Abstract

Among the multitude of optical polarization contrasts that can be observed in complex biological specimens, linear diattenuation (LD) imaging has received little attention. It is indeed challenging to image LD with basic polarizing microscopes because it is often relatively small in comparison with linear retardance (LR). In addition, interpretation of LD images is not straightforward when experiments are conducted in the visible range because LD can be produced by both dichroism and anisotropic scattering. Mueller polarimetry is a powerful implementation of polarization sensing able to differentiate and measure the anisotropies of specimens. In this article, near infrared transmission Mueller scanning microscopy is used to image LD in thin biological specimen sections made of various proteins with unprecedented resolution and sensitivity. The near infrared spectral range makes it possible to lower the contribution of dichroism to the total linear diattenuation in order to highlight anisotropic scattering. Pixel-by-pixel comparison of LD images with LR and multiphoton images demonstrates that LD is produced by under-resolved structures that are not revealed by other means, notably within the sarcomere of skeletal muscles. LD microscopy appears as a powerful tool to provide new insights into the macro-molecular organization of biological specimens at the sub-microscopic scale without labelling.

© 2020 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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2020 (2)

R. Marongiu, A. Le Gratiet, L. Pesce, P. Bianchini, and A. Diaspro, “ExCIDS: a combined approach coupling Expansion Microscopy (ExM) and Circular Intensity Differential Scattering (CIDS) for chromatin-DNA imaging,” OSA Continuum 3(7), 1770–1780 (2020).
[Crossref]

P. Li, H. R. Lee, S. Chandel, C. Lotz, F. K. Groeber-Becker, S. Dembski, R. Ossikovski, H. Ma, and T. Novikova, “Analysis of tissue microstructure with Mueller microscopy: logarithmic decomposition and Monte Carlo modeling,” J. Biomed. Opt. 25(1), 1 (2020).
[Crossref]

2019 (6)

S. Karpf and B. Jalali, “Frequency-doubled FDML-MOPA laser in the visible,” Opt. Lett. 44(24), 5913–5916 (2019).
[Crossref]

A. Sharma, A. Campbell, J. Leoni, Y. T. Cheng, M. Müllner, and G. Lakhwan, “Circular Intensity Differential Scattering Reveals the Internal Structure of Polymer Fibrils,” J. Phys. Chem. Lett. 10(24), 7547–7553 (2019).
[Crossref]

H. He, R. Liao, N. Zeng, P. Li, Z. Chen, X. Liu, and H. Ma, “Mueller Matrix Polarimetry—An Emerging New Tool for Characterizing the Microstructural Feature of Complex Biological Specimen,” J. Lightwave Technol. 37(11), 2534–2548 (2019).
[Crossref]

A. Le Gratiet, M. d’Amora, M. Duocastella, R. Marongiu, A. Bendandi, S. Giordani, P. Bianchini, and A. Diaspro, “Zebrafish structural development in Mueller-matrix scanning microscopy,” Sci. Rep. 9(1), 19974 (2019).
[Crossref]

M. Menzel, M. Axer, K. Amunts, H. De Raedt, and K. Michielsen, “Diattenuation Imaging reveals different brain tissue properties,” Sci. Rep. 9(1), 1939 (2019).
[Crossref]

S. Rivet, M. Dubreuil, A. Bradu, and Y. Le Grand, “Fast spectrally encoded Mueller optical scanning microscopy,” Sci. Rep. 9(1), 3972 (2019).
[Crossref]

2018 (3)

2017 (5)

2016 (4)

A. Le Gratiet, M. Dubreuil, S. Rivet, and Y. Le Grand, “Scanning Mueller polarimetric microscopy,” Opt. Lett. 41(18), 4336–4339 (2016).
[Crossref]

V. V. Tuchin, “Polarized light interaction with tissues,” J. Biomed. Opt. 21(7), 071114 (2016).
[Crossref]

A. Rodger, G. Dorrington, and D. L. Ang, “Linear dichroism as a probe of molecular structure and interactions,” Analyst 141(24), 6490–6498 (2016).
[Crossref]

F. Tissier, Y. Mallem, C. Goanvec, R. Didier, T. Aubry, N. Bourgeois, J.-C. Desfontis, M. Dubreuil, Y. Le Grand, J. Mansourati, K. Pichavant-Rafini, E. Plee-Gautier, P. Roquefort, M. Theron, and M. Gilard, “A non-hypocholesterolemic atorvastatin treatment improves vessel elasticity by acting on elastin composition in WHHL rabbits,” Atherosclerosis 251, 70–77 (2016).
[Crossref]

2015 (4)

A. Le Gratiet, S. Rivet, M. Dubreuil, and Y. Le Grand, “100kHz-Mueller polarimeter in reflection configuration,” Opt. Lett. 40(4), 645–648 (2015).
[Crossref]

B. de Campos Vidal, E. H. Dos Anjos, and M. L. Mello, “Optical anisotropy reveals molecular order in a mouse enthesis,” Cell Tissue Res. 362(1), 177–185 (2015).
[Crossref]

K. A. Min, W. G. Rajeswaran, R. Oldenbourg, G. Harris, R. K. Keswani, M. Chiang, P. Rzeczycki, A. Talattof, M. Hafeez, R. W. Horobin, S. D. Larsen, K. A. Stringer, and G. R. Rosania, “Massive Bioaccumulation and Self-Assembly of Phenazine Compounds in Live Cells,” Adv. Sci. 2(8), 1500025 (2015).
[Crossref]

S. Alali and A. Vitkin, “Polarized light imaging in biomedicine: emerging Mueller matrix methodologies for bulk tissue assessment,” J. Biomed. Opt. 20(6), 061104 (2015).
[Crossref]

2014 (3)

2013 (3)

S. L. Jacques, “Optical properties of biological tissues: a review,” Phys. Med. Biol. 58(11), R37–R61 (2013).
[Crossref]

M. Mesradi, A. Genoux, V. Cuplov, D. Abi-Haidar, S. Jan, I. Buvat, and F. Pain, “Experimental and analytical comparative study of optical coefficient of fresh and frozen rat tissues,” J. Biomed. Opt. 18(11), 117010 (2013).
[Crossref]

S. B. Mehta, M. Shribak, and R. Oldenburg, “Polarized light imaging of birefringence and diattenuation at high resolution and high sensitivity,” J. Opt. 15(9), 094007 (2013).
[Crossref]

2012 (1)

T. J. Allen, P. C. Beard, A. Hall, A. P. Dhillon, and J. S. Owen, “Spectroscopic photoacoustic imaging of lipid-rich plaques in the human aorta in the 740 to 1400 nm wavelength range,” J. Biomed. Opt. 17(6), 061209 (2012).
[Crossref]

2011 (3)

P. G. Ellingsen, M. B. Lilledahl, L. M. S. Aas, C. de Lange Davies, and M. Kildemo, “Quantitative characterization of articular cartilage using Mueller matrix imaging and multiphoton microscopy,” J. Biomed. Opt. 16(11), 116002 (2011).
[Crossref]

N. Gosh and I. A. Vitkin, “Tissue polarimetry: concepts, challenges, applications, and outlook,” J. Biomed. Opt. 16(11), 110801 (2011).
[Crossref]

M. Axer, K. Amunts, D. Grässel, C. Palm, J. Dammers, H. Axer, U. Pietrzyk, and K. Zilles, “A novel approach to the human connectome: Ultra-high resolution mapping of fiber tracts in the brain,” NeuroImage 54(2), 1091–1101 (2011).
[Crossref]

2010 (2)

M. F. G. Wood, N. Ghosh, M. A. Wallenburg, S.-H. Li, R. D. Weisel, B. C. Wilson, R.-K. Li, and I. A. Vitkin, “Polarization birefringence measurements for characterizing the myocardium, including healthy, infarcted, and stem-cell-regenerated tissues,” J. Biomed. Opt. 15(4), 047009 (2010).
[Crossref]

H. He, N. Zeng, R. Liao, T. Yun, W. Li, Y. He, and H. Ma, “Application of sphere-cylinder scattering model to skeletal muscle,” Opt. Express 18(14), 15104–15112 (2010).
[Crossref]

2009 (1)

B. Ranjbar and P. Gill, “Circular dichroism techniques: biomolecular and nanostructural analyses- a review,” Chem. Biol. Drug Des. 74(2), 101–120 (2009).
[Crossref]

2008 (2)

C. Odin, Y. Le Grand, A. Renault, L. Gailhouste, and G. Baffet, “Orientation fields of nonlinear biological fibrils by second harmonic generation microscopy,” J. Microsc. 229(1), 32–38 (2008).
[Crossref]

C. Odin, T. Guilbert, A. Alkilani, O. P. Boryskina, V. Fleury, and Y. Le Grand, “Collagen and myosin characterization by orientation field second harmonic microscopy,” Opt. Express 16(20), 16151–16165 (2008).
[Crossref]

2007 (2)

B. M. Bulheller, A. Rodger, and J. D. Hirst, “Circular and linear dichroism of proteins,” Phys. Chem. Chem. Phys. 9(17), 2020–2035 (2007).
[Crossref]

M. Dubreuil, S. Rivet, B. Le Jeune, and J. Cariou, “Snapshot Mueller matrix polarimeter by wavelength polarization coding,” Opt. Express 15(21), 13660–13668 (2007).
[Crossref]

2006 (2)

T. Boulesteix, A.-M. Pena, N. Pagès, G. Godeau, M.-P. Sauviat, E. Beaurepaire, and M.-C. Schanne-Klein, “Micrometer scale ex vivo multiphoton imaging of unstained arterial wall structure,” Cytometry, Part A 69A(1), 20–26 (2006).
[Crossref]

J. Xia, A. Weaver, D. E. Gerrard, and G. Yao, “Monitoring sarcomere structure changes in whole muscle using diffuse light reflectance,” J. Biomed. Opt. 11(4), 040504 (2006).
[Crossref]

2005 (1)

2004 (1)

2003 (3)

L.-W. Jin, K. A. Claborn, M. Kurimoto, M. A. Geday, I. Maezawa, F. Sohraby, M. Estrada, W. Kaminksy, and B. Kahr, “Imaging linear birefringence and dichroism in cerebral amyloid pathologies,” Proc. Natl. Acad. Sci. U. S. A. 100(26), 15294–15298 (2003).
[Crossref]

M. Shribak and R. Oldenburg, “Techniques for fast and sensitive measurements of two-dimensional birefringence distributions,” Appl. Opt. 42(16), 3009–3017 (2003).
[Crossref]

W. R. Zipfel, R. M. Williams, and W. W. Webb, “Nonlinear magic: multiphoton microscopy in the biosciences,” Nat. Biotechnol. 21(11), 1369–1377 (2003).
[Crossref]

1996 (2)

1993 (1)

M. Irving, “Birefringence changes associated with isometric contraction and rapid shortening steps in frog skeletal muscle fibers,” J. Physiol. 472(1), 127–156 (1993).
[Crossref]

1990 (1)

W. F. Cheong, S. A. Prahl, and A. J. Welch, “A review of the optical properties of biological tissues,” IEEE J. Quantum Electron. 26(12), 2166–2185 (1990).
[Crossref]

1989 (1)

R. C. Haskell, F. D. Carlson, and P. S. Blank, “Form birefringence of muscle,” Biophys. J. 56(2), 401–413 (1989).
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1987 (1)

A. Diaspro and C. A. Nicolini, “Circular intensity differential scattering and chromatin-DNA structure,” Cell Biophys. 10(1), 45–60 (1987).
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1983 (1)

C. Bustamante, I. Tinoco, and M. F. Maestre, “Circular differential scattering can be an important part of the circular dichroism of macromolecules,” Proc. Natl. Acad. Sci. U. S. A. 80(12), 3568–3572 (1983).
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1980 (1)

C. Bustamante, M. F. Maestre, and I. Tinoco, “Circular intensity differential scattering of light by helical structures. I. Theory,” J. Chem. Phys. 73(9), 4273–4281 (1980).
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Supplementary Material (1)

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Figures (3)

Fig. 1.
Fig. 1. Multimodal microscope composed of one Mueller matrix and two multiphoton imaging modalities. M: flip mirror. GS: galvo scanners. MO: microscope objective. Mueller matrix imaging modality: PSG (Polarization State Generator), PSA (Polarization State Analyzer), APD (Avalanche Photo Diode). Multiphoton imaging modality: PMT (Photo Multiplier Tube), IF (Interferential Filter), D (Dichroic mirror).
Fig. 2.
Fig. 2. Multimodal imaging of a rabbit aortic wall cross section (thickness 5 µm). (a) Multiphoton images including TPEF, SHG, merged TPEF/SHG and P-SHG. The P-SHG image displays the orientation of collagen fibers. (b) Mueller images (5 times averaging), including LR and LD images, encoded in the HSV colormap described in Methods. The V channel range corresponds to a magnitude of LR and LD respectively between 0° and 10°, and 0 and 0.03. (c) SHG and TPEF intensity profiles along the red line displayed in the LR image. (d) LR and LD magnitudes profiles along the red line displayed in the LR image. The dotted black lines delimit the outer region of the aorta that contains type I-collagen.
Fig. 3.
Fig. 3. Multimodal imaging of a rat striated muscle fiber longitudinal section (thickness 10 µm). (a) Schematic representation of the sarcomere of a myofibril. (b) Multiphoton images including TPEF, SHG, merged TPEF/SHG and P-SHG. The P-SHG image displays the orientation of myosin filaments. (c) Mueller matrix images (5 times averaging), including LR and LD images, encoded in the HSV colormap described in Methods. The V channel range corresponds to a magnitude of LR (respectively LD) between 0° and 15° (respectively between 0 and 0.03). (d) SHG and TPEF intensity profiles (e) LD and LR magnitude profiles. The color of the line represents the orientation of LD/LR, according to the same colormap as the one used for the images. The profiles were obtained by first binning the values within the red dotted rectangle along the transverse direction of the myofibril, and then plotting these values versus the longitudinal direction. Two vertical dashed lines were superimposed to the profiles in order to locate the center of the A band and the I band.

Equations (6)

Equations on this page are rendered with MathJax. Learn more.

LR = R H 2 + R 45 2 , φ R = arctan ( R 45 R H )
LD = D H 2 + D 45 2 , φ D = arctan ( D 45 D H )
R = | δ q δ r |
D = T q T r T q + T r
D = T q T r 2 T u
D max = 1 T u T u 1 T u

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