Abstract

Optical microscopy is a valuable tool for in vivo monitoring of biological structures and functions because of its non-invasiveness. However, imaging deep into biological tissues is challenging due to the scattering and absorption of light. Previous research has shown that 1300 nm and 1700 nm are the two best wavelength windows for deep brain imaging. Here, we combined long-wavelength illumination of ~1700 nm with reflectance confocal microscopy and achieved an imaging depth of ~1.3 mm with ~1-micrometer spatial resolution in adult mouse brains, which is 3-4 times deeper than that of conventional confocal microscopy using visible wavelength. We showed that the method can be added to any laser-scanning microscopy with simple and low-cost sources and detectors, such as continuous-wave diode lasers and InGaAs photodiodes. The long-wavelength, reflectance confocal imaging we demonstrated is label-free, and requires low illumination power. Furthermore, the imaging system is simple and low-cost, potentially creating new opportunities for biomedical research and clinical applications.

© 2018 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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References

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2018 (1)

2017 (2)

J. Kwon, M. Kim, H. Park, B. M. Kang, Y. Jo, J. H. Kim, O. James, S. H. Yun, S. G. Kim, M. Suh, and M. Choi, “Label-free nanoscale optical metrology on myelinated axons in vivo,” Nat. Commun. 8(1), 1832 (2017).
[Crossref] [PubMed]

D. G. Ouzounov, T. Wang, M. Wang, D. D. Feng, N. G. Horton, J. C. Cruz-Hernández, Y. T. Cheng, J. Reimer, A. S. Tolias, N. Nishimura, and C. Xu, “In vivo three-photon imaging of activity of GCaMP6-labeled neurons deep in intact mouse brain,” Nat. Methods 14(4), 388–390 (2017).
[Crossref] [PubMed]

2016 (1)

M. Yamanaka, T. Teranishi, H. Kawagoe, and N. Nishizawa, “Optical coherence microscopy in 1700 nm spectral band for high-resolution label-free deep-tissue imaging,” Sci. Rep. 6(1), 31715 (2016).
[Crossref] [PubMed]

2015 (2)

2014 (2)

A. J. Schain, R. A. Hill, and J. Grutzendler, “Label-free in vivo imaging of myelinated axons in health and disease with spectral confocal reflectance microscopy,” Nat. Med. 20(4), 443–449 (2014).
[Crossref] [PubMed]

E. Cinotti, L. Gergelé, J. L. Perrot, A. Dominé, B. Labeille, P. Borelli, and F. Cambazard, “Quantification of capillary blood cell flow using reflectance confocal microscopy,” Skin Res. Technol. 20(3), 373–378 (2014).
[Crossref] [PubMed]

2013 (1)

N. G. Horton, K. Wang, D. Kobat, C. G. Clark, F. W. Wise, C. B. Schaffer, and C. Xu, “In vivo three-photon microscopy of subcortical structures within an intact mouse brain,” Nat. Photonics 7(3), 205–209 (2013).
[Crossref] [PubMed]

2012 (1)

2011 (6)

J. W. Lichtman and W. Denk, “The big and the small: challenges of imaging the brain’s circuits,” Science 334(6056), 618–623 (2011).
[Crossref] [PubMed]

S. Witte, A. Negrean, J. C. Lodder, C. P. J. de Kock, G. Testa Silva, H. D. Mansvelder, and M. Louise Groot, “Label-free live brain imaging and targeted patching with third-harmonic generation microscopy,” Proc. Natl. Acad. Sci. U.S.A. 108(15), 5970–5975 (2011).
[Crossref] [PubMed]

M. Rehberg, F. Krombach, U. Pohl, and S. Dietzel, “Label-free 3D visualization of cellular and tissue structures in intact muscle with second and third harmonic generation microscopy,” PLoS One 6(11), e28237 (2011).
[Crossref] [PubMed]

M. J. Farrar, F. W. Wise, J. R. Fetcho, and C. B. Schaffer, “In vivo imaging of myelin in the vertebrate central nervous system using third harmonic generation microscopy,” Biophys. J. 100(5), 1362–1371 (2011).
[Crossref] [PubMed]

J. Binding, J. Ben Arous, J.-F. Léger, S. Gigan, C. Boccara, and L. Bourdieu, “Brain refractive index measured in vivo with high-NA defocus-corrected full-field OCT and consequences for two-photon microscopy,” Opt. Express 19(6), 4833–4847 (2011).
[Crossref] [PubMed]

B. Larson, S. Abeytunge, and M. Rajadhyaksha, “Performance of full-pupil line-scanning reflectance confocal microscopy in human skin and oral mucosa in vivo,” Biomed. Opt. Express 2(7), 2055–2067 (2011).
[Crossref] [PubMed]

2010 (1)

A. Scope, U. Mahmood, D. S. Gareau, M. Kenkre, J. A. Lieb, K. S. Nehal, and M. Rajadhyaksha, “In vivo reflectance confocal microscopy of shave biopsy wounds: feasibility of intraoperative mapping of cancer margins,” Br. J. Dermatol. 163(6), 1218–1228 (2010).
[Crossref] [PubMed]

2009 (4)

M. Friebel, J. Helfmann, U. Netz, and M. Meinke, “Influence of oxygen saturation on the optical scattering properties of human red blood cells in the spectral range 250 to 2,000 nm,” J. Biomed. Opt. 14(3), 034001 (2009).
[Crossref] [PubMed]

S.-Y. Chen, H.-Y. Wu, and C.-K. Sun, “In vivo harmonic generation biopsy of human skin,” J. Biomed. Opt. 14(6), 060505 (2009).
[Crossref] [PubMed]

J. Scholz, M. C. Klein, T. E. J. Behrens, and H. Johansen-Berg, “Training induces changes in white-matter architecture,” Nat. Neurosci. 12(11), 1370–1371 (2009).
[Crossref] [PubMed]

D. Kobat, M. E. Durst, N. Nishimura, A. W. Wong, C. B. Schaffer, and C. Xu, “Deep tissue multiphoton microscopy using longer wavelength excitation,” Opt. Express 17(16), 13354–13364 (2009).
[Crossref] [PubMed]

2008 (2)

P. Calzavara-Pinton, C. Longo, M. Venturini, R. Sala, and G. Pellacani, “Reflectance confocal microscopy for in vivo skin imaging,” Photochem. Photobiol. 84(6), 1421–1430 (2008).
[Crossref] [PubMed]

R. D. Fields, “White matter in learning, cognition and psychiatric disorders,” Trends Neurosci. 31(7), 361–370 (2008).
[Crossref] [PubMed]

2007 (2)

M. D. Budde, J. H. Kim, H.-F. Liang, R. E. Schmidt, J. H. Russell, A. H. Cross, and S.-K. Song, “Toward accurate diagnosis of white matter pathology using diffusion tensor imaging,” Magn. Reson. Med. 57(4), 688–695 (2007).
[Crossref] [PubMed]

M. Inagaki, E. Yoshikawa, Y. Matsuoka, Y. Sugawara, T. Nakano, T. Akechi, N. Wada, S. Imoto, K. Murakami, and Y. Uchitomi, “Smaller regional volumes of brain gray and white matter demonstrated in breast cancer survivors exposed to adjuvant chemotherapy,” Cancer 109(1), 146–156 (2007).
[Crossref] [PubMed]

2004 (2)

N. D. Prins, E. J. van Dijk, T. den Heijer, S. E. Vermeer, P. J. Koudstaal, M. Oudkerk, A. Hofman, and M. M. B. Breteler, “Cerebral white matter lesions and the risk of dementia,” Arch. Neurol. 61(10), 1531–1534 (2004).
[Crossref] [PubMed]

C. Loo, A. Lin, L. Hirsch, M.-H. Lee, J. Barton, N. Halas, J. West, and R. Drezek, “Nanoshell-enabled photonics-based imaging and therapy of cancer,” Technol. Cancer Res. Treat. 3(1), 33–40 (2004).
[Crossref] [PubMed]

2003 (1)

2002 (1)

R. M. Woodward, B. E. Cole, V. P. Wallace, R. J. Pye, D. D. Arnone, E. H. Linfield, and M. Pepper, “Terahertz pulse imaging in reflection geometry of human skin cancer and skin tissue,” Phys. Med. Biol. 47(21), 3853–3863 (2002).
[Crossref] [PubMed]

2001 (2)

M. Huzaira, F. Rius, M. Rajadhyaksha, R. R. Anderson, and S. González, “Topographic variations in normal skin, as viewed by in vivo reflectance confocal microscopy,” J. Invest. Dermatol. 116(6), 846–852 (2001).
[Crossref] [PubMed]

C. Bjartmar, R. P. Kinkel, G. Kidd, R. A. Rudick, and B. D. Trapp, “Axonal loss in normal-appearing white matter in a patient with acute MS,” Neurology 57(7), 1248–1252 (2001).
[Crossref] [PubMed]

1999 (3)

A. Roggan, M. Friebel, K. Dö Rschel, A. Hahn, and G. Mu Ller, “Optical properties of circulating human blood in the wavelength range 400-2500 nm,” J. Biomed. Opt. 4(1), 36–46 (1999).
[Crossref] [PubMed]

D. Yelin and Y. Silberberg, “Laser scanning third-harmonic-generation microscopy in biology,” Opt. Express 5(8), 169–175 (1999).
[Crossref] [PubMed]

R. C. Gur, B. I. Turetsky, M. Matsui, M. Yan, W. Bilker, P. Hughett, and R. E. Gur, “Sex differences in brain gray and white matter in healthy young adults: correlations with cognitive performance,” J. Neurosci. 19(10), 4065–4072 (1999).
[Crossref] [PubMed]

1998 (1)

1997 (1)

Y. Barad, H. Eisenberg, M. Horowitz, and Y. Silberberg, “Nonlinear scanning laser microscopy by third harmonic generation,” Appl. Phys. Lett. 70(8), 922–924 (1997).
[Crossref]

1996 (1)

1995 (1)

J. G. Fujimoto, M. E. Brezinski, G. J. Tearney, S. A. Boppart, B. Bouma, M. R. Hee, J. F. Southern, and E. A. Swanson, “Optical biopsy and imaging using optical coherence tomography,” Nat. Med. 1(9), 970–972 (1995).
[Crossref] [PubMed]

1994 (1)

1991 (1)

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 et, “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
[Crossref] [PubMed]

1990 (1)

W. Denk, J. H. Strickler, and W. W. Webb, “Two-photon laser scanning fluorescence microscopy,” Science 248(4951), 73–76 (1990).
[Crossref] [PubMed]

1969 (1)

P. Davidovits and M. D. Egger, “Scanning laser microscope,” Nature 223(5208), 831 (1969).
[Crossref] [PubMed]

Abeytunge, S.

Akechi, T.

M. Inagaki, E. Yoshikawa, Y. Matsuoka, Y. Sugawara, T. Nakano, T. Akechi, N. Wada, S. Imoto, K. Murakami, and Y. Uchitomi, “Smaller regional volumes of brain gray and white matter demonstrated in breast cancer survivors exposed to adjuvant chemotherapy,” Cancer 109(1), 146–156 (2007).
[Crossref] [PubMed]

Anderson, R. R.

M. Huzaira, F. Rius, M. Rajadhyaksha, R. R. Anderson, and S. González, “Topographic variations in normal skin, as viewed by in vivo reflectance confocal microscopy,” J. Invest. Dermatol. 116(6), 846–852 (2001).
[Crossref] [PubMed]

Arnone, D. D.

R. M. Woodward, B. E. Cole, V. P. Wallace, R. J. Pye, D. D. Arnone, E. H. Linfield, and M. Pepper, “Terahertz pulse imaging in reflection geometry of human skin cancer and skin tissue,” Phys. Med. Biol. 47(21), 3853–3863 (2002).
[Crossref] [PubMed]

Barad, Y.

Y. Barad, H. Eisenberg, M. Horowitz, and Y. Silberberg, “Nonlinear scanning laser microscopy by third harmonic generation,” Appl. Phys. Lett. 70(8), 922–924 (1997).
[Crossref]

Barton, J.

C. Loo, A. Lin, L. Hirsch, M.-H. Lee, J. Barton, N. Halas, J. West, and R. Drezek, “Nanoshell-enabled photonics-based imaging and therapy of cancer,” Technol. Cancer Res. Treat. 3(1), 33–40 (2004).
[Crossref] [PubMed]

Behrens, T. E. J.

J. Scholz, M. C. Klein, T. E. J. Behrens, and H. Johansen-Berg, “Training induces changes in white-matter architecture,” Nat. Neurosci. 12(11), 1370–1371 (2009).
[Crossref] [PubMed]

Ben Arous, J.

Bilker, W.

R. C. Gur, B. I. Turetsky, M. Matsui, M. Yan, W. Bilker, P. Hughett, and R. E. Gur, “Sex differences in brain gray and white matter in healthy young adults: correlations with cognitive performance,” J. Neurosci. 19(10), 4065–4072 (1999).
[Crossref] [PubMed]

Binding, J.

Bjartmar, C.

C. Bjartmar, R. P. Kinkel, G. Kidd, R. A. Rudick, and B. D. Trapp, “Axonal loss in normal-appearing white matter in a patient with acute MS,” Neurology 57(7), 1248–1252 (2001).
[Crossref] [PubMed]

Boccara, C.

Boppart, S. A.

J. G. Fujimoto, M. E. Brezinski, G. J. Tearney, S. A. Boppart, B. Bouma, M. R. Hee, J. F. Southern, and E. A. Swanson, “Optical biopsy and imaging using optical coherence tomography,” Nat. Med. 1(9), 970–972 (1995).
[Crossref] [PubMed]

Borelli, P.

E. Cinotti, L. Gergelé, J. L. Perrot, A. Dominé, B. Labeille, P. Borelli, and F. Cambazard, “Quantification of capillary blood cell flow using reflectance confocal microscopy,” Skin Res. Technol. 20(3), 373–378 (2014).
[Crossref] [PubMed]

Bouma, B.

J. G. Fujimoto, M. E. Brezinski, G. J. Tearney, S. A. Boppart, B. Bouma, M. R. Hee, J. F. Southern, and E. A. Swanson, “Optical biopsy and imaging using optical coherence tomography,” Nat. Med. 1(9), 970–972 (1995).
[Crossref] [PubMed]

Bourdieu, L.

Brakenhoff, G.

Breteler, M. M. B.

N. D. Prins, E. J. van Dijk, T. den Heijer, S. E. Vermeer, P. J. Koudstaal, M. Oudkerk, A. Hofman, and M. M. B. Breteler, “Cerebral white matter lesions and the risk of dementia,” Arch. Neurol. 61(10), 1531–1534 (2004).
[Crossref] [PubMed]

Brezinski, M. E.

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A. Roggan, M. Friebel, K. Dö Rschel, A. Hahn, and G. Mu Ller, “Optical properties of circulating human blood in the wavelength range 400-2500 nm,” J. Biomed. Opt. 4(1), 36–46 (1999).
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E. Cinotti, L. Gergelé, J. L. Perrot, A. Dominé, B. Labeille, P. Borelli, and F. Cambazard, “Quantification of capillary blood cell flow using reflectance confocal microscopy,” Skin Res. Technol. 20(3), 373–378 (2014).
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C. Loo, A. Lin, L. Hirsch, M.-H. Lee, J. Barton, N. Halas, J. West, and R. Drezek, “Nanoshell-enabled photonics-based imaging and therapy of cancer,” Technol. Cancer Res. Treat. 3(1), 33–40 (2004).
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Durst, M. E.

Egger, M. D.

P. Davidovits and M. D. Egger, “Scanning laser microscope,” Nature 223(5208), 831 (1969).
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Y. Barad, H. Eisenberg, M. Horowitz, and Y. Silberberg, “Nonlinear scanning laser microscopy by third harmonic generation,” Appl. Phys. Lett. 70(8), 922–924 (1997).
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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 et, “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
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M. J. Farrar, F. W. Wise, J. R. Fetcho, and C. B. Schaffer, “In vivo imaging of myelin in the vertebrate central nervous system using third harmonic generation microscopy,” Biophys. J. 100(5), 1362–1371 (2011).
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M. J. Farrar, F. W. Wise, J. R. Fetcho, and C. B. Schaffer, “In vivo imaging of myelin in the vertebrate central nervous system using third harmonic generation microscopy,” Biophys. J. 100(5), 1362–1371 (2011).
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M. Friebel, J. Helfmann, U. Netz, and M. Meinke, “Influence of oxygen saturation on the optical scattering properties of human red blood cells in the spectral range 250 to 2,000 nm,” J. Biomed. Opt. 14(3), 034001 (2009).
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J. G. Fujimoto, M. E. Brezinski, G. J. Tearney, S. A. Boppart, B. Bouma, M. R. Hee, J. F. Southern, and E. A. Swanson, “Optical biopsy and imaging using optical coherence tomography,” Nat. Med. 1(9), 970–972 (1995).
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A. Scope, U. Mahmood, D. S. Gareau, M. Kenkre, J. A. Lieb, K. S. Nehal, and M. Rajadhyaksha, “In vivo reflectance confocal microscopy of shave biopsy wounds: feasibility of intraoperative mapping of cancer margins,” Br. J. Dermatol. 163(6), 1218–1228 (2010).
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E. Cinotti, L. Gergelé, J. L. Perrot, A. Dominé, B. Labeille, P. Borelli, and F. Cambazard, “Quantification of capillary blood cell flow using reflectance confocal microscopy,” Skin Res. Technol. 20(3), 373–378 (2014).
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González, S.

M. Huzaira, F. Rius, M. Rajadhyaksha, R. R. Anderson, and S. González, “Topographic variations in normal skin, as viewed by in vivo reflectance confocal microscopy,” J. Invest. Dermatol. 116(6), 846–852 (2001).
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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 et, “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
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A. J. Schain, R. A. Hill, and J. Grutzendler, “Label-free in vivo imaging of myelinated axons in health and disease with spectral confocal reflectance microscopy,” Nat. Med. 20(4), 443–449 (2014).
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R. C. Gur, B. I. Turetsky, M. Matsui, M. Yan, W. Bilker, P. Hughett, and R. E. Gur, “Sex differences in brain gray and white matter in healthy young adults: correlations with cognitive performance,” J. Neurosci. 19(10), 4065–4072 (1999).
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Gur, R. E.

R. C. Gur, B. I. Turetsky, M. Matsui, M. Yan, W. Bilker, P. Hughett, and R. E. Gur, “Sex differences in brain gray and white matter in healthy young adults: correlations with cognitive performance,” J. Neurosci. 19(10), 4065–4072 (1999).
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A. Roggan, M. Friebel, K. Dö Rschel, A. Hahn, and G. Mu Ller, “Optical properties of circulating human blood in the wavelength range 400-2500 nm,” J. Biomed. Opt. 4(1), 36–46 (1999).
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C. Loo, A. Lin, L. Hirsch, M.-H. Lee, J. Barton, N. Halas, J. West, and R. Drezek, “Nanoshell-enabled photonics-based imaging and therapy of cancer,” Technol. Cancer Res. Treat. 3(1), 33–40 (2004).
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J. G. Fujimoto, M. E. Brezinski, G. J. Tearney, S. A. Boppart, B. Bouma, M. R. Hee, J. F. Southern, and E. A. Swanson, “Optical biopsy and imaging using optical coherence tomography,” Nat. Med. 1(9), 970–972 (1995).
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J. A. Izatt, M. R. Hee, G. M. Owen, E. A. Swanson, and J. G. Fujimoto, “Optical coherence microscopy in scattering media,” Opt. Lett. 19(8), 590–592 (1994).
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M. Friebel, J. Helfmann, U. Netz, and M. Meinke, “Influence of oxygen saturation on the optical scattering properties of human red blood cells in the spectral range 250 to 2,000 nm,” J. Biomed. Opt. 14(3), 034001 (2009).
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A. J. Schain, R. A. Hill, and J. Grutzendler, “Label-free in vivo imaging of myelinated axons in health and disease with spectral confocal reflectance microscopy,” Nat. Med. 20(4), 443–449 (2014).
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C. Loo, A. Lin, L. Hirsch, M.-H. Lee, J. Barton, N. Halas, J. West, and R. Drezek, “Nanoshell-enabled photonics-based imaging and therapy of cancer,” Technol. Cancer Res. Treat. 3(1), 33–40 (2004).
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N. D. Prins, E. J. van Dijk, T. den Heijer, S. E. Vermeer, P. J. Koudstaal, M. Oudkerk, A. Hofman, and M. M. B. Breteler, “Cerebral white matter lesions and the risk of dementia,” Arch. Neurol. 61(10), 1531–1534 (2004).
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Y. Barad, H. Eisenberg, M. Horowitz, and Y. Silberberg, “Nonlinear scanning laser microscopy by third harmonic generation,” Appl. Phys. Lett. 70(8), 922–924 (1997).
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D. G. Ouzounov, T. Wang, M. Wang, D. D. Feng, N. G. Horton, J. C. Cruz-Hernández, Y. T. Cheng, J. Reimer, A. S. Tolias, N. Nishimura, and C. Xu, “In vivo three-photon imaging of activity of GCaMP6-labeled neurons deep in intact mouse brain,” Nat. Methods 14(4), 388–390 (2017).
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N. G. Horton, K. Wang, D. Kobat, C. G. Clark, F. W. Wise, C. B. Schaffer, and C. Xu, “In vivo three-photon microscopy of subcortical structures within an intact mouse brain,” Nat. Photonics 7(3), 205–209 (2013).
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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 et, “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
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Hughett, P.

R. C. Gur, B. I. Turetsky, M. Matsui, M. Yan, W. Bilker, P. Hughett, and R. E. Gur, “Sex differences in brain gray and white matter in healthy young adults: correlations with cognitive performance,” J. Neurosci. 19(10), 4065–4072 (1999).
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M. Huzaira, F. Rius, M. Rajadhyaksha, R. R. Anderson, and S. González, “Topographic variations in normal skin, as viewed by in vivo reflectance confocal microscopy,” J. Invest. Dermatol. 116(6), 846–852 (2001).
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James, O.

J. Kwon, M. Kim, H. Park, B. M. Kang, Y. Jo, J. H. Kim, O. James, S. H. Yun, S. G. Kim, M. Suh, and M. Choi, “Label-free nanoscale optical metrology on myelinated axons in vivo,” Nat. Commun. 8(1), 1832 (2017).
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J. Kwon, M. Kim, H. Park, B. M. Kang, Y. Jo, J. H. Kim, O. James, S. H. Yun, S. G. Kim, M. Suh, and M. Choi, “Label-free nanoscale optical metrology on myelinated axons in vivo,” Nat. Commun. 8(1), 1832 (2017).
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J. Scholz, M. C. Klein, T. E. J. Behrens, and H. Johansen-Berg, “Training induces changes in white-matter architecture,” Nat. Neurosci. 12(11), 1370–1371 (2009).
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J. Kwon, M. Kim, H. Park, B. M. Kang, Y. Jo, J. H. Kim, O. James, S. H. Yun, S. G. Kim, M. Suh, and M. Choi, “Label-free nanoscale optical metrology on myelinated axons in vivo,” Nat. Commun. 8(1), 1832 (2017).
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M. Yamanaka, T. Teranishi, H. Kawagoe, and N. Nishizawa, “Optical coherence microscopy in 1700 nm spectral band for high-resolution label-free deep-tissue imaging,” Sci. Rep. 6(1), 31715 (2016).
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A. Scope, U. Mahmood, D. S. Gareau, M. Kenkre, J. A. Lieb, K. S. Nehal, and M. Rajadhyaksha, “In vivo reflectance confocal microscopy of shave biopsy wounds: feasibility of intraoperative mapping of cancer margins,” Br. J. Dermatol. 163(6), 1218–1228 (2010).
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C. Bjartmar, R. P. Kinkel, G. Kidd, R. A. Rudick, and B. D. Trapp, “Axonal loss in normal-appearing white matter in a patient with acute MS,” Neurology 57(7), 1248–1252 (2001).
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J. Kwon, M. Kim, H. Park, B. M. Kang, Y. Jo, J. H. Kim, O. James, S. H. Yun, S. G. Kim, M. Suh, and M. Choi, “Label-free nanoscale optical metrology on myelinated axons in vivo,” Nat. Commun. 8(1), 1832 (2017).
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M. D. Budde, J. H. Kim, H.-F. Liang, R. E. Schmidt, J. H. Russell, A. H. Cross, and S.-K. Song, “Toward accurate diagnosis of white matter pathology using diffusion tensor imaging,” Magn. Reson. Med. 57(4), 688–695 (2007).
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Kim, M.

J. Kwon, M. Kim, H. Park, B. M. Kang, Y. Jo, J. H. Kim, O. James, S. H. Yun, S. G. Kim, M. Suh, and M. Choi, “Label-free nanoscale optical metrology on myelinated axons in vivo,” Nat. Commun. 8(1), 1832 (2017).
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Kim, S. G.

J. Kwon, M. Kim, H. Park, B. M. Kang, Y. Jo, J. H. Kim, O. James, S. H. Yun, S. G. Kim, M. Suh, and M. Choi, “Label-free nanoscale optical metrology on myelinated axons in vivo,” Nat. Commun. 8(1), 1832 (2017).
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C. Bjartmar, R. P. Kinkel, G. Kidd, R. A. Rudick, and B. D. Trapp, “Axonal loss in normal-appearing white matter in a patient with acute MS,” Neurology 57(7), 1248–1252 (2001).
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J. Scholz, M. C. Klein, T. E. J. Behrens, and H. Johansen-Berg, “Training induces changes in white-matter architecture,” Nat. Neurosci. 12(11), 1370–1371 (2009).
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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, “In vivo three-photon microscopy of subcortical structures within an intact mouse brain,” Nat. Photonics 7(3), 205–209 (2013).
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D. Kobat, M. E. Durst, N. Nishimura, A. W. Wong, C. B. Schaffer, and C. Xu, “Deep tissue multiphoton microscopy using longer wavelength excitation,” Opt. Express 17(16), 13354–13364 (2009).
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N. D. Prins, E. J. van Dijk, T. den Heijer, S. E. Vermeer, P. J. Koudstaal, M. Oudkerk, A. Hofman, and M. M. B. Breteler, “Cerebral white matter lesions and the risk of dementia,” Arch. Neurol. 61(10), 1531–1534 (2004).
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Krombach, F.

M. Rehberg, F. Krombach, U. Pohl, and S. Dietzel, “Label-free 3D visualization of cellular and tissue structures in intact muscle with second and third harmonic generation microscopy,” PLoS One 6(11), e28237 (2011).
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Krubitzer, L.

Kwon, J.

J. Kwon, M. Kim, H. Park, B. M. Kang, Y. Jo, J. H. Kim, O. James, S. H. Yun, S. G. Kim, M. Suh, and M. Choi, “Label-free nanoscale optical metrology on myelinated axons in vivo,” Nat. Commun. 8(1), 1832 (2017).
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Labeille, B.

E. Cinotti, L. Gergelé, J. L. Perrot, A. Dominé, B. Labeille, P. Borelli, and F. Cambazard, “Quantification of capillary blood cell flow using reflectance confocal microscopy,” Skin Res. Technol. 20(3), 373–378 (2014).
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Larson, B.

Lee, M.-H.

C. Loo, A. Lin, L. Hirsch, M.-H. Lee, J. Barton, N. Halas, J. West, and R. Drezek, “Nanoshell-enabled photonics-based imaging and therapy of cancer,” Technol. Cancer Res. Treat. 3(1), 33–40 (2004).
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Lee, S. J.

Léger, J.-F.

Li, B.

Liang, H.-F.

M. D. Budde, J. H. Kim, H.-F. Liang, R. E. Schmidt, J. H. Russell, A. H. Cross, and S.-K. Song, “Toward accurate diagnosis of white matter pathology using diffusion tensor imaging,” Magn. Reson. Med. 57(4), 688–695 (2007).
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Lichtman, J. W.

J. W. Lichtman and W. Denk, “The big and the small: challenges of imaging the brain’s circuits,” Science 334(6056), 618–623 (2011).
[Crossref] [PubMed]

Lieb, J. A.

A. Scope, U. Mahmood, D. S. Gareau, M. Kenkre, J. A. Lieb, K. S. Nehal, and M. Rajadhyaksha, “In vivo reflectance confocal microscopy of shave biopsy wounds: feasibility of intraoperative mapping of cancer margins,” Br. J. Dermatol. 163(6), 1218–1228 (2010).
[Crossref] [PubMed]

Lin, A.

C. Loo, A. Lin, L. Hirsch, M.-H. Lee, J. Barton, N. Halas, J. West, and R. Drezek, “Nanoshell-enabled photonics-based imaging and therapy of cancer,” Technol. Cancer Res. Treat. 3(1), 33–40 (2004).
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Lin, B.-L.

Lin, C. P.

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 et, “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
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Linfield, E. H.

R. M. Woodward, B. E. Cole, V. P. Wallace, R. J. Pye, D. D. Arnone, E. H. Linfield, and M. Pepper, “Terahertz pulse imaging in reflection geometry of human skin cancer and skin tissue,” Phys. Med. Biol. 47(21), 3853–3863 (2002).
[Crossref] [PubMed]

Lodder, J. C.

S. Witte, A. Negrean, J. C. Lodder, C. P. J. de Kock, G. Testa Silva, H. D. Mansvelder, and M. Louise Groot, “Label-free live brain imaging and targeted patching with third-harmonic generation microscopy,” Proc. Natl. Acad. Sci. U.S.A. 108(15), 5970–5975 (2011).
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Supplementary Material (1)

NameDescription
» Visualization 1       Stack of confocal images of adult mouse brain from 0 to 1.3 mm. The number on the left top indicates the imaging depth (unit: µm). Video is set to 10 frames/second.

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Figures (5)

Fig. 1
Fig. 1 (a) Schematic illustration of the imaging system. BE: beam expander, PBS: polarizing beam splitter, λ/2: half-waveplate, λ/4: quarter-waveplate, MMF: multimode fiber, DM: dichroic mirror. The focal length for the scan lens and tube lens is 150 mm and 750 mm, respectively. The photocathodes for PMT1 and PMT2 are, respectively, InGaAs and ultra bialkali. An InGaAs photodiode (PD) is also used for some of the experiments. Schematic illustrations of the imaging sites. Left side: surgery/imaging site for Figs. 1-3 and 5; right side: surgery/imaging site of the cerebellum of the mouse brain for Fig. 4. (b) Lateral and axial intensity profiles of axons at 400 μm depth (along the yellow line in the image on the left). The FWHMs are indicated in the plots. Scale bar: 10 μm. (c) mouse brain image obtained when mounted with common coverslip glass window. Scale bar: 30 μm. (d) mouse brain image obtained when mounted with quarter-waveplate window. Scale bar: 30 μm.
Fig. 2
Fig. 2 Comparison of reflectance confocal and THG images through the mouse visual cortex. (a) Reflectance confocal (top, cyan), THG (middle, yellow) and merged reflectance confocal and THG images (bottom) at various depths: 140 μm, 235 μm, 360 μm, 450 μm, 641 μm, 774 μm and 804 μm. Myelinated axons are indicated with white arrows; blood vessels are indicated with red arrows. Scale bars are 30 μm. (b) Enlarged images at depth 450 μm and 641 μm from (a) are shown, where blood vessels are indicated in red and myelinated axons are indicated in white. Scale bars are 30 μm.
Fig. 3
Fig. 3 Comparison of LM-RCM (top, cyan) and THG images (middle, yellow) at different depths in mouse cerebellum: 50 μm, 150 μm, 300 μm, 450 μm, 600 μm and 800 μm. Myelinated axons are indicated with white arrows. Scale bar: 30 μm.
Fig. 4
Fig. 4 (a) In vivo reflectance confocal images at various depths through the mouse visual cortex. Scale bar 30 μm. (b) Semi-logarithmic plot of reflectance confocal signal (normalized to the signal at the surface and to the optical power) as a function of imaging depth. (c) Images at 770 μm obtained by CW lasers at 1630 nm (left) and 1060 nm (right). Scale bar 30 μm.
Fig. 5
Fig. 5 (a) White matter image at ~700 μm depth acquired with different combination of detectors and laser sources through the mouse visual cortex. CW + PD: CW laser illumination at 1630 nm with InGaAs PD as detector; CW + PMT: CW laser illumination at 1630 nm with InGaAs PMT as detector; Pulsed + PD: pulsed laser illumination at 1650 nm with InGaAs PD as detector. (b) In vivo mouse white matter image at depth of 700 μm obtained using 8 kHz resonant scanner (RESSCAN-GEN, Cambridge Inc.) at frame rate of 30 Hz, scale bar: 30 μm. (c) Confocal images of white matter under CW and pulsed laser illumination with the same power at 1310 nm, 1610 nm, 1630 nm, and 1650 nm at ~800 μm. The scale bars are 30 μm.

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