Abstract

We propose a new method and optical instrumentation for mouse brain imaging based on extended-focus optical coherence microscopy. This in vivo imaging technique allows the evaluation of the cytoarchitecture at cellular level and the circulation system dynamics in three dimensions. This minimally invasive and non-contact approach is performed without the application of contrasting agents. The optical design achieved a resolution of 2.2 μm over a distance of 800 μm, which was sufficient to obtain a detailed three-dimensional image of a wild-type mouse’s brain down to the layer III of the cortex. Intrinsically contrasted microvessels and structures similar to the bodies of neurons were distinguishable.

© 2016 Optical Society of America

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References

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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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    [Crossref] [PubMed]

2016 (3)

2015 (3)

U. Baran, Y. Li, and R. K. Wang, “Vasodynamics of pial and penetrating arterioles in relation to arteriolo-arteriolar anastomosis after focal stroke,” Neurophotonics 2(2), 025006 (2015).
[Crossref] [PubMed]

W. J. Choi and R. K. Wang, “Swept-source optical coherence tomography powered by a 1.3-μm vertical cavity surface emitting laser enables 2.3-mm-deep brain imaging in mice in vivo,” J. Biomed. Opt. 20(10), 106004 (2015).
[Crossref] [PubMed]

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] [PubMed]

2014 (4)

J. You, C. Du, N. D. Volkow, and Y. Pan, “Optical coherence Doppler tomography for quantitative cerebral blood flow imaging,” Biomed. Opt. Express 5(9), 3217–3230 (2014).
[Crossref] [PubMed]

G. Hong, S. Diao, J. Chang, A. L. Antaris, C. Chen, B. Zhang, S. Zhao, D. N. Atochin, P. L. Huang, K. I. Andreasson, C. J. Kuo, and H. Dai, “Through-skull fluorescence imaging of the brain in a new near-infrared window,” Nat. Photonics 8(9), 723–730 (2014).
[Crossref]

E. A. Susaki, K. Tainaka, D. Perrin, F. Kishino, T. Tawara, T. M. Watanabe, C. Yokoyama, H. Onoe, M. Eguchi, S. Yamaguchi, T. Abe, H. Kiyonari, Y. Shimizu, A. Miyawaki, H. Yokota, and H. R. Ueda, “Whole-Brain Imaging with Single-Cell Resolution Using Chemical Cocktails and Computational Analysis,” Cell 157(3), 726–739 (2014).
[Crossref] [PubMed]

A. Bouwens, T. Bolmont, D. Szlag, C. Berclaz, and T. Lasser, “Quantitative cerebral blood flow imaging with extended-focus optical coherence microscopy,” Opt. Lett. 39(1), 37–40 (2014).
[Crossref] [PubMed]

2013 (2)

L.-D. Liao, V. Tsytsarev, I. Delgado-Martínez, M.-L. Li, R. Erzurumlu, A. Vipin, J. Orellana, Y.-R. Lin, H.-Y. Lai, Y.-Y. Chen, and N. V. Thakor, “Neurovascular coupling: in vivo optical techniques for functional brain imaging,” Biomed. Eng. Online 12(1), 38 (2013).
[Crossref] [PubMed]

C. Leahy, H. Radhakrishnan, and V. J. Srinivasan, “Volumetric imaging and quantification of cytoarchitecture and myeloarchitecture with intrinsic scattering contrast,” Biomed. Opt. Express 4(10), 1978–1990 (2013).
[Crossref] [PubMed]

2012 (4)

D. Lorenser, X. Yang, and D. D. Sampson, “Ultrathin fiber probes with extended depth of focus for optical coherence tomography,” Opt. Lett. 37(10), 1616–1618 (2012).
[Crossref] [PubMed]

V. J. Srinivasan, H. Radhakrishnan, J. Y. Jiang, S. Barry, and A. E. Cable, “Optical coherence microscopy for deep tissue imaging of the cerebral cortex with intrinsic contrast,” Opt. Express 20(3), 2220–2239 (2012).
[Crossref] [PubMed]

A. Devor, S. Sakadžić, V. J. Srinivasan, M. A. Yaseen, K. Nizar, P. A. Saisan, P. Tian, A. M. Dale, S. A. Vinogradov, M. A. Franceschini, and D. A. Boas, “Frontiers in optical imaging of cerebral blood flow and metabolism,” J. Cereb. Blood Flow Metab. 32(7), 1259–1276 (2012).
[Crossref] [PubMed]

T. Bolmont, A. Bouwens, C. Pache, M. Dimitrov, C. Berclaz, M. Villiger, B. M. Wegenast-Braun, T. Lasser, and P. C. Fraering, “Label-free imaging of cerebral β-amyloidosis with extended-focus optical coherence microscopy,” J. Neurosci. 32(42), 14548–14556 (2012).
[Crossref] [PubMed]

2011 (1)

L. Liu, J. A. Gardecki, S. K. Nadkarni, J. D. Toussaint, Y. Yagi, B. E. Bouma, and G. J. Tearney, “Imaging the subcellular structure of human coronary atherosclerosis using micro-optical coherence tomography,” Nat. Med. 17(8), 1010–1014 (2011).
[Crossref] [PubMed]

2009 (1)

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]

2007 (3)

T. S. Ralston, D. L. Marks, P. S. Carney, and S. A. Boppart, “Interferometric synthetic aperture microscopy,” Nat. Phys. 3(2), 129–134 (2007).
[Crossref] [PubMed]

E. M. C. Hillman, “Optical brain imaging in vivo: techniques and applications from animal to man,” J. Biomed. Opt. 12(5), 051402 (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. Express 15(20), 12636–12653 (2007).
[Crossref] [PubMed]

2006 (1)

2002 (1)

J. DeFelipe, L. Alonso-Nanclares, and J. I. Arellano, “Microstructure of the neocortex: comparative aspects,” J. Neurocytol. 31(3-5), 299–316 (2002).
[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,” Nature 324(6095), 361–364 (1986).
[Crossref] [PubMed]

Abe, T.

E. A. Susaki, K. Tainaka, D. Perrin, F. Kishino, T. Tawara, T. M. Watanabe, C. Yokoyama, H. Onoe, M. Eguchi, S. Yamaguchi, T. Abe, H. Kiyonari, Y. Shimizu, A. Miyawaki, H. Yokota, and H. R. Ueda, “Whole-Brain Imaging with Single-Cell Resolution Using Chemical Cocktails and Computational Analysis,” Cell 157(3), 726–739 (2014).
[Crossref] [PubMed]

Alonso-Nanclares, L.

J. DeFelipe, L. Alonso-Nanclares, and J. I. Arellano, “Microstructure of the neocortex: comparative aspects,” J. Neurocytol. 31(3-5), 299–316 (2002).
[Crossref] [PubMed]

Andreasson, K. I.

G. Hong, S. Diao, J. Chang, A. L. Antaris, C. Chen, B. Zhang, S. Zhao, D. N. Atochin, P. L. Huang, K. I. Andreasson, C. J. Kuo, and H. Dai, “Through-skull fluorescence imaging of the brain in a new near-infrared window,” Nat. Photonics 8(9), 723–730 (2014).
[Crossref]

Antaris, A. L.

G. Hong, S. Diao, J. Chang, A. L. Antaris, C. Chen, B. Zhang, S. Zhao, D. N. Atochin, P. L. Huang, K. I. Andreasson, C. J. Kuo, and H. Dai, “Through-skull fluorescence imaging of the brain in a new near-infrared window,” Nat. Photonics 8(9), 723–730 (2014).
[Crossref]

Arellano, J. I.

J. DeFelipe, L. Alonso-Nanclares, and J. I. Arellano, “Microstructure of the neocortex: comparative aspects,” J. Neurocytol. 31(3-5), 299–316 (2002).
[Crossref] [PubMed]

Atochin, D. N.

G. Hong, S. Diao, J. Chang, A. L. Antaris, C. Chen, B. Zhang, S. Zhao, D. N. Atochin, P. L. Huang, K. I. Andreasson, C. J. Kuo, and H. Dai, “Through-skull fluorescence imaging of the brain in a new near-infrared window,” Nat. Photonics 8(9), 723–730 (2014).
[Crossref]

Bachmann, A. H.

Baran, U.

U. Baran and R. K. Wang, “Review of optical coherence tomography based angiography in neuroscience,” Neurophotonics 3(1), 010902 (2016).
[Crossref] [PubMed]

U. Baran, Y. Li, and R. K. Wang, “Vasodynamics of pial and penetrating arterioles in relation to arteriolo-arteriolar anastomosis after focal stroke,” Neurophotonics 2(2), 025006 (2015).
[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]

Berclaz, C.

A. Bouwens, T. Bolmont, D. Szlag, C. Berclaz, and T. Lasser, “Quantitative cerebral blood flow imaging with extended-focus optical coherence microscopy,” Opt. Lett. 39(1), 37–40 (2014).
[Crossref] [PubMed]

T. Bolmont, A. Bouwens, C. Pache, M. Dimitrov, C. Berclaz, M. Villiger, B. M. Wegenast-Braun, T. Lasser, and P. C. Fraering, “Label-free imaging of cerebral β-amyloidosis with extended-focus optical coherence microscopy,” J. Neurosci. 32(42), 14548–14556 (2012).
[Crossref] [PubMed]

Boas, D. A.

A. Devor, S. Sakadžić, V. J. Srinivasan, M. A. Yaseen, K. Nizar, P. A. Saisan, P. Tian, A. M. Dale, S. A. Vinogradov, M. A. Franceschini, and D. A. Boas, “Frontiers in optical imaging of cerebral blood flow and metabolism,” J. Cereb. Blood Flow Metab. 32(7), 1259–1276 (2012).
[Crossref] [PubMed]

Bolmont, T.

A. Bouwens, T. Bolmont, D. Szlag, C. Berclaz, and T. Lasser, “Quantitative cerebral blood flow imaging with extended-focus optical coherence microscopy,” Opt. Lett. 39(1), 37–40 (2014).
[Crossref] [PubMed]

T. Bolmont, A. Bouwens, C. Pache, M. Dimitrov, C. Berclaz, M. Villiger, B. M. Wegenast-Braun, T. Lasser, and P. C. Fraering, “Label-free imaging of cerebral β-amyloidosis with extended-focus optical coherence microscopy,” J. Neurosci. 32(42), 14548–14556 (2012).
[Crossref] [PubMed]

Boppart, S. A.

T. S. Ralston, D. L. Marks, P. S. Carney, and S. A. Boppart, “Interferometric synthetic aperture microscopy,” Nat. Phys. 3(2), 129–134 (2007).
[Crossref] [PubMed]

Bouma, B. E.

L. Liu, J. A. Gardecki, S. K. Nadkarni, J. D. Toussaint, Y. Yagi, B. E. Bouma, and G. J. Tearney, “Imaging the subcellular structure of human coronary atherosclerosis using micro-optical coherence tomography,” Nat. Med. 17(8), 1010–1014 (2011).
[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]

Bouwens, A.

A. Bouwens, T. Bolmont, D. Szlag, C. Berclaz, and T. Lasser, “Quantitative cerebral blood flow imaging with extended-focus optical coherence microscopy,” Opt. Lett. 39(1), 37–40 (2014).
[Crossref] [PubMed]

T. Bolmont, A. Bouwens, C. Pache, M. Dimitrov, C. Berclaz, M. Villiger, B. M. Wegenast-Braun, T. Lasser, and P. C. Fraering, “Label-free imaging of cerebral β-amyloidosis with extended-focus optical coherence microscopy,” J. Neurosci. 32(42), 14548–14556 (2012).
[Crossref] [PubMed]

Cable, A. E.

Carney, P. S.

T. S. Ralston, D. L. Marks, P. S. Carney, and S. A. Boppart, “Interferometric synthetic aperture microscopy,” Nat. Phys. 3(2), 129–134 (2007).
[Crossref] [PubMed]

Chang, J.

G. Hong, S. Diao, J. Chang, A. L. Antaris, C. Chen, B. Zhang, S. Zhao, D. N. Atochin, P. L. Huang, K. I. Andreasson, C. J. Kuo, and H. Dai, “Through-skull fluorescence imaging of the brain in a new near-infrared window,” Nat. Photonics 8(9), 723–730 (2014).
[Crossref]

Chen, C.

G. Hong, S. Diao, J. Chang, A. L. Antaris, C. Chen, B. Zhang, S. Zhao, D. N. Atochin, P. L. Huang, K. I. Andreasson, C. J. Kuo, and H. Dai, “Through-skull fluorescence imaging of the brain in a new near-infrared window,” Nat. Photonics 8(9), 723–730 (2014).
[Crossref]

Chen, Y.-Y.

L.-D. Liao, V. Tsytsarev, I. Delgado-Martínez, M.-L. Li, R. Erzurumlu, A. Vipin, J. Orellana, Y.-R. Lin, H.-Y. Lai, Y.-Y. Chen, and N. V. Thakor, “Neurovascular coupling: in vivo optical techniques for functional brain imaging,” Biomed. Eng. Online 12(1), 38 (2013).
[Crossref] [PubMed]

Choi, W. J.

W. J. Choi and R. K. Wang, “Swept-source optical coherence tomography powered by a 1.3-μm vertical cavity surface emitting laser enables 2.3-mm-deep brain imaging in mice in vivo,” J. Biomed. Opt. 20(10), 106004 (2015).
[Crossref] [PubMed]

Chong, S. P.

Chu, K. K.

Cooke, D. F.

Dai, H.

G. Hong, S. Diao, J. Chang, A. L. Antaris, C. Chen, B. Zhang, S. Zhao, D. N. Atochin, P. L. Huang, K. I. Andreasson, C. J. Kuo, and H. Dai, “Through-skull fluorescence imaging of the brain in a new near-infrared window,” Nat. Photonics 8(9), 723–730 (2014).
[Crossref]

Dale, A. M.

A. Devor, S. Sakadžić, V. J. Srinivasan, M. A. Yaseen, K. Nizar, P. A. Saisan, P. Tian, A. M. Dale, S. A. Vinogradov, M. A. Franceschini, and D. A. Boas, “Frontiers in optical imaging of cerebral blood flow and metabolism,” J. Cereb. Blood Flow Metab. 32(7), 1259–1276 (2012).
[Crossref] [PubMed]

DeFelipe, J.

J. DeFelipe, L. Alonso-Nanclares, and J. I. Arellano, “Microstructure of the neocortex: comparative aspects,” J. Neurocytol. 31(3-5), 299–316 (2002).
[Crossref] [PubMed]

Delgado-Martínez, I.

L.-D. Liao, V. Tsytsarev, I. Delgado-Martínez, M.-L. Li, R. Erzurumlu, A. Vipin, J. Orellana, Y.-R. Lin, H.-Y. Lai, Y.-Y. Chen, and N. V. Thakor, “Neurovascular coupling: in vivo optical techniques for functional brain imaging,” Biomed. Eng. Online 12(1), 38 (2013).
[Crossref] [PubMed]

Devor, A.

A. Devor, S. Sakadžić, V. J. Srinivasan, M. A. Yaseen, K. Nizar, P. A. Saisan, P. Tian, A. M. Dale, S. A. Vinogradov, M. A. Franceschini, and D. A. Boas, “Frontiers in optical imaging of cerebral blood flow and metabolism,” J. Cereb. Blood Flow Metab. 32(7), 1259–1276 (2012).
[Crossref] [PubMed]

Dholakia, K.

D. McGloin and K. Dholakia, “Bessel Beams: Diffraction in a new light,” (2005).

Diao, S.

G. Hong, S. Diao, J. Chang, A. L. Antaris, C. Chen, B. Zhang, S. Zhao, D. N. Atochin, P. L. Huang, K. I. Andreasson, C. J. Kuo, and H. Dai, “Through-skull fluorescence imaging of the brain in a new near-infrared window,” Nat. Photonics 8(9), 723–730 (2014).
[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, “Label-free imaging of cerebral β-amyloidosis with extended-focus optical coherence microscopy,” J. Neurosci. 32(42), 14548–14556 (2012).
[Crossref] [PubMed]

Du, C.

Eguchi, M.

E. A. Susaki, K. Tainaka, D. Perrin, F. Kishino, T. Tawara, T. M. Watanabe, C. Yokoyama, H. Onoe, M. Eguchi, S. Yamaguchi, T. Abe, H. Kiyonari, Y. Shimizu, A. Miyawaki, H. Yokota, and H. R. Ueda, “Whole-Brain Imaging with Single-Cell Resolution Using Chemical Cocktails and Computational Analysis,” Cell 157(3), 726–739 (2014).
[Crossref] [PubMed]

Erzurumlu, R.

L.-D. Liao, V. Tsytsarev, I. Delgado-Martínez, M.-L. Li, R. Erzurumlu, A. Vipin, J. Orellana, Y.-R. Lin, H.-Y. Lai, Y.-Y. Chen, and N. V. Thakor, “Neurovascular coupling: in vivo optical techniques for functional brain imaging,” Biomed. Eng. Online 12(1), 38 (2013).
[Crossref] [PubMed]

Fingler, J.

Fraering, P. C.

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Supplementary Material (1)

NameDescription
» Visualization 1: MP4 (13716 KB)      Fly-through across the whole 3D structural data set from the mouse brain after spatio-temporal averaging.

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Figures (9)

Fig. 1
Fig. 1

(a) Experimental setup; (b) example of image obtained in the brightfield preview mode; (c) anesthetized animal during experimentation (distance between the tip of the microscopic objective and the cranial window: 10 mm).

Fig. 2
Fig. 2

(a) The phantom used for the PSF measurement; (b) schematic of the Bessel beam geometry and photograph of the Bessel beam scattered in the phantom used for the measurement of PSF; (c) structural B-scan (logarithmic scale) of the phantom with color-coded depth; (d) en face image of the artifact, depth coded as in (c) Scale bar: 20 μm.

Fig. 3
Fig. 3

PSF cross sections of the optical setup reconstructed at variable depths (logarithmic intensity scale).

Fig. 4
Fig. 4

(a) Structural B-scan of the mouse brain (b) after spatial averaging and (c) after spatio-temporal averaging. Scale bars: 100 µm. A fly-through projection across the whole 3D structural data set represented by (c) is presented in Visualization 1.

Fig. 5
Fig. 5

Spatial distribution of the neuron-like structures detected in the mouse cerebral cortex.

Fig. 6
Fig. 6

Mean density of the counted neuron-like structures versus depth.

Fig. 7
Fig. 7

Two-dimensional neuron density maps for various depths (indicated in the top structural B-scan).

Fig. 8
Fig. 8

a) Angiographic B-scan; b) angiographic B-scan overlaid on the corresponding structural image.

Fig. 9
Fig. 9

Wide-field maps of a) the structure and b) the flow of the mouse brain. Scale bar: 200 μm.

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