Abstract

Non-degenerate two-photon excitation (ND-TPE) has been explored in two-photon excitation microscopy. However, a systematic study of the efficiency of ND-TPE to guide the selection of fluorophore excitation wavelengths is missing. We measured the relative non-degenerate two-photon absorption cross-section (ND-TPACS) of several commonly used fluorophores (two fluorescent proteins and three small-molecule dyes) and generated 2-dimensional ND-TPACS spectra. We observed that the shape of a ND-TPACS spectrum follows that of the corresponding degenerate two-photon absorption cross-section (D-TPACS) spectrum, but is higher in magnitude. We found that the observed enhancements are higher than theoretical predictions.

© 2019 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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References

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2019 (1)

2017 (2)

E. P. Perillo, J. W. Jarrett, Y.-L. Liu, A. Hassan, D. C. Fernée, J. R. Goldak, A. Bonteanu, D. J. Spence, H.-C. Yeh, and A. K. Dunn, “Two-color multiphoton in vivo imaging with a femtosecond diamond raman laser,” Light: Sci. Appl. 6(11), e17095 (2017).
[Crossref]

D. R. Miller, J. W. Jarrett, A. M. Hassan, and A. K. Dunn, “Deep tissue imaging with multiphoton fluorescence microscopy,” Curr. Opin. Biomed. Eng. 4, 32–39 (2017).
[Crossref]

2016 (5)

H. S. Pattanaik, M. Reichert, J. B. Khurgin, D. J. Hagan, and E. W. Van Stryland, “Enhancement of two-photon absorption in quantum wells for extremely nondegenerate photon pairs,” IEEE J. Quantum Electron. 52(3), 1–14 (2016).
[Crossref]

K. Podgorski and G. Ranganathan, “Brain heating induced by near-infrared lasers during multiphoton microscopy,” J. Neurophysiol. 116(3), 1012–1023 (2016).
[Crossref]

T. V. Esipova, H. J. Rivera-Jacquez, B. Weber, A. E. Masunov, and S. A. Vinogradov, “Two-photon absorbing phosphorescent metalloporphyrins: effects of $\pi$π-extension and peripheral substitution,” J. Am. Chem. Soc. 138(48), 15648–15662 (2016).
[Crossref]

S. de Reguardati, J. Pahapill, A. Mikhailov, Y. Stepanenko, and A. Rebane, “High-accuracy reference standards for two-photon absorption in the 680–1050 nm wavelength range,” Opt. Express 24(8), 9053–9066 (2016).
[Crossref]

M.-H. Yang, M. Abashin, P. A. Saisan, P. Tian, C. G. Ferri, A. Devor, and Y. Fainman, “Non-degenerate 2-photon excitation in scattering medium for fluorescence microscopy,” Opt. Express 24(26), 30173–30187 (2016).
[Crossref]

2015 (1)

A. Rebane, G. Wicks, M. Drobizhev, T. Cooper, A. Trummal, and M. Uudsemaa, “Two-photon voltmeter for measuring a molecular electric field,” Angew. Chem., Int. Ed. 54(26), 7582–7586 (2015).
[Crossref]

2014 (1)

K. M. Dean and A. E. Palmer, “Advances in fluorescence labeling strategies for dynamic cellular imaging,” Nat. Chem. Biol. 10(7), 512–523 (2014).
[Crossref]

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]

2012 (2)

P. Mahou, M. Zimmerley, K. Loulier, K. S. Matho, G. Labroille, X. Morin, W. Supatto, J. Livet, D. Débarre, and E. Beaurepaire, “Multicolor two-photon tissue imaging by wavelength mixing,” Nat. Methods 9(8), 815–818 (2012).
[Crossref]

J. Mütze, V. Iyer, J. J. Macklin, J. Colonell, B. Karsh, Z. Petrášek, P. Schwille, L. L. Looger, L. D. Lavis, and T. D. Harris, “Excitation spectra and brightness optimization of two-photon excited probes,” Biophys. J. 102(4), 934–944 (2012).
[Crossref]

2011 (2)

A. Devor, S. Sakadžić, P. A. Saisan, M. A. Yaseen, E. Roussakis, V. J. Srinivasan, S. A. Vinogradov, B. R. Rosen, R. B. Buxton, A. M. Dale, and D. A. Boas, “Overshoot of o2 is required to maintain baseline tissue oxygenation at locations distal to blood vessels,” J. Neurosci. 31(38), 13676–13681 (2011).
[Crossref]

M. Drobizhev, N. S. Makarov, S. E. Tillo, T. E. Hughes, and A. Rebane, “Two-photon absorption properties of fluorescent proteins,” Nat. Methods 8(5), 393–399 (2011).
[Crossref]

2010 (2)

S. Sakadžić, E. Roussakis, M. A. Yaseen, E. T. Mandeville, V. J. Srinivasan, K. Arai, S. Ruvinskaya, A. Devor, E. H. Lo, S. A. Vinogradov, and D. A. Boas, “Two-photon high-resolution measurement of partial pressure of oxygen in cerebral vasculature and tissue,” Nat. Methods 7(9), 755–759 (2010).
[Crossref]

A. Rebane, M. Drobizhev, N. Makarov, E. Beuerman, S. Tillo, and T. Hughes, “New all-optical method for measuring molecular permanent dipole moment difference using two-photon absorption spectroscopy,” J. Lumin. 130(9), 1619–1623 (2010).
[Crossref]

2009 (1)

S. Quentmeier, S. Denicke, and K.-H. Gericke, “Two-color two-photon fluorescence laser scanning microscopy,” J. Fluoresc. 19(6), 1037–1043 (2009).
[Crossref]

2008 (6)

W.-C. A. Lee, J. L. Chen, H. Huang, J. H. Leslie, Y. Amitai, P. T. So, and E. Nedivi, “A dynamic zone defines interneuron remodeling in the adult neocortex,” Proc. Natl. Acad. Sci. 105(50), 19968–19973 (2008).
[Crossref]

M. Mank, A. F. Santos, S. Direnberger, T. D. Mrsic-Flogel, S. B. Hofer, V. Stein, T. Hendel, D. F. Reiff, C. Levelt, and A. Borstet al., “A genetically encoded calcium indicator for chronic in vivo two-photon imaging,” Nat. Methods 5(9), 805–811 (2008).
[Crossref]

N. L. Rochefort and A. Konnerth, “Genetically encoded ca 2+ sensors come of age,” Nat. Methods 5(9), 761–762 (2008).
[Crossref]

M. Drobizhev, N. S. Makarov, A. Rebane, G. de la Torre, and T. Torres, “Strong two-photon absorption in push- pull phthalocyanines: Role of resonance enhancement and permanent dipole moment change upon excitation,” J. Phys. Chem. C 112(3), 848–859 (2008).
[Crossref]

A. Sakaue-Sawano, H. Kurokawa, T. Morimura, A. Hanyu, H. Hama, H. Osawa, S. Kashiwagi, K. Fukami, T. Miyata, H. Miyoshi, T. Imamura, M. Ogawa, H. Masai, and A. Miyawaki, “Visualizing spatiotemporal dynamics of multicellular cell-cycle progression,” Cell 132(3), 487–498 (2008).
[Crossref]

C. Wang, L. Qiao, Z. Mao, Y. Cheng, and Z. Xu, “Reduced deep-tissue image degradation in three-dimensional multiphoton microscopy with concentric two-color two-photon fluorescence excitation,” J. Opt. Soc. Am. B 25(6), 976–982 (2008).
[Crossref]

2007 (1)

S. Nagayama, S. Zeng, W. Xiong, M. L. Fletcher, A. V. Masurkar, D. J. Davis, V. A. Pieribone, and W. R. Chen, “In vivo simultaneous tracing and ca2+ imaging of local neuronal circuits,” Neuron 53(6), 789–803 (2007).
[Crossref]

2005 (3)

E. M. Callaway, “A molecular and genetic arsenal for systems neuroscience,” Trends Neurosci. 28(4), 196–201 (2005).
[Crossref]

N. C. Shaner, P. A. Steinbach, and R. Y. Tsien, “A guide to choosing fluorescent proteins,” Nat. Methods 2(12), 905–909 (2005).
[Crossref]

G. McNamara, M. Difilippantonio, T. Ried, and F. R. Bieber, “Microscopy and image analysis,” Curr. Protoc. Hum. Genet. 46(1), 441–4434 (2005).
[Crossref]

2004 (3)

C. Ibáïez-López, I. Escobar, G. Saavedra, and M. Martínez-Corral, “Optical-sectioning improvement in two-color excitation scanning microscopy,” Microsc. Res. Tech. 64(2), 96–102 (2004).
[Crossref]

J. M. Hales, D. J. Hagan, E. W. Van Stryland, K. Schafer, A. Morales, K. D. Belfield, P. Pacher, O. Kwon, E. Zojer, and J.-L. Brédas, “Resonant enhancement of two-photon absorption in substituted fluorene molecules,” J. Chem. Phys. 121(7), 3152–3160 (2004).
[Crossref]

A. Nimmerjahn, F. Kirchhoff, J. N. Kerr, and F. Helmchen, “Sulforhodamine 101 as a specific marker of astroglia in the neocortex in vivo,” Nat. Methods 1(1), 31–37 (2004).
[Crossref]

2001 (2)

Y. Okubo, S. Kakizawa, K. Hirose, and M. Iino, “Visualization of ip3 dynamics reveals a novel AMPA receptor-triggered ip3 production pathway mediated by voltage-dependent ca2+ influx in purkinje cells,” Neuron 32(1), 113–122 (2001).
[Crossref]

C. M. Blanca and C. Saloma, “Two-color excitation fluorescence microscopy through highly scattering media,” Appl. Opt. 40(16), 2722–2729 (2001).
[Crossref]

2000 (2)

A. A. Oliva, M. Jiang, T. Lam, K. L. Smith, and J. W. Swann, “Novel hippocampal interneuronal subtypes identified using transgenic mice that express green fluorescent protein in GABAergic interneurons,” J. Neurosci. 20(9), 3354–3368 (2000).
[Crossref]

M. O. Cambaliza and C. Saloma, “Advantages of two-color excitation fluorescence microscopy with two confocal excitation beams,” Opt. Commun. 184(1-4), 25–35 (2000).
[Crossref]

1999 (1)

1998 (1)

D. Kleinfeld, P. P. Mitra, F. Helmchen, and W. Denk, “Fluctuations and stimulus-induced changes in blood flow observed in individual capillaries in layers 2 through 4 of rat neocortex,” Proc. Natl. Acad. Sci. 95(26), 15741–15746 (1998).
[Crossref]

1996 (3)

B. P. Cormack, R. H. Valdivia, and S. Falkow, “FACS-optimized mutants of the green fluorescent protein (gfp),” Gene 173(1), 33–38 (1996).
[Crossref]

J. Bhawalkar, G. He, and P. Prasad, “Nonlinear multiphoton processes in organic and polymeric materials,” Rep. Prog. Phys. 59(9), 1041–1070 (1996).
[Crossref]

C. Xu and W. W. Webb, “Measurement of two-photon excitation cross sections of molecular fluorophores with data from 690 to 1050 nm,” J. Opt. Soc. Am. B 13(3), 481–491 (1996).
[Crossref]

1995 (1)

R. Sjöback, J. Nygren, and M. Kubista, “Absorption and fluorescence properties of fluorescein,” Spectrochim. Acta, Part A 51(6), L7–L21 (1995).
[Crossref]

1992 (1)

C. W. Dirk, L.-T. Cheng, and M. G. Kuzyk, “A simplified three-level model describing the molecular third-order nonlinear optical susceptibility,” Int. J. Quantum Chem. 43(1), 27–36 (1992).
[Crossref]

1990 (1)

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

1986 (1)

R. R. Birge and B. M. Pierce, “Semiclassical time-dependent theory of two-photon spectroscopy. the effect of dephasing in the virtual level on the two-photon excitation spectrum of isotachysterol,” Int. J. Quantum Chem. 29(4), 639–656 (1986).
[Crossref]

1975 (1)

G. Reynolds and K. H. Drexhage, “New coumarin dyes with rigidized structure for flashlamp-pumped dye lasers,” Opt. Commun. 13(3), 222–225 (1975).
[Crossref]

1967 (1)

W. L. Peticolas, “Multiphoton spectroscopy,” Annu. Rev. Phys. Chem. 18(1), 233–260 (1967).
[Crossref]

Abashin, M.

Amitai, Y.

W.-C. A. Lee, J. L. Chen, H. Huang, J. H. Leslie, Y. Amitai, P. T. So, and E. Nedivi, “A dynamic zone defines interneuron remodeling in the adult neocortex,” Proc. Natl. Acad. Sci. 105(50), 19968–19973 (2008).
[Crossref]

Arai, K.

S. Sakadžić, E. Roussakis, M. A. Yaseen, E. T. Mandeville, V. J. Srinivasan, K. Arai, S. Ruvinskaya, A. Devor, E. H. Lo, S. A. Vinogradov, and D. A. Boas, “Two-photon high-resolution measurement of partial pressure of oxygen in cerebral vasculature and tissue,” Nat. Methods 7(9), 755–759 (2010).
[Crossref]

Beaurepaire, E.

P. Mahou, M. Zimmerley, K. Loulier, K. S. Matho, G. Labroille, X. Morin, W. Supatto, J. Livet, D. Débarre, and E. Beaurepaire, “Multicolor two-photon tissue imaging by wavelength mixing,” Nat. Methods 9(8), 815–818 (2012).
[Crossref]

Belfield, K. D.

J. M. Hales, D. J. Hagan, E. W. Van Stryland, K. Schafer, A. Morales, K. D. Belfield, P. Pacher, O. Kwon, E. Zojer, and J.-L. Brédas, “Resonant enhancement of two-photon absorption in substituted fluorene molecules,” J. Chem. Phys. 121(7), 3152–3160 (2004).
[Crossref]

Beuerman, E.

A. Rebane, M. Drobizhev, N. Makarov, E. Beuerman, S. Tillo, and T. Hughes, “New all-optical method for measuring molecular permanent dipole moment difference using two-photon absorption spectroscopy,” J. Lumin. 130(9), 1619–1623 (2010).
[Crossref]

Bhawalkar, J.

J. Bhawalkar, G. He, and P. Prasad, “Nonlinear multiphoton processes in organic and polymeric materials,” Rep. Prog. Phys. 59(9), 1041–1070 (1996).
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Figures (8)

Fig. 1.
Fig. 1. ND-TPE spectroscopy. a) Color-coded, normalized ND-TPACS spectra for EGFP, mKO2, Fluorescein, Coumarin 343, and SR101 showing the dependence of the normalized ND-TPACS on NIR and IR wavelengths. The ND-TPACS at each combination of wavelengths was normalized by the peak D-TPACS value of the fluorophore. The isoclines corresponding to the ground to excited state transition energy ($hc/\lambda _{\mathrm {NIR}}+hc/\lambda _{\mathrm {IR}}=2.66$ eV for EGFP, $2.6$ eV for mKO2, $2.7$ eV for Fluorescein, and $2.76$ eV for SR101) are overlaid as dashed black lines. b) ND-TPACS normalized by the peak D-TPACS as a function of the equivalent degenerate wavelength $2/\lambda _{\mathrm {D}}=1/\lambda _{\mathrm {NIR}}+1/\lambda _{\mathrm {IR}}$ are shown in red. Along any energy isocline, multiple excitation wavelength combinations within our tuning range sum to the same total energy and, therefore, the same equivalent wavelength. Thus, for each $\lambda _{\mathrm {D}}$ value we report several values of ND-TPACS (red dots). Independently measured D-TPACS normalized by its peak within the equivalent range of the total photon energy ($2.3-2.9$ eV) are shown in black. The black dashed vertical line indicates the position of the peak D-TPACS used for the normalization procedure ($930$ nm for EGFP, $950$ nm for mKO2, $920$ nm for Fluorescein, $860$ nm for Coumarin 343, and $900$ nm for SR101). These wavelengths correspond to the energy isoclines shown in panel (a).
Fig. 2.
Fig. 2. Choice of excitation wavelengths in ND-TPE microscopy. a) Effects of scattering and absorption (adapted from [21]): photon fraction at depth of $1$ mm, considering both absorption and scattering, for average brain tissue optical properties is shown as blue line. Percent of the photons absorbed by brain tissue in $1$ mm is shown as red line. b) Simulation results for tissue heating by a scanned focused light: ratio of the maximum tissue temperature change under simultaneous excitation by NIR and IR beam to maximum temperature change under excitation with a single beam with equivalent degenerate wavelength, $2hc/\lambda _{\mathrm {D}}=hc/\lambda _{\mathrm {NIR}}+hc/\lambda _{\mathrm {IR}}$ and $\lambda _{\mathrm {D}}=920$ nm, versus $\lambda _{\mathrm {IR}}$ assuming equal total excitation power $P_{\mathrm {NIR}}+P_{\mathrm {IR}}=P_{\mathrm {D}}=100$ mW at focal point ($250$ $\mu$m below surface).
Fig. 3.
Fig. 3. a) Experimental setup for ND-TPACS measurement. L, lens; PBS, polarizing beam splitter; $\lambda$/2, half wave plate; GS, glass slide; M, mirror; DM, dichroic mirror; BD, beam dump; FS, fluorescent sample; OL, objective lens; BPF, band pass filter; PM, power meter; and PMT, photomultiplier tube. b) A typical plot of fluorescence intensity as a function of the temporal offset between NIR and IR pulses. The increase in the signal at zero temporal offset is due to ND-TPE. The red line shows the fitted model (Eq. (3)).
Fig. 4.
Fig. 4. Linear dependence of non-degenerate two-photon fluorescence excitation on a) NIR excitation power ($P_{\mathrm {IR}}= 15$ mW), and b) IR excitation power ($P_{\mathrm {NIR}}$= 5 mW). The power dependence was tested at wavelength combinations $\lambda _{\mathrm {NIR}}=740$ nm and $\lambda _{\mathrm {IR}}=1230$ nm for all measured fluorophores.
Fig. 5.
Fig. 5. Characterization of the experimental error in ND-TPACS measurements via repetitive measurements of ND-TPACS along one isocline. Here we show $10$ measurements of normalized ND-TPACS of EGFP along the $hc/\lambda _{\mathrm {NIR}}+hc/\lambda _{\mathrm {IR}}=2.66$ eV isocline vs $\lambda _{\mathrm {NIR}}$. The measured relative experimental error is $\sim 15\%$.
Fig. 6.
Fig. 6. Normalized one-photon absorption spectra of Coumarin 343 (cyan), EGFP (green), Fluorescein (yellow), mKO2 (red), and SR101 (dark red).
Fig. 7.
Fig. 7. Graphical representation of Table 1 for comparison of the experimental and theoretical (two-level approximation, Eq. (1)) values of the ISRE for $\hbar \omega _{\mathrm {NIR}}+\hbar \omega _{\mathrm {IR}}=2.66$  eV for EGFP, $2.6$ eV for mKO2, $2.7$ eV for Fluorescein, and $2.76$ eV for SR101. Experimental data (solid line) and theoretical results (dashed line) are overlaid.
Fig. 8.
Fig. 8. Tissue heating simulations. Simulation code was provided by K. Podgorski [37]. a-d) Simulated spatial temperature profile in brain tissue with cover glass and immersion water (temperature of the immersion water $1$ mm above cover glass was kept constant at $25$ $^{\circ }$C). Profiles are shown for no illumination, $100$ mW at $920$ nm, $50$ mW at $1230$ nm, and $50$ mW at $740$ nm. e-g) Simulated temperature change for $100$ mW at $920$ nm, $50$ mW at $1230$ nm, and $50$ mW at $740$ nm. Contour lines are shown for $1$ $^{\circ }$C intervals. All powers are given for a focal plane $250$ $\mu$m below the surface.

Tables (3)

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Table 1. Comparison between experimental and theoretical (two-level approximation, Eq. (1)) values of the ISRE2 for $\hbar \omega _{\mathrm {NIR}}+\hbar \omega _{\mathrm {IR}}=2.66$ eV for EGFP, $2.6$ eV for mKO2, $2.7$ eV for Fluorescein, and $2.76$ eV for SR101. (See Fig. 7 for the graphical representation of the results)

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Table 2. Fluorophore concentrations.

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Table 3. Optical parameters for average brain tissue [21,47] that were used in our heating simulations. $\mu _a$ and $\mu _s$ are the absorption and scattering coefficients, respectively, and $T=100\times e^{-(\mu _a+\mu _s)z}$ is the light transmission percentage at depth $z$. We set $z=250$$\mu$m for our tissue heating simulations.

Equations (11)

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I S R E 2 = σ N D ( ω N I R , ω I R ) σ D ( ω D ) = ( ω N I R + ω I R ) 2 4 ω N I R ω I R
F D = π C P 2 λ ϕ η σ D ( 2 ) ( λ ) 4 f c 2 h 2 Γ .
F ( τ ) = π C P N I R 2 λ N I R ϕ η σ D ( 2 ) ( λ N I R ) 4 f c 2 h 2 Γ N I R + π C P I R 2 λ I R ϕ η σ D ( 2 ) ( λ I R ) 4 f c 2 h 2 Γ I R   + 2 π C P N I R P I R λ N I R λ I R ϕ η σ N D ( 2 ) ( λ N I R , λ I R ) f c 2 h 2 Γ x λ N I R 2 + λ I R 2 exp ( τ 2 2 Γ x 2 ) .
| S ( f ) | 2 = | i [ ( e 1 μ i 0 ) ( μ f i e 2 ) E i ω 1 + i ξ i + ( e 1 μ i 0 ) ( μ f i e 2 ) E i ω 2 + i ξ i ] | 2 ,
σ N D ( ω 1 , ω 2 ) ω 1 ω 2 | S ( f ) | 2 ρ f ( ω N I R + ω I R ω f ) ,
| S ( f ) | 2 = | i [ μ i 0 μ f i E i ω 1 + i ξ i + μ i 0 μ f i E i ω 2 + i ξ i ] | 2 .
| S ( f ) | 2 = | [ μ 00 μ f 0 E 0 ω 1 + i ξ 0 + μ 00 μ f 0 E 0 ω 2 + i ξ 0 ] + [ μ f 0 μ f f E f ω 1 + i ξ f + μ f 0 μ f f E f ω 2 + i ξ f ] | 2 .
| S ( f ) | 2 [ μ f 0 ( μ f f μ 00 ) ] 2 ( 1 ω 1 + 1 ω 2 ) 2 .
σ N D ( ω 1 , ω 2 ) ( ω 1 + ω 2 ) 2 ω 1 ω 2 ,
I S R E 2 = σ N D ( ω N I R , ω I R ) σ D ( ω D ) = ( ω D ) 2 ω N I R ω I R = ( ω N I R + ω I R ) 2 4 ω N I R ω I R ,
I S R E 3 = ω N I R ω I R | μ f 0 ( μ 00 μ f f ) ( 1 ω N I R + 1 ω I R ) + μ i 0 μ f i ( 1 E i ω N I R + 1 E i ω I R ) | 2 ( ω D ) 2 | μ f 0 ( μ 00 μ f f ) ( 2 ω D ) + μ i 0 μ f i ( 2 E i ω D ) | 2 .

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