Abstract

Three-dimensional fluorescence imaging has been a longstanding goal for microscopists, made all the more challenging when aiming for a trifecta of resolution, speed, and field of view. The purpose of this review is to summarize some current strategies in volumetric microscopy, both camera- and scanning-based.

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

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2019 (7)

B. Yang, X. Chen, Y. Wang, S. Feng, V. Pessino, N. Stuurman, N. H. Cho, K. W. Cheng, S. J. Lord, L. Xu, D. Xie, R. D. Mullins, M. D. Leonetti, and B. Huang, “Epi-illumination SPIM for volumetric imaging with high spatial-temporal resolution,” Nat. Methods 16, 501–504 (2019).
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N. Wagner, N. Norlin, J. Gierten, G. de Medeiros, B. Balázs, J. Wittbrodt, L. Hufnagel, and R. Prevedel, “Instantaneous isotropic volumetric imaging of fast biological processes,” Nat. Methods 16, 497–500 (2019).
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S. Han, W. Yang, and R. Yuste, “Two-color volumetric imaging of neuronal activity of cortical columns,” Cell Rep. 27, 2229–2240 (2019).
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S. Weisenburger, F. Tejera, J. Demas, B. Chen, J. Manley, F. T. Sparks, F. M. 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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H. Li, C. Guo, D. Kim-Holzapfel, W. Li, Y. Altshuller, B. Schroeder, W. Liu, Y. Meng, J. B. French, K.-I. Takamaru, M. A. Frohman, and S. Jia, “Fast, volumetric live-cell imaging using high-resolution light-field microscopy,” Biomed. Opt. Express 10, 29–49 (2019).
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E. Z. Chong, M. Panniello, I. Barreiros, M. M. Kohl, and M. J. Booth, “Quasi-simultaneous multiplane calcium imaging of neuronal circuits,” Biomed. Opt. Express 10, 267–282 (2019).
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A. Badon, S. Bensussen, H. J. Gritton, M. R. Awal, C. V. Gabel, X. Han, and J. Mertz, “Video-rate large-scale imaging with Multi-Z confocal microscopy,” Optica 6, 389–395 (2019).
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2018 (11)

Y. Zhou, P. Zammit, G. Carles, and A. R. Harvey, “Computational localization microscopy with extended axial range,” Opt. Express 26, 7563–7577 (2018).
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W. J. Shain, N. A. Vickers, J. Li, X. Han, T. Bifano, and J. Mertz, “Axial localization with modulated-illumination extended-depth-of-field microscopy,” Biomed. Opt. Express 9, 1771–1782 (2018).
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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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C. Rodríguez, Y. Liang, R. Lu, and N. Ji, “Three-photon fluorescence microscopy with an axially elongated Bessel focus,” Opt. Lett. 43, 1914–1917 (2018).
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K. Charan, B. Li, M. Wang, C. P. Lin, and C. Xu, “Fiber-based tunable repetition rate source for deep tissue two-photon fluorescence microscopy,” Biomed. Opt. Express 9, 2304–2311 (2018).
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M. Kumar, S. Kishore, J. Nasenbeny, D. L. McLean, and Y. Kozorovitskiy, “Integrated one- and two-photon scanned oblique plane illumination (SOPi) microscopy for rapid volumetric imaging,” Opt. Express 26, 13027–13041 (2018).
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S. Li, J. Wu, H. Li, D. Lin, B. Yu, and J. Qu, “Rapid 3D image scanning microscopy with multi-spot excitation and double-helix point spread function detection,” Opt. Express 26, 23585–23593 (2018).
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O. Skocek, T. Nöbauer, L. Weilguny, F. M. Traub, C. N. Xia, M. I. Molodtsov, A. Grama, M. Yamagata, D. Aharoni, D. D. Cox, P. Golshani, and A. Vaziri, “High-speed volumetric imaging of neuronal activity in freely moving rodents,” Nat. Methods 15, 429–432 (2018).
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M. Martínez-Corral and B. Javidi, “Fundamentals of 3D imaging and displays: a tutorial on integral imaging, light-field, and plenoptic systems,” Adv. Opt. Photonics 10, 512–566 (2018).
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Y. Wu and H. Shroff, “Faster, sharper, and deeper: structured illumination microscopy for biological imaging,” Nat. Methods 15, 1011–1019 (2018).
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S. Xiao, H. Tseng, H. Gritton, X. Han, and J. Mertz, “Video-rate volumetric neuronal imaging using 3D targeted illumination,” Sci. Rep. 8, 7921 (2018).
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2017 (10)

L. Cong, Z. Wang, Y. Chai, W. Hang, C. Shang, W. Yang, L. Bai, J. Du, K. Wang, and Q. Wen, “Rapid whole brain imaging of neural activity in freely behaving larval zebrafish (Danio rerio),” eLife 6, e28158 (2017).
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R. Lu, W. Sun, Y. Liang, A. Kerlin, J. Bierfeld, J. D. Seelig, D. E. Wilson, B. Scholl, B. Mohar, M. Tanimoto, M. Koyama, D. Fitzpatrick, M. B. Orger, and N. Ji, “Video-rate volumetric functional imaging of the brain at synaptic resolution,” Nat. Neurosci. 20, 620–628 (2017).
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A. Song, A. S. Charles, S. A. Koay, J. L. Gauthier, S. Y. Thiberge, J. W. Pillow, and D. W. Tank, “Volumetric two-photon imaging of neurons using stereoscopy (vTwINS),” Nat. Methods 14, 420–426 (2017).
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R. M. Power and J. Huisken, “A guide to light-sheet fluorescence microscopy for multiscale imaging,” Nat. Methods 14, 360–373 (2017).
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M. Duocastella, G. Sancataldo, P. Saggau, P. Ramoino, P. Bianchini, and A. Diaspro, “Fast inertia-free volumetric light-sheet microscope,” ACS Photonics 4, 1797–1804 (2017).
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K. M. Dean, P. Roudot, E. S. Welf, T. Pohlkamp, G. Garrelts, J. Herz, and R. Fiolka, “Imaging subcellular dynamics with fast and light-efficient volumetrically parallelized microscopy,” Optica 4, 263–271 (2017).
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W. J. Shain, N. A. Vickers, B. B. Goldberg, T. Bifano, and J. Mertz, “Extended depth-of-field microscopy with a high-speed deformable mirror,” Opt. Lett. 42, 995–998 (2017).
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H.-Y. Liu, J. Zhong, and L. Waller, “Multiplexed phase-space imaging for 3D fluorescence microscopy,” Opt. Express 25, 14986–14995 (2017).
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W. J. Shain, N. A. Vickers, A. Negash, T. Bifano, A. Sentenac, and J. Mertz, “Dual fluorescence-absorption deconvolution applied to extended-depth-of-field microscopy,” Opt. Lett. 42, 4183–4186 (2017).
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C. Roider, R. Piestun, and A. Jesacher, “3D image scanning microscopy with engineered excitation and detection,” Optica 4, 1373–1381 (2017).
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2016 (14)

S. Quirin, N. Vladimirov, C.-T. Yang, D. S. Peterka, R. Yuste, and B. M. Ahrens, “Calcium imaging of neural circuits with extended depth-of-field light-sheet microscopy,” Opt. Lett. 41, 855–858 (2016).
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P. Rupprecht, A. Prendergast, C. Wyart, and R. W. Friedrich, “Remote z-scanning with a macroscopic voice coil motor for fast 3D multiphoton laser scanning microscopy,” Biomed. Opt. Express 7, 1656–1671 (2016).
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N. C. Pégard, H.-Y. Liu, N. Antipa, M. Gerlock, H. Adesnik, and L. Waller, “Compressive light-field microscopy for 3D neural activity recording,” Optica 3, 517–524 (2016).
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C. Roider, R. Heintzmann, R. Piestun, and A. Jesacher, “Deconvolution approach for 3D scanning microscopy with helical phase engineering,” Opt. Express 24, 15456–15467 (2016).
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W. Yang, J. K. Miller, L. Carrillo-Reid, E. Pnevmatikakis, L. Paninski, R. Yuste, and D. S. Peterka, “Simultaneous multi-plane imaging of neural circuits,” Neuron 89, 269–284 (2016).
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Y. Shechtman, L. E. Weiss, A. S. Backer, M. Y. Lee, and W. E. Moerner, “Multicolour localization microscopy by point-spread-function engineering,” Nat. Photonics 10, 590–594 (2016).
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Q. Ma, B. Khademhosseinieh, E. Huang, H. Qian, M. A. Bakowski, E. R. Troemel, and Z. Liu, “Three-dimensional fluorescent microscopy via simultaneous illumination and detection at multiple planes,” Sci. Rep. 6, 31445 (2016).
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J. L. Chen, F. F. Voigt, M. Javadzadeh, R. Krueppel, and F. Helmchen, “Long-range population dynamics of anatomically defined neocortical networks,” eLife 5, e14679 (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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E. A. Pnevmatikakis, D. Soudry, Y. Gao, T. A. Machado, J. Merel, D. Pfau, T. Reardon, Y. Mu, C. Lacefield, W. Yang, M. Ahrens, R. Bruno, T. M. Jessell, D. S. Peterka, R. Yuste, and L. Paninski, “Simultaneous denoising, deconvolution, and demixing of calcium imaging data,” Neuron 89, 285–299 (2016).
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Y. Yang, B. Yao, M. Lei, D. Dan, R. Li, M. Van Horn, X. Chen, Y. Li, and T. Ye, “Two-photon laser scanning stereomicroscopy for fast volumetric imaging,” PLOS ONE 11, e0168885 (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, e14472 (2016).
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R. Prevedel, A. J. Verhoef, A. J. Pernía-Andrade, S. Weisenburger, B. S. Huang, T. Nöbauer, A. Fernández, J. E. Delcour, P. Golshani, A. Baltuska, and A. Vaziri, “Fast volumetric calcium imaging across multiple cortical layers using sculpted light,” Nat. Methods 13, 1021–1028 (2016).
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2015 (11)

Y. Shechtman, L. E. Weiss, A. S. Backer, S. J. Sahl, and W. E. Moerner, “Precise three-dimensional scan-free multiple-particle tracking over large axial ranges with tetrapod point spread functions,” Nano Lett. 15, 4194–4199 (2015).
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L. Kong, J. Tang, J. P. Little, Y. Yu, T. Lämmermann, C. P. Lin, R. N. Germain, and M. Cui, “Continuous volumetric imaging via an optical phase-locked ultrasound lens,” Nat. Methods 12, 759–762 (2015).
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R. Tomer, M. Lovett-Barron, I. Kauvar, A. S. Andalman, V. M. Burns, S. Sankaran, L. Grosenick, M. Broxton, S. Yang, and K. Deisseroth, “SPED light sheet microscopy: fast mapping of biological system structure and function,” Cell 163, 1796–1806 (2015).
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D. Weigel, H. Babovsky, A. Kiessling, and R. Kowarschik, “Widefield microscopy with infinite depth of field and enhanced lateral resolution based on an image inverting interferometer,” Opt. Commun. 342, 102–108 (2015).
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R. K. Chhetri, F. Amat, Y. Wan, B. Höckendorf, W. C. Lemon, and P. J. Keller, “Whole-animal functional and developmental imaging with isotropic spatial resolution,” Nat. Methods 12, 1171–1178 (2015).
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M. B. Bouchard, V. Voleti, C. S. Mendes, C. Lacefield, W. B. Grueber, R. S. Mann, R. M. Bruno, and E. M. C. Hillman, “Swept confocally-aligned planar excitation (SCAPE) microscopy for high-speed volumetric imaging of behaving organisms,” Nat. Photonics 9, 113–119 (2015).
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P. Rupprecht, R. Prevedel, F. Groessl, W. E. Haubensak, and A. Vaziri, “Optimizing and extending light-sculpting microscopy for fast functional imaging in neuroscience,” Biomed. Opt. Express 6, 353–368 (2015).
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H.-Y. Liu, E. Jonas, L. Tian, J. Zhong, B. Recht, and L. Waller, “3D imaging in volumetric scattering media using phase-space measurements,” Opt. Express 23, 14461–14471 (2015).
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O. E. Olarte, J. Andilla, D. Artigas, and P. Loza-Alvarez, “Decoupled illumination detection in light sheet microscopy for fast volumetric imaging,” Optica 2, 702–705 (2015).
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J. Jiang, D. Zhang, S. Walker, C. Gu, Y. Ke, W. H. Yung, and S.-C. Chen, “Fast 3-D temporal focusing microscopy using an electrically tunable lens,” Opt. Express 23, 24362–24368 (2015).
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M. Martínez-Corral, P.-Y. Hsieh, A. Doblas, E. Sánchez-Ortiga, G. Saavedra, and Y.-P. Huang, “Fast axial-scanning widefield microscopy with constant magnification and resolution,” J. Display Technol. 11, 913–920 (2015).
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J.-C. Baritaux, C. R. Chan, J. Li, and J. Mertz, “View synthesis with a partitioned-aperture microscope,” Opt. Lett. 39, 685–688 (2014).
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J. M. Jabbour, B. H. Malik, C. Olsovsky, R. Cuenca, S. Cheng, J. A. Jo, Y.-S. L. Cheng, J. M. Wright, and K. C. Maitland, “Optical axial scanning in confocal microscopy using an electrically tunable lens,” Biomed. Opt. Express 5, 645–652 (2014).
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M. Duocastella, G. Vicidomini, and A. Diaspro, “Simultaneous multiplane confocal microscopy using acoustic tunable lenses,” Opt. Express 22, 19293–19301 (2014).
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P. Zammit, A. R. Harvey, and G. Carles, “Extended depth-of-field imaging and ranging in a snapshot,” Optica 1, 209–216 (2014).
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N. Cohen, S. Yang, A. Andalman, M. Broxton, L. Grosenick, K. Deisseroth, M. Horowitz, and M. Levoy, “Enhancing the performance of the light field microscope using wavefront coding,” Opt. Express 22, 24817–24839 (2014).
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T. Li, S. Ota, J. Kim, Z. J. Wong, Y. Wang, X. Yin, and X. Zhang, “Axial plane optical microscopy,” Sci. Rep. 4, 7253 (2014).
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T. Vettenburg, H. I. C. Dalgarno, J. Nylk, C. Coll-Lladó, D. E. K. Ferrier, T. Čižmár, F. J. Gunn-Moore, and K. Dholakia, “Light-sheet microscopy using an Airy beam,” Nat. Methods 11, 541–544 (2014).
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B.-C. Chen, W. R. Legant, K. Wang, L. Shao, D. E. Milkie, M. W. Davidson, C. Janetopoulos, X. S. Wu, J. A. Hammer, Z. Liu, B. P. English, Y. Mimori-Kiyosue, D. P. Romero, A. T. Ritter, J. Lippincott-Schwartz, L. Fritz-Laylin, R. D. Mullins, D. M. Mitchell, J. N. Bembenek, A.-C. Reymann, R. Böhme, S. W. Grill, J. T. Wang, G. Seydoux, U. S. Tulu, D. P. Kiehart, and E. Betzig, “Lattice light-sheet microscopy: imaging molecules to embryos at high spatiotemporal resolution,” Science 346, 1257998 (2014).
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Y. Shechtman, S. J. Sahl, A. S. Backer, and W. E. Moerner, “Optimal point spread function design for 3D imaging,” Phys. Rev. Lett. 113, 133902 (2014).
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G. Katona, G. Szalay, P. Maák, A. Kaszás, M. Veress, D. Hillier, B. Chiovini, E. S. Vizi, B. Roska, and B. Rózsa, “Fast two-photon in vivo imaging with three-dimensional random-access scanning in large tissue volumes,” Nat. Methods 9, 201–208 (2012).
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C. Yang, K. Shi, M. Zhou, S. Zheng, S. Yin, and Z. Liu, “Z-microscopy for parallel axial imaging with micro mirror array,” Appl. Phys. Lett. 101, 231111 (2012).
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2011 (6)

T. V. Truong, W. Supatto, D. S. Koos, J. M. Choi, and S. E. Fraser, “Deep and fast live imaging with two-photon scanned light-sheet microscopy,” Nat. Methods 8, 757–760 (2011).
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S. Kumar, D. Wilding, M. B. Sikkel, A. R. Lyon, K. T. MacLeod, and C. Dunsby, “Application of oblique plane microscopy to high speed live cell imaging,” Proc. SPIE 8086, 80860V (2011).
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A. Cheng, J. T. Gonçalves, P. Golshani, K. Arisaka, and C. Portera-Cailliau, “Simultaneous two-photon calcium imaging at different depths with spatiotemporal multiplexing,” Nat. Methods 8, 139–142 (2011).
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S. Liu and H. Hua, “Extended depth-of-field microscopic imaging with a variable focus microscope objective,” Opt. Express 19, 353–362 (2011).
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B. F. Grewe, F. F. Voigt, M. van’t Hoff, and F. Helmchen, “Fast two-layer two-photon imaging of neuronal cell populations using an electrically tunable lens,” Biomed. Opt. Express 2, 2035–2046 (2011).
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M. D. Maschio, A. M. D. Stasi, F. Benfenati, and T. Fellin, “Three-dimensional in vivo scanning microscopy with inertia-free focus control,” Opt. Lett. 36, 3503–3505 (2011).
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A. Mermillod-Blondin, E. McLeod, and C. B. Arnold, “High-speed varifocal imaging with a tunable acoustic gradient index of refraction lens,” Opt. Lett. 33, 2146–2148 (2008).
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C. Dunsby, “Optically sectioned imaging by oblique plane microscopy,” Opt. Express 16, 20306–20316 (2008).
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K. Chu, N. George, and W. Chi, “Extending the depth of field through unbalanced optical path difference,” Appl. Opt. 47, 6895–6903 (2008).
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R. G. Duemani, K. Kelleher, R. Fink, and P. Saggau, “Three-dimensional random access multiphoton microscopy for functional imaging of neuronal activity,” Nat. Neurosci. 11, 713–720 (2008).
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Y. Otsu, V. Bormuth, J. Wong, B. Mathieu, G. P. Dugué, A. Feltz, and S. Dieudonné, “Optical monitoring of neuronal activity at high frame rate with a digital random-access multiphoton (RAMP) microscope,” J. Neurosci. Methods 173, 259–270 (2008).
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Figures (8)

Fig. 1.
Fig. 1. By scanning an oblique light sheet (blue), and descanning the resultant fluorescence (green, yellow orange) with the same mechanical scanner, the light sheet and (oblique) focal planes are automatically co-registered with no other moving parts. The stationary intermediate oblique image plane is then projected onto a downstream camera. Reproduced with permission from [18], 2015, Springer Nature. Alternative scan strategies that maintain a fixed light sheet tilt are described in [17,19].
Fig. 2.
Fig. 2. Axially distributed focal planes in the primary image space (conjugate to the sample) are transversely distributed onto a camera plane (final image) with the use of a multi-focus grating (MFG). An additional chromatic correction grating (CDG) and prism assembly compensate for chromatic dispersion, leading to an aberration corrected multi-focus microscope. Reproduced with permission from [29], 2013, Springer Nature.
Fig. 3.
Fig. 3. Objective configuration of an orthogonal-view light field microscope (blue, excitation; green fluorescence detection with microlens arrays not shown). Each view separately leads to poor axial resolution, whereas both views together lead to isotropic resolution (PSF) upon image reconstruction. Adapted with permission from [38], 2019, Springer Nature.
Fig. 4.
Fig. 4. Different masks applied to the illumination pupil of a (swept-beam) light sheet microscope. A, a Gaussian beam at the pupil leads to a Gaussian beam at the sample that, when swept, becomes a light sheet. B, an annular beam at the pupil leads to a Bessel beam light sheet. C, a square lattice at the pupil optimizes the confinement to the central Bessel plane. D, a hexagonal lattice optimizes the overall light sheet axial resolution. Reproduced with permission from [69], 2014, AAAS.
Fig. 5.
Fig. 5. A, scanning a standard Gaussian focus (yellow) in the x–y plane probes structures in a thin optical section, whereas scanning a Bessel focus (orange) in the x–y plane probes structures throughout a 3D volume. B, a Bessel beam can be created by inserting a SLM and mask to achieve annular illumination in the pupil plane of a two-photon microscope. Reproduced with permission from [78], 2017, Springer Nature.
Fig. 6.
Fig. 6. Multi-Z confocal imaging can be achieved by underfilling the illumination pupil while utilizing the full detection pupil and detecting the resultant fluorescence with a series of axially distributed reflecting pinholes. Here, four optically sectioned are acquired simultaneously. More can be acquired sequentially with the addition of an ETL. Adapted with permission from [90], 2019, OSA.
Fig. 7.
Fig. 7. Schematic of a hybrid microscope that provides simultaneous two- (red) and three- (blue) photon excitation, using a custom-built laser. Resulting fluorescence is in green. This microscope includes a time multiplexing module for near-instantaneous four-plane two-photon imaging, a temporal focusing module to tailor the spatial resolution for video-rate scanning, and a remote focusing module for axial scanning of the four-plane stack. Reproduced with permission from [111], 2019, Elsevier.
Fig. 8.
Fig. 8. Arbitrary number of focal planes can be near-instantaneously captured by inserting a reverberation loop in the excitation beam of a multi-photon microscope [112]. A lens (or equivalent) in the loop causes each subsequent beamlet to focus to increasingly shallower depths all the way to the sample surface. With a 50:50 loop beam splitter, half the laser power targets the deepest plane and the other half targets all the other planes, while producing roughly equal fluorescence power per plane.