Abstract

Multiphoton microscopy (MPM) plays important role in biological imaging for its low scattering nature, yet it typically requires high illumination intensity. Although time-stretch of the ultrashort pulse can achieve ultrahigh speed scanning and deep penetration, the near-infrared illumination yields a compromised resolution because of its long wavelength. Here, by combining structured illumination with up-conversion materials, a multiphoton up-conversion time-encoded structured illumination microscopy (MUTE-SIM) with the scanning rate of 50 MHz is developed, which overcomes the limitation on the resolution. The resolution limit of near-infrared light is surpassed by a factor of 223.3% with low illumination intensity. This imaging strategy provides an ultrafast, low intensity, super-resolution MPM approach imaging, which has great potential in deep-tissue with high spatial resolution.

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

Full Article  |  PDF Article
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2018 (6)

J. Liang, L. Zhu, and L. V. Wang, “Single-shot real-time femtosecond imaging of temporal focusing,” Light: Sci. Appl. 7(1), 42 (2018).
[Crossref]

D. Jin, P. Xi, B. Wang, L. Zhang, J. Enderlein, and A. M. van Oijen, “Nanoparticles for super-resolution microscopy and single-molecule tracking,” Nat. Methods 15(6), 415–423 (2018).
[Crossref]

C. Chen, F. Wang, S. Wen, Q. P. Su, M. C. L. Wu, Y. Liu, B. Wang, D. Li, X. Shan, M. Kianinia, I. Aharonovich, M. Toth, S. P. Jackson, P. Xi, and D. Jin, “Multi-photon near-infrared emission saturation nanoscopy using upconversion nanoparticles,” Nat. Commun. 9(1), 3290 (2018).
[Crossref]

X. Huang, J. Fan, L. Li, H. Liu, R. Wu, Y. Wu, L. Wei, H. Mao, A. Lal, P. Xi, L. Tang, Y. Zhang, Y. Liu, S. Tan, and L. Chen, “Fast, long-term, super-resolution imaging with hessian structured illumination microscopy,” Nat. Biotechnol. 36(5), 451–459 (2018).
[Crossref]

H. Chen, X. Wu, Y. Zhang, Y. Yang, C. Min, S. Zhu, X. Yuan, Q. Bao, and J. Bu, “Wide-field in situ multiplexed raman imaging with superresolution,” Photonics Res. 6(6), 530–534 (2018).
[Crossref]

A. Lal, C. Shan, K. Zhao, W. Liu, X. Huang, W. Zong, L. Chen, and P. Xi, “A frequency domain sim reconstruction algorithm using reduced number of images,” IEEE Trans. on Image Process. 27(9), 4555–4570 (2018).
[Crossref]

2017 (6)

J. Demmerle, C. Innocent, A. J. North, G. Ball, M. Müller, E. Miron, A. Matsuda, I. M. Dobbie, Y. Markaki, and L. Schermelleh, “Strategic and practical guidelines for successful structured illumination microscopy,” Nat. Protoc. 12(5), 988–1010 (2017).
[Crossref]

Z. Li, J. Hou, J. Suo, C. Qiao, L. Kong, and Q. Dai, “Contrast and resolution enhanced optical sectioning in scattering tissue using line-scanning two-photon structured illumination microscopy,” Opt. Express 25(25), 32010–32020 (2017).
[Crossref]

Q. Li, M. Reinig, D. Kamiyama, B. Huang, X. Tao, A. Bardales, and J. Kubby, “Woofer–tweeter adaptive optical structured illumination microscopy,” Photonics Res. 5(4), 329–334 (2017).
[Crossref]

W. Yan, Y. Yang, Y. Tan, X. Chen, Y. Li, J. Qu, and T. Ye, “Coherent optical adaptive technique improves the spatial resolution of sted microscopy in thick samples,” Photonics Res. 5(3), 176–181 (2017).
[Crossref]

Q. Wu, B. Huang, X. Peng, S. He, and Q. Zhan, “Non-bleaching fluorescence emission difference microscopy using single 808-nm laser excited red upconversion emission,” Opt. Express 25(25), 30885–30894 (2017).
[Crossref]

K.-J. Hsu, K.-Y. Li, Y.-Y. Lin, A.-S. Chiang, and S.-W. Chu, “Optimizing depth-of-field extension in optical sectioning microscopy techniques using a fast focus-tunable lens,” Opt. Express 25(14), 16783–16794 (2017).
[Crossref]

2016 (3)

Y. Wang, Q. Guo, H. Chen, M. Chen, S. Yang, and S. Xie, “Time-encoded structured illumination microscopy: toward ultrafast superresolution imaging,” Opt. Lett. 41(16), 3755–3758 (2016).
[Crossref]

M. Müller, V. Mönkemöller, S. Hennig, W. Hübner, and T. Huser, “Open-source image reconstruction of super-resolution structured illumination microscopy data in imagej,” Nat. Commun. 7(1), 10980 (2016).
[Crossref]

A. Lal, C. Shan, and P. Xi, “Structured illumination microscopy image reconstruction algorithm,” IEEE J. Sel. Top. Quantum Electron. 22(4), 50–63 (2016).
[Crossref]

2015 (6)

J. Liu, R. Wu, N. Li, X. Zhang, Q. Zhan, and S. He, “Deep, high contrast microscopic cell imaging using three-photon luminescence of β-(NaYF 4: Er 3+/NaYF 4) nanoprobe excited by 1480-nm cw laser of only 1.5-mw,” Biomed. Opt. Express 6(5), 1857–1866 (2015).
[Crossref]

A. C. Chan, A. K. Lau, K. K. Wong, E. Y. Lam, and K. K. Tsia, “Arbitrary two-dimensional spectrally encoded pattern generation-a new strategy for high-speed patterned illumination imaging,” Optica 2(12), 1037–1044 (2015).
[Crossref]

G. Ball, J. Demmerle, R. Kaufmann, I. Davis, I. M. Dobbie, and L. Schermelleh, “Simcheck: a toolbox for successful super-resolution structured illumination microscopy,” Sci. Rep. 5(1), 15915 (2015).
[Crossref]

B. E. Urban, J. Yi, S. Chen, B. Dong, Y. Zhu, S. H. DeVries, V. Backman, and H. F. Zhang, “Super-resolution two-photon microscopy via scanning patterned illumination,” Phys. Rev. E 91(4), 042703 (2015).
[Crossref]

Y. Zhi, R. Lu, B. Wang, Q. Zhang, and X. Yao, “Rapid super-resolution line-scanning microscopy through virtually structured detection,” Opt. Lett. 40(8), 1683–1686 (2015).
[Crossref]

B. Zhou, B. Shi, D. Jin, and X. Liu, “Controlling upconversion nanocrystals for emerging applications,” Nat. Nanotechnol. 10(11), 924–936 (2015).
[Crossref]

2014 (5)

P. W. Winter, A. G. York, D. Dalle Nogare, M. Ingaramo, R. Christensen, A. Chitnis, G. H. Patterson, and H. Shroff, “Two-photon instant structured illumination microscopy improves the depth penetration of super-resolution imaging in thick scattering samples,” Optica 1(3), 181–191 (2014).
[Crossref]

M.-Y. Chen, G.-Y. Zhuo, K.-C. Chen, P.-C. Wu, T.-Y. Hsieh, T.-M. Liu, and S.-W. Chu, “Multiphoton imaging to identify grana, stroma thylakoid, and starch inside an intact leaf,” BMC Plant Biol. 14(1), 175 (2014).
[Crossref]

K. Nakagawa, A. Iwasaki, Y. Oishi, R. Horisaki, A. Tsukamoto, A. Nakamura, K. Hirosawa, H. Liao, T. Ushida, K. Goda, F. Kannari, and I. Sakuma, “Sequentially timed all-optical mapping photography (STAMP),” Nat. Photonics 8(9), 695–700 (2014).
[Crossref]

L. Gao, J. Liang, C. Li, and L. V. Wang, “Single-shot compressed ultrafast photography at one hundred billion frames per second,” Nature 516(7529), 74–77 (2014).
[Crossref]

G. P. Laporte, N. Stasio, C. J. Sheppard, and D. Psaltis, “Resolution enhancement in nonlinear scanning microscopy through post-detection digital computation,” Optica 1(6), 455–460 (2014).
[Crossref]

2013 (2)

R.-W. Lu, B.-Q. Wang, Q.-X. Zhang, and X.-C. Yao, “Super-resolution scanning laser microscopy through virtually structured detection,” Biomed. Opt. Express 4(9), 1673–1682 (2013).
[Crossref]

J. Zhao, D. Jin, E. P. Schartner, Y. Lu, Y. Liu, A. V. Zvyagin, L. Zhang, J. M. Dawes, P. Xi, J. A. Piper, E. M. Goldys, and T. M. Monro, “Single-nanocrystal sensitivity achieved by enhanced upconversion luminescence,” Nat. Nanotechnol. 8(10), 729–734 (2013).
[Crossref]

2012 (1)

K. Goda, A. Mahjoubfar, C. Wang, A. Fard, J. Adam, D. R. Gossett, A. Ayazi, E. Sollier, O. Malik, E. Chen, Y. Liu, R. Brown, N. Sarkhosh, D. Di Carlo, and B. Jalali, “Hybrid dispersion laser scanner,” Sci. Rep. 2(1), 445 (2012).
[Crossref]

2010 (2)

P. J. Keller, A. D. Schmidt, A. Santella, K. Khairy, Z. Bao, J. Wittbrodt, and E. H. Stelzer, “Fast, high-contrast imaging of animal development with scanned light sheet–based structured-illumination microscopy,” Nat. Methods 7(8), 637–642 (2010).
[Crossref]

K. Zheng, D. Zhao, D. Zhang, N. Liu, and W. Qin, “Ultraviolet upconversion fluorescence of Er 3+ induced by 1560 nm laser excitation,” Opt. Lett. 35(14), 2442–2444 (2010).
[Crossref]

2009 (3)

J. Lu, W. Min, J.-A. Conchello, X. S. Xie, and J. W. Lichtman, “Super-resolution laser scanning microscopy through spatiotemporal modulation,” Nano Lett. 9(11), 3883–3889 (2009).
[Crossref]

F. Wang and X. Liu, “Recent advances in the chemistry of lanthanide-doped upconversion nanocrystals,” Chem. Soc. Rev. 38(4), 976–989 (2009).
[Crossref]

K. Goda, D. R. Solli, K. K. Tsia, and B. Jalali, “Theory of amplified dispersive fourier transformation,” Phys. Rev. A 80(4), 043821 (2009).
[Crossref]

2008 (2)

H. Shroff, C. G. Galbraith, J. A. Galbraith, and E. Betzig, “Live-cell photoactivated localization microscopy of nanoscale adhesion dynamics,” Nat. Methods 5(5), 417–423 (2008).
[Crossref]

R. Fiolka, M. Beck, and A. Stemmer, “Structured illumination in total internal reflection fluorescence microscopy using a spatial light modulator,” Opt. Lett. 33(14), 1629–1631 (2008).
[Crossref]

2007 (1)

T. G. Etoh, C. V. Le, Y. Hashishin, N. Otsuka, K. Takehara, H. Ohtake, T. Hayashida, and H. Maruyama, “Evolution of ultra-high-speed CCD imagers,” Plasma Fusion Res. 2, S1021 (2007).
[Crossref]

2006 (1)

M. J. Rust, M. Bates, and X. Zhuang, “Stochastic optical reconstruction microscopy (STORM) provides sub-diffraction-limit image resolution,” Nat. Methods 3(10), 793–796 (2006).
[Crossref]

2005 (2)

F. Helmchen and W. Denk, “Deep tissue two-photon microscopy,” Nat. Methods 2(12), 932–940 (2005).
[Crossref]

J. Suyver, A. Aebischer, S. García-Revilla, P. Gerner, and H. Güdel, “Anomalous power dependence of sensitized upconversion luminescence,” Phys. Rev. B 71(12), 125123 (2005).
[Crossref]

2003 (1)

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]

2002 (1)

M. D. Cahalan, I. Parker, S. H. Wei, and M. J. Miller, “Two-photon tissue imaging: seeing the immune system in a fresh light,” Nat. Rev. Immunol. 2(11), 872–880 (2002).
[Crossref]

2000 (1)

M. G. Gustafsson, “Surpassing the lateral resolution limit by a factor of two using structured illumination microscopy,” J. Microsc. 198(2), 82–87 (2000).
[Crossref]

1995 (1)

W. A. Carrington, R. M. Lynch, E. Moore, G. Isenberg, K. E. Fogarty, and F. S. Fay, “Superresolution three-dimensional images of fluorescence in cells with minimal light exposure,” Science 268(5216), 1483–1487 (1995).
[Crossref]

1994 (1)

1990 (1)

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

Adam, J.

K. Goda, A. Mahjoubfar, C. Wang, A. Fard, J. Adam, D. R. Gossett, A. Ayazi, E. Sollier, O. Malik, E. Chen, Y. Liu, R. Brown, N. Sarkhosh, D. Di Carlo, and B. Jalali, “Hybrid dispersion laser scanner,” Sci. Rep. 2(1), 445 (2012).
[Crossref]

Aebischer, A.

J. Suyver, A. Aebischer, S. García-Revilla, P. Gerner, and H. Güdel, “Anomalous power dependence of sensitized upconversion luminescence,” Phys. Rev. B 71(12), 125123 (2005).
[Crossref]

Aharonovich, I.

C. Chen, F. Wang, S. Wen, Q. P. Su, M. C. L. Wu, Y. Liu, B. Wang, D. Li, X. Shan, M. Kianinia, I. Aharonovich, M. Toth, S. P. Jackson, P. Xi, and D. Jin, “Multi-photon near-infrared emission saturation nanoscopy using upconversion nanoparticles,” Nat. Commun. 9(1), 3290 (2018).
[Crossref]

Ayazi, A.

K. Goda, A. Mahjoubfar, C. Wang, A. Fard, J. Adam, D. R. Gossett, A. Ayazi, E. Sollier, O. Malik, E. Chen, Y. Liu, R. Brown, N. Sarkhosh, D. Di Carlo, and B. Jalali, “Hybrid dispersion laser scanner,” Sci. Rep. 2(1), 445 (2012).
[Crossref]

Backman, V.

B. E. Urban, J. Yi, S. Chen, B. Dong, Y. Zhu, S. H. DeVries, V. Backman, and H. F. Zhang, “Super-resolution two-photon microscopy via scanning patterned illumination,” Phys. Rev. E 91(4), 042703 (2015).
[Crossref]

Ball, G.

J. Demmerle, C. Innocent, A. J. North, G. Ball, M. Müller, E. Miron, A. Matsuda, I. M. Dobbie, Y. Markaki, and L. Schermelleh, “Strategic and practical guidelines for successful structured illumination microscopy,” Nat. Protoc. 12(5), 988–1010 (2017).
[Crossref]

G. Ball, J. Demmerle, R. Kaufmann, I. Davis, I. M. Dobbie, and L. Schermelleh, “Simcheck: a toolbox for successful super-resolution structured illumination microscopy,” Sci. Rep. 5(1), 15915 (2015).
[Crossref]

Bao, Q.

H. Chen, X. Wu, Y. Zhang, Y. Yang, C. Min, S. Zhu, X. Yuan, Q. Bao, and J. Bu, “Wide-field in situ multiplexed raman imaging with superresolution,” Photonics Res. 6(6), 530–534 (2018).
[Crossref]

Bao, Z.

P. J. Keller, A. D. Schmidt, A. Santella, K. Khairy, Z. Bao, J. Wittbrodt, and E. H. Stelzer, “Fast, high-contrast imaging of animal development with scanned light sheet–based structured-illumination microscopy,” Nat. Methods 7(8), 637–642 (2010).
[Crossref]

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H. Chen, X. Wu, Y. Zhang, Y. Yang, C. Min, S. Zhu, X. Yuan, Q. Bao, and J. Bu, “Wide-field in situ multiplexed raman imaging with superresolution,” Photonics Res. 6(6), 530–534 (2018).
[Crossref]

Wu, Y.

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[Crossref]

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X. Huang, J. Fan, L. Li, H. Liu, R. Wu, Y. Wu, L. Wei, H. Mao, A. Lal, P. Xi, L. Tang, Y. Zhang, Y. Liu, S. Tan, and L. Chen, “Fast, long-term, super-resolution imaging with hessian structured illumination microscopy,” Nat. Biotechnol. 36(5), 451–459 (2018).
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A. Lal, C. Shan, and P. Xi, “Structured illumination microscopy image reconstruction algorithm,” IEEE J. Sel. Top. Quantum Electron. 22(4), 50–63 (2016).
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H. Chen, X. Wu, Y. Zhang, Y. Yang, C. Min, S. Zhu, X. Yuan, Q. Bao, and J. Bu, “Wide-field in situ multiplexed raman imaging with superresolution,” Photonics Res. 6(6), 530–534 (2018).
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W. Yan, Y. Yang, Y. Tan, X. Chen, Y. Li, J. Qu, and T. Ye, “Coherent optical adaptive technique improves the spatial resolution of sted microscopy in thick samples,” Photonics Res. 5(3), 176–181 (2017).
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Yao, X.-C.

Ye, T.

W. Yan, Y. Yang, Y. Tan, X. Chen, Y. Li, J. Qu, and T. Ye, “Coherent optical adaptive technique improves the spatial resolution of sted microscopy in thick samples,” Photonics Res. 5(3), 176–181 (2017).
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H. Chen, X. Wu, Y. Zhang, Y. Yang, C. Min, S. Zhu, X. Yuan, Q. Bao, and J. Bu, “Wide-field in situ multiplexed raman imaging with superresolution,” Photonics Res. 6(6), 530–534 (2018).
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J. Zhao, D. Jin, E. P. Schartner, Y. Lu, Y. Liu, A. V. Zvyagin, L. Zhang, J. M. Dawes, P. Xi, J. A. Piper, E. M. Goldys, and T. M. Monro, “Single-nanocrystal sensitivity achieved by enhanced upconversion luminescence,” Nat. Nanotechnol. 8(10), 729–734 (2013).
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Zhang, Q.-X.

Zhang, X.

Zhang, Y.

H. Chen, X. Wu, Y. Zhang, Y. Yang, C. Min, S. Zhu, X. Yuan, Q. Bao, and J. Bu, “Wide-field in situ multiplexed raman imaging with superresolution,” Photonics Res. 6(6), 530–534 (2018).
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X. Huang, J. Fan, L. Li, H. Liu, R. Wu, Y. Wu, L. Wei, H. Mao, A. Lal, P. Xi, L. Tang, Y. Zhang, Y. Liu, S. Tan, and L. Chen, “Fast, long-term, super-resolution imaging with hessian structured illumination microscopy,” Nat. Biotechnol. 36(5), 451–459 (2018).
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Zhao, D.

Zhao, J.

J. Zhao, D. Jin, E. P. Schartner, Y. Lu, Y. Liu, A. V. Zvyagin, L. Zhang, J. M. Dawes, P. Xi, J. A. Piper, E. M. Goldys, and T. M. Monro, “Single-nanocrystal sensitivity achieved by enhanced upconversion luminescence,” Nat. Nanotechnol. 8(10), 729–734 (2013).
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Zhao, K.

A. Lal, C. Shan, K. Zhao, W. Liu, X. Huang, W. Zong, L. Chen, and P. Xi, “A frequency domain sim reconstruction algorithm using reduced number of images,” IEEE Trans. on Image Process. 27(9), 4555–4570 (2018).
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B. E. Urban, J. Yi, S. Chen, B. Dong, Y. Zhu, S. H. DeVries, V. Backman, and H. F. Zhang, “Super-resolution two-photon microscopy via scanning patterned illumination,” Phys. Rev. E 91(4), 042703 (2015).
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Figures (8)

Fig. 1.
Fig. 1. Generation of structured illumination with the MUTE-SIM geometry. (a)(b)(c) correspond to the time domain waveforms, spectrum, and spatial scanning spot of the broadband femtosecond laser, respectively. (d) shows the pulses are temporally stretched by the dispersive fiber, thus each wavelength will be separated in time. (f) The spectrum of the laser pulses is mapped into space by using a diffraction grating, different wavelengths correspond to different positions of the scanning spot. (g) Time domain waveforms of the pulses after modulation by a high-speed arbitrary waveform generator (AWG) together with a high-bandwidth optical modulator. (h)(i) The spectrum and spatial pattern correspond to the time domain modulation waveforms, respectively. Time coordinate t, spectral coordinate $\lambda$, spatial coordinate $x$ are one-to-one correspondence.
Fig. 2.
Fig. 2. Multiphoton process. (a) Normalized profiles of $h_{\textrm {em}} (k)$ and $h_{\textrm {eff-ex}} (k)$ under different relationship between excitation power and emission intensity. (b) Normalized profiles of $\tilde h_{\textrm {em}} (k)$ and $\tilde h_{\textrm {eff-ex}} (k)$ under different relationship between excitation power and emission intensity. (c) The contrast of different pattern spatial frequency in the MUTE-SIM system, and initial modulation (the modulation before the excitation pulse enters the objective) is set to 1.
Fig. 3.
Fig. 3. The schematic diagram of the proposed MUTE-SIM system.
Fig. 4.
Fig. 4. (a)-(c) The time domain waveforms. (d)-(f) The corresponding spectrum. (g)-(i) The corresponding spatial pattern whose periods are 8 $\upmu$m, 4 $\upmu$m, 2 $\upmu$m respectively.
Fig. 5.
Fig. 5. Patterns with different phases. (a) Pattern with phase $\phi =0$. (b) Pattern with phase $\phi =\pi /2$. (c) Pattern with phase $\phi =\pi$. (d) The profile across the horizontal red line of (a)(b)(c).
Fig. 6.
Fig. 6. Multiphoton wide-field SIM super-resolution imaging with UCNPs. (a) Wide field image without pattern, scale bar: 10 $\upmu$m. (b) The intensity profile across the horizontal line of (a). (c) Reconstructed Linear SIM image, scale bar: 10 $\upmu$m. (d) The intensity profile across the horizontal line of (c). (e) The enlarge image of red box in (a), scale bar: 0.4 $\upmu$m. (f) The intensity profile across the red line of (e). (g) The enlarge image of red box in (c), scale bar: 0.4 $\upmu$m. (h) The intensity profile across the red line of (g).
Fig. 7.
Fig. 7. Emission spectrum and core-shell. (a) The emission spectrum of UCNPs measured under 1560 nm laser of 25mW. ①CWL:379nm,FWHM:4nm. ②CWL:408nm,FWHM:8nm. ③CWL:525nm,FWHM:12nm. ④CWL:540nm,FWHM:5nm. ⑤WL:660nm,FWHM:8nm. (b) TEM images of core-shell nanostructure of $\beta \textrm {-}NaYF_4: 25\% Er^{3+} @ NaYF_4$ with the size of 22.1 nm, scale bar 0.05$\upmu$m. (c) Size distribution histograms corresponding to TEM image (b), $22.1 \pm 0.9 nm$, respectively. Histograms of the crystals sizes are drawn from analysis of >150 crystals. (d) Energy level diagram of $\beta \textrm {-}NaYF_4: 25\% Er^{3+} @ NaYF_4$ nanocrystals.
Fig. 8.
Fig. 8. (a) Pump-power dependence of $\beta \textrm {-}NaYF_4: 25\% Er^{3+} @ NaYF_4$ with 1560nm excitation, 540nm emission in log-log scale. (b) The relationship between slope n and power density.

Equations (11)

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

I camera ( x ) = M ( t ) h ex ( r t ) S ( r ) h em ( x r ) d r d t
M ( t ) = I 0 { 1 + m cos ( ω t + ϕ ) }
I ~ camera ( k ) = { [ M ~ ( k ) h ~  ex ( k ) ] S ~ ( k ) } h ~  em ( k )
Δ X = f d cos β Δ λ
Δ λ  =  Δ t GVD
Δ x  grating  =  f N d cos β λ
Δ x objective  = 0 .61 λ N A
f N A l cos β
Δ t min = 0 .61 λ N A d cos β f GVD
FOV = f d cos β Δ λ band
I camera ( x ) = M ( t ) h ex ( r t ) S ( r ) h em ( x r ) d r d t

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