Abstract

Three-photon microscopy has been increasingly adopted for probing neural activities beyond the typical two-photon imaging depth. In this review, we outline the unique properties that differentiate three-photon microscopy from two-photon microscopy for in vivo imaging in biological samples, especially in the mouse brain. We present a systematic summary of the optimization of three-photon imaging parameters for neural imaging, based on their effects on calcium imaging quality and perturbation to brain tissues. Furthermore, we review the existing techniques for volumetric imaging and discuss their prospects in mesoscale three-photon imaging in deep tissue.

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

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2020 (6)

K. Takasaki, R. Abbasi-Asl, and J. Waters, “Superficial bound of the depth limit of 2-photon imaging in mouse brain,” eNeuro 7, 271 (2020).
[Crossref]

A. Klioutchnikov, D. J. Wallace, M. H. Frosz, R. Zeltner, J. Sawinski, V. Pawlak, K.-M. Voit, P. St. J. Russell, and J. N. D. Kerr, “Three-photon head-mounted microscope for imaging deep cortical layers in freely moving rats,” Nat. Methods 17, 509–513 (2020).
[Crossref]

T. Wang, C. Wu, D. G. Ouzounov, W. Gu, F. Xia, M. Kim, X. Yang, M. R. Warden, and C. Xu, “Quantitative analysis of 1300-nm three-photon calcium imaging in the mouse brain,” Elife 9, e53205 (2020).
[Crossref]

B. Li, C. Wu, M. Wang, K. Charan, and C. Xu, “An adaptive excitation source for high-speed multiphoton microscopy,” Nat. Methods 17, 163–167 (2020).
[Crossref]

R. Lu, Y. Liang, G. Meng, P. Zhou, K. Svoboda, L. Paninski, and N. Ji, “Rapid mesoscale volumetric imaging of neural activity with synaptic resolution,” Nat. Methods 17, 291–294 (2020).
[Crossref]

D. R. Beaulieu, I. G. Davison, K. Kılıç, T. G. Bifano, and J. Mertz, “Simultaneous multiplane imaging with reverberation two-photon microscopy,” Nat. Methods 17, 283–286 (2020).
[Crossref]

2019 (9)

D. G. Ouzounov, T. Wang, C. Wu, and C. Xu, “GCaMP6 ΔF/F dependence on the excitation wavelength in 3-photon and 2-photon microscopy of mouse brain activity,” Biomed. Opt. Express 10, 3343 (2019).
[Crossref]

K. T. Takasaki, D. Tsyboulski, and J. Waters, “Dual-plane 3-photon microscopy with remote focusing,” Biomed. Opt. Express 10, 5585–5599 (2019).
[Crossref]

H. Dana, Y. Sun, B. Mohar, B. K. Hulse, A. M. Kerlin, J. P. Hasseman, G. Tsegaye, A. Tsang, A. Wong, R. Patel, J. J. Macklin, Y. Chen, A. Konnerth, V. Jayaraman, L. L. Looger, E. R. Schreiter, K. Svoboda, and D. S. Kim, “High-performance calcium sensors for imaging activity in neuronal populations and microcompartments,” Nat. Methods 16, 649–657 (2019).
[Crossref]

S. F. Owen, M. H. Liu, and A. C. Kreitzer, “Thermal constraints on in vivo optogenetic manipulations,” Nat. Neurosci. 22, 1061–1065 (2019).
[Crossref]

S. Weisenburger, F. Tejera, J. Demas, B. Chen, J. Manley, F. T. Sparks, F. Martínez Traub, T. Daigle, H. Zeng, A. Losonczy, and A. Vaziri, “Volumetric Ca2+ imaging in the mouse brain using hybrid multiplexed sculpted light microscopy,” Cell 177, 1050–1066 (2019).
[Crossref]

M. Yildirim, H. Sugihara, P. T. C. So, and M. Sur, “Functional imaging of visual cortical layers and subplate in awake mice with optimized three-photon microscopy,” Nat. Commun. 10, 177 (2019).
[Crossref]

H. Liu, X. Deng, S. Tong, C. He, H. Cheng, Z. Zhuang, M. Gan, J. Li, W. Xie, P. Qiu, and K. Wang, “In vivo deep-brain structural and hemodynamic multiphoton microscopy enabled by quantum dots,” Nano Lett. 19, 5260–5265 (2019).
[Crossref]

K.-J. Hsu, Y.-Y. Lin, A.-S. Chiang, and S.-W. Chu, “Optical properties of adult Drosophila brains in one-, two-, and three-photon microscopy,” Biomed. Opt. Express 10, 1627–1637 (2019).
[Crossref]

K. Wang, Y. Du, H. Liu, M. Gan, S. Tong, W. Wen, Z. Zhuang, and P. Qiu, “Visualizing the ‘sandwich’ structure of osteocytes in their native environment deep in bone in vivo,” J. Biophoton. 12, e201800360 (2019).
[Crossref]

2018 (7)

B. Chen, X. Huang, D. Gou, J. Zeng, G. Chen, M. Pang, Y. Hu, Z. Zhao, Y. Zhang, Z. Zhou, H. Wu, H. Cheng, Z. Zhang, C. Xu, Y. Li, L. Chen, and A. Wang, “Rapid volumetric imaging with Bessel-Beam three-photon microscopy,” Biomed. Opt. Express 9, 1992–2000 (2018).
[Crossref]

T. Wang, D. G. Ouzounov, C. Wu, N. G. Horton, B. Zhang, C.-H. Wu, Y. Zhang, M. J. Schnitzer, and C. Xu, “Three-photon imaging of mouse brain structure and function through the intact skull,” Nat. Methods 15, 789–792 (2018).
[Crossref]

M. Wang, C. Wu, D. Sinefeld, B. Li, F. Xia, and C. Xu, “Comparing the effective attenuation lengths for long wavelength in vivo imaging of the mouse brain,” Biomed. Opt. Express 9, 3534–3543 (2018).
[Crossref]

C. Rodríguez, Y. Liang, R. Lu, and J. Na, “Three-photon fluorescence microscopy with an axially elongated Bessel focus,” Opt. Lett. 43, 1914–1917 (2018).
[Crossref]

C. Rodríguez and N. Ji, “Adaptive optical microscopy for neurobiology,” Curr. Opin. Neurobiol. 50, 83–91 (2018).
[Crossref]

A. Escobet-Montalbán, F. M. Gasparoli, J. Nylk, P. Liu, Z. Yang, and K. Dholakia, “Three-photon light-sheet fluorescence microscopy,” Opt. Lett. 43, 5484–5487 (2018).
[Crossref]

K. Guesmi, L. Abdeladim, S. Tozer, P. Mahou, T. Kumamoto, K. Jurkus, P. Rigaud, K. Loulier, N. Dray, P. Georges, M. Hanna, J. Livet, W. Supatto, E. Beaurepaire, and F. Druon, “Dual-color deep-tissue three-photon microscopy with a multiband infrared laser,” Light Sci. Appl. 7, 12 (2018).
[Crossref]

2017 (5)

C. J. Rowlands, D. Park, O. T. Bruns, K. D. Piatkevich, D. Fukumura, R. K. Jain, M. G. Bawendi, E. S. Boyden, and P. T. C. So, “Wide-field three-photon excitation in biological samples,” Light Sci. Appl. 6, e16255 (2017).
[Crossref]

E. P. Perillo, J. W. Jarrett, Y. Liu, A. Hassan, D. C. Fernée, J. R. Goldak, A. Bonteanu, D. J. Spence, H. Yeh, and A. K. Dunn, “Two-color multiphoton in vivo imaging with a femtosecond diamond Raman laser,” Light Sci. Appl. 6, e17095 (2017).
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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, 388–390 (2017).
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X. Tao, H.-H. Lin, T. Lam, R. Rodriguez, J. W. Wang, and J. Kubby, “Transcutical imaging with cellular and subcellular resolution,” Biomed. Opt. Express 8, 1277–1289 (2017).
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M. Kondo, K. Kobayashi, M. Ohkura, J. Nakai, and M. Matsuzaki, “Two-photon calcium imaging of the medial prefrontal cortex and hippocampus without cortical invasion,” Elife 6, 1–20 (2017).
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2016 (7)

G.-A. Pilz, S. Carta, A. Stauble, A. Ayaz, S. Jessberger, and F. Helmchen, “Functional imaging of dentate granule cells in the adult mouse hippocampus,” J. Neurosci. 36, 7407–7414 (2016).
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M. Z. Lin and M. J. Schnitzer, “Genetically encoded indicators of neuronal activity,” Nat. Neurosci. 19, 1142–1153 (2016).
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N. Ji, J. Freeman, and S. L. Smith, “Technologies for imaging neural activity in large volumes,” Nat. Neurosci. 19, 1154–1164 (2016).
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K. Podgorski and G. Ranganathan, “Brain heating induced by near infrared lasers during multi-photon microscopy,” J. Neurophysiol. 116, 1012–1023 (2016).
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N. J. Sofroniew, D. Flickinger, J. King, and K. Svoboda, “A large field of view two-photon mesoscope with subcellular resolution for in vivo imaging,” Elife 5, 1–20 (2016).
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J. N. Stirman, I. T. Smith, M. W. Kudenov, and S. L. Smith, “Wide field-of-view, multi-region, two-photon imaging of neuronal activity in the mammalian brain,” Nat. Biotechnol. 34, 857–862 (2016).
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H. Dana, B. Mohar, Y. Sun, S. Narayan, A. Gordus, J. P. Hasseman, G. Tsegaye, G. T. Holt, A. Hu, D. Walpita, R. Patel, J. J. Macklin, C. I. Bargmann, M. B. Ahrens, E. R. Schreiter, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Sensitive red protein calcium indicators for imaging neural activity,” Elife 5, 1–24 (2016).
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2015 (6)

J. M. Stujenske, T. Spellman, and J. A. Gordon, “Modeling the spatiotemporal dynamics of light and heat propagation for in vivo optogenetics,” Cell Rep. 12, 525–534 (2015).
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D. Sinefeld, H. P. Paudel, D. G. Ouzounov, T. G. Bifano, and C. Xu, “Adaptive optics in multiphoton microscopy: comparison of two, three and four photon fluorescence,” Opt. Express 23, 31472 (2015).
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P. S. Tsai, C. Mateo, J. J. Field, C. B. Schaffer, M. E. Anderson, and D. Kleinfeld, “Ultra-large field-of-view two-photon microscopy,” Opt. Express 23, 13833–13847 (2015).
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K. Wang, R. Liang, and P. Qiu, “Fluorescence signal generation optimization by optimal filling of the high numerical aperture objective lens for high-order deep-tissue multiphoton fluorescence microscopy,” IEEE Photon. J. 7, 2600908 (2015).
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C. Tischbirek, A. Birkner, H. Jia, B. Sakmann, and A. Konnerth, “Deep two-photon brain imaging with a red-shifted fluorometric Ca2+ indicator,” Proc. Natl. Acad. Sci. USA 112, 11377–11382 (2015).
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A. Attardo, J. E. Fitzgerald, and M. J. Schnitzer, “Impermanence of dendritic spines in live adult CA1 hippocampus,” Nature 523, 592–596 (2015).
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2014 (3)

R. J. Low, Y. Gu, and D. W. Tank, “Cellular resolution optical access to brain regions in fissures: imaging medial prefrontal cortex and grid cells in entorhinal cortex,” Proc. Natl. Acad. Sci. USA 111, 18739–18744 (2014).
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L.-C. Cheng, N. G. Horton, K. Wang, S.-J. Chen, and C. Xu, “Measurements of multiphoton action cross sections for multiphoton microscopy,” Biomed. Opt. Express 5, 3427–3433 (2014).
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N. Bosschaart, G. J. Edelman, M. C. G. Aalders, T. G. Van Leeuwen, and D. J. Faber, “A literature review and novel theoretical approach on the optical properties of whole blood,” Laser Med. Sci. 29, 453–479 (2014).
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2013 (4)

S. L. Jacques, “Optical properties of biological tissues: a review,” Phys. Med. Biol. 58, R37–61 (2013).
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B. A. Wilt, J. E. Fitzgerald, and M. J. Schnitzer, “Photon shot noise limits on optical detection of neuronal spikes and estimation of spike timing,” Biophys. J. 104, 51–62 (2013).
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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, 205–209 (2013).
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T.-W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499, 295–300 (2013).
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2012 (2)

A. S. Kalmbach and J. Waters, “Brain surface temperature under a craniotomy,” J. Neurophysiol. 108, 3138–3146 (2012).
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E. J. Botcherby, C. W. Smith, M. M. Kohl, D. Débarre, M. J. Booth, R. Juškaitis, O. Paulsen, and T. Wilson, “Aberration-free three-dimensional multiphoton imaging of neuronal activity at kHz rates,” Proc. Natl. Acad. Sci. USA 109, 2919–2924 (2012).
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2011 (3)

E. E. Hoover, M. D. Young, E. V. Chandler, A. Luo, J. J. Field, K. E. Sheetz, A. W. Sylvester, and J. A. Squier, “Remote focusing for programmable multi-layer differential multiphoton microscopy,” Biomed. Opt. Express 2, 113–122 (2011).
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D. Kobat, N. G. Horton, and C. Xu, “In vivo two-photon microscopy to 1.6-mm depth in mouse cortex.,” J. Biomed. Opt. 16, 106014 (2011).
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N. J. Durr, A. Ben-Yakar, C. T. Weisspfennig, and B. A. Holfeld, “Maximum imaging depth of two-photon autofluorescence microscopy in epithelial tissues,” J. Biomed. Opt. 16, 026008 (2011).
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2010 (2)

D. A. Dombeck, C. D. Harvey, L. Tian, L. L. Looger, and D. W. Tank, “Functional imaging of hippocampal place cells at cellular resolution during virtual navigation,” Nat. Neurosci. 13, 1433–1440 (2010).
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A. Monmayrant, S. Weber, and B. Chatel, “A newcomer’s guide to ultrashort pulse shaping and characterization,” J. Phys. B 43, 103001 (2010).
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2009 (1)

P. S. Tsai, P. Blinder, B. J. Migliori, J. Neev, Y. Jin, J. A. Squier, and D. Klenfeld, “Plasma-mediated ablation: an optical tool for submicrometer surgery on neuronal and vascular systems,” Curr. Opin. Biotechnol. 20, 90–99 (2009).
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2008 (2)

M. E. Durst, G. Zhu, and C. Xu, “Simultaneous spatial and temporal focusing in nonlinear microscopy,” Opt. Commun. 281, 1796–1805 (2008).
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E. J. Botcherby, R. Juškaitis, M. J. Booth, and T. Wilson, “An optical technique for remote focusing in microscopy,” Opt. Commun. 281, 880–887 (2008).
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2006 (1)

2005 (3)

2003 (1)

1999 (1)

H. J. Koester, D. Baur, R. Uhl, and S. W. Hell, “Ca2+ fluorescence imaging with pico- and femtosecond two-photon excitation: signal and photodamage,” Biophys. J. 77, 2226–2236 (1999).
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1997 (3)

K. König, P. T. C. So, W. W. Mantulin, and E. Gratton, “Cellular response to near-infrared femtosecond laser pulses in two-photon microscopes,” Opt. Lett. 22, 135–136 (1997).
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W. Denk and K. Svoboda, “Photon upmanship: why multiphoton imaging is more than a gimmick,” Neuron 18, 351–357 (1997).
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S. Maiti, J. B. Shear, R. M. Williams, W. R. Zipfel, and W. W. Webb, “Measuring serotonin distribution in live cells with three-photon excitation,” Science 275, 530–532 (1997).
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1996 (3)

D. L. Wokosin, V. E. Centonze, S. Crittenden, and J. White, “Three-photon excitation fluorescence imaging of biological specimens using an all-solid-state laser,” Bioimaging 4, 208–214 (1996).
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S. W. Hell, K. Bahlmann, M. Schrader, A. Soini, H. M. Malak, I. Gryczynski, and J. R. Lakowicz, “Three-photon excitation in fluorescence microscopy,” J. Biomed. Opt. 1, 71–74 (1996).
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C. Xu, W. Zipfel, J. B. Shear, R. M. Williams, and W. W. Webb, “Multiphoton fluorescence excitation: new spectral windows for biological nonlinear microscopy,” Proc. Natl. Acad. Sci. USA 93, 10763–10768 (1996).
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1990 (1)

W. Denk, J. H. Strickler, and W. W. Webb, “Two-photon laser scanning fluorescence microscopy,” Science 248, 73–76 (1990).
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1973 (1)

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Abbasi-Asl, R.

K. Takasaki, R. Abbasi-Asl, and J. Waters, “Superficial bound of the depth limit of 2-photon imaging in mouse brain,” eNeuro 7, 271 (2020).
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K. Guesmi, L. Abdeladim, S. Tozer, P. Mahou, T. Kumamoto, K. Jurkus, P. Rigaud, K. Loulier, N. Dray, P. Georges, M. Hanna, J. Livet, W. Supatto, E. Beaurepaire, and F. Druon, “Dual-color deep-tissue three-photon microscopy with a multiband infrared laser,” Light Sci. Appl. 7, 12 (2018).
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H. Dana, B. Mohar, Y. Sun, S. Narayan, A. Gordus, J. P. Hasseman, G. Tsegaye, G. T. Holt, A. Hu, D. Walpita, R. Patel, J. J. Macklin, C. I. Bargmann, M. B. Ahrens, E. R. Schreiter, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Sensitive red protein calcium indicators for imaging neural activity,” Elife 5, 1–24 (2016).
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Anderson, M. E.

Attardo, A.

A. Attardo, J. E. Fitzgerald, and M. J. Schnitzer, “Impermanence of dendritic spines in live adult CA1 hippocampus,” Nature 523, 592–596 (2015).
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Ayaz, A.

G.-A. Pilz, S. Carta, A. Stauble, A. Ayaz, S. Jessberger, and F. Helmchen, “Functional imaging of dentate granule cells in the adult mouse hippocampus,” J. Neurosci. 36, 7407–7414 (2016).
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S. W. Hell, K. Bahlmann, M. Schrader, A. Soini, H. M. Malak, I. Gryczynski, and J. R. Lakowicz, “Three-photon excitation in fluorescence microscopy,” J. Biomed. Opt. 1, 71–74 (1996).
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T.-W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499, 295–300 (2013).
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Bargmann, C. I.

H. Dana, B. Mohar, Y. Sun, S. Narayan, A. Gordus, J. P. Hasseman, G. Tsegaye, G. T. Holt, A. Hu, D. Walpita, R. Patel, J. J. Macklin, C. I. Bargmann, M. B. Ahrens, E. R. Schreiter, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Sensitive red protein calcium indicators for imaging neural activity,” Elife 5, 1–24 (2016).
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Baur, D.

H. J. Koester, D. Baur, R. Uhl, and S. W. Hell, “Ca2+ fluorescence imaging with pico- and femtosecond two-photon excitation: signal and photodamage,” Biophys. J. 77, 2226–2236 (1999).
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D. R. Beaulieu, I. G. Davison, K. Kılıç, T. G. Bifano, and J. Mertz, “Simultaneous multiplane imaging with reverberation two-photon microscopy,” Nat. Methods 17, 283–286 (2020).
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K. Guesmi, L. Abdeladim, S. Tozer, P. Mahou, T. Kumamoto, K. Jurkus, P. Rigaud, K. Loulier, N. Dray, P. Georges, M. Hanna, J. Livet, W. Supatto, E. Beaurepaire, and F. Druon, “Dual-color deep-tissue three-photon microscopy with a multiband infrared laser,” Light Sci. Appl. 7, 12 (2018).
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N. J. Durr, A. Ben-Yakar, C. T. Weisspfennig, and B. A. Holfeld, “Maximum imaging depth of two-photon autofluorescence microscopy in epithelial tissues,” J. Biomed. Opt. 16, 026008 (2011).
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D. R. Beaulieu, I. G. Davison, K. Kılıç, T. G. Bifano, and J. Mertz, “Simultaneous multiplane imaging with reverberation two-photon microscopy,” Nat. Methods 17, 283–286 (2020).
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D. Sinefeld, H. P. Paudel, D. G. Ouzounov, T. G. Bifano, and C. Xu, “Adaptive optics in multiphoton microscopy: comparison of two, three and four photon fluorescence,” Opt. Express 23, 31472 (2015).
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C. Tischbirek, A. Birkner, H. Jia, B. Sakmann, and A. Konnerth, “Deep two-photon brain imaging with a red-shifted fluorometric Ca2+ indicator,” Proc. Natl. Acad. Sci. USA 112, 11377–11382 (2015).
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P. S. Tsai, P. Blinder, B. J. Migliori, J. Neev, Y. Jin, J. A. Squier, and D. Klenfeld, “Plasma-mediated ablation: an optical tool for submicrometer surgery on neuronal and vascular systems,” Curr. Opin. Biotechnol. 20, 90–99 (2009).
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E. P. Perillo, J. W. Jarrett, Y. Liu, A. Hassan, D. C. Fernée, J. R. Goldak, A. Bonteanu, D. J. Spence, H. Yeh, and A. K. Dunn, “Two-color multiphoton in vivo imaging with a femtosecond diamond Raman laser,” Light Sci. Appl. 6, e17095 (2017).
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E. J. Botcherby, C. W. Smith, M. M. Kohl, D. Débarre, M. J. Booth, R. Juškaitis, O. Paulsen, and T. Wilson, “Aberration-free three-dimensional multiphoton imaging of neuronal activity at kHz rates,” Proc. Natl. Acad. Sci. USA 109, 2919–2924 (2012).
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E. J. Botcherby, R. Juškaitis, M. J. Booth, and T. Wilson, “An optical technique for remote focusing in microscopy,” Opt. Commun. 281, 880–887 (2008).
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N. Bosschaart, G. J. Edelman, M. C. G. Aalders, T. G. Van Leeuwen, and D. J. Faber, “A literature review and novel theoretical approach on the optical properties of whole blood,” Laser Med. Sci. 29, 453–479 (2014).
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E. J. Botcherby, C. W. Smith, M. M. Kohl, D. Débarre, M. J. Booth, R. Juškaitis, O. Paulsen, and T. Wilson, “Aberration-free three-dimensional multiphoton imaging of neuronal activity at kHz rates,” Proc. Natl. Acad. Sci. USA 109, 2919–2924 (2012).
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E. J. Botcherby, R. Juškaitis, M. J. Booth, and T. Wilson, “An optical technique for remote focusing in microscopy,” Opt. Commun. 281, 880–887 (2008).
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C. J. Rowlands, D. Park, O. T. Bruns, K. D. Piatkevich, D. Fukumura, R. K. Jain, M. G. Bawendi, E. S. Boyden, and P. T. C. So, “Wide-field three-photon excitation in biological samples,” Light Sci. Appl. 6, e16255 (2017).
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C. J. Rowlands, D. Park, O. T. Bruns, K. D. Piatkevich, D. Fukumura, R. K. Jain, M. G. Bawendi, E. S. Boyden, and P. T. C. So, “Wide-field three-photon excitation in biological samples,” Light Sci. Appl. 6, e16255 (2017).
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Carta, S.

G.-A. Pilz, S. Carta, A. Stauble, A. Ayaz, S. Jessberger, and F. Helmchen, “Functional imaging of dentate granule cells in the adult mouse hippocampus,” J. Neurosci. 36, 7407–7414 (2016).
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D. L. Wokosin, V. E. Centonze, S. Crittenden, and J. White, “Three-photon excitation fluorescence imaging of biological specimens using an all-solid-state laser,” Bioimaging 4, 208–214 (1996).
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Chandler, E. V.

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B. Li, C. Wu, M. Wang, K. Charan, and C. Xu, “An adaptive excitation source for high-speed multiphoton microscopy,” Nat. Methods 17, 163–167 (2020).
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A. Monmayrant, S. Weber, and B. Chatel, “A newcomer’s guide to ultrashort pulse shaping and characterization,” J. Phys. B 43, 103001 (2010).
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Chen, B.

S. Weisenburger, F. Tejera, J. Demas, B. Chen, J. Manley, F. T. Sparks, F. Martínez Traub, T. Daigle, H. Zeng, A. Losonczy, and A. Vaziri, “Volumetric Ca2+ imaging in the mouse brain using hybrid multiplexed sculpted light microscopy,” Cell 177, 1050–1066 (2019).
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B. Chen, X. Huang, D. Gou, J. Zeng, G. Chen, M. Pang, Y. Hu, Z. Zhao, Y. Zhang, Z. Zhou, H. Wu, H. Cheng, Z. Zhang, C. Xu, Y. Li, L. Chen, and A. Wang, “Rapid volumetric imaging with Bessel-Beam three-photon microscopy,” Biomed. Opt. Express 9, 1992–2000 (2018).
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Chen, G.

Chen, L.

Chen, S.-J.

Chen, T.-W.

T.-W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499, 295–300 (2013).
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Chen, Y.

H. Dana, Y. Sun, B. Mohar, B. K. Hulse, A. M. Kerlin, J. P. Hasseman, G. Tsegaye, A. Tsang, A. Wong, R. Patel, J. J. Macklin, Y. Chen, A. Konnerth, V. Jayaraman, L. L. Looger, E. R. Schreiter, K. Svoboda, and D. S. Kim, “High-performance calcium sensors for imaging activity in neuronal populations and microcompartments,” Nat. Methods 16, 649–657 (2019).
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Cheng, H.

H. Liu, X. Deng, S. Tong, C. He, H. Cheng, Z. Zhuang, M. Gan, J. Li, W. Xie, P. Qiu, and K. Wang, “In vivo deep-brain structural and hemodynamic multiphoton microscopy enabled by quantum dots,” Nano Lett. 19, 5260–5265 (2019).
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B. Chen, X. Huang, D. Gou, J. Zeng, G. Chen, M. Pang, Y. Hu, Z. Zhao, Y. Zhang, Z. Zhou, H. Wu, H. Cheng, Z. Zhang, C. Xu, Y. Li, L. Chen, and A. Wang, “Rapid volumetric imaging with Bessel-Beam three-photon microscopy,” Biomed. Opt. Express 9, 1992–2000 (2018).
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Cheng, L.-C.

Cheng, Y.-T.

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, 388–390 (2017).
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Chiang, A.-S.

Chu, S.-W.

Clark, C. G.

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, 205–209 (2013).
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Crittenden, S.

D. L. Wokosin, V. E. Centonze, S. Crittenden, and J. White, “Three-photon excitation fluorescence imaging of biological specimens using an all-solid-state laser,” Bioimaging 4, 208–214 (1996).
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Cruz-Hernández, J. C.

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, 388–390 (2017).
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Daigle, T.

S. Weisenburger, F. Tejera, J. Demas, B. Chen, J. Manley, F. T. Sparks, F. Martínez Traub, T. Daigle, H. Zeng, A. Losonczy, and A. Vaziri, “Volumetric Ca2+ imaging in the mouse brain using hybrid multiplexed sculpted light microscopy,” Cell 177, 1050–1066 (2019).
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Dana, H.

H. Dana, Y. Sun, B. Mohar, B. K. Hulse, A. M. Kerlin, J. P. Hasseman, G. Tsegaye, A. Tsang, A. Wong, R. Patel, J. J. Macklin, Y. Chen, A. Konnerth, V. Jayaraman, L. L. Looger, E. R. Schreiter, K. Svoboda, and D. S. Kim, “High-performance calcium sensors for imaging activity in neuronal populations and microcompartments,” Nat. Methods 16, 649–657 (2019).
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H. Dana, B. Mohar, Y. Sun, S. Narayan, A. Gordus, J. P. Hasseman, G. Tsegaye, G. T. Holt, A. Hu, D. Walpita, R. Patel, J. J. Macklin, C. I. Bargmann, M. B. Ahrens, E. R. Schreiter, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Sensitive red protein calcium indicators for imaging neural activity,” Elife 5, 1–24 (2016).
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Davison, I. G.

D. R. Beaulieu, I. G. Davison, K. Kılıç, T. G. Bifano, and J. Mertz, “Simultaneous multiplane imaging with reverberation two-photon microscopy,” Nat. Methods 17, 283–286 (2020).
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Débarre, D.

E. J. Botcherby, C. W. Smith, M. M. Kohl, D. Débarre, M. J. Booth, R. Juškaitis, O. Paulsen, and T. Wilson, “Aberration-free three-dimensional multiphoton imaging of neuronal activity at kHz rates,” Proc. Natl. Acad. Sci. USA 109, 2919–2924 (2012).
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Demas, J.

S. Weisenburger, F. Tejera, J. Demas, B. Chen, J. Manley, F. T. Sparks, F. Martínez Traub, T. Daigle, H. Zeng, A. Losonczy, and A. Vaziri, “Volumetric Ca2+ imaging in the mouse brain using hybrid multiplexed sculpted light microscopy,” Cell 177, 1050–1066 (2019).
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Deng, X.

H. Liu, X. Deng, S. Tong, C. He, H. Cheng, Z. Zhuang, M. Gan, J. Li, W. Xie, P. Qiu, and K. Wang, “In vivo deep-brain structural and hemodynamic multiphoton microscopy enabled by quantum dots,” Nano Lett. 19, 5260–5265 (2019).
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P. Theer and W. Denk, “On the fundamental imaging-depth limit in two-photon microscopy,” J. Opt. Soc. Am. A 23, 3139–3149 (2006).
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P. Theer, M. T. Hasan, and W. Denk, “Two-photon imaging to a depth of 1000  microm in living brains by use of a Ti:Al2O3 regenerative amplifier,” Opt. Lett. 28, 1022–1024 (2003).
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W. Denk and K. Svoboda, “Photon upmanship: why multiphoton imaging is more than a gimmick,” Neuron 18, 351–357 (1997).
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W. Denk, J. H. Strickler, and W. W. Webb, “Two-photon laser scanning fluorescence microscopy,” Science 248, 73–76 (1990).
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Figures (7)

Fig. 1.
Fig. 1. Cause-and-effect diagram on the imaging properties resulted from the long-wavelength 3PE, in comparison to 2PE of the same fluorophores. The topics are discussed in detail in the subsections indicated in each box.
Fig. 2.
Fig. 2. Wavelength dependence of mouse brain effective attenuation length and its impact on two- and three-photon excitation signal crossover for deep imaging. (A) The theoretical model of the effective attenuation length based on water absorption and Mie scattering. The black triangles indicate the measured effective attenuation lengths in mouse brains in vivo. Reproduced with permission from Ref. [16], 2018, © The Optical Society. (B) Schematic illustration of the signal and $d^{\prime}$ crossover between 2PM and 3PM in the same sample, with the same pulse energy on the sample surface (i.e., the same average power and repetition rate). (C) Measurement data for the signal crossover depth in the mouse brain (top) and the $d^{\prime}$ crossover depth in the presence of background (bottom). Reproduced with permission from Ref. [17], 2020, eLife Sciences Publications.
Fig. 3.
Fig. 3. Background reduction by 3PE. (A) Illustrations of the two types of background encountered by multiphoton imaging in deep tissue or through turbid layers. (B) Demonstration of the bulk background by comparing 920 nm 2PM and 1300 nm 3PM for neuron imaging at the same location in the deep cortical layers (at 780 µm below the brain surface) in a transgenic mouse brain (CamKII- tTA/tetO-GCaMP6s) through a cranial window. Scale bar, 20 µm. Reproduced with permission from Ref. [9], 2017, Springer Nature. (C) Demonstration of the defocus background by comparing 920 nm 2PM and 1320 nm 3PM for neuron imaging at the same location through the intact skull (${\sim}{{150}}\;\unicode{x00B5}{\rm m}$ deep in the brain, with an additional of ${\sim}{{105}}\;\unicode{x00B5}{\rm m}$ skull thickness above the brain surface) in a transgenic mouse (CamKII- tTA/tetO-GCaMP6s). Scale bar, 20 µm. Reproduced with permission from Ref. [10], 2018, Springer Nature. (D) 3PE significantly reduces the side lobes of a Bessel beam compared to 2PE. Reproduced with permission from Ref. [21], 2018, © The Optical Society. (E) Through skull imaging showing 3PE preserves both the lateral and axial resolution, by comparing 2PM and 3PM images with the same excitation wavelength of 1320 nm. The imaging depth in the brain excludes the thickness of the intact skull. Reproduced with permission from Ref. [10], 2018, Springer Nature.
Fig. 4.
Fig. 4. Effects of 3PE wavelength on GCaMP6 performance and brain tissue heating. (A) The wavelength dependence of the sensitivity and brightness of GCaMP6. Reproduced with permission from Ref. [43], 2019, © The Optical Society. Light intensity distribution and brain temperature profile simulated for 920 nm 2PM and 1320 nm 3PM, after 60 s of continuous scanning (sufficient to reach steady states) at the given average power (the bottom left corner of each plot). For 1320 nm, the distinction is made between the average power after the objective lens and at the brain surface (in the bracket), due to the absorption by the immersion water ($\rm H_{2}O$). The absorption by immersion water is negligible at 920 nm, and the power at the brain surface is equal to that after the objective lens. The thickness of the immersion water is calculated as the working distance of the objective (assumed to be 2 mm in these plots) minus the thickness of the cover glass and the imaging depth. (C) The maximum brain temperature as a function of imaging depth and average power, calculated by Monte Carlo simulation for 920, 1320, and 1280 nm. Reproduced with permission from Ref. [17], 2020, eLife Sciences Publications. (D) The power absorbed by the brain tissue (dashed line) and the power dissipated through a 4 mm cranial window (solid lines), simulated for different imaging depth and average power at 920, 1320, and 1280 nm.
Fig. 5.
Fig. 5. Optimization of 3P imaging average power and pulse energy within the limits imposed by brain heating and nonlinear effects. (A) Immunostaining results reveal brain heating effects by 1320 nm 3PM after 20 min continuous scanning with 150 mW average power at 1 mm imaging depth. The power indicated in the figure is the average power after the objective lens (with a 2 mm working distance). (B) Tissue ablation induced by intense excitation pulses at the focus. The plot on the left shows the probability of damage (damaged area/total scanned area) versus pulse energy (40 fs pulse duration, 1.0 NA, focused at 150 µm depth). The plot on the right shows the tissue appearance before and after the ablation. Reproduced with permission from Ref. [11], 2019, Springer Nature. (C) Visualization of 3P imaging optimization in the parameter space formed by the pulse energy at the brain surface and the average repetition rate at two imaging depths in the mouse brain. The green region indicates the combinations of the average power and the repetition rate that are allowed and practical for 3P imaging. The yellow star indicates the optimal parameters that maximize the total 3PE signal at the given imaging depth.
Fig. 6.
Fig. 6. Three-photon neuronal activity imaging as a constrained optimization problem and the procedure to reach the solution.
Fig. 7.
Fig. 7. Strategies for enhancing the imaging volume of 3PM. (A) Illustrations of temporal focusing, Bessel beam, and remote focusing. For temporal focusing, the excitation beam is pseudo-colored to denote the spatial separation of wavelength along the $x$ axis. For remote focusing, two focal depths are illustrated. The focus and the corresponding beam at the objective back aperture are plotted with the same color. (B) In vivo volumetric imaging of neurons in the mouse cortex with a Bessel beam. A depth-resolved stack taken by a Gaussian beam is compared to the same stack acquired by a single-frame scan with a Bessel beam. The maximum intensity projection of both stacks is shown, and the imaging depth in the Gaussian beam stack is color-coded. Reproduced with permission from Ref. [38], 2018, © The Optical Society. (C) High-speed and volumetric 3PM imaging of GCaMP6f-labeled neurons in the mouse hippocampus through the intact cortex. The recording depth was 750–1000 mm, with ${{340}}\;\unicode{x00B5}{\rm m} \times {{340}}\;\unicode{x00B5}{\rm m} \times {{250}}\,\,{\unicode{x00B5}\rm m}$ imaging volume and 3.9 Hz volume rate. Reproduced with permission from Ref. [14], 2019, Elsevier. (D) The working principle of an adaptive excitation source (AES). (E) 1700 nm 3P ${\rm{C}}{{\rm{a}}^{2 +}}$ imaging of jRGECO1a-labeled neurons 750 µm below the brain surface with an AES, taken at ${{620}}\;\unicode{x00B5}{\rm m} \times {{620}}\;\unicode{x00B5}{\rm m}$ FOV at 30 Hz frame rate. Reproduced with permission from Ref. [46], 2020, Springer Nature.

Equations (3)

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d 1 1 + 1 / S B R Δ F F F 0 τ C a 2 ,
2 P E s i g n a l p h o t o n s p e r p u l s e = S 2 P f = 1 2 g p ( 2 ) τ ϕ C ( η σ 2 ) n 0 π λ 2 P ( P 2 P f ) 2 ,
3 P E s i g n a l p h o t o n s p e r p u l s e = S 3 P f = 1 3 g p ( 3 ) τ 2 ϕ C ( η σ 3 ) n 0 2 π 2 3 λ 3 P 3 × ( λ 3 P π w 0 ) 2 ( P 3 P f ) 3 ,

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