Abstract

Optical Coherence Tomography (OCT) angiography was applied to image functional hyperemia in different vascular compartments in the rat somatosensory cortex. Dynamic backscattering changes, indicative of changes in dynamic red blood cell (dRBC) content, were used to monitor the hemodynamic response. Three-dimensional movies depicting the microvascular response to neuronal activation were created for the first time. An increase in the attenuation coefficient during activation was identified, and a simple normalization procedure was proposed to correct for it. This procedure was applied to determine compartment-resolved backscattering changes caused by dRBC content changes during functional activation. Increases in dRBC content were observed in all vascular compartments (arterial, arteriolar, capillary, and venular), with the largest responses found in the arterial and arteriolar compartments. dRBC content increased with dilation in arteries but with barely detectable dilation in veins. dRBC content increased in capillaries without significant “all or none” capillary recruitment.

© 2013 OSA

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2013 (1)

C. Martin, Y. Zheng, N. R. Sibson, J. E. Mayhew, and J. Berwick, “Complex spatiotemporal haemodynamic response following sensory stimulation in the awake rat,” Neuroimage66, 1–8 (2013).
[PubMed]

2012 (3)

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

A. Y. Shih, J. D. Driscoll, P. J. Drew, N. Nishimura, C. B. Schaffer, and D. Kleinfeld, “Two-photon microscopy as a tool to study blood flow and neurovascular coupling in the rodent brain,” J. Cereb. Blood Flow Metab.32(7), 1277–1309 (2012).
[CrossRef] [PubMed]

V. J. Srinivasan, H. Radhakrishnan, E. H. Lo, E. T. Mandeville, J. Y. Jiang, S. Barry, and A. E. Cable, “OCT methods for capillary velocimetry,” Biomed. Opt. Express3(3), 612–629 (2012).
[CrossRef] [PubMed]

2011 (6)

E. Macé, G. Montaldo, I. Cohen, M. Baulac, M. Fink, and M. Tanter, “Functional ultrasound imaging of the brain,” Nat. Methods8(8), 662–664 (2011).
[CrossRef] [PubMed]

S. Yousefi, Z. Zhi, and R. K. Wang, “Eigendecomposition-based clutter filtering technique for optical micro-angiography,” IEEE Trans. Biomed. Eng.58(8), 2316–2323 (2011).
[CrossRef] [PubMed]

V. J. Srinivasan, D. N. Atochin, H. Radhakrishnan, J. Y. Jiang, S. Ruvinskaya, W. Wu, S. Barry, A. E. Cable, C. Ayata, P. L. Huang, and D. A. Boas, “Optical coherence tomography for the quantitative study of cerebrovascular physiology,” J. Cereb. Blood Flow Metab.31(6), 1339–1345 (2011).
[CrossRef] [PubMed]

P. Cimalla, J. Walther, M. Mittasch, and E. Koch, “Shear flow-induced optical inhomogeneity of blood assessed in vivo and in vitro by spectral domain optical coherence tomography in the 1.3 μm wavelength range,” J. Biomed. Opt.16(11), 116020 (2011).
[CrossRef] [PubMed]

Y. Mutalifu, L. Holm, C. Ince, E. Theodorsson, and F. Sjöberg, “Multiple different laminar velocity profiles in separate veins in the microvascular network of brain cortex in rats,” Int. J. Clin. Exp. Med.4(1), 10–16 (2011).
[PubMed]

P. J. Drew, A. Y. Shih, and D. Kleinfeld, “Fluctuating and sensory-induced vasodynamics in rodent cortex extend arteriole capacity,” Proc. Natl. Acad. Sci. U.S.A.108(20), 8473–8478 (2011).
[CrossRef] [PubMed]

2010 (3)

2009 (4)

D. J. Faber and T. G. van Leeuwen, “Are quantitative attenuation measurements of blood by optical coherence tomography feasible?” Opt. Lett.34(9), 1435–1437 (2009).
[CrossRef] [PubMed]

V. J. Srinivasan, S. Sakadzić, I. Gorczynska, S. Ruvinskaya, W. Wu, J. G. Fujimoto, and D. A. Boas, “Depth-resolved microscopy of cortical hemodynamics with optical coherence tomography,” Opt. Lett.34(20), 3086–3088 (2009).
[CrossRef] [PubMed]

E. M. Hillman and S. A. Burgess, “Sub-millimeter resolution 3D optical imaging of living tissue using laminar optical tomography,” Laser Photon Rev3(1-2), 159–179 (2009).
[CrossRef] [PubMed]

B. J. Vakoc, R. M. Lanning, J. A. Tyrrell, T. P. Padera, L. A. Bartlett, T. Stylianopoulos, L. L. Munn, G. J. Tearney, D. Fukumura, R. K. Jain, and B. E. Bouma, “Three-dimensional microscopy of the tumor microenvironment in vivo using optical frequency domain imaging,” Nat. Med.15(10), 1219–1223 (2009).
[CrossRef] [PubMed]

2008 (4)

R. Samatham, S. L. Jacques, and P. Campagnola, “Optical properties of mutant versus wild-type mouse skin measured by reflectance-mode confocal scanning laser microscopy (rCSLM),” J. Biomed. Opt.13(4), 041309 (2008).
[CrossRef] [PubMed]

B. Stefanovic, E. Hutchinson, V. Yakovleva, V. Schram, J. T. Russell, L. Belluscio, A. P. Koretsky, and A. C. Silva, “Functional reactivity of cerebral capillaries,” J. Cereb. Blood Flow Metab.28(5), 961–972 (2008).
[CrossRef] [PubMed]

A. Mariampillai, B. A. Standish, E. H. Moriyama, M. Khurana, N. R. Munce, M. K. K. Leung, J. Y. Jiang, A. E. Cable, B. C. Wilson, I. A. Vitkin, and V. X. D. Yang, “Speckle variance detection of microvasculature using swept-source optical coherence tomography,” Opt. Lett.33(13), 1530–1532 (2008).
[CrossRef] [PubMed]

Y. K. Tao, A. M. Davis, and J. A. Izatt, “Single-pass volumetric bidirectional blood flow imaging spectral domain optical coherence tomography using a modified Hilbert transform,” Opt. Express16(16), 12350–12361 (2008).
[CrossRef] [PubMed]

2007 (4)

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]

J. Fingler, D. Schwartz, C. Yang, and S. E. Fraser, “Mobility and transverse flow visualization using phase variance contrast with spectral domain optical coherence tomography,” Opt. Express15(20), 12636–12653 (2007).
[CrossRef] [PubMed]

A. Devor, P. Tian, N. Nishimura, I. C. Teng, E. M. Hillman, S. N. Narayanan, I. Ulbert, D. A. Boas, D. Kleinfeld, and A. M. Dale, “Suppressed neuronal activity and concurrent arteriolar vasoconstriction may explain negative blood oxygenation level-dependent signal,” J. Neurosci.27(16), 4452–4459 (2007).
[CrossRef] [PubMed]

E. M. Hillman, A. Devor, M. B. Bouchard, A. K. Dunn, G. W. Krauss, J. Skoch, B. J. Bacskai, A. M. Dale, and D. A. Boas, “Depth-resolved optical imaging and microscopy of vascular compartment dynamics during somatosensory stimulation,” Neuroimage35(1), 89–104 (2007).
[CrossRef] [PubMed]

2006 (3)

H. Ren, T. Sun, D. J. MacDonald, M. J. Cobb, and X. Li, “Real-time in vivo blood-flow imaging by moving-scatterer-sensitive spectral-domain optical Doppler tomography,” Opt. Lett.31(7), 927–929 (2006).
[CrossRef] [PubMed]

M. E. Raichle and M. A. Mintun, “Brain work and brain imaging,” Annu. Rev. Neurosci.29(1), 449–476 (2006).
[CrossRef] [PubMed]

R. C. Koehler, D. Gebremedhin, and D. R. Harder, “Role of astrocytes in cerebrovascular regulation,” J. Appl. Physiol.100(1), 307–317 (2006).
[CrossRef] [PubMed]

2005 (1)

I. Vanzetta, R. Hildesheim, and A. Grinvald, “Compartment-resolved imaging of activity-dependent dynamics of cortical blood volume and oximetry,” J. Neurosci.25(9), 2233–2244 (2005).
[CrossRef] [PubMed]

2004 (3)

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

E. Hamel, “Cholinergic modulation of the cortical microvascular bed,” Prog. Brain Res.145, 171–178 (2004).
[CrossRef] [PubMed]

B. Cauli, X. K. Tong, A. Rancillac, N. Serluca, B. Lambolez, J. Rossier, and E. Hamel, “Cortical GABA interneurons in neurovascular coupling: relays for subcortical vasoactive pathways,” J. Neurosci.24(41), 8940–8949 (2004).
[CrossRef] [PubMed]

2003 (1)

J. P. Culver, T. Durduran, C. Cheung, A. G. Yodh, D. Furuya, and J. H. Greenberg, “Diffuse optical measurement of hemoglobin and cerebral blood flow in rat brain during hypercapnia, hypoxia and cardiac arrest,” Adv. Exp. Med. Biol.510, 293–297 (2003).
[CrossRef] [PubMed]

2001 (1)

N. K. Logothetis, J. Pauls, M. Augath, T. Trinath, and A. Oeltermann, “Neurophysiological investigation of the basis of the fMRI signal,” Nature412(6843), 150–157 (2001).
[CrossRef] [PubMed]

1999 (1)

J. B. Mandeville, J. J. Marota, C. Ayata, M. A. Moskowitz, R. M. Weisskoff, and B. R. Rosen, “MRI measurement of the temporal evolution of relative CMRO2 during rat forepaw stimulation,” Magn. Reson. Med.42(5), 944–951 (1999).
[CrossRef] [PubMed]

1996 (1)

A. R. Pries, T. W. Secomb, and P. Gaehtgens, “Biophysical aspects of blood flow in the microvasculature,” Cardiovasc. Res.32(4), 654–667 (1996).
[PubMed]

1994 (1)

A. Villringer, A. Them, U. Lindauer, K. Einhäupl, and U. Dirnagl, “Capillary perfusion of the rat brain cortex. An in vivo confocal microscopy study,” Circ. Res.75(1), 55–62 (1994).
[CrossRef] [PubMed]

1992 (3)

K. K. Kwong, J. W. Belliveau, D. A. Chesler, I. E. Goldberg, R. M. Weisskoff, B. P. Poncelet, D. N. Kennedy, B. E. Hoppel, M. S. Cohen, R. Turner, H.-M. Cheng, T. J. Brady, and B. R. Rosen, “Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation,” Proc. Natl. Acad. Sci. U.S.A.89(12), 5675–5679 (1992).
[CrossRef] [PubMed]

S. Ogawa, D. W. Tank, R. Menon, J. M. Ellermann, S.-G. Kim, H. Merkle, and K. Ugurbil, “Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging,” Proc. Natl. Acad. Sci. U.S.A.89(13), 5951–5955 (1992).
[CrossRef] [PubMed]

A. R. Pries, D. Neuhaus, and P. Gaehtgens, “Blood viscosity in tube flow: dependence on diameter and hematocrit,” Am. J. Physiol.263(6 Pt 2), H1770–H1778 (1992).
[PubMed]

1991 (2)

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]

R. A. Stepnoski, A. LaPorta, F. Raccuia-Behling, G. E. Blonder, R. E. Slusher, and D. Kleinfeld, “Noninvasive detection of changes in membrane potential in cultured neurons by light scattering,” Proc. Natl. Acad. Sci. U.S.A.88(21), 9382–9386 (1991).
[CrossRef] [PubMed]

1986 (1)

A. Grinvald, E. Lieke, R. D. Frostig, C. D. Gilbert, and T. N. Wiesel, “Functional architecture of cortex revealed by optical imaging of intrinsic signals,” Nature324(6095), 361–364 (1986).
[CrossRef] [PubMed]

1931 (1)

R. Fahraeus and T. Lindqvist, “The viscosity of the blood in narrow capillary tubes,” Am. J. Physiol.96, 562–568 (1931).

Atochin, D. N.

V. J. Srinivasan, D. N. Atochin, H. Radhakrishnan, J. Y. Jiang, S. Ruvinskaya, W. Wu, S. Barry, A. E. Cable, C. Ayata, P. L. Huang, and D. A. Boas, “Optical coherence tomography for the quantitative study of cerebrovascular physiology,” J. Cereb. Blood Flow Metab.31(6), 1339–1345 (2011).
[CrossRef] [PubMed]

Augath, M.

N. K. Logothetis, J. Pauls, M. Augath, T. Trinath, and A. Oeltermann, “Neurophysiological investigation of the basis of the fMRI signal,” Nature412(6843), 150–157 (2001).
[CrossRef] [PubMed]

Ayata, C.

V. J. Srinivasan, D. N. Atochin, H. Radhakrishnan, J. Y. Jiang, S. Ruvinskaya, W. Wu, S. Barry, A. E. Cable, C. Ayata, P. L. Huang, and D. A. Boas, “Optical coherence tomography for the quantitative study of cerebrovascular physiology,” J. Cereb. Blood Flow Metab.31(6), 1339–1345 (2011).
[CrossRef] [PubMed]

J. B. Mandeville, J. J. Marota, C. Ayata, M. A. Moskowitz, R. M. Weisskoff, and B. R. Rosen, “MRI measurement of the temporal evolution of relative CMRO2 during rat forepaw stimulation,” Magn. Reson. Med.42(5), 944–951 (1999).
[CrossRef] [PubMed]

Bacskai, B. J.

E. M. Hillman, A. Devor, M. B. Bouchard, A. K. Dunn, G. W. Krauss, J. Skoch, B. J. Bacskai, A. M. Dale, and D. A. Boas, “Depth-resolved optical imaging and microscopy of vascular compartment dynamics during somatosensory stimulation,” Neuroimage35(1), 89–104 (2007).
[CrossRef] [PubMed]

Barry, S.

Bartlett, L. A.

B. J. Vakoc, R. M. Lanning, J. A. Tyrrell, T. P. Padera, L. A. Bartlett, T. Stylianopoulos, L. L. Munn, G. J. Tearney, D. Fukumura, R. K. Jain, and B. E. Bouma, “Three-dimensional microscopy of the tumor microenvironment in vivo using optical frequency domain imaging,” Nat. Med.15(10), 1219–1223 (2009).
[CrossRef] [PubMed]

Baulac, M.

E. Macé, G. Montaldo, I. Cohen, M. Baulac, M. Fink, and M. Tanter, “Functional ultrasound imaging of the brain,” Nat. Methods8(8), 662–664 (2011).
[CrossRef] [PubMed]

Belliveau, J. W.

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K. K. Kwong, J. W. Belliveau, D. A. Chesler, I. E. Goldberg, R. M. Weisskoff, B. P. Poncelet, D. N. Kennedy, B. E. Hoppel, M. S. Cohen, R. Turner, H.-M. Cheng, T. J. Brady, and B. R. Rosen, “Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation,” Proc. Natl. Acad. Sci. U.S.A.89(12), 5675–5679 (1992).
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E. Macé, G. Montaldo, I. Cohen, M. Baulac, M. Fink, and M. Tanter, “Functional ultrasound imaging of the brain,” Nat. Methods8(8), 662–664 (2011).
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M. A. Franceschini, H. Radhakrishnan, K. Thakur, W. Wu, S. Ruvinskaya, S. Carp, and D. A. Boas, “The effect of different anesthetics on neurovascular coupling,” Neuroimage51(4), 1367–1377 (2010).
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J. P. Culver, T. Durduran, C. Cheung, A. G. Yodh, D. Furuya, and J. H. Greenberg, “Diffuse optical measurement of hemoglobin and cerebral blood flow in rat brain during hypercapnia, hypoxia and cardiac arrest,” Adv. Exp. Med. Biol.510, 293–297 (2003).
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Greenberg, J. H.

J. P. Culver, T. Durduran, C. Cheung, A. G. Yodh, D. Furuya, and J. H. Greenberg, “Diffuse optical measurement of hemoglobin and cerebral blood flow in rat brain during hypercapnia, hypoxia and cardiac arrest,” Adv. Exp. Med. Biol.510, 293–297 (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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A. Grinvald, E. Lieke, R. D. Frostig, C. D. Gilbert, and T. N. Wiesel, “Functional architecture of cortex revealed by optical imaging of intrinsic signals,” Nature324(6095), 361–364 (1986).
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Hanson, S. R.

Harder, D. R.

R. C. Koehler, D. Gebremedhin, and D. R. Harder, “Role of astrocytes in cerebrovascular regulation,” J. Appl. Physiol.100(1), 307–317 (2006).
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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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I. Vanzetta, R. Hildesheim, and A. Grinvald, “Compartment-resolved imaging of activity-dependent dynamics of cortical blood volume and oximetry,” J. Neurosci.25(9), 2233–2244 (2005).
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E. M. Hillman and S. A. Burgess, “Sub-millimeter resolution 3D optical imaging of living tissue using laminar optical tomography,” Laser Photon Rev3(1-2), 159–179 (2009).
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A. Devor, P. Tian, N. Nishimura, I. C. Teng, E. M. Hillman, S. N. Narayanan, I. Ulbert, D. A. Boas, D. Kleinfeld, and A. M. Dale, “Suppressed neuronal activity and concurrent arteriolar vasoconstriction may explain negative blood oxygenation level-dependent signal,” J. Neurosci.27(16), 4452–4459 (2007).
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Y. Mutalifu, L. Holm, C. Ince, E. Theodorsson, and F. Sjöberg, “Multiple different laminar velocity profiles in separate veins in the microvascular network of brain cortex in rats,” Int. J. Clin. Exp. Med.4(1), 10–16 (2011).
[PubMed]

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K. K. Kwong, J. W. Belliveau, D. A. Chesler, I. E. Goldberg, R. M. Weisskoff, B. P. Poncelet, D. N. Kennedy, B. E. Hoppel, M. S. Cohen, R. Turner, H.-M. Cheng, T. J. Brady, and B. R. Rosen, “Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation,” Proc. Natl. Acad. Sci. U.S.A.89(12), 5675–5679 (1992).
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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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V. J. Srinivasan, D. N. Atochin, H. Radhakrishnan, J. Y. Jiang, S. Ruvinskaya, W. Wu, S. Barry, A. E. Cable, C. Ayata, P. L. Huang, and D. A. Boas, “Optical coherence tomography for the quantitative study of cerebrovascular physiology,” J. Cereb. Blood Flow Metab.31(6), 1339–1345 (2011).
[CrossRef] [PubMed]

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Hutchinson, E.

B. Stefanovic, E. Hutchinson, V. Yakovleva, V. Schram, J. T. Russell, L. Belluscio, A. P. Koretsky, and A. C. Silva, “Functional reactivity of cerebral capillaries,” J. Cereb. Blood Flow Metab.28(5), 961–972 (2008).
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Y. Mutalifu, L. Holm, C. Ince, E. Theodorsson, and F. Sjöberg, “Multiple different laminar velocity profiles in separate veins in the microvascular network of brain cortex in rats,” Int. J. Clin. Exp. Med.4(1), 10–16 (2011).
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Jacques, S. L.

R. Samatham, S. L. Jacques, and P. Campagnola, “Optical properties of mutant versus wild-type mouse skin measured by reflectance-mode confocal scanning laser microscopy (rCSLM),” J. Biomed. Opt.13(4), 041309 (2008).
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B. J. Vakoc, R. M. Lanning, J. A. Tyrrell, T. P. Padera, L. A. Bartlett, T. Stylianopoulos, L. L. Munn, G. J. Tearney, D. Fukumura, R. K. Jain, and B. E. Bouma, “Three-dimensional microscopy of the tumor microenvironment in vivo using optical frequency domain imaging,” Nat. Med.15(10), 1219–1223 (2009).
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Jiang, J. Y.

Kennedy, D. N.

K. K. Kwong, J. W. Belliveau, D. A. Chesler, I. E. Goldberg, R. M. Weisskoff, B. P. Poncelet, D. N. Kennedy, B. E. Hoppel, M. S. Cohen, R. Turner, H.-M. Cheng, T. J. Brady, and B. R. Rosen, “Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation,” Proc. Natl. Acad. Sci. U.S.A.89(12), 5675–5679 (1992).
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Kim, S.-G.

S. Ogawa, D. W. Tank, R. Menon, J. M. Ellermann, S.-G. Kim, H. Merkle, and K. Ugurbil, “Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging,” Proc. Natl. Acad. Sci. U.S.A.89(13), 5951–5955 (1992).
[CrossRef] [PubMed]

Kleinfeld, D.

A. Y. Shih, J. D. Driscoll, P. J. Drew, N. Nishimura, C. B. Schaffer, and D. Kleinfeld, “Two-photon microscopy as a tool to study blood flow and neurovascular coupling in the rodent brain,” J. Cereb. Blood Flow Metab.32(7), 1277–1309 (2012).
[CrossRef] [PubMed]

P. J. Drew, A. Y. Shih, and D. Kleinfeld, “Fluctuating and sensory-induced vasodynamics in rodent cortex extend arteriole capacity,” Proc. Natl. Acad. Sci. U.S.A.108(20), 8473–8478 (2011).
[CrossRef] [PubMed]

A. Devor, P. Tian, N. Nishimura, I. C. Teng, E. M. Hillman, S. N. Narayanan, I. Ulbert, D. A. Boas, D. Kleinfeld, and A. M. Dale, “Suppressed neuronal activity and concurrent arteriolar vasoconstriction may explain negative blood oxygenation level-dependent signal,” J. Neurosci.27(16), 4452–4459 (2007).
[CrossRef] [PubMed]

R. A. Stepnoski, A. LaPorta, F. Raccuia-Behling, G. E. Blonder, R. E. Slusher, and D. Kleinfeld, “Noninvasive detection of changes in membrane potential in cultured neurons by light scattering,” Proc. Natl. Acad. Sci. U.S.A.88(21), 9382–9386 (1991).
[CrossRef] [PubMed]

Koch, E.

P. Cimalla, J. Walther, M. Mittasch, and E. Koch, “Shear flow-induced optical inhomogeneity of blood assessed in vivo and in vitro by spectral domain optical coherence tomography in the 1.3 μm wavelength range,” J. Biomed. Opt.16(11), 116020 (2011).
[CrossRef] [PubMed]

Koehler, R. C.

R. C. Koehler, D. Gebremedhin, and D. R. Harder, “Role of astrocytes in cerebrovascular regulation,” J. Appl. Physiol.100(1), 307–317 (2006).
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A. Villringer, A. Them, U. Lindauer, K. Einhäupl, and U. Dirnagl, “Capillary perfusion of the rat brain cortex. An in vivo confocal microscopy study,” Circ. Res.75(1), 55–62 (1994).
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