Abstract

A spectral/Fourier domain optical coherence tomography (OCT) intravital microscope using a supercontinuum light source at 1.7 μm was developed to study subcortical structures noninvasively in the living mouse brain. The benefits of 1.7 μm for deep tissue brain imaging are demonstrated by quantitatively comparing OCT signal attenuation characteristics of cortical tissue across visible and near-infrared wavelengths. Imaging of hippocampal tissue architecture and white matter microvasculature are demonstrated in vivo through thinned-skull, glass coverslip-reinforced cranial windows in mice. Applications of this novel platform include monitoring disease progression and pathophysiology in rodent models of Alzheimer’s disease and subcortical dementias, including vascular dementia.

© 2015 Optical Society of America

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References

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2009 (2)

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2006 (2)

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F. Helmchen and W. Denk, Nat. Methods 2, 932 (2005).
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G. S. Hong, S. Diao, J. L. Chang, A. L. Antaris, C. X. Chen, B. Zhang, S. Zhao, D. N. Atochin, P. L. Huang, K. I. Andreasson, C. J. Kuo, and H. J. Dai, Nat. Photonics 8, 723 (2014).
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G. S. Hong, S. Diao, J. L. Chang, A. L. Antaris, C. X. Chen, B. Zhang, S. Zhao, D. N. Atochin, P. L. Huang, K. I. Andreasson, C. J. Kuo, and H. J. Dai, Nat. Photonics 8, 723 (2014).
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Hurst, S.

Hwang, S. H.

E. J. Jung, J. H. Lee, B. S. Rho, M. J. Kim, S. H. Hwang, W.-J. Lee, J.-J. Song, M. Y. Jeong, and C.-S. Kim, IEEE J. Sel. Top. Quantum Electron. 18, 1200 (2012).
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Ishida, S.

S. Ishida and N. Nishizawa, Biomed. Opt. Express 3, 282 (2012).
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S. Ishida, N. Nishizawa, T. Ohta, and K. Itoh, Appl. Phys. Express 4, 052501 (2011).
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S. Ishida, N. Nishizawa, T. Ohta, and K. Itoh, Appl. Phys. Express 4, 052501 (2011).
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S. L. Jacques, Phys. Med. Biol. 58, R37 (2013).
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R. K. Wang, S. L. Jacques, Z. Ma, S. Hurst, S. R. Hanson, and A. Gruber, Opt. Express 15, 4083 (2007).
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S. L. Jacques, D. Levitz, R. Samatham, D. S. Gareau, N. Choudhury, and F. Truffer, in Biomedical Applications of Light Scattering, W. Adam and B. Vadim, eds. (McGraw-Hill, 2010), pp. 171–191.

Jeon, S. W.

S. W. Jeon, M. A. Shure, K. B. Baker, D. Huang, A. M. Rollins, A. Chahlavi, and A. R. Rezai, J. Neurosci. Methods 154, 96 (2006).
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E. J. Jung, J. H. Lee, B. S. Rho, M. J. Kim, S. H. Hwang, W.-J. Lee, J.-J. Song, M. Y. Jeong, and C.-S. Kim, IEEE J. Sel. Top. Quantum Electron. 18, 1200 (2012).
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E. J. Jung, J. H. Lee, B. S. Rho, M. J. Kim, S. H. Hwang, W.-J. Lee, J.-J. Song, M. Y. Jeong, and C.-S. Kim, IEEE J. Sel. Top. Quantum Electron. 18, 1200 (2012).
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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, Nat. Methods 7, 981 (2010).
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Knutsen, P. M.

P. J. Drew, A. Y. Shih, J. D. Driscoll, P. M. Knutsen, P. Blinder, D. Davalos, K. Akassoglou, P. S. Tsai, and D. Kleinfeld, Nat. Methods 7, 981 (2010).
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Kobat, D.

N. G. Horton, K. Wang, D. Kobat, C. G. Clark, F. W. Wise, C. B. Schaffer, and C. Xu, Nat. Photonics 7, 205 (2013).
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D. Kobat, M. E. Durst, N. Nishimura, A. W. Wong, C. B. Schaffer, and C. Xu, Opt. Express 17, 13354 (2009).
[Crossref]

Kuo, C. J.

G. S. Hong, S. Diao, J. L. Chang, A. L. Antaris, C. X. Chen, B. Zhang, S. Zhao, D. N. Atochin, P. L. Huang, K. I. Andreasson, C. J. Kuo, and H. J. Dai, Nat. Photonics 8, 723 (2014).
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Leahy, C.

Lee, J. H.

E. J. Jung, J. H. Lee, B. S. Rho, M. J. Kim, S. H. Hwang, W.-J. Lee, J.-J. Song, M. Y. Jeong, and C.-S. Kim, IEEE J. Sel. Top. Quantum Electron. 18, 1200 (2012).
[Crossref]

Lee, W.-J.

E. J. Jung, J. H. Lee, B. S. Rho, M. J. Kim, S. H. Hwang, W.-J. Lee, J.-J. Song, M. Y. Jeong, and C.-S. Kim, IEEE J. Sel. Top. Quantum Electron. 18, 1200 (2012).
[Crossref]

Levitz, D.

S. L. Jacques, D. Levitz, R. Samatham, D. S. Gareau, N. Choudhury, and F. Truffer, in Biomedical Applications of Light Scattering, W. Adam and B. Vadim, eds. (McGraw-Hill, 2010), pp. 171–191.

Lo, E. H.

Ma, Z.

Makita, S.

Mandeville, E. T.

Merkle, C. W.

Nishimura, N.

Nishizawa, N.

S. Ishida and N. Nishizawa, Biomed. Opt. Express 3, 282 (2012).
[Crossref]

S. Ishida, N. Nishizawa, T. Ohta, and K. Itoh, Appl. Phys. Express 4, 052501 (2011).
[Crossref]

Ohta, T.

S. Ishida, N. Nishizawa, T. Ohta, and K. Itoh, Appl. Phys. Express 4, 052501 (2011).
[Crossref]

Radhakrishnan, H.

Reinoso, R. F.

R. F. Reinoso, B. A. Telfer, and M. Rowland, J. Pharmacol. Toxicol. Methods 38, 87 (1997).
[Crossref]

Rezai, A. R.

S. W. Jeon, M. A. Shure, K. B. Baker, D. Huang, A. M. Rollins, A. Chahlavi, and A. R. Rezai, J. Neurosci. Methods 154, 96 (2006).
[Crossref]

Rho, B. S.

E. J. Jung, J. H. Lee, B. S. Rho, M. J. Kim, S. H. Hwang, W.-J. Lee, J.-J. Song, M. Y. Jeong, and C.-S. Kim, IEEE J. Sel. Top. Quantum Electron. 18, 1200 (2012).
[Crossref]

Rollins, A. M.

S. W. Jeon, M. A. Shure, K. B. Baker, D. Huang, A. M. Rollins, A. Chahlavi, and A. R. Rezai, J. Neurosci. Methods 154, 96 (2006).
[Crossref]

Rowland, M.

R. F. Reinoso, B. A. Telfer, and M. Rowland, J. Pharmacol. Toxicol. Methods 38, 87 (1997).
[Crossref]

Samatham, R.

S. L. Jacques, D. Levitz, R. Samatham, D. S. Gareau, N. Choudhury, and F. Truffer, in Biomedical Applications of Light Scattering, W. Adam and B. Vadim, eds. (McGraw-Hill, 2010), pp. 171–191.

Sato, T. R.

N. Ji, T. R. Sato, and E. Betzig, Proc. Natl. Acad. Sci. USA 109, 22 (2012).
[Crossref]

Schaffer, C. B.

N. G. Horton, K. Wang, D. Kobat, C. G. Clark, F. W. Wise, C. B. Schaffer, and C. Xu, Nat. Photonics 7, 205 (2013).
[Crossref]

D. Kobat, M. E. Durst, N. Nishimura, A. W. Wong, C. B. Schaffer, and C. Xu, Opt. Express 17, 13354 (2009).
[Crossref]

Schmitt, J. M.

Sharma, U.

Shih, A. Y.

P. J. Drew, A. Y. Shih, J. D. Driscoll, P. M. Knutsen, P. Blinder, D. Davalos, K. Akassoglou, P. S. Tsai, and D. Kleinfeld, Nat. Methods 7, 981 (2010).
[Crossref]

Shure, M. A.

S. W. Jeon, M. A. Shure, K. B. Baker, D. Huang, A. M. Rollins, A. Chahlavi, and A. R. Rezai, J. Neurosci. Methods 154, 96 (2006).
[Crossref]

Song, J.-J.

E. J. Jung, J. H. Lee, B. S. Rho, M. J. Kim, S. H. Hwang, W.-J. Lee, J.-J. Song, M. Y. Jeong, and C.-S. Kim, IEEE J. Sel. Top. Quantum Electron. 18, 1200 (2012).
[Crossref]

Srinivasan, V. J.

Telfer, B. A.

R. F. Reinoso, B. A. Telfer, and M. Rowland, J. Pharmacol. Toxicol. Methods 38, 87 (1997).
[Crossref]

Theer, P.

Truffer, F.

S. L. Jacques, D. Levitz, R. Samatham, D. S. Gareau, N. Choudhury, and F. Truffer, in Biomedical Applications of Light Scattering, W. Adam and B. Vadim, eds. (McGraw-Hill, 2010), pp. 171–191.

Tsai, P. S.

P. J. Drew, A. Y. Shih, J. D. Driscoll, P. M. Knutsen, P. Blinder, D. Davalos, K. Akassoglou, P. S. Tsai, and D. Kleinfeld, Nat. Methods 7, 981 (2010).
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van der Meer, F. J.

van Leeuwen, T. G.

Wang, K.

N. G. Horton, K. Wang, D. Kobat, C. G. Clark, F. W. Wise, C. B. Schaffer, and C. Xu, Nat. Photonics 7, 205 (2013).
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Wang, R. K.

Wise, F. W.

N. G. Horton, K. Wang, D. Kobat, C. G. Clark, F. W. Wise, C. B. Schaffer, and C. Xu, Nat. Photonics 7, 205 (2013).
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Wong, A. W.

Xu, C.

N. G. Horton, K. Wang, D. Kobat, C. G. Clark, F. W. Wise, C. B. Schaffer, and C. Xu, Nat. Photonics 7, 205 (2013).
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D. Kobat, M. E. Durst, N. Nishimura, A. W. Wong, C. B. Schaffer, and C. Xu, Opt. Express 17, 13354 (2009).
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Figures (4)

Fig. 1.
Fig. 1. (A) 1.7 μm OCT intravital microscope. The NKT supercontinuum light source was filtered by a short-pass filter (SPF) and a long-pass filter (LPF) after 7% reflection by a sapphire window before fiber coupling. M, mirror; PP, prism pair; NDF, neutral density filter; L, lens; DG, diffraction grating; LSC, line-scan camera; OBJ, objective lens. (B) Spectra measured either using a Fourier transform optical spectrum analyzer (blue solid line, OSA) or using our custom-made spectrometer (red-dotted line, LSC) agree. The FWHM bandwidths were almost identical, 170 nm , yielding a theoretical axial resolution of 7.5 μm in air ( 5.6 μm in tissue), though shaping due to water absorption will reduce the resolution in vivo. The total spectral range of our spectrometer was 246 nm . (C) The sensitivity roll-off of the system was approximately 10 dB over 2.5 mm in air (dotted line shows parabolic fit on a log scale).
Fig. 2.
Fig. 2. In vivo imaging of the mouse brain through a thinned-skull cranial window was performed by visible (A), 1.3 μm (B), and 1.7 μm (C) OCT, by placing the focus at the cortical surface. Scale bars in (C) represent 0.5 mm and apply for all images, and the full axial imaging range for each system is displayed. Subcortical backscattering is only noted at 1700 nm (C, red arrow). Rostral is right and dorsal is up. (D) Absorption and scattering spectra of relevant brain tissue constituents, with dashed boxes showing wavelengths ranges for (A)–(C). (E) The attenuation of the OCT signal was determined using a simple exponential fit, Aexp( μ t z ), where z is the imaging depth, over the first 200 μm of cortical tissue [boxes in (A)–(C)]. (F) Comparison of attenuation coefficients, measured at multiple coregistered locations in the same brain, shows that the 1.7 μm OCT attenuation coefficient was significantly lower than the attenuation coefficients at the other wavelengths ( * p < 0.05 , ** p < 0.01 , paired t-test). (G) A young mouse (5 weeks) had a lower attenuation coefficient ( * p < 0.05 , unpaired t-test) than an older mouse (5 months), most likely due to increased myelination and scattering with age.
Fig. 3.
Fig. 3. In vivo imaging of subcortical regions through the thinned skull was achieved by deep focusing using 1.7 μm OCT. (A) A maximum intensity projection of a series of cross-sectional images shows subcortical structures, including the hippocampus. Multiple subcortical layers can be distinguished, with corresponding layers highlighted with blue and red arrows. Green arrows show the corpus callosum. Orange arrows mark a blood vessel visible in (A) and (C). (B) Outlines of corresponding anatomical structures derived from photomicrographs of Nissl (C) and myelin-stained (D) tissue from the same brain that was imaged. Divisions of the hippocampus are dashed. cc, corpus callosum; Or, stratum oriens; Py, stratum pyramidale; Rad, stratum radiatum; and LMol, stratum lacunosum-moleculare. Scale bar: 0.2 mm. Rostral is right and dorsal is up.
Fig. 4.
Fig. 4. In vivo imaging of subcortical regions noninvasively through the thinned skull was achieved by deep focusing using 1.7 μm OCT. (A) A maximum intensity projection of a series of cross-sectional images shows subcortical structures, including the hippocampus proper. (B) Microvasculature in deep white matter regions is visualized using an OCT angiography method and a maximum intensity projection. Scale bars: 0.2 mm.

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