. Furuya, C. Cheung, J. H. Greenberg, and A. G. Yodh, “Diffuse optical tomography of cerebral blood flow, oxygenation, and metabolism in rat during focal ischemia,” J. Cereb. Blood Flow Metab. 23(8), 911–924 (2003).
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Chong, S. P.

Climov, M.

V. J. Srinivasan, E. T. Mandeville, A. Can, F. Blasi, M. Climov, A. Daneshmand, J. H. Lee, E. Yu, H. Radhakrishnan, E. H. Lo, S. Sakadžić, K. Eikermann-Haerter, and C. Ayata, “Multiparametric, longitudinal optical coherence tomography imaging reveals acute injury and chronic recovery in experimental ischemic stroke,” PLoS One 8(8), e71478 (2013).
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Colonna, E. T.

W. Cui, X. H. Zhu, M. L. Vollmers, E. T. Colonna, G. Adriany, B. Tramm, J. M. Dubinsky, and G. Öz, “Non-invasive measurement of cerebral oxygen metabolism in the mouse brain by ultra-high field (17)O MR spectroscopy,” J. Cereb. Blood Flow Metab. 33(12), 1846–1849 (2013).
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Contini, D.

A. Torricelli, D. Contini, A. Pifferi, M. Caffini, R. Re, L. Zucchelli, and L. Spinelli, “Time domain functional NIRS imaging for human brain mapping,” Neuroimage 85(Pt 1), 28–50 (2014).
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Cope, M.

D. T. Delpy, S. R. Arridge, M. Cope, D. Edwards, E. O. Reynolds, C. E. Richardson, S. Wray, J. Wyatt, and P. van der Zee, “Quantitation of pathlength in optical spectroscopy,” Adv. Exp. Med. Biol. 248, 41–46 (1989).
[Crossref] [PubMed]

Cui, W.

W. Cui, X. H. Zhu, M. L. Vollmers, E. T. Colonna, G. Adriany, B. Tramm, J. M. Dubinsky, and G. Öz, “Non-invasive measurement of cerebral oxygen metabolism in the mouse brain by ultra-high field (17)O MR spectroscopy,” J. Cereb. Blood Flow Metab. 33(12), 1846–1849 (2013).
[Crossref] [PubMed]

Culver, J. P.

J. P. Culver, T. Durduran, D. Furuya, C. Cheung, J. H. Greenberg, and A. G. Yodh, “Diffuse optical tomography of cerebral blood flow, oxygenation, and metabolism in rat during focal ischemia,” J. Cereb. Blood Flow Metab. 23(8), 911–924 (2003).
[Crossref] [PubMed]

Dale, A. M.

A. K. Dunn, A. Devor, A. M. Dale, and D. A. Boas, “Spatial extent of oxygen metabolism and hemodynamic changes during functional activation of the rat somatosensory cortex,” Neuroimage 27(2), 279–290 (2005).
[Crossref] [PubMed]

Daneshmand, A.

V. J. Srinivasan, E. T. Mandeville, A. Can, F. Blasi, M. Climov, A. Daneshmand, J. H. Lee, E. Yu, H. Radhakrishnan, E. H. Lo, S. Sakadžić, K. Eikermann-Haerter, and C. Ayata, “Multiparametric, longitudinal optical coherence tomography imaging reveals acute injury and chronic recovery in experimental ischemic stroke,” PLoS One 8(8), e71478 (2013).
[Crossref] [PubMed]

Davalos, D.

P. J. Drew, A. Y. Shih, J. D. Driscoll, P. M. Knutsen, P. Blinder, D. Davalos, K. Akassoglou, P. S. Tsai, and D. Kleinfeld, “Chronic optical access through a polished and reinforced thinned skull,” Nat. Methods 7(12), 981–984 (2010).
[Crossref] [PubMed]

Dave, D.

Davis, T. L.

T. L. Davis, K. K. Kwong, R. M. Weisskoff, and B. R. Rosen, “Calibrated functional MRI: mapping the dynamics of oxidative metabolism,” Proc. Natl. Acad. Sci. U.S.A. 95(4), 1834–1839 (1998).
[Crossref] [PubMed]

Delpy, D. T.

D. T. Delpy, S. R. Arridge, M. Cope, D. Edwards, E. O. Reynolds, C. E. Richardson, S. Wray, J. Wyatt, and P. van der Zee, “Quantitation of pathlength in optical spectroscopy,” Adv. Exp. Med. Biol. 248, 41–46 (1989).
[Crossref] [PubMed]

Devor, A.

A. K. Dunn, A. Devor, A. M. Dale, and D. A. Boas, “Spatial extent of oxygen metabolism and hemodynamic changes during functional activation of the rat somatosensory cortex,” Neuroimage 27(2), 279–290 (2005).
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Dirnagl, U.

U. Dirnagl, C. Iadecola, and M. A. Moskowitz, “Pathobiology of ischaemic stroke: an integrated view,” Trends Neurosci. 22(9), 391–397 (1999).
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A. Villringer, J. Planck, C. Hock, L. Schleinkofer, and U. Dirnagl, “Near infrared spectroscopy (NIRS): a new tool to study hemodynamic changes during activation of brain function in human adults,” Neurosci. Lett. 154(1-2), 101–104 (1993).
[Crossref] [PubMed]

U. Dirnagl, B. Kaplan, M. Jacewicz, and W. Pulsinelli, “Continuous measurement of cerebral cortical blood flow by laser-Doppler flowmetry in a rat stroke model,” J. Cereb. Blood Flow Metab. 9(5), 589–596 (1989).
[Crossref] [PubMed]

Drasbek, K. R.

L. Østergaard, T. S. Engedal, R. Aamand, R. Mikkelsen, N. K. Iversen, M. Anzabi, E. T. Næss-Schmidt, K. R. Drasbek, V. Bay, J. U. Blicher, A. Tietze, I. K. Mikkelsen, B. Hansen, S. N. Jespersen, N. Juul, J. C. Sørensen, and M. Rasmussen, “Capillary transit time heterogeneity and flow-metabolism coupling after traumatic brain injury,” J. Cereb. Blood Flow Metab. 34(10), 1585–1598 (2014).
[Crossref] [PubMed]

Drew, P. J.

P. J. Drew, A. Y. Shih, J. D. Driscoll, P. M. Knutsen, P. Blinder, D. Davalos, K. Akassoglou, P. S. Tsai, and D. Kleinfeld, “Chronic optical access through a polished and reinforced thinned skull,” Nat. Methods 7(12), 981–984 (2010).
[Crossref] [PubMed]

Driscoll, J. D.

P. J. Drew, A. Y. Shih, J. D. Driscoll, P. M. Knutsen, P. Blinder, D. Davalos, K. Akassoglou, P. S. Tsai, and D. Kleinfeld, “Chronic optical access through a polished and reinforced thinned skull,” Nat. Methods 7(12), 981–984 (2010).
[Crossref] [PubMed]

Dubinsky, J. M.

W. Cui, X. H. Zhu, M. L. Vollmers, E. T. Colonna, G. Adriany, B. Tramm, J. M. Dubinsky, and G. Öz, “Non-invasive measurement of cerebral oxygen metabolism in the mouse brain by ultra-high field (17)O MR spectroscopy,” J. Cereb. Blood Flow Metab. 33(12), 1846–1849 (2013).
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Dunn, A. K.

A. K. Dunn, “Laser speckle contrast imaging of cerebral blood flow,” Ann. Biomed. Eng. 40(2), 367–377 (2012).
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A. D. Estrada, A. Ponticorvo, T. N. Ford, and A. K. Dunn, “Microvascular oxygen quantification using two-photon microscopy,” Opt. Lett. 33(10), 1038–1040 (2008).
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A. K. Dunn, A. Devor, A. M. Dale, and D. A. Boas, “Spatial extent of oxygen metabolism and hemodynamic changes during functional activation of the rat somatosensory cortex,” Neuroimage 27(2), 279–290 (2005).
[Crossref] [PubMed]

Durduran, T.

T. Durduran and A. G. Yodh, “Diffuse correlation spectroscopy for non-invasive, micro-vascular cerebral blood flow measurement,” Neuroimage 85(Pt 1), 51–63 (2014).
[Crossref] [PubMed]

J. P. Culver, T. Durduran, D. Furuya, C. Cheung, J. H. Greenberg, and A. G. Yodh, “Diffuse optical tomography of cerebral blood flow, oxygenation, and metabolism in rat during focal ischemia,” J. Cereb. Blood Flow Metab. 23(8), 911–924 (2003).
[Crossref] [PubMed]

Edwards, D.

D. T. Delpy, S. R. Arridge, M. Cope, D. Edwards, E. O. Reynolds, C. E. Richardson, S. Wray, J. Wyatt, and P. van der Zee, “Quantitation of pathlength in optical spectroscopy,” Adv. Exp. Med. Biol. 248, 41–46 (1989).
[Crossref] [PubMed]

Eikermann-Haerter, K.

V. J. Srinivasan, E. T. Mandeville, A. Can, F. Blasi, M. Climov, A. Daneshmand, J. H. Lee, E. Yu, H. Radhakrishnan, E. H. Lo, S. Sakadžić, K. Eikermann-Haerter, and C. Ayata, “Multiparametric, longitudinal optical coherence tomography imaging reveals acute injury and chronic recovery in experimental ischemic stroke,” PLoS One 8(8), e71478 (2013).
[Crossref] [PubMed]

Ellermann, J. M.

S. Ogawa, R. S. Menon, D. W. Tank, S. G. Kim, H. Merkle, J. M. Ellermann, and K. Ugurbil, “Functional brain mapping by blood oxygenation level-dependent contrast magnetic resonance imaging. A comparison of signal characteristics with a biophysical model,” Biophys. J. 64(3), 803–812 (1993).
[Crossref] [PubMed]

Engedahl, T.

L. Østergaard, S. N. Jespersen, T. Engedahl, E. Gutiérrez Jiménez, M. Ashkanian, M. B. Hansen, S. Eskildsen, and K. Mouridsen, “Capillary dysfunction: its detection and causative role in dementias and stroke,” Curr. Neurol. Neurosci. Rep. 15(6), 37 (2015).
[Crossref] [PubMed]

Engedal, T. S.

L. Østergaard, T. S. Engedal, R. Aamand, R. Mikkelsen, N. K. Iversen, M. Anzabi, E. T. Næss-Schmidt, K. R. Drasbek, V. Bay, J. U. Blicher, A. Tietze, I. K. Mikkelsen, B. Hansen, S. N. Jespersen, N. Juul, J. C. Sørensen, and M. Rasmussen, “Capillary transit time heterogeneity and flow-metabolism coupling after traumatic brain injury,” J. Cereb. Blood Flow Metab. 34(10), 1585–1598 (2014).
[Crossref] [PubMed]

Eskildsen, S.

L. Østergaard, S. N. Jespersen, T. Engedahl, E. Gutiérrez Jiménez, M. Ashkanian, M. B. Hansen, S. Eskildsen, and K. Mouridsen, “Capillary dysfunction: its detection and causative role in dementias and stroke,” Curr. Neurol. Neurosci. Rep. 15(6), 37 (2015).
[Crossref] [PubMed]

Espinoza, J.

B. J. Tromberg, N. Shah, R. Lanning, A. Cerussi, J. Espinoza, T. Pham, L. Svaasand, and J. Butler, “Non-invasive in vivo characterization of breast tumors using photon migration spectroscopy,” Neoplasia 2(1-2), 26–40 (2000).
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Estrada, A. D.

Fantini, S.

Fawzi, A. A.

W. Song, Q. Wei, W. Liu, T. Liu, J. Yi, N. Sheibani, A. A. Fawzi, R. A. Linsenmeier, S. Jiao, and H. F. Zhang, “A combined method to quantify the retinal metabolic rate of oxygen using photoacoustic ophthalmoscopy and optical coherence tomography,” Sci. Rep. 4, 6525 (2014).
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Fishkin, J. B.

Flammer, J.

M. Mozaffarieh, M. C. Grieshaber, and J. Flammer, “Oxygen and blood flow: players in the pathogenesis of glaucoma,” Mol. Vis. 14, 224–233 (2008).
[PubMed]

Ford, T. N.

Fortman, J. D.

B. M. Raabe, J. E. Artwohl, J. E. Purcell, J. Lovaglio, and J. D. Fortman, “Effects of weekly blood collection in C57BL/6 mice,” J. Am. Assoc. Lab. Anim. Sci. 50(5), 680–685 (2011).
[PubMed]

Foster, T. H.

K. A. Kasischke, E. M. Lambert, B. Panepento, A. Sun, H. A. Gelbard, R. W. Burgess, T. H. Foster, and M. Nedergaard, “Two-photon NADH imaging exposes boundaries of oxygen diffusion in cortical vascular supply regions,” J. Cereb. Blood Flow Metab. 31(1), 68–81 (2011).
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Fox, P. T.

S. H. Yee, K. Lee, P. A. Jerabek, and P. T. Fox, “Quantitative measurement of oxygen metabolic rate in the rat brain using microPET imaging of briefly inhaled 15O-labelled oxygen gas,” Nucl. Med. Commun. 27(7), 573–581 (2006).
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Franceschini, M. A.

Frostig, R. D.

R. D. Frostig, E. E. Lieke, D. Y. Ts’o, and A. Grinvald, “Cortical functional architecture and local coupling between neuronal activity and the microcirculation revealed by in vivo high-resolution optical imaging of intrinsic signals,” Proc. Natl. Acad. Sci. U.S.A. 87(16), 6082–6086 (1990).
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Figures (5)

Fig. 1
Fig. 1 Absolute CBF measurements were obtained from a volumetric Doppler OCT data set acquired from the mouse (C57BL/6) neocortex through a thinned-skull cranial window. (A) OCT angiogram showing vasculature and numbered transverse locations of vessels designated for absolute flow measurements. (B) Synthesized Doppler OCT image showing axial velocity profiles (in mm/s) at all designated transverse locations (obtained at different depths). Flux (F) was determined based on the product of the area in the en face plane (Axy) and average axial velocity (vz) over this area for a particular ascending venule numbered 16 (white arrow). (C) Bar graph shows the flow contributions of individual vessels, at the corresponding numbered locations shown in (A) to the total flow over the field of view (ml/100g/min). Absolute flow was calculated from the flux magnitude assuming a cortical thickness of 1.5 mm and a tissue density of 1.05 g/ml [46]. CBF was estimated as the average of the summed arteriolar flow and summed venular flow.
Fig. 2
Fig. 2 Absolute measurements of total intravascular hemoglobin concentration (CHbT) in the mouse (C57BL/6) neocortex through a thinned-skull cranial window. (A) Locations for CHbT measurements. (B) Absolute CHbT values were obtained from the slope of LCHbT versus depth, where LCHbT was obtained by spectroscopic fitting at each depth [40]; the vertical red dotted-lines represent the approximate vessel boundaries. (C) Absolute CHbT measurements at the numbered locations in (A).
Fig. 3
Fig. 3 Imaging of oxygen saturation changes during modulation of FiO2 in the mouse (Crl:SKH1-Hrhr) neocortex through a thinned-skull cranial window. Microvascular oxygen saturation was mapped using visible light spectroscopic OCT and displayed on a false-color scale during (A) 36% FiO2, (B) 16% FiO2. Since arterial and venous oxygen saturation decreased by equal amounts as FiO2 was decreased, oxygen extraction remained approximately constant for this experiment. An artery and vein are labelled as “a” and “v” respectively.
Fig. 4
Fig. 4 Imaging of oxygen saturation changes during modulation of FiCO2 in the mouse (C57BL/6) neocortex through a thinned-skull cranial window. Microvascular oxygen saturation was mapped using visible light spectroscopic OCT and displayed on a false-color scale during (A) 0% FiCO2, (B) 5% FiCO2. A large increase in oxygen saturation was observed in veins, while the sO2 in arteries remained unchanged. The reduced oxygen extraction is a consequence of arterial and arteriolar dilation and subsequently, increased CBF during hypercapnia. Note the heterogeneity of oxygen extraction, as evidenced by regionally varying venous sO2 values both before and after hypercapnia (white and gray arrows). An artery and vein are labeled as “a” and “v” respectively.
Fig. 5
Fig. 5 (A-C) Oxygen extraction (OE), cerebral blood flow (CBF), and hemoglobin concentration (CHbT) were measured in a range of states (achieved by mild modulation of FiO2 and FiCO2) and mice (C57BL/6, N = 3). The OE standard deviation estimate (A) was determined as the square root of the sum of the arterial and venous sO2 variance estimates, obtained from measurements at different locations. The CBF standard deviation estimate (B) was obtained from the summed arteriolar flow and summed venular flow values. (C) The CHbT standard deviation estimate was obtained from measurements at multiple locations. (D) A CMRO2 histogram was generated for each animal and state based on applying Eq. (1) to all possible combinations of arterial saturations (different locations), venous saturations (different locations), CBF values (arteriolar and venular), and CHbT values (different locations). (E) CMRO2 means and standard deviations were estimated from this histogram and shown across states and mice. (F) OE varied inversely with CBF, leading to a lower coefficient of variation for CMRO2 (0.17) as compared with OE (0.70). Error bars in (A-F) are standard deviations.

Equations (2)

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CMR O 2 =OE×CBF×[HbT]=( s O 2,a s O 2,v )×CBF×[HbT]
σ ^ CMR O 2 = ( m CBF m [ HbT ] σ OE ) 2 + ( m OE m [ HbT ] σ CBF ) 2 + ( m CBF m OE σ [ HbT ] ) 2

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