Abstract

Quantitative three-dimensional blood flow imaging is a valuable technique to investigate the physiology of the brain. Two-photon microscopy (2PM) allows quantification of the local blood flow velocity with micrometric resolution by performing repeated line scans, but prohibitively long measurement times would be required to apply this technique to full three-dimensional volumes. By multiplexing the image acquisition over depth, Fourier domain optical coherence tomography (FDOCT) enables quantification of blood flow velocities with a high volume acquisition rate, albeit at a relatively low spatial resolution. Extended-focus optical coherence microscopy (xfOCM) increases the lateral resolution without sacrificing depth of field and therefore combines the high volume acquisition rate of FDOCT with a resolution comparable to 2PM. Here, we demonstrate high-resolution quantitative imaging of the blood flow velocity vector’s magnitude in the adult murine brain with xfOCM.

© 2013 Optical Society of America

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2013 (2)

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V. J. Srinivasan, H. Radhakrishnan, E. H. Lo, E. T. Mandeville, J. Y. Jiang, S. Barry, and A. E. Cable, Biomed. Opt. Express 3, 612 (2012).
[CrossRef]

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[CrossRef]

J. K. Hefendehl, D. Milford, D. Eicke, B. M. Wegenast-Braun, M. E. Calhoun, S. A. Grathwohl, M. Jucker, and C. Liebig, J. Neurosci. Methods 205, 357 (2012).
[CrossRef]

T. Bolmont, A. Bouwens, C. Pache, M. Dimitrov, C. Berclaz, M. Villiger, B. M. Wegenast-Braun, T. Lasser, and P. C. Fraering, J. Neurosci. 32, 14548 (2012).
[CrossRef]

2011 (3)

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, J. Cereb. Blood Flow Metab. 31, 1339 (2011).
[CrossRef]

C. Blatter, B. Grajciar, C. M. Eigenwillig, W. Wieser, B. R. Biedermann, R. Huber, and R. A. Leitgeb, Opt. Express 19, 12141 (2011).
[CrossRef]

J. Lee, V. Srinivasan, H. Radhakrishnan, and D. A. Boas, Opt. Express 19, 21258 (2011).
[CrossRef]

2010 (3)

W. S. Kamoun, S.-S. Chae, D. a. Lacorre, J. A. Tyrrell, M. Mitre, M. A. Gillissen, D. Fukumura, R. K. Jain, and L. L. Munn, Nat. Methods 7, 655 (2010).
[CrossRef]

F. Fernández-Klett, N. Offenhauser, U. Dirnagl, J. Priller, and U. Lindauer, Proc. Natl. Acad. Sci. USA 107, 22290 (2010).
[CrossRef]

V. J. Srinivasan, S. Sakadzić, I. Gorczynska, S. Ruvinskaya, W. Wu, J. G. Fujimoto, and D. A. Boas, Opt. Express 18, 2477 (2010).
[CrossRef]

2009 (1)

2008 (1)

2007 (1)

2006 (1)

2003 (2)

2002 (1)

2000 (1)

1998 (1)

D. Kleinfeld, P. P. Mitra, F. Helmchen, and W. Denk, Proc. Natl. Acad. Sci. USA 95, 15741 (1998).
[CrossRef]

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, J. Cereb. Blood Flow Metab. 31, 1339 (2011).
[CrossRef]

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, J. Cereb. Blood Flow Metab. 31, 1339 (2011).
[CrossRef]

Bachmann, A. H.

Bajraszewski, T.

Barry, S.

V. J. Srinivasan, H. Radhakrishnan, E. H. Lo, E. T. Mandeville, J. Y. Jiang, S. Barry, and A. E. Cable, Biomed. Opt. Express 3, 612 (2012).
[CrossRef]

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, J. Cereb. Blood Flow Metab. 31, 1339 (2011).
[CrossRef]

Berclaz, C.

T. Bolmont, A. Bouwens, C. Pache, M. Dimitrov, C. Berclaz, M. Villiger, B. M. Wegenast-Braun, T. Lasser, and P. C. Fraering, J. Neurosci. 32, 14548 (2012).
[CrossRef]

Biedermann, B. R.

Blatter, C.

Boas, D. A.

J. Lee, V. Srinivasan, H. Radhakrishnan, and D. A. Boas, Opt. Express 19, 21258 (2011).
[CrossRef]

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, J. Cereb. Blood Flow Metab. 31, 1339 (2011).
[CrossRef]

V. J. Srinivasan, S. Sakadzić, I. Gorczynska, S. Ruvinskaya, W. Wu, J. G. Fujimoto, and D. A. Boas, Opt. Express 18, 2477 (2010).
[CrossRef]

Bolmont, T.

A. Bouwens, D. Szlag, M. Szkulmowski, T. Bolmont, M. Wojtkowski, and T. Lasser, Opt. Express 21, 17711 (2013).
[CrossRef]

T. Bolmont, A. Bouwens, C. Pache, M. Dimitrov, C. Berclaz, M. Villiger, B. M. Wegenast-Braun, T. Lasser, and P. C. Fraering, J. Neurosci. 32, 14548 (2012).
[CrossRef]

Bouwens, A.

A. Bouwens, D. Szlag, M. Szkulmowski, T. Bolmont, M. Wojtkowski, and T. Lasser, Opt. Express 21, 17711 (2013).
[CrossRef]

T. Bolmont, A. Bouwens, C. Pache, M. Dimitrov, C. Berclaz, M. Villiger, B. M. Wegenast-Braun, T. Lasser, and P. C. Fraering, J. Neurosci. 32, 14548 (2012).
[CrossRef]

Braaf, B.

Brecke, K. M.

Cable, A. E.

V. J. Srinivasan, H. Radhakrishnan, E. H. Lo, E. T. Mandeville, J. Y. Jiang, S. Barry, and A. E. Cable, Biomed. Opt. Express 3, 612 (2012).
[CrossRef]

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, J. Cereb. Blood Flow Metab. 31, 1339 (2011).
[CrossRef]

Calhoun, M. E.

J. K. Hefendehl, D. Milford, D. Eicke, B. M. Wegenast-Braun, M. E. Calhoun, S. A. Grathwohl, M. Jucker, and C. Liebig, J. Neurosci. Methods 205, 357 (2012).
[CrossRef]

Cense, B.

Chae, S.-S.

W. S. Kamoun, S.-S. Chae, D. a. Lacorre, J. A. Tyrrell, M. Mitre, M. A. Gillissen, D. Fukumura, R. K. Jain, and L. L. Munn, Nat. Methods 7, 655 (2010).
[CrossRef]

Chen, Z.

de Boer, J. F.

Denk, W.

D. Kleinfeld, P. P. Mitra, F. Helmchen, and W. Denk, Proc. Natl. Acad. Sci. USA 95, 15741 (1998).
[CrossRef]

Dimitrov, M.

T. Bolmont, A. Bouwens, C. Pache, M. Dimitrov, C. Berclaz, M. Villiger, B. M. Wegenast-Braun, T. Lasser, and P. C. Fraering, J. Neurosci. 32, 14548 (2012).
[CrossRef]

Ding, Z.

Dirnagl, U.

F. Fernández-Klett, N. Offenhauser, U. Dirnagl, J. Priller, and U. Lindauer, Proc. Natl. Acad. Sci. USA 107, 22290 (2010).
[CrossRef]

Eicke, D.

J. K. Hefendehl, D. Milford, D. Eicke, B. M. Wegenast-Braun, M. E. Calhoun, S. A. Grathwohl, M. Jucker, and C. Liebig, J. Neurosci. Methods 205, 357 (2012).
[CrossRef]

Eigenwillig, C. M.

Fernández-Klett, F.

F. Fernández-Klett, N. Offenhauser, U. Dirnagl, J. Priller, and U. Lindauer, Proc. Natl. Acad. Sci. USA 107, 22290 (2010).
[CrossRef]

Fraering, P. C.

T. Bolmont, A. Bouwens, C. Pache, M. Dimitrov, C. Berclaz, M. Villiger, B. M. Wegenast-Braun, T. Lasser, and P. C. Fraering, J. Neurosci. 32, 14548 (2012).
[CrossRef]

Fujimoto, J. G.

Fukumura, D.

W. S. Kamoun, S.-S. Chae, D. a. Lacorre, J. A. Tyrrell, M. Mitre, M. A. Gillissen, D. Fukumura, R. K. Jain, and L. L. Munn, Nat. Methods 7, 655 (2010).
[CrossRef]

Geissbuehler, M.

Gillissen, M. A.

W. S. Kamoun, S.-S. Chae, D. a. Lacorre, J. A. Tyrrell, M. Mitre, M. A. Gillissen, D. Fukumura, R. K. Jain, and L. L. Munn, Nat. Methods 7, 655 (2010).
[CrossRef]

Gorczynska, I.

Grajciar, B.

Grathwohl, S. A.

J. K. Hefendehl, D. Milford, D. Eicke, B. M. Wegenast-Braun, M. E. Calhoun, S. A. Grathwohl, M. Jucker, and C. Liebig, J. Neurosci. Methods 205, 357 (2012).
[CrossRef]

Grulkowski, I.

He, Y.

Hefendehl, J. K.

J. K. Hefendehl, D. Milford, D. Eicke, B. M. Wegenast-Braun, M. E. Calhoun, S. A. Grathwohl, M. Jucker, and C. Liebig, J. Neurosci. Methods 205, 357 (2012).
[CrossRef]

Helmchen, F.

D. Kleinfeld, P. P. Mitra, F. Helmchen, and W. Denk, Proc. Natl. Acad. Sci. USA 95, 15741 (1998).
[CrossRef]

Huang, P. L.

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, J. Cereb. Blood Flow Metab. 31, 1339 (2011).
[CrossRef]

Huber, R.

Jain, R. K.

W. S. Kamoun, S.-S. Chae, D. a. Lacorre, J. A. Tyrrell, M. Mitre, M. A. Gillissen, D. Fukumura, R. K. Jain, and L. L. Munn, Nat. Methods 7, 655 (2010).
[CrossRef]

Jiang, J. Y.

V. J. Srinivasan, H. Radhakrishnan, E. H. Lo, E. T. Mandeville, J. Y. Jiang, S. Barry, and A. E. Cable, Biomed. Opt. Express 3, 612 (2012).
[CrossRef]

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, J. Cereb. Blood Flow Metab. 31, 1339 (2011).
[CrossRef]

Jucker, M.

J. K. Hefendehl, D. Milford, D. Eicke, B. M. Wegenast-Braun, M. E. Calhoun, S. A. Grathwohl, M. Jucker, and C. Liebig, J. Neurosci. Methods 205, 357 (2012).
[CrossRef]

Kamoun, W. S.

W. S. Kamoun, S.-S. Chae, D. a. Lacorre, J. A. Tyrrell, M. Mitre, M. A. Gillissen, D. Fukumura, R. K. Jain, and L. L. Munn, Nat. Methods 7, 655 (2010).
[CrossRef]

Kleinfeld, D.

D. Kleinfeld, P. P. Mitra, F. Helmchen, and W. Denk, Proc. Natl. Acad. Sci. USA 95, 15741 (1998).
[CrossRef]

Kowalczyk, A.

Lacorre, D. a.

W. S. Kamoun, S.-S. Chae, D. a. Lacorre, J. A. Tyrrell, M. Mitre, M. A. Gillissen, D. Fukumura, R. K. Jain, and L. L. Munn, Nat. Methods 7, 655 (2010).
[CrossRef]

Lasser, T.

Lee, J.

Leitgeb, R. A.

Liebig, C.

J. K. Hefendehl, D. Milford, D. Eicke, B. M. Wegenast-Braun, M. E. Calhoun, S. A. Grathwohl, M. Jucker, and C. Liebig, J. Neurosci. Methods 205, 357 (2012).
[CrossRef]

Lindauer, U.

F. Fernández-Klett, N. Offenhauser, U. Dirnagl, J. Priller, and U. Lindauer, Proc. Natl. Acad. Sci. USA 107, 22290 (2010).
[CrossRef]

Lo, E. H.

Mandeville, E. T.

Milford, D.

J. K. Hefendehl, D. Milford, D. Eicke, B. M. Wegenast-Braun, M. E. Calhoun, S. A. Grathwohl, M. Jucker, and C. Liebig, J. Neurosci. Methods 205, 357 (2012).
[CrossRef]

Mitra, P. P.

D. Kleinfeld, P. P. Mitra, F. Helmchen, and W. Denk, Proc. Natl. Acad. Sci. USA 95, 15741 (1998).
[CrossRef]

Mitre, M.

W. S. Kamoun, S.-S. Chae, D. a. Lacorre, J. A. Tyrrell, M. Mitre, M. A. Gillissen, D. Fukumura, R. K. Jain, and L. L. Munn, Nat. Methods 7, 655 (2010).
[CrossRef]

Munn, L. L.

W. S. Kamoun, S.-S. Chae, D. a. Lacorre, J. A. Tyrrell, M. Mitre, M. A. Gillissen, D. Fukumura, R. K. Jain, and L. L. Munn, Nat. Methods 7, 655 (2010).
[CrossRef]

Nassif, N.

Nelson, J. S.

Offenhauser, N.

F. Fernández-Klett, N. Offenhauser, U. Dirnagl, J. Priller, and U. Lindauer, Proc. Natl. Acad. Sci. USA 107, 22290 (2010).
[CrossRef]

Pache, C.

T. Bolmont, A. Bouwens, C. Pache, M. Dimitrov, C. Berclaz, M. Villiger, B. M. Wegenast-Braun, T. Lasser, and P. C. Fraering, J. Neurosci. 32, 14548 (2012).
[CrossRef]

Pierce, M.

Priller, J.

F. Fernández-Klett, N. Offenhauser, U. Dirnagl, J. Priller, and U. Lindauer, Proc. Natl. Acad. Sci. USA 107, 22290 (2010).
[CrossRef]

Proskurin, S. G.

Radhakrishnan, H.

V. J. Srinivasan, H. Radhakrishnan, E. H. Lo, E. T. Mandeville, J. Y. Jiang, S. Barry, and A. E. Cable, Biomed. Opt. Express 3, 612 (2012).
[CrossRef]

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, J. Cereb. Blood Flow Metab. 31, 1339 (2011).
[CrossRef]

J. Lee, V. Srinivasan, H. Radhakrishnan, and D. A. Boas, Opt. Express 19, 21258 (2011).
[CrossRef]

Ren, H.

Ruvinskaya, S.

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, J. Cereb. Blood Flow Metab. 31, 1339 (2011).
[CrossRef]

V. J. Srinivasan, S. Sakadzić, I. Gorczynska, S. Ruvinskaya, W. Wu, J. G. Fujimoto, and D. A. Boas, Opt. Express 18, 2477 (2010).
[CrossRef]

Sakadzic, S.

Saxer, C.

Srinivasan, V.

Srinivasan, V. J.

Steinmann, L.

Szkulmowska, A.

Szkulmowski, M.

Szlag, D.

Tyrrell, J. A.

W. S. Kamoun, S.-S. Chae, D. a. Lacorre, J. A. Tyrrell, M. Mitre, M. A. Gillissen, D. Fukumura, R. K. Jain, and L. L. Munn, Nat. Methods 7, 655 (2010).
[CrossRef]

Vermeer, K. A.

Vienola, K. V.

Villiger, M.

T. Bolmont, A. Bouwens, C. Pache, M. Dimitrov, C. Berclaz, M. Villiger, B. M. Wegenast-Braun, T. Lasser, and P. C. Fraering, J. Neurosci. 32, 14548 (2012).
[CrossRef]

R. A. Leitgeb, M. Villiger, A. H. Bachmann, L. Steinmann, and T. Lasser, Opt. Lett. 31, 2450 (2006).
[CrossRef]

Villiger, M. L.

Wang, R. K.

Wegenast-Braun, B. M.

T. Bolmont, A. Bouwens, C. Pache, M. Dimitrov, C. Berclaz, M. Villiger, B. M. Wegenast-Braun, T. Lasser, and P. C. Fraering, J. Neurosci. 32, 14548 (2012).
[CrossRef]

J. K. Hefendehl, D. Milford, D. Eicke, B. M. Wegenast-Braun, M. E. Calhoun, S. A. Grathwohl, M. Jucker, and C. Liebig, J. Neurosci. Methods 205, 357 (2012).
[CrossRef]

White, B.

Wieser, W.

Wojtkowski, M.

Wu, W.

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, J. Cereb. Blood Flow Metab. 31, 1339 (2011).
[CrossRef]

V. J. Srinivasan, S. Sakadzić, I. Gorczynska, S. Ruvinskaya, W. Wu, J. G. Fujimoto, and D. A. Boas, Opt. Express 18, 2477 (2010).
[CrossRef]

Xiang, S.

Zhao, Y.

Biomed. Opt. Express (1)

J. Cereb. Blood Flow Metab. (1)

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, J. Cereb. Blood Flow Metab. 31, 1339 (2011).
[CrossRef]

J. Neurosci. (1)

T. Bolmont, A. Bouwens, C. Pache, M. Dimitrov, C. Berclaz, M. Villiger, B. M. Wegenast-Braun, T. Lasser, and P. C. Fraering, J. Neurosci. 32, 14548 (2012).
[CrossRef]

J. Neurosci. Methods (1)

J. K. Hefendehl, D. Milford, D. Eicke, B. M. Wegenast-Braun, M. E. Calhoun, S. A. Grathwohl, M. Jucker, and C. Liebig, J. Neurosci. Methods 205, 357 (2012).
[CrossRef]

Nat. Methods (1)

W. S. Kamoun, S.-S. Chae, D. a. Lacorre, J. A. Tyrrell, M. Mitre, M. A. Gillissen, D. Fukumura, R. K. Jain, and L. L. Munn, Nat. Methods 7, 655 (2010).
[CrossRef]

Opt. Express (10)

Opt. Lett. (4)

Proc. Natl. Acad. Sci. USA (2)

F. Fernández-Klett, N. Offenhauser, U. Dirnagl, J. Priller, and U. Lindauer, Proc. Natl. Acad. Sci. USA 107, 22290 (2010).
[CrossRef]

D. Kleinfeld, P. P. Mitra, F. Helmchen, and W. Denk, Proc. Natl. Acad. Sci. USA 95, 15741 (1998).
[CrossRef]

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Figures (3)

Fig. 1.
Fig. 1.

Validity of the model for erythrocytes. (a) Illustration of the xfOCM illumination and detection modes and definition of the angle α of the flow channel. (b) Lateral flow profile in the capillary of the axial flow velocity component vz, for different flow rates F set by the syringe pump. Points represent averages over 10 measurements. (c) Flow profile of the lateral velocity component vl. (d) Comparison between the total flow velocities vtot as estimated from vz and from vl (values taken at the maximum of the parabolic flow profiles). Error bars indicate ± standard deviation over 10 measurements.

Fig. 2.
Fig. 2.

Quantitative cerebral blood flow in the mouse cortex. Images are maximum absolute value projections over 380 μm of (a) the mean Doppler frequency and (b) the standard deviation of Doppler frequencies. (c) Length vtot of the velocity vector. (d) Depth-coded representation of the data in (c). Scale bars: 100 μm.

Fig. 3.
Fig. 3.

Cross sections at the junction of two blood-vessels, indicated by the black vertical dashed line in Fig. 2(c). (a) Axial flow velocity component vz. (b) Magnitude vtot of the flow velocity vector. A dark transparent mask (vz>0.22mm/s) was applied to suppress the shadow artifact seen below the vessel. (c) Profile of vz averaged within the dashed white rectangle in (a). (d) Profile of vtot averaged within the dashed white rectangle in (b).

Equations (2)

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μ[fD]nk0πvz,
σ2[fD]n2k024π2f2A2(vx2+vy2)+kσ2n2π2vz2,

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