Abstract

Optical wavefront shaping is a powerful technique to control the distribution of light in the focus of a microscope. This ability, combined with optogenetics, holds great promise for precise manipulation of neuronal activity with light. However, a deeper understanding of complex brain circuits requires pushing light-shaping methods into a new regime: the simultaneous excitation of several tens of targets, arbitrarily distributed in the three dimensions, with single-cell resolution. To this end, we developed a new optical scheme, based on the spatio-temporal shaping of a pulsed laser beam, to project several tens of spatially confined two-photon excitation patterns in a large volume. Compatibility with several different phase-shaping strategies allows the system to be optimized towards flexibility, simplicity, or multiple independent light manipulations, thus providing new routes for precise three-dimensional optogenetics. To validate the method, we performed multi-cell volumetric excitation of photoactivatable GCaMP in the central nervous system of drosophila larvae, a challenging structure with densely arrayed neurons, and photoconversion of the fluorescent protein Kaede in zebrafish larvae.

© 2018 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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References

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2018 (5)

W. Yang, L. Carrillo-Reid, Y. Bando, D. S. Peterka, and R. Yuste, “Simultaneous two-photon imaging and two-photon optogenetics of cortical circuits in three dimensions,” eLife 7, e32671 (2018).
[Crossref]

E. Papagiakoumou, E. Ronzitti, I.-W. Chen, M. Gajowa, A. Picot, and V. Emiliani, “Two-photon optogenetics by computer-generated holography,” Neuromethods 133, 175–197 (2018).
[Crossref]

B. Sun, P. S. Salter, C. Roider, A. Jesacher, J. Strauss, J. Heberle, M. Schmidt, and M. J. Booth, “Four-dimensional light shaping: manipulating ultrafast spatio-temporal foci in space and time,” Light Sci. Appl. 7, 17117 (2018).
[Crossref]

A. R. Mardinly, I. A. Oldenburg, N. C. Pégard, S. Sridharan, E. H. Lyall, K. Chesnov, S. G. Brohawn, L. Waller, and H. Adesnik, “Precise multimodal optical control of neural ensemble activity,” Nat. Neurosci. 21, 881–893 (2018).
[Crossref]

I. Chen, E. Papagiakoumou, and V. Emiliani, “Towards circuit optogenetics,” Curr. Opin. Neurobiol. 50, 179–189 (2018).
[Crossref]

2017 (6)

N. M. Pégard, I. Oldenburg, S. Sridharan, L. Walller, and H. Adesnik, “3D scanless holographic optogenetics with temporal focusing,” Nat. Commun. 8, 1228 (2017).
[Crossref]

O. A. Shemesh, D. Tanese, V. Zampini, C. Linghu, K. Piatkevich, E. Ronzitti, E. Papagiakoumou, E. S. Boyden, and V. Emiliani, “Temporally precise single-cell resolution optogenetics,” Nat. Neurosci. 20, 1796–1806 (2017).
[Crossref]

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).
[Crossref]

A. Bañas and J. Glückstad, “Holo-GPC: holographic generalized phase contrast,” Opt. Commun. 392, 190–195 (2017).
[Crossref]

E. Ronzitti, C. Ventalon, M. Canepari, B. C. Forget, E. Papagiakoumou, and V. Emiliani, “Recent advances in patterned photostimulation for optogenetics,” J. Opt. 19, 113001 (2017).
[Crossref]

E. Ronzitti, R. Conti, V. Zampini, D. Tanese, A. J. Foust, N. Klapoetke, E. S. Boyden, E. Papagiakoumou, and V. Emiliani, “Sub-millisecond optogenetic control of neuronal firing with two-photon holographic photoactivation of Chronos,” J. Neurosci. 37, 10679–10689 (2017).
[Crossref]

2016 (8)

E. Chaigneau, E. Ronzitti, A. M. Gajowa, J. G. Soler-Llavina, D. Tanese, Y. B. A. Brureau, E. Papagiakoumou, H. Zeng, and V. Emiliani, “Two-photon holographic stimulation of ReaChR,” Front. Cell. Neurosci. 10, 234 (2016).
[Crossref]

O. Hernandez, E. Papagiakoumou, D. Tanesee, K. Fidelin, C. Wyart, and V. Emiliani, “Three-dimensional spatiotemporal focusing of holographic patterns,” Nat. Commun. 7, 11928 (2016).
[Crossref]

L. Carrillo-reid, W. Yang, Y. Bando, D. S. Peterka, and R. Yuste, “Imprinting and recalling cortical ensembles,” Science 353, 691–694 (2016).
[Crossref]

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).
[Crossref]

N. Ji, J. Freeman, and S. L. Smith, “Technologies for imaging neural activity in large volumes,” Nat. Neurosci. 19, 1154–1164 (2016).
[Crossref]

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).
[Crossref]

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).
[Crossref]

R. Conti, O. Assayag, V. De Sars, M. Guillon, and V. Emiliani, “Computer generated holography with intensity-graded patterns,” Front. Cell. Neurosci. 10, 236 (2016).
[Crossref]

2015 (4)

S. J. Yang, W. E. Allen, I. Kauvar, A. S. Andalman, N. P. Young, C. K. Kim, J. H. Marshel, G. Wetzstein, and K. Deisseroth, “Extended field-of-view and increased-signal 3D holographic illumination with time-division multiplexing,” Opt. Express 23, 32573–32581 (2015).
[Crossref]

K. Deisseroth, “Optogenetics : 10 years of microbial opsins in neuroscience,” Nat. Neurosci. 18, 1213–1225 (2015).
[Crossref]

A. M. Packer, L. E. Russell, H. W. P. Dalgleish, and M. Häusser, “Simultaneous all-optical manipulation and recording of neural circuit activity with cellular resolution in vivo,” Nat. Methods 12, 140–146 (2015).
[Crossref]

S. Berlin, E. C. Carroll, Z. L. Newman, H. O. Okada, C. M. Quinn, B. Kallman, N. C. Rockwell, S. S. Martin, J. C. Lagarias, and E. Y. Isacoff, “Photoactivatable genetically encoded calcium indicators for targeted neuronal imaging,” Nat. Methods 12, 852–858 (2015).
[Crossref]

2014 (5)

2013 (3)

A. Bègue, E. Papagiakoumou, B. Leshem, R. Conti, L. Enke, D. Oron, and V. Emiliani, “Two-photon excitation in scattering media by spatiotemporally shaped beams and their application in optogenetic stimulation,” Biomed. Opt. Express 4, 2869–2879 (2013).
[Crossref]

G. Sela, H. Dana, and S. Shoham, “Ultra-deep penetration of temporally-focused two-photon excitation,” Proc. SPIE 8588, 858824 (2013).
[Crossref]

E. Papagiakoumou, A. Bègue, B. Leshem, O. Schwartz, B. M. Stell, J. Bradley, D. Oron, and V. Emiliani, “Functional patterned multiphoton excitation deep inside scattering tissue,” Nat. Photonics 7, 274–278 (2013).
[Crossref]

2012 (3)

A. M. Packer, D. S. Peterka, J. J. Hirtz, R. Prakash, K. Deisseroth, R. Yuste, O. Yizhar, B. Grewe, C. Ramakrishnan, N. Wang, I. Goshen, A. M. Packer, D. S. Peterka, R. Yuste, M. J. Schnitzer, and K. Deisseroth, “Two-photon optogenetics of dendritic spines and neural circuits,” Nat. Methods 9, 1202–1205 (2012).
[Crossref]

R. Prakash, O. Yizhar, B. Grewe, C. Ramakrishnan, N. Wang, I. Goshen, A. M. Packer, D. S. Peterka, R. Yuste, M. J. Schnitzer, and K. Deisseroth, “Two-photon optogenetic toolbox for fast inhibition, excitation and bistable modulation,” Nat. Methods 9, 1171–1179 (2012).
[Crossref]

F. Burmeister, S. Steenhusen, R. Houbertz, U. D. Zeitner, S. Nolte, and A. Tünnermann, “Materials and technologies for fabrication of three-dimensional microstructures with sub-100 nm feature sizes by two-photon polymerization,” J. Laser Appl. 24, 042014 (2012).
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2011 (5)

L. Kelemen, P. Ormos, and G. Vizsnyiczai, “Two-photon polymerization with optimized spatial light modulator,” J. Eur. Opt. Soc. 6, 11029 (2011).
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M. A. Go, P.-F. Ng, H. A. Bachor, and V. R. Daria, “Optimal complex field holographic projection,” Opt. Lett. 36, 3073–3075 (2011).
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S. Yang, E. Papagiakoumou, M. Guillon, V. de Sars, C. M. Tang, and V. Emiliani, “Three-dimensional holographic photostimulation of the dendritic arbor,” J. Neural Eng. 8, 046002 (2011).
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F. Anselmi, C. Ventalon, A. Begue, D. Ogden, V. Emiliani, A. Bègue, D. Ogden, and V. Emiliani, “Three-dimensional imaging and photostimulation by remote-focusing and holographic light patterning,” Proc. Natl. Acad. Sci. USA 108, 19504–19509 (2011).
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K. Deisseroth, “Optogenetics,” Nat. Methods 8, 26–29 (2011).
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2010 (4)

B. K. Andrasfalvy, B. V. Zemelman, J. Tang, and A. Vaziri, “Two-photon single-cell optogenetic control of neuronal activity by sculpted light,” Proc. Natl. Acad. Sci. USA 107, 11981–11986 (2010).

E. Papagiakoumou, F. Anselmi, A. Bègue, V. de Sars, J. Glückstad, E. Y. Isacoff, and V. Emiliani, “Scanless two-photon excitation of channelrhodopsin-2,” Nat. Methods 7, 848–854 (2010).
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A. Jesacher and M. J. Booth, “Parallel direct laser writing in three dimensions with spatially dependent aberration correction,” Opt. Express 18, 21090–21099 (2010).
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K. Isobe, H. Hashimoto, A. Suda, F. Kannari, H. Kawano, H. Mizuno, A. Miyawaki, and K. Midorikawa, “Measurement of two-photon excitation spectrum used to photoconvert a fluorescent protein (Kaede) by nonlinear Fourier-transform spectroscopy,” Biomed. Opt. Express 1, 687–693 (2010).
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2009 (2)

V. R. Daria, C. Stricker, R. Bowman, S. Redman, and H. A. Bachor, “Arbitrary multisite two-photon excitation in four dimensions,” Appl. Phys. Lett. 95, 093701 (2009).
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J. P. Rickgauer and D. W. Tank, “Two-photon excitation of channelrhodopsin-2 at saturation,” Proc. Natl. Acad. Sci. USA 106, 15025–15030 (2009).

2008 (4)

M. Tomura, N. Yoshida, J. Tanaka, S. Karasawa, Y. Miwa, A. Miyawaki, and O. Kanagawa, “Monitoring cellular movement in vivo with photoconvertible fluorescence protein “Kaede” transgenic mice,” Proc. Natl. Acad. Sci. USA 105, 10871–10876 (2008).

C. Lutz, T. S. Otis, V. DeSars, S. Charpak, D. A. Digregorio, and V. Emiliani, “Holographic photolysis of caged neurotransmitters,” Nat. Methods 5, 821–827 (2008).
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V. Nikolenko, B. O. Watson, R. Araya, A. Woodruff, D. S. Peterka, and R. Yuste, “SLM microscopy: scanless two-photon imaging and photostimulation with spatial light modulators,” Front. Neural Circuits 2, 5 (2008).
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E. Papagiakoumou, V. de Sars, D. Oron, and V. Emiliani, “Patterned two-photon illumination by spatiotemporal shaping of ultrashort pulses,” Opt. Express 16, 22039–22047 (2008).
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2007 (3)

2006 (1)

2005 (3)

2003 (1)

D. M. Chudakov, V. V. Belousov, A. G. Zaraisky, V. V. Novoselov, D. B. Staroverov, D. B. Zorov, S. Lukyanov, and K. A. Lukyanov, “Kindling fluorescent proteins for precise in vivo photolabeling,” Nat. Biotechnol. 21, 191–194 (2003).
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2002 (4)

G. H. Patterson and J. Lippincott-Schwartz, “A photoactivatable GFP for selective photolabeling of proteins and cells,” Science 297, 1873–1877 (2002).
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R. Ando, H. Hama, M. Yamamoto-Hino, H. Mizuno, and A. Miyawaki, “An optical marker based on the UV-induced green-to-red photoconversion of a fluorescent protein,” Proc. Natl. Acad. Sci. USA 99, 12651–12656 (2002).

H. Aberle, A. P. Haghighi, R. D. Fetter, B. D. McCabe, T. R. Magalhães, and C. S. Goodman, “Wishful thinking encodes a BMP type II receptor that regulates synaptic growth in Drosophila,” Neuron 33, 545–558 (2002).
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J. E. Curtis, B. A. Koss, and D. G. Grier, “Dynamic holographic optical tweezers,” Opt. Commun. 207, 169–175 (2002).
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2001 (1)

A. Hopt and E. Neher, “Highly nonlinear photodamage in two-photon fluorescence microscopy,” Biophys. J. 80, 2029–2036 (2001).
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2000 (1)

A. M. Weiner, “Femtosecond pulse shaping using spatial light modulators,” Rev. Sci. Instrum. 71, 1929–1960 (2000).
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1996 (1)

J. Glückstad, “Phase contrast image synthesis,” Opt. Commun. 130, 225–230 (1996).
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1972 (1)

R. W. Gerchberg and W. O. Saxton, “A practical algorithm for the determination of the phase from image and diffraction pictures,” Optik 35, 237–246 (1972).

Aabo, T.

Aberle, H.

H. Aberle, A. P. Haghighi, R. D. Fetter, B. D. McCabe, T. R. Magalhães, and C. S. Goodman, “Wishful thinking encodes a BMP type II receptor that regulates synaptic growth in Drosophila,” Neuron 33, 545–558 (2002).
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Adesnik, H.

A. R. Mardinly, I. A. Oldenburg, N. C. Pégard, S. Sridharan, E. H. Lyall, K. Chesnov, S. G. Brohawn, L. Waller, and H. Adesnik, “Precise multimodal optical control of neural ensemble activity,” Nat. Neurosci. 21, 881–893 (2018).
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N. M. Pégard, I. Oldenburg, S. Sridharan, L. Walller, and H. Adesnik, “3D scanless holographic optogenetics with temporal focusing,” Nat. Commun. 8, 1228 (2017).
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P. Nicolas, A. Mardinly, I. Oldenburg, L. Waller, and H. Adesnik, “Partially coherent holographic temporal focusing for 3D light sculpting with single neuron resolution,” in Optics and the Brain (Optical Society of America, 2018) paper BW2C.2.

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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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R. Ando, H. Hama, M. Yamamoto-Hino, H. Mizuno, and A. Miyawaki, “An optical marker based on the UV-induced green-to-red photoconversion of a fluorescent protein,” Proc. Natl. Acad. Sci. USA 99, 12651–12656 (2002).

Andrasfalvy, B. K.

B. K. Andrasfalvy, B. V. Zemelman, J. Tang, and A. Vaziri, “Two-photon single-cell optogenetic control of neuronal activity by sculpted light,” Proc. Natl. Acad. Sci. USA 107, 11981–11986 (2010).

Anselmi, F.

F. Anselmi, C. Ventalon, A. Begue, D. Ogden, V. Emiliani, A. Bègue, D. Ogden, and V. Emiliani, “Three-dimensional imaging and photostimulation by remote-focusing and holographic light patterning,” Proc. Natl. Acad. Sci. USA 108, 19504–19509 (2011).
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E. Papagiakoumou, F. Anselmi, A. Bègue, V. de Sars, J. Glückstad, E. Y. Isacoff, and V. Emiliani, “Scanless two-photon excitation of channelrhodopsin-2,” Nat. Methods 7, 848–854 (2010).
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Araya, R.

V. Nikolenko, B. O. Watson, R. Araya, A. Woodruff, D. S. Peterka, and R. Yuste, “SLM microscopy: scanless two-photon imaging and photostimulation with spatial light modulators,” Front. Neural Circuits 2, 5 (2008).
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R. Conti, O. Assayag, V. De Sars, M. Guillon, and V. Emiliani, “Computer generated holography with intensity-graded patterns,” Front. Cell. Neurosci. 10, 236 (2016).
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M. A. Go, P.-F. Ng, H. A. Bachor, and V. R. Daria, “Optimal complex field holographic projection,” Opt. Lett. 36, 3073–3075 (2011).
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V. R. Daria, C. Stricker, R. Bowman, S. Redman, and H. A. Bachor, “Arbitrary multisite two-photon excitation in four dimensions,” Appl. Phys. Lett. 95, 093701 (2009).
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Baier, H.

M. dal Maschio, J. C. Donovan, T. O. Helmbrecht, and H. Baier, “Linking neurons to network function and behavior by two-photon holographic optogenetics and volumetric imaging,” Neuron94, 774–789.e5 (2017).
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W. Yang, L. Carrillo-Reid, Y. Bando, D. S. Peterka, and R. Yuste, “Simultaneous two-photon imaging and two-photon optogenetics of cortical circuits in three dimensions,” eLife 7, e32671 (2018).
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L. Carrillo-reid, W. Yang, Y. Bando, D. S. Peterka, and R. Yuste, “Imprinting and recalling cortical ensembles,” Science 353, 691–694 (2016).
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F. Anselmi, C. Ventalon, A. Begue, D. Ogden, V. Emiliani, A. Bègue, D. Ogden, and V. Emiliani, “Three-dimensional imaging and photostimulation by remote-focusing and holographic light patterning,” Proc. Natl. Acad. Sci. USA 108, 19504–19509 (2011).
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Bègue, A.

E. Papagiakoumou, A. Bègue, B. Leshem, O. Schwartz, B. M. Stell, J. Bradley, D. Oron, and V. Emiliani, “Functional patterned multiphoton excitation deep inside scattering tissue,” Nat. Photonics 7, 274–278 (2013).
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A. Bègue, E. Papagiakoumou, B. Leshem, R. Conti, L. Enke, D. Oron, and V. Emiliani, “Two-photon excitation in scattering media by spatiotemporally shaped beams and their application in optogenetic stimulation,” Biomed. Opt. Express 4, 2869–2879 (2013).
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F. Anselmi, C. Ventalon, A. Begue, D. Ogden, V. Emiliani, A. Bègue, D. Ogden, and V. Emiliani, “Three-dimensional imaging and photostimulation by remote-focusing and holographic light patterning,” Proc. Natl. Acad. Sci. USA 108, 19504–19509 (2011).
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E. Papagiakoumou, F. Anselmi, A. Bègue, V. de Sars, J. Glückstad, E. Y. Isacoff, and V. Emiliani, “Scanless two-photon excitation of channelrhodopsin-2,” Nat. Methods 7, 848–854 (2010).
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Belousov, V. V.

D. M. Chudakov, V. V. Belousov, A. G. Zaraisky, V. V. Novoselov, D. B. Staroverov, D. B. Zorov, S. Lukyanov, and K. A. Lukyanov, “Kindling fluorescent proteins for precise in vivo photolabeling,” Nat. Biotechnol. 21, 191–194 (2003).
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S. Berlin, E. C. Carroll, Z. L. Newman, H. O. Okada, C. M. Quinn, B. Kallman, N. C. Rockwell, S. S. Martin, J. C. Lagarias, and E. Y. Isacoff, “Photoactivatable genetically encoded calcium indicators for targeted neuronal imaging,” Nat. Methods 12, 852–858 (2015).
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Berto, P.

A. Picot, S. Dominguez, C. Liu, I. W. Chen, D. Tanese, E. Ronzitti, P. Berto, E. Papagiakoumou, D. Oron, G. Tessier, B. C. Forget, and V. Emiliani, “Temperature rise under two-photon optogenetic brain stimulation,” Cell Rep.24, 1243–1253.e5 (2018).
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Booth, M. J.

Bowman, R.

V. R. Daria, C. Stricker, R. Bowman, S. Redman, and H. A. Bachor, “Arbitrary multisite two-photon excitation in four dimensions,” Appl. Phys. Lett. 95, 093701 (2009).
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E. Ronzitti, R. Conti, V. Zampini, D. Tanese, A. J. Foust, N. Klapoetke, E. S. Boyden, E. Papagiakoumou, and V. Emiliani, “Sub-millisecond optogenetic control of neuronal firing with two-photon holographic photoactivation of Chronos,” J. Neurosci. 37, 10679–10689 (2017).
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O. A. Shemesh, D. Tanese, V. Zampini, C. Linghu, K. Piatkevich, E. Ronzitti, E. Papagiakoumou, E. S. Boyden, and V. Emiliani, “Temporally precise single-cell resolution optogenetics,” Nat. Neurosci. 20, 1796–1806 (2017).
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Bradley, J.

E. Papagiakoumou, A. Bègue, B. Leshem, O. Schwartz, B. M. Stell, J. Bradley, D. Oron, and V. Emiliani, “Functional patterned multiphoton excitation deep inside scattering tissue,” Nat. Photonics 7, 274–278 (2013).
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Brohawn, S. G.

A. R. Mardinly, I. A. Oldenburg, N. C. Pégard, S. Sridharan, E. H. Lyall, K. Chesnov, S. G. Brohawn, L. Waller, and H. Adesnik, “Precise multimodal optical control of neural ensemble activity,” Nat. Neurosci. 21, 881–893 (2018).
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Bruno, R.

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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Brureau, Y. B. A.

E. Chaigneau, E. Ronzitti, A. M. Gajowa, J. G. Soler-Llavina, D. Tanese, Y. B. A. Brureau, E. Papagiakoumou, H. Zeng, and V. Emiliani, “Two-photon holographic stimulation of ReaChR,” Front. Cell. Neurosci. 10, 234 (2016).
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Burmeister, F.

F. Burmeister, S. Steenhusen, R. Houbertz, U. D. Zeitner, S. Nolte, and A. Tünnermann, “Materials and technologies for fabrication of three-dimensional microstructures with sub-100 nm feature sizes by two-photon polymerization,” J. Laser Appl. 24, 042014 (2012).
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Canepari, M.

E. Ronzitti, C. Ventalon, M. Canepari, B. C. Forget, E. Papagiakoumou, and V. Emiliani, “Recent advances in patterned photostimulation for optogenetics,” J. Opt. 19, 113001 (2017).
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Carrillo-Reid, L.

W. Yang, L. Carrillo-Reid, Y. Bando, D. S. Peterka, and R. Yuste, “Simultaneous two-photon imaging and two-photon optogenetics of cortical circuits in three dimensions,” eLife 7, e32671 (2018).
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L. Carrillo-reid, W. Yang, Y. Bando, D. S. Peterka, and R. Yuste, “Imprinting and recalling cortical ensembles,” Science 353, 691–694 (2016).
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Carroll, E. C.

S. Berlin, E. C. Carroll, Z. L. Newman, H. O. Okada, C. M. Quinn, B. Kallman, N. C. Rockwell, S. S. Martin, J. C. Lagarias, and E. Y. Isacoff, “Photoactivatable genetically encoded calcium indicators for targeted neuronal imaging,” Nat. Methods 12, 852–858 (2015).
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Chaigneau, E.

E. Chaigneau, E. Ronzitti, A. M. Gajowa, J. G. Soler-Llavina, D. Tanese, Y. B. A. Brureau, E. Papagiakoumou, H. Zeng, and V. Emiliani, “Two-photon holographic stimulation of ReaChR,” Front. Cell. Neurosci. 10, 234 (2016).
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Charles, A. S.

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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Charpak, S.

C. Lutz, T. S. Otis, V. DeSars, S. Charpak, D. A. Digregorio, and V. Emiliani, “Holographic photolysis of caged neurotransmitters,” Nat. Methods 5, 821–827 (2008).
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I. Chen, E. Papagiakoumou, and V. Emiliani, “Towards circuit optogenetics,” Curr. Opin. Neurobiol. 50, 179–189 (2018).
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Chen, I. W.

A. Picot, S. Dominguez, C. Liu, I. W. Chen, D. Tanese, E. Ronzitti, P. Berto, E. Papagiakoumou, D. Oron, G. Tessier, B. C. Forget, and V. Emiliani, “Temperature rise under two-photon optogenetic brain stimulation,” Cell Rep.24, 1243–1253.e5 (2018).
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Chen, I.-W.

E. Papagiakoumou, E. Ronzitti, I.-W. Chen, M. Gajowa, A. Picot, and V. Emiliani, “Two-photon optogenetics by computer-generated holography,” Neuromethods 133, 175–197 (2018).
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I.-W. Chen, E. Ronzitti, R. B. Lee, L. T. Daigle, H. Zeng, E. Papagiakoumou, and V. Emiliani, “Parallel holographic illumination enables sub-millisecond two-photon optogenetic activation in mouse visual cortex in vivo,” bioRxiv (2017), pp. 1–21.

Chesnov, K.

A. R. Mardinly, I. A. Oldenburg, N. C. Pégard, S. Sridharan, E. H. Lyall, K. Chesnov, S. G. Brohawn, L. Waller, and H. Adesnik, “Precise multimodal optical control of neural ensemble activity,” Nat. Neurosci. 21, 881–893 (2018).
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Chudakov, D. M.

D. M. Chudakov, V. V. Belousov, A. G. Zaraisky, V. V. Novoselov, D. B. Staroverov, D. B. Zorov, S. Lukyanov, and K. A. Lukyanov, “Kindling fluorescent proteins for precise in vivo photolabeling,” Nat. Biotechnol. 21, 191–194 (2003).
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Conti, R.

E. Ronzitti, R. Conti, V. Zampini, D. Tanese, A. J. Foust, N. Klapoetke, E. S. Boyden, E. Papagiakoumou, and V. Emiliani, “Sub-millisecond optogenetic control of neuronal firing with two-photon holographic photoactivation of Chronos,” J. Neurosci. 37, 10679–10689 (2017).
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R. Conti, O. Assayag, V. De Sars, M. Guillon, and V. Emiliani, “Computer generated holography with intensity-graded patterns,” Front. Cell. Neurosci. 10, 236 (2016).
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A. Bègue, E. Papagiakoumou, B. Leshem, R. Conti, L. Enke, D. Oron, and V. Emiliani, “Two-photon excitation in scattering media by spatiotemporally shaped beams and their application in optogenetic stimulation,” Biomed. Opt. Express 4, 2869–2879 (2013).
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Cooper, J.

Courtial, J.

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C. H. J. Schmitz, J. P. Spatz, and J. E. Curtis, “High-precision steering of multiple holographic optical traps,” Opt. Express 13, 8678–8685 (2005).
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J. E. Curtis, B. A. Koss, and D. G. Grier, “Dynamic holographic optical tweezers,” Opt. Commun. 207, 169–175 (2002).
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I.-W. Chen, E. Ronzitti, R. B. Lee, L. T. Daigle, H. Zeng, E. Papagiakoumou, and V. Emiliani, “Parallel holographic illumination enables sub-millisecond two-photon optogenetic activation in mouse visual cortex in vivo,” bioRxiv (2017), pp. 1–21.

dal Maschio, M.

M. dal Maschio, J. C. Donovan, T. O. Helmbrecht, and H. Baier, “Linking neurons to network function and behavior by two-photon holographic optogenetics and volumetric imaging,” Neuron94, 774–789.e5 (2017).
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A. M. Packer, L. E. Russell, H. W. P. Dalgleish, and M. Häusser, “Simultaneous all-optical manipulation and recording of neural circuit activity with cellular resolution in vivo,” Nat. Methods 12, 140–146 (2015).
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G. Sela, H. Dana, and S. Shoham, “Ultra-deep penetration of temporally-focused two-photon excitation,” Proc. SPIE 8588, 858824 (2013).
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De Sars, V.

R. Conti, O. Assayag, V. De Sars, M. Guillon, and V. Emiliani, “Computer generated holography with intensity-graded patterns,” Front. Cell. Neurosci. 10, 236 (2016).
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S. Yang, E. Papagiakoumou, M. Guillon, V. de Sars, C. M. Tang, and V. Emiliani, “Three-dimensional holographic photostimulation of the dendritic arbor,” J. Neural Eng. 8, 046002 (2011).
[Crossref]

E. Papagiakoumou, F. Anselmi, A. Bègue, V. de Sars, J. Glückstad, E. Y. Isacoff, and V. Emiliani, “Scanless two-photon excitation of channelrhodopsin-2,” Nat. Methods 7, 848–854 (2010).
[Crossref]

E. Papagiakoumou, V. de Sars, D. Oron, and V. Emiliani, “Patterned two-photon illumination by spatiotemporal shaping of ultrashort pulses,” Opt. Express 16, 22039–22047 (2008).
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Deisseroth, K.

S. J. Yang, W. E. Allen, I. Kauvar, A. S. Andalman, N. P. Young, C. K. Kim, J. H. Marshel, G. Wetzstein, and K. Deisseroth, “Extended field-of-view and increased-signal 3D holographic illumination with time-division multiplexing,” Opt. Express 23, 32573–32581 (2015).
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R. Prakash, O. Yizhar, B. Grewe, C. Ramakrishnan, N. Wang, I. Goshen, A. M. Packer, D. S. Peterka, R. Yuste, M. J. Schnitzer, and K. Deisseroth, “Two-photon optogenetic toolbox for fast inhibition, excitation and bistable modulation,” Nat. Methods 9, 1171–1179 (2012).
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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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DeSars, V.

C. Lutz, T. S. Otis, V. DeSars, S. Charpak, D. A. Digregorio, and V. Emiliani, “Holographic photolysis of caged neurotransmitters,” Nat. Methods 5, 821–827 (2008).
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Di Leonardo, R.

Digregorio, D. A.

C. Lutz, T. S. Otis, V. DeSars, S. Charpak, D. A. Digregorio, and V. Emiliani, “Holographic photolysis of caged neurotransmitters,” Nat. Methods 5, 821–827 (2008).
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A. Picot, S. Dominguez, C. Liu, I. W. Chen, D. Tanese, E. Ronzitti, P. Berto, E. Papagiakoumou, D. Oron, G. Tessier, B. C. Forget, and V. Emiliani, “Temperature rise under two-photon optogenetic brain stimulation,” Cell Rep.24, 1243–1253.e5 (2018).
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Zeng, H.

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Appl. Opt. (2)

Appl. Phys. Lett. (1)

V. R. Daria, C. Stricker, R. Bowman, S. Redman, and H. A. Bachor, “Arbitrary multisite two-photon excitation in four dimensions,” Appl. Phys. Lett. 95, 093701 (2009).
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Supplementary Material (2)

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» Supplement 1       Supplemental document
» Visualization 1       Volume representation of the 50 holographic spots shown in Fig. 2 of the main manuscript

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Figures (7)

Fig. 1.
Fig. 1. Experimental setup and principle of MTF-LS. (a) In a first realization, the beam-shaping unit consisted of a dynamic CGH system, composed of a beam expander (BE) to match the active area of a SLM (SLM1), which performed the appropriate phase modulation for generating the desired 2D pattern. The 2D speckled illumination pattern was then focused on the grating ( G ) for TF through lens L1. The first diffraction order was collimated by lens L2 and directed to the second SLM (SLM2), which created the predefined 3D distribution of diffraction-limited spots at the sample positions, thereby replicating the 2D pattern generated by SLM1. Lenses L3 and L4 conjugated the SLM2 plane at the objective (OBJ) back focal plane and scaled the beam by fitting the long axis of the SLM at the objective back aperture. Close to SLM2 is shown the x y illumination of SLM2. In the case of MTF-CGH, the full active area of SLM2 was illuminated. Inset: the second realization of the beam-shaping unit was obtained by replacing SLM1 with a static phase mask producing a circular 20-μm-diameter holographic spot. The telescope constituted by lenses L 1 PM and L 2 PM magnified the size of the static phase mask, to match the size of SLM2. (b) In a third realization, the beam shaper was a GPC interferometer. Binary phase modulation for a circular spot of 12-μm diameter was imposed on SLM1, and lens L 1 GPC focused the beam on the phase contrast filter (PCF), which introduced a λ / 2 phase delay to the low-spatial-frequency components over the high-spatial frequencies. Finally, lens L 2 GPC recombined high- and low-spatial frequencies to form the interference pattern at the output plane of the GPC shaper, which coincided with the grating plane. In the case of MTF-GPC, the x y light distribution on SLM2 resulted in a single focused line of dispersed colors, covering all the SLM active area in the x direction but greatly underfilling SLM2 in the y direction. (c) The fourth configuration, MTF-MS, was obtained from the MTF-GPC one by removing the PCF and using SLM1 to perform both amplitude shaping to create the desired shapes and phase shaping to optimize the illumination of SLM2. In the example, SLM1 is used to create two different shapes. A holographic prism effect is imposed on the desired shapes to separate them from the unwanted light in the x direction, such as to create two spots aligned in the y direction after L 1 GPC . A beam stop blocks the undesired non-diffracted light (zero order), leaving only the desired shapes at the grating. The two shapes result in two parallel lines at SLM2, which is addressed with two different multiplexing holograms. (a)–(c) bottom, schematic principle of MTF-LS showing the phases applied on both SLMs, the 2D shape(s) at the diffraction grating position, and the distribution of the targets at the sample position.
Fig. 2.
Fig. 2. MTF-CGH with two SLMs. (a) 2PE fluorescence volume representation of 50 holographic circular spots of 15-μm diameter, each of them lying on a different plane, in a volume of 300    μm × 300    μm × 500    μm . Average laser power at the sample position = 450 mW. (b)  x y , x z , and y z projections of three spots, located at z = 250    μm , 0 μm, 240 μm from the focal plane. Scale bar, 15 μm. (c) Histogram of the maximal 2PE fluorescence intensity for each spot, normalized to the average intensity of all spots, after diffraction efficiency correction. The results represent an average for each plane from four different realizations of 50-spots light configuration. (d) Axial confinement, calculated as the FWHM of the axial intensity profile of each spot, as a function of the z position. Red stars represent the individual measurements for each spot (average on four different realizations of 50 spots), and blue bars show the mean values in a range of 50 μm around the designated z position. The mean value across the whole FOE was 11.1 ± 1.8    μm FWHM.
Fig. 3.
Fig. 3. MTF-CGH with a static phase mask. (a) Left, picture of the holographic static phase mask mounted on a 1-inch circular holder. Right, eight-level computer-generated hologram used to fabricate the static phase mask. (b) 2PE fluorescence volume representation of 20 holographic circular spots of 20-μm diameter, each of them lying on a different plane, in a volume of 130    μm × 130    μm × 400    μm . Average laser power at the sample position = 200 mW. (c)  x y , x z , and y z projections of three spots, located at z = 200    μm , 0 μm, 200 μm from the focal plane. Scale bar, 20 μm. (d) Axial confinement, calculated as the FWHM of the axial intensity profile of each spot, as a function of the z position. The mean value across the whole FOE was 11.0 ± 4.0    μm FWHM.
Fig. 4.
Fig. 4. MTF-GPC. (a) 2PE fluorescence volume representation of 20 GPC circular spots of 12-μm diameter, each of them lying on a different plane, in a volume of 200    μm × 200    μm × 200    μm . Average laser power at the sample position = 150 mW. (b)  x y , x z , and y z projections of three spots, located at z = 95    μm , 0 μm, 100 μm from the focal plane. Scale bar, 12 μm. (c) Axial confinement, calculated as the FWHM of the axial intensity profile of each spot, as a function of the z position. The mean value across the whole FOE was 6.0 ± 1.5    μm FWHM.
Fig. 5.
Fig. 5. MTF-MS. (a) Phase applied on SLM1 made up of four different shapes encoded with different prism holographic phases. The unshaped light was blocked using a beam stop. The shapes are elongated on SLM1 to compensate for the tilted illumination of the diffraction grating. After the diffraction grating, the four shapes converted into four parallel lines at SLM2, which independently multiplexed them. (b) and (c) Top and side views of a 2PE fluorescence image of 40 spots, 10 for each shape, in a volume of 300    μm × 300    μm × 400    μm . Average laser power at the sample position = 400 mW. (d)  x y , x z , and y z projections of the four different shapes at different planes. Scale bar = 15 μm. (e) Axial confinement, calculated as the FWHM of the axial intensity profile of each spot, as a function of the z position. The mean value across the whole FOE was 9.5 ± 1.5    μm FWHM. Red stars represent the FWHM measurements at each z position (average on four different realizations of 40 spots), and blue bars show the mean values in a range of 50 μm around the designated z position.
Fig. 6.
Fig. 6. Simultaneous photoconversion of Kaede-expressing neurons in zebrafish. (a) Superposed brightfield and widefield fluorescence images of the head of a double transgenic Tg(HuC:gal4; UAS:kaede) zebrafish larva. The dashed square represents the approximate area where we performed photoconversion. Scale bar, 100 μm. (b) 3D view of a 2P stack ( λ imaging = 780    nm ) merging green and red fluorescence after targeted simultaneous 2P photoconversion ( λ conversion = 800    nm ) of a set of 11 neurons. Represented volume: 178    μm × 178    μm × 251    μm . The inset represents the 3D MTF-CGH illumination pattern composed of multiple 6-μm-diameter spots used for photoconversion. (c) Top and side single frame views extracted from the 2P stack reported in (b), zooming on three representative photoconverted cells [labeled 1–3 in panel (b)]. Scale bar: 20 μm. (d) Normalized axial intensity profiles of green and red fluorescence integrated over z for the three cells reported in (c).
Fig. 7.
Fig. 7. Photoactivation of sPA-GCaMP in drosophila larvae. (a) Schematic representation of a dissected drosophila larva. The dissection exposes the ventral cord (red rectangle) in which motor neurons co-express nuclear mCherry (red dots) and photoactivable sPA-GCaMP6f. (b) Max projection of a z -stack of green (sPA-GCaMP6f) and red (mCherry) fluorescence performed after wide 1P (405 nm) photoactivation of motorneurons of the ventral central cord (see Methods). Image acquired on a confocal microscope. Scale bar, 30 μm. (c) 3D view of a 2P stack ( λ imaging = 920    nm ) merging green and red fluorescence after 2P ( λ activation = 760    nm ) targeted simultaneous photoactivation of a set of six motor neurons (labeled with numbers). Represented volume: 178    μm × 178    μm × 140    μm . The inset represents the 3D MTF-CGH illumination pattern composed of multiple 5-μm-diameter spots used for photoactivation. (d) Top (up) and side (down) max projection of green and red fluorescent after photoconversion, corresponding to panel (c). Numbers label targeted photoactivated neurons. Scale bar, 30 μm.

Tables (1)

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Table 1. Comparison of the Four Different MTF-LS Methods Presented in this Studya