Abstract

We longitudinally imaged both the superficial and deep cortical microvascular networks in brains of healthy mice and in a mouse model of stroke in vivo using visible-light optical coherence tomography (vis-OCT). We surgically implanted a microprism in mouse brains sealed by a chronic cranial window. The microprism enabled vis-OCT to image the entire depth of the mouse cortex. Following microprism implantation, we imaged the mice for 28 days and found that that it took around 15 days for both the superficial and deep cortical microvessels to recover from the implantation surgery. After the brains recovered, we introduced ischemic strokes by transient middle cerebral artery occlusion (tMCAO). We monitored the strokes for up to 60 days and observed different microvascular responses to tMCAO at different cortical depths in both the acute and chronic phases of the stroke. This work demonstrates that the combined microprism and cranial window is well-suited for longitudinal investigation of cortical microvascular disorders using vis-OCT.

© 2019 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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2019 (1)

C. W. Merkle, J. Zhu, M. T. Bernucci, and V. J. Srinivasan, “Dynamic Contrast Optical Coherence Tomography reveals laminar microvascular hemodynamics in the mouse neocortex in vivo,” NeuroImage 202, 116067 (2019).
[Crossref]

2018 (4)

2017 (6)

X. Shu, L. J. Beckmann, and H. F. Zhang, “Visible-light optical coherence tomography: a review,” J. Biomed. Opt. 22(12), 1–14 (2017).
[Crossref]

W. Liu, S. Wang, B. Soetikno, J. Yi, K. Zhang, S. Chen, R. A. Linsenmeier, C. M. Sorenson, N. Sheibani, and H. F. Zhang, “Increased Retinal Oxygen Metabolism Precedes Microvascular Alterations in Type 1 Diabetic Mice,” Invest. Ophthalmol. Visual Sci. 58(2), 981–989 (2017).
[Crossref]

S. Chen, X. Shu, P. L. Nesper, W. Liu, A. A. Fawzi, and H. F. Zhang, “Retinal oximetry in humans using visible-light optical coherence tomography [Invited],” Biomed. Opt. Express 8(3), 1415–1429 (2017).
[Crossref]

A. Lichtenegger, D. J. Harper, M. Augustin, P. Eugui, M. Muck, J. Gesperger, C. K. Hitzenberger, A. Woehrer, and B. Baumann, “Spectroscopic imaging with spectral domain visible light optical coherence microscopy in Alzheimer’s disease brain samples,” Biomed. Opt. Express 8(9), 4007–4025 (2017).
[Crossref]

S. S. J. Rewell, L. Churilov, T. K. Sidon, E. Aleksoska, S. F. Cox, M. R. Macleod, and D. W. Howells, “Evolution of ischemic damage and behavioural deficit over 6 months after MCAo in the rat: Selecting the optimal outcomes and statistical power for multi-centre preclinical trials,” PLoS One 12(2), e0171688 (2017).
[Crossref]

N. Percie du Sert, A. Alfieri, S. M. Allan, H. V. Carswell, G. A. Deuchar, T. D. Farr, P. Flecknell, L. Gallagher, C. L. Gibson, M. J. Haley, M. R. Macleod, B. W. McColl, C. McCabe, A. Morancho, L. D. Moon, M. J. O’Neill, I. Pérez de Puig, A. Planas, C. I. Ragan, A. Rosell, L. A. Roy, K. O. Ryder, A. Simats, E. S. Sena, B. A. Sutherland, M. D. Tricklebank, R. C. Trueman, L. Whitfield, R. Wong, and I. M. Macrae, “The IMPROVE Guidelines (Ischaemia Models: Procedural Refinements Of in Vivo Experiments),” J. Cereb. Blood Flow Metab. 37(11), 3488–3517 (2017).
[Crossref]

2016 (2)

S. Chen, Q. Liu, X. Shu, B. Soetikno, S. Tong, and H. F. Zhang, “Imaging hemodynamic response after ischemic stroke in mouse cortex using visible-light optical coherence tomography,” Biomed. Opt. Express 7(9), 3377–3389 (2016).
[Crossref]

E. Cuccione, G. Padovano, A. Versace, C. Ferrarese, and S. Beretta, “Cerebral collateral circulation in experimental ischemic stroke,” Exp. Transl. Stroke Med. 8(1), 2 (2016).
[Crossref]

2015 (9)

J. Liu, “Post stroke angiogenesis: Blood, bloom or brood,” Stroke 46(5), e105–e106 (2015).
[Crossref]

B. T. Soetikno, J. Yi, R. Shah, W. Liu, P. Purta, H. F. Zhang, and A. A. Fawzi, “Inner retinal oxygen metabolism in the 50/10 oxygen-induced retinopathy model,” Sci. Rep. 5(1), 16752 (2015).
[Crossref]

J. Yi, W. Liu, S. Chen, V. Backman, N. Sheibani, C. M. Sorenson, A. A. Fawzi, R. A. Linsenmeier, and H. F. Zhang, “Visible light optical coherence tomography measures retinal oxygen metabolic response to systemic oxygenation,” Light: Sci. Appl. 4(9), e334 (2015).
[Crossref]

S. P. Chong, C. W. Merkle, C. Leahy, H. Radhakrishnan, and V. J. Srinivasan, “Quantitative microvascular hemoglobin mapping using visible light spectroscopic Optical Coherence Tomography,” Biomed. Opt. Express 6(4), 1429–1450 (2015).
[Crossref]

S. P. Chong, C. W. Merkle, C. Leahy, and V. J. Srinivasan, “Cerebral metabolic rate of oxygen (CMRO(2)) assessed by combined Doppler and spectroscopic OCT,” Biomed. Opt. Express 6(10), 3941–3951 (2015).
[Crossref]

J. Yi, S. Chen, X. Shu, A. A. Fawzi, and H. F. Zhang, “Human retinal imaging using visible-light optical coherence tomography guided by scanning laser ophthalmoscopy,” Biomed. Opt. Express 6(10), 3701–3713 (2015).
[Crossref]

S. P. Chong, C. W. Merkle, D. F. Cooke, T. Zhang, H. Radhakrishnan, L. Krubitzer, and V. J. Srinivasan, “Noninvasive, in vivo imaging of subcortical mouse brain regions with 1.7  µm optical coherence tomography,” Opt. Lett. 40(21), 4911–4914 (2015).
[Crossref]

D. L. Adams, V. Piserchia, J. R. Economides, and J. C. Horton, “Vascular Supply of the Cerebral Cortex is Specialized for Cell Layers but Not Columns,” Cereb. Cortex 25(10), 3673–3681 (2015).
[Crossref]

I. Perez-de-Puig, F. Miró-Mur, M. Ferrer-Ferrer, E. Gelpi, J. Pedragosa, C. Justicia, X. Urra, A. Chamorro, and A. M. Planas, “Neutrophil recruitment to the brain in mouse and human ischemic stroke,” Acta Neuropathol. 129(2), 239–257 (2015).
[Crossref]

2014 (2)

2013 (3)

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]

M. A. Mirza, L. A. Capozzi, Y. Xu, L. D. McCullough, and F. Liu, “Knockout of vascular early response gene worsens chronic stroke outcomes in neonatal mice,” Brain Res. Bull. 98, 111–121 (2013).
[Crossref]

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]

2012 (2)

A. Ergul, A. Alhusban, and S. C. Fagan, “Angiogenesis: A Harmonized Target for Recovery after Stroke,” Stroke 43(8), 2270–2274 (2012).
[Crossref]

C. A. Schneider, W. S. Rasband, and K. W. Eliceiri, “NIH Image to ImageJ: 25 years of image analysis,” Nat. Methods 9(7), 671–675 (2012).
[Crossref]

2011 (3)

E. Zudaire, L. Gambardella, C. Kurcz, and S. Vermeren, “A Computational Tool for Quantitative Analysis of Vascular Networks,” PLoS One 6(11), e27385 (2011).
[Crossref]

T. G. Belgard, A. C. Marques, P. L. Oliver, H. O. Abaan, T. M. Sirey, A. Hoerder-Suabedissen, F. García-Moreno, Z. Molnár, E. H. Margulies, and C. P. Ponting, “A transcriptomic atlas of mouse neocortical layers,” Neuron 71(4), 605–616 (2011).
[Crossref]

Y. Jia, M. R. Grafe, A. Gruber, N. J. Alkayed, and R. K. Wang, “In vivo optical imaging of revascularization after brain trauma in mice,” Microvasc. Res. 81(1), 73–80 (2011).
[Crossref]

2010 (2)

T. H. Chia and M. J. Levene, “Multi-Layer In Vivo Imaging of Neocortex Using a Microprism,” Cold Spring Harb Protoc 2010(8), pdb.prot5476 (2010).
[Crossref]

A. Sigler and T. H. Murphy, “In vivo 2-photon imaging of fine structure in the rodent brain: before, during, and after stroke,” Stroke 41(10, Supplement 1), S117–S123 (2010).
[Crossref]

2009 (3)

T. H. Chia and M. J. Levene, “Microprisms for In Vivo Multilayer Cortical Imaging,” J. Neurophysiol. 102(2), 1310–1314 (2009).
[Crossref]

D. Navaratna, S. Guo, K. Arai, and E. H. Lo, “Mechanisms and targets for angiogenic therapy after stroke,” Cell Adhes. Migr. 3(2), 216–223 (2009).
[Crossref]

P. S. Tsai, J. P. Kaufhold, P. Blinder, B. Friedman, P. J. Drew, H. J. Karten, P. D. Lyden, and D. Kleinfeld, “Correlations of neuronal and microvascular densities in murine cortex revealed by direct counting and colocalization of nuclei and vessels,” J. Neurosci. 29(46), 14553–14570 (2009).
[Crossref]

2007 (1)

2006 (1)

T. Hayashi, K. Deguchi, S. Nagotani, H. Zhang, Y. Sehara, A. Tsuchiya, and K. Abe, “Cerebral ischemia and angiogenesis,” Curr. Neurovasc. Res. 3(2), 119–129 (2006).
[Crossref]

2002 (1)

A. N. Yaroslavsky, P. C. Schulze, I. V. Yaroslavsky, R. Schober, F. Ulrich, and H. J. Schwarzmaier, “Optical properties of selected native and coagulated human brain tissues in vitro in the visible and near infrared spectral range,” Phys. Med. Biol. 47(12), 2059–2073 (2002).
[Crossref]

1994 (1)

K. A. Rempp, G. Brix, F. Wenz, C. R. Becker, F. Gückel, and W. J. Lorenz, “Quantification of regional cerebral blood flow and volume with dynamic susceptibility contrast-enhanced MR imaging,” Radiology 193(3), 637–641 (1994).
[Crossref]

Abaan, H. O.

T. G. Belgard, A. C. Marques, P. L. Oliver, H. O. Abaan, T. M. Sirey, A. Hoerder-Suabedissen, F. García-Moreno, Z. Molnár, E. H. Margulies, and C. P. Ponting, “A transcriptomic atlas of mouse neocortical layers,” Neuron 71(4), 605–616 (2011).
[Crossref]

Abe, K.

T. Hayashi, K. Deguchi, S. Nagotani, H. Zhang, Y. Sehara, A. Tsuchiya, and K. Abe, “Cerebral ischemia and angiogenesis,” Curr. Neurovasc. Res. 3(2), 119–129 (2006).
[Crossref]

Abliz, E.

Adams, D. L.

D. L. Adams, V. Piserchia, J. R. Economides, and J. C. Horton, “Vascular Supply of the Cerebral Cortex is Specialized for Cell Layers but Not Columns,” Cereb. Cortex 25(10), 3673–3681 (2015).
[Crossref]

Agrawal, A.

Aleksoska, E.

S. S. J. Rewell, L. Churilov, T. K. Sidon, E. Aleksoska, S. F. Cox, M. R. Macleod, and D. W. Howells, “Evolution of ischemic damage and behavioural deficit over 6 months after MCAo in the rat: Selecting the optimal outcomes and statistical power for multi-centre preclinical trials,” PLoS One 12(2), e0171688 (2017).
[Crossref]

Alfieri, A.

N. Percie du Sert, A. Alfieri, S. M. Allan, H. V. Carswell, G. A. Deuchar, T. D. Farr, P. Flecknell, L. Gallagher, C. L. Gibson, M. J. Haley, M. R. Macleod, B. W. McColl, C. McCabe, A. Morancho, L. D. Moon, M. J. O’Neill, I. Pérez de Puig, A. Planas, C. I. Ragan, A. Rosell, L. A. Roy, K. O. Ryder, A. Simats, E. S. Sena, B. A. Sutherland, M. D. Tricklebank, R. C. Trueman, L. Whitfield, R. Wong, and I. M. Macrae, “The IMPROVE Guidelines (Ischaemia Models: Procedural Refinements Of in Vivo Experiments),” J. Cereb. Blood Flow Metab. 37(11), 3488–3517 (2017).
[Crossref]

Alhusban, A.

A. Ergul, A. Alhusban, and S. C. Fagan, “Angiogenesis: A Harmonized Target for Recovery after Stroke,” Stroke 43(8), 2270–2274 (2012).
[Crossref]

Alkayed, N. J.

Y. Jia, M. R. Grafe, A. Gruber, N. J. Alkayed, and R. K. Wang, “In vivo optical imaging of revascularization after brain trauma in mice,” Microvasc. Res. 81(1), 73–80 (2011).
[Crossref]

Allan, S. M.

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Figures (7)

Fig. 1.
Fig. 1. (a) Schematic of the experimental vis-OCT system. C: collimator; CL: camera lens; DC: dispersion compensation; FC: fiber coupler; G: grating; GS: galvanometer scanners; LC: line camera; M: mirror; SC: supercontinuum; SL: scan lens; SM: spectrometer. (b) Reference arm and sample arm spectra. (c) Fourier transform of the spectrum. (d) Sensitivity roll-off.
Fig. 2.
Fig. 2. (a) Schematic of the cranial window-microprism assembly and implantation. CX: cortex; WM: white matter; (b) Relationship between the top-view and side-view images. Yellow dashed square: side-view from the microprism; blue dashed square: top-view; (c) Imaging volume acquired from top-view (blue cuboid); (d) Imaging volume acquired from side-view (yellow cuboid); (e) Illustration of top-view and side-view en face vis-OCTA images and B-scan image with respect to their geometries.
Fig. 3.
Fig. 3. (a) Optical microscopic image of the entire cranial window with both top-view (blue dash square) and side-view (yellow dash square) from the prism; (b) Magnified optical microscopic image of the area corresponding to the blue dashed area in panel a; (c) Magnified optical microscopic image of the area corresponding to the yellow dashed area in panel a. Yellow arrows: vessels in the deep cortex area; blue dash area: white matter. (d) Top-view en face vis-OCT image; (e) Side-view en face vis-OCT image; (f) Top-view vis-OCTA image with color-coded vessel depths; (g) Side-view en face vis-OCTA image with color-coded vessel depth. Purple area: deep cortex imaged through the prism. Blue dashed area: white matter; (h, i) vis-OCT & vis-OCTA B-scan images acquired from the top-view. White arrows: vessel shadows from top block signal beneath them; Red arrow: effective image depth around 250 µm calculated from the vis-OCTA vessel signal; (j, k) Vis-OCT & Vis-OCTA B-scan images acquired from the side view. green arrow: 1 mm image depth through the prism; blue arrow and dash area: higher backscattering intensity from white matter. (White scale bar: 200 µm).
Fig. 4.
Fig. 4. Longitudinal monitoring of the structure and circulatory change after surgical implantation of the microprism and cranial window from day 2 to day 28. (a1-a5) Optical microscopic images from top-view after implantation. Blue arrows: bleeding; (b1-b5) Top-view vis-OCTA en face images acquired from. Blue arrows: bleeding. Yellow arrow heads: vessel diameter variation; Yellow-line: B-scan image positions; (c1-c5) Vis-OCT B-scan images of superficial cortex. Blue stars: liquid accumulation between the brain tissue and cranial window; (d1-d5) Side-view vis-OCTA en face images. Yellow stars: non-vascular area; Red stars: vessel reappearance; Red arrows: diameter variation of the same vessel; Blue lines: B-scan positions; (e1-e5) Vis-OCT B-scan images of deep cortex; Blue stars: liquid accumulation between the brain tissue and prism; Blue arrows: full depth of cortex; Orange arrows: white matter. Yellow scale bar: 200 µm.
Fig. 5.
Fig. 5. Determining blood vessel stability using vessel morphology, diameter, and density. (a) Overlaid top-view vis-OCTA en face images from day 15 and day 28; (b) Overlaid side-view vis-OCT en face images from day 15 and day 28. Yellow color: overlapped regions. (c) Top-view vis-OCT image from day 3; (d) Top-view vis-OCT image from day 15. The yellow dashed lines highlight the main vessel within the field of view. The red lines highlight where vessel diameters were measured; (e) Side-view vis-OCTA image on day 11; (f) Vessel segmentation using AngioTool. Yellow: boundaries of automatically detected vessels. Red: centerlines of vessels; (g) Changes in vessel diameters from day 3 to day 28 from both top-view and side-view vis-OCTA images. Mean and standard deviations are plotted. (h) Changes in vessel area density from day 3 to day 28 from both top-view and side-view vis-OCTA images. Mean and standard deviations are plotted. Statistical analysis is compared with Day 28. ns: no significant difference. *: P < 0.05, **: P < 0.01, ***: P < 0.001, ****: P < 0.0001.
Fig. 6.
Fig. 6. Longitudinal monitoring of acute (day 1 to day 3) and chronic (day 30 and day 60) changes after tMCAO. (a1-a6) Optical microscopic images from top-view before and after tMCAO. Yellow dashed square: side view from the microprism; blue dashed square: top-view; (b1-b6) Top-view vis-OCTA en face images before and after tMCAO. Blue arrow heads: vessel dilation (b2-b4); vessel constriction (b5-b6). Blue stars: reduced flow signal. Red arrows: bounded neovascularization. (c1-c6) Side-view vis-OCTA en face images before and after tMCAO. Green arrows: vessel dilation (c3-c4); vessel narrowing (c5-c6). Yellow stars: reduced flow signal. Red stars: overgrown neovascularization. (Black scale bar: 1mm; Red scale bar: 400 µm, Yellow scale bar: 200 µm)
Fig. 7.
Fig. 7. Vascular changes during the first week after stroke. (a) Side-view vis-OCTA en face image showing the cortical layer separations, with the three layer groups highlighted by the green horizontal lines. L1-3: layers 1-3 of the cortex; L4: layer 4 of the cortex; L5-6: layers 5 and 6 of the cortex. (b) Changes in vessel density from day 0 (acquired immediately before performing the stroke) to day 7 after the stroke, separated by cortical layer groups. Mean and standard deviation across three mice are plotted. (c1-c5) Top-view vis-OCTA en face images pseudo-colored according to measured sO2, from immediately before stroke to 7 days after stroke. (d1-d5) Side-view vis-OCTA en face images pseudo-colored according to measured sO2, from immediately before stroke to 7 days after stroke.

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