Abstract

Patterned illumination through the phase modulation of light is increasingly recognized as a powerful tool to investigate biological tissues in combination with two-photon excitation and light-sensitive molecules. However, to date two-photon patterned illumination has only been coupled to traditional microscope objectives, thus limiting the applicability of these methods to superficial biological structures. Here, we show that phase modulation can be used to efficiently project complex two-photon light patterns, including arrays of points and large shapes, in the focal plane of graded index (GRIN) lenses. Moreover, using this approach in combination with the genetically encoded calcium indicator GCaMP6, we validate our system performing scanless functional imaging in rodent hippocampal networks in vivo ~1.2 mm below the brain surface. Our results open the way to the application of patterned illumination approaches to deep regions of highly scattering biological tissues, such as the mammalian brain.

© 2016 Optical Society of America

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  1. T. Knöpfel, “Genetically encoded optical indicators for the analysis of neuronal circuits,” Nat. Rev. Neurosci. 13(10), 687–700 (2012).
    [PubMed]
  2. F. Zhang, A. M. Aravanis, A. Adamantidis, L. de Lecea, and K. Deisseroth, “Circuit-breakers: optical technologies for probing neural signals and systems,” Nat. Rev. Neurosci. 8(8), 577–581 (2007).
    [Crossref] [PubMed]
  3. F. Zhang, V. Gradinaru, A. R. Adamantidis, R. Durand, R. D. Airan, L. de Lecea, and K. Deisseroth, “Optogenetic interrogation of neural circuits: technology for probing mammalian brain structures,” Nat. Protoc. 5(3), 439–456 (2010).
    [Crossref] [PubMed]
  4. 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, 5–19 (2008).
    [Crossref] [PubMed]
  5. M. Dal Maschio, F. Difato, R. Beltramo, A. Blau, F. Benfenati, and T. Fellin, “Simultaneous two-photon imaging and photo-stimulation with structured light illumination,” Opt. Express 18(18), 18720–18731 (2010).
    [Crossref] [PubMed]
  6. M. Dal Maschio, A. M. De Stasi, F. Benfenati, and T. Fellin, “Three-dimensional in vivo scanning microscopy with inertia-free focus control,” Opt. Lett. 36(17), 3503–3505 (2011).
    [Crossref] [PubMed]
  7. S. Quirin, D. S. Peterka, and R. Yuste, “Instantaneous three-dimensional sensing using spatial light modulator illumination with extended depth of field imaging,” Opt. Express 21(13), 16007–16021 (2013).
    [Crossref] [PubMed]
  8. S. Quirin, J. Jackson, D. S. Peterka, and R. Yuste, “Simultaneous imaging of neural activity in three dimensions,” Front. Neural Circuits 8, 29 (2014).
    [Crossref] [PubMed]
  9. 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(25), 32573–32581 (2015).
    [Crossref] [PubMed]
  10. W. Yang, J. E. Miller, L. Carrillo-Reid, E. Pnevmatikakis, L. Paninski, R. Yuste, and D. S. Peterka, “Simultaneous Multi-plane Imaging of Neural Circuits,” Neuron 89(2), 269–284 (2016).
    [Crossref] [PubMed]
  11. S. Bovetti and T. Fellin, “Optical dissection of brain circuits with patterned illumination through the phase modulation of light,” J. Neurosci. Methods 241, 66–77 (2015).
    [Crossref] [PubMed]
  12. E. Papagiakoumou, V. de Sars, D. Oron, and V. Emiliani, “Patterned two-photon illumination by spatiotemporal shaping of ultrashort pulses,” Opt. Express 16(26), 22039–22047 (2008).
    [Crossref] [PubMed]
  13. E. Papagiakoumou, V. de Sars, V. Emiliani, and D. Oron, “Temporal focusing with spatially modulated excitation,” Opt. Express 17(7), 5391–5401 (2009).
    [Crossref] [PubMed]
  14. 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(10), 848–854 (2010).
    [Crossref] [PubMed]
  15. E. Papagiakoumou, A. Bégue, B. Leshem, O. Schwartz, B. M. Stell, J. Bradley, D. Oron, and V. Emiliani, “Funtional patterned multiphoton excitation deep inside scattering tissue,” Nat. Photonics 7(4), 274–278 (2013).
    [Crossref]
  16. 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(12), 2869–2879 (2013).
    [Crossref] [PubMed]
  17. A. M. Packer, L. E. Russell, H. W. Dalgleish, and M. Hausser, “Simultaneous all-optical manipulation and recording of neural circuit activity with cellular resolution in vivo,” Nat. Methods 12(2), 140–146 (2014).
    [Crossref] [PubMed]
  18. J. P. Rickgauer, K. Deisseroth, and D. W. Tank, “Simultaneous cellular-resolution optical perturbation and imaging of place cell firing fields,” Nat. Neurosci. 17(12), 1816–1824 (2014).
    [Crossref] [PubMed]
  19. K. König, M. Weinigel, D. Hoppert, R. Bückle, H. Schubert, M. J. Köhler, M. Kaatz, and P. Elsner, “Multiphoton tissue imaging using high-NA microendoscopes and flexible scan heads for clinical studies and small animal research,” J. Biophotonics 1(6), 506–513 (2008).
    [Crossref] [PubMed]
  20. R. P. Barretto, B. Messerschmidt, and M. J. Schnitzer, “In vivo fluorescence imaging with high-resolution microlenses,” Nat. Methods 6(7), 511–512 (2009).
    [Crossref] [PubMed]
  21. Grintech product datasheet, “High-NA Endomicroscopic Imaging Objective for 2-Photon Microscopy” (Grintech, 2016). http://www.grintech.de/grin-lens-systems-for-medical-applications.html
  22. C. J. R. Sheppard and M. Gu, “Image formation in two-photon fluroescence microscopy,” Optik (Stuttg.) 86, 104–106 (1990).
  23. F. Helmchen and W. Denk, “Deep tissue two-photon microscopy,” Nat. Methods 2(12), 932–940 (2005).
    [Crossref] [PubMed]
  24. F. Anselmi, C. Ventalon, A. Bègue, D. Ogden, and V. Emiliani, “Three-dimensional imaging and photostimulation by remote-focusing and holographic light patterning,” Proc. Natl. Acad. Sci. U.S.A. 108(49), 19504–19509 (2011).
    [Crossref] [PubMed]
  25. A. Antonini, C. Liberale, and T. Fellin, “Fluorescent layers for characterization of sectioning microscopy with coverslip-uncorrected and water immersion objectives,” Opt. Express 22(12), 14293–14304 (2014).
    [Crossref] [PubMed]
  26. R. Di Leonardo, F. Ianni, and G. Ruocco, “Computer generation of optimal holograms for optical trap arrays,” Opt. Express 15(4), 1913–1922 (2007).
    [Crossref] [PubMed]
  27. V. A. Soifer, Methods for Computer Design of Diffractive Optical Elements, (John Wiley & Sons, Inc., 2002).
  28. D. Gandolfi, P. Pozzi, M. Tognolina, G. Chirico, J. Mapelli, and E. D’Angelo, “The spatiotemporal organization of cerebellar network activity resolved by two-photon imaging of multiple single neurons,” Front. Cell. Neurosci. 8, 92 (2014).
    [Crossref] [PubMed]
  29. 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(7458), 295–300 (2013).
    [Crossref] [PubMed]
  30. G. Paxinos and K. B. J. Franklin, The Mouse Brain in Stereotaxic Coordinates (Academic Press, ed., 2012).
  31. M. E. Bocarsly, W. C. Jiang, C. Wang, J. T. Dudman, N. Ji, and Y. Aponte, “Minimally invasive microendoscopy system for in vivo functional imaging of deep nuclei in the mouse brain,” Biomed. Opt. Express 6(11), 4546–4556 (2015).
    [Crossref] [PubMed]
  32. V. Szabo, C. Ventalon, V. De Sars, J. Bradley, and V. Emiliani, “Spatially selective holographic photoactivation and functional fluorescence imaging in freely behaving mice with a fiberscope,” Neuron 84(6), 1157–1169 (2014).
    [Crossref] [PubMed]

2016 (1)

W. Yang, J. E. Miller, L. Carrillo-Reid, E. Pnevmatikakis, L. Paninski, R. Yuste, and D. S. Peterka, “Simultaneous Multi-plane Imaging of Neural Circuits,” Neuron 89(2), 269–284 (2016).
[Crossref] [PubMed]

2015 (3)

2014 (6)

V. Szabo, C. Ventalon, V. De Sars, J. Bradley, and V. Emiliani, “Spatially selective holographic photoactivation and functional fluorescence imaging in freely behaving mice with a fiberscope,” Neuron 84(6), 1157–1169 (2014).
[Crossref] [PubMed]

A. Antonini, C. Liberale, and T. Fellin, “Fluorescent layers for characterization of sectioning microscopy with coverslip-uncorrected and water immersion objectives,” Opt. Express 22(12), 14293–14304 (2014).
[Crossref] [PubMed]

D. Gandolfi, P. Pozzi, M. Tognolina, G. Chirico, J. Mapelli, and E. D’Angelo, “The spatiotemporal organization of cerebellar network activity resolved by two-photon imaging of multiple single neurons,” Front. Cell. Neurosci. 8, 92 (2014).
[Crossref] [PubMed]

A. M. Packer, L. E. Russell, H. W. Dalgleish, and M. Hausser, “Simultaneous all-optical manipulation and recording of neural circuit activity with cellular resolution in vivo,” Nat. Methods 12(2), 140–146 (2014).
[Crossref] [PubMed]

J. P. Rickgauer, K. Deisseroth, and D. W. Tank, “Simultaneous cellular-resolution optical perturbation and imaging of place cell firing fields,” Nat. Neurosci. 17(12), 1816–1824 (2014).
[Crossref] [PubMed]

S. Quirin, J. Jackson, D. S. Peterka, and R. Yuste, “Simultaneous imaging of neural activity in three dimensions,” Front. Neural Circuits 8, 29 (2014).
[Crossref] [PubMed]

2013 (4)

S. Quirin, D. S. Peterka, and R. Yuste, “Instantaneous three-dimensional sensing using spatial light modulator illumination with extended depth of field imaging,” Opt. Express 21(13), 16007–16021 (2013).
[Crossref] [PubMed]

E. Papagiakoumou, A. Bégue, B. Leshem, O. Schwartz, B. M. Stell, J. Bradley, D. Oron, and V. Emiliani, “Funtional patterned multiphoton excitation deep inside scattering tissue,” Nat. Photonics 7(4), 274–278 (2013).
[Crossref]

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(12), 2869–2879 (2013).
[Crossref] [PubMed]

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(7458), 295–300 (2013).
[Crossref] [PubMed]

2012 (1)

T. Knöpfel, “Genetically encoded optical indicators for the analysis of neuronal circuits,” Nat. Rev. Neurosci. 13(10), 687–700 (2012).
[PubMed]

2011 (2)

M. Dal Maschio, A. M. De Stasi, F. Benfenati, and T. Fellin, “Three-dimensional in vivo scanning microscopy with inertia-free focus control,” Opt. Lett. 36(17), 3503–3505 (2011).
[Crossref] [PubMed]

F. Anselmi, C. Ventalon, A. Bègue, D. Ogden, and V. Emiliani, “Three-dimensional imaging and photostimulation by remote-focusing and holographic light patterning,” Proc. Natl. Acad. Sci. U.S.A. 108(49), 19504–19509 (2011).
[Crossref] [PubMed]

2010 (3)

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(10), 848–854 (2010).
[Crossref] [PubMed]

M. Dal Maschio, F. Difato, R. Beltramo, A. Blau, F. Benfenati, and T. Fellin, “Simultaneous two-photon imaging and photo-stimulation with structured light illumination,” Opt. Express 18(18), 18720–18731 (2010).
[Crossref] [PubMed]

F. Zhang, V. Gradinaru, A. R. Adamantidis, R. Durand, R. D. Airan, L. de Lecea, and K. Deisseroth, “Optogenetic interrogation of neural circuits: technology for probing mammalian brain structures,” Nat. Protoc. 5(3), 439–456 (2010).
[Crossref] [PubMed]

2009 (2)

E. Papagiakoumou, V. de Sars, V. Emiliani, and D. Oron, “Temporal focusing with spatially modulated excitation,” Opt. Express 17(7), 5391–5401 (2009).
[Crossref] [PubMed]

R. P. Barretto, B. Messerschmidt, and M. J. Schnitzer, “In vivo fluorescence imaging with high-resolution microlenses,” Nat. Methods 6(7), 511–512 (2009).
[Crossref] [PubMed]

2008 (3)

E. Papagiakoumou, V. de Sars, D. Oron, and V. Emiliani, “Patterned two-photon illumination by spatiotemporal shaping of ultrashort pulses,” Opt. Express 16(26), 22039–22047 (2008).
[Crossref] [PubMed]

K. König, M. Weinigel, D. Hoppert, R. Bückle, H. Schubert, M. J. Köhler, M. Kaatz, and P. Elsner, “Multiphoton tissue imaging using high-NA microendoscopes and flexible scan heads for clinical studies and small animal research,” J. Biophotonics 1(6), 506–513 (2008).
[Crossref] [PubMed]

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, 5–19 (2008).
[Crossref] [PubMed]

2007 (2)

F. Zhang, A. M. Aravanis, A. Adamantidis, L. de Lecea, and K. Deisseroth, “Circuit-breakers: optical technologies for probing neural signals and systems,” Nat. Rev. Neurosci. 8(8), 577–581 (2007).
[Crossref] [PubMed]

R. Di Leonardo, F. Ianni, and G. Ruocco, “Computer generation of optimal holograms for optical trap arrays,” Opt. Express 15(4), 1913–1922 (2007).
[Crossref] [PubMed]

2005 (1)

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

1990 (1)

C. J. R. Sheppard and M. Gu, “Image formation in two-photon fluroescence microscopy,” Optik (Stuttg.) 86, 104–106 (1990).

Adamantidis, A.

F. Zhang, A. M. Aravanis, A. Adamantidis, L. de Lecea, and K. Deisseroth, “Circuit-breakers: optical technologies for probing neural signals and systems,” Nat. Rev. Neurosci. 8(8), 577–581 (2007).
[Crossref] [PubMed]

Adamantidis, A. R.

F. Zhang, V. Gradinaru, A. R. Adamantidis, R. Durand, R. D. Airan, L. de Lecea, and K. Deisseroth, “Optogenetic interrogation of neural circuits: technology for probing mammalian brain structures,” Nat. Protoc. 5(3), 439–456 (2010).
[Crossref] [PubMed]

Airan, R. D.

F. Zhang, V. Gradinaru, A. R. Adamantidis, R. Durand, R. D. Airan, L. de Lecea, and K. Deisseroth, “Optogenetic interrogation of neural circuits: technology for probing mammalian brain structures,” Nat. Protoc. 5(3), 439–456 (2010).
[Crossref] [PubMed]

Allen, W. E.

Andalman, A. S.

Anselmi, F.

F. Anselmi, C. Ventalon, A. Bègue, D. Ogden, and V. Emiliani, “Three-dimensional imaging and photostimulation by remote-focusing and holographic light patterning,” Proc. Natl. Acad. Sci. U.S.A. 108(49), 19504–19509 (2011).
[Crossref] [PubMed]

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(10), 848–854 (2010).
[Crossref] [PubMed]

Antonini, A.

Aponte, Y.

Aravanis, A. M.

F. Zhang, A. M. Aravanis, A. Adamantidis, L. de Lecea, and K. Deisseroth, “Circuit-breakers: optical technologies for probing neural signals and systems,” Nat. Rev. Neurosci. 8(8), 577–581 (2007).
[Crossref] [PubMed]

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, 5–19 (2008).
[Crossref] [PubMed]

Baohan, A.

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(7458), 295–300 (2013).
[Crossref] [PubMed]

Barretto, R. P.

R. P. Barretto, B. Messerschmidt, and M. J. Schnitzer, “In vivo fluorescence imaging with high-resolution microlenses,” Nat. Methods 6(7), 511–512 (2009).
[Crossref] [PubMed]

Bégue, A.

E. Papagiakoumou, A. Bégue, B. Leshem, O. Schwartz, B. M. Stell, J. Bradley, D. Oron, and V. Emiliani, “Funtional patterned multiphoton excitation deep inside scattering tissue,” Nat. Photonics 7(4), 274–278 (2013).
[Crossref]

Bègue, A.

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(12), 2869–2879 (2013).
[Crossref] [PubMed]

F. Anselmi, C. Ventalon, A. Bègue, D. Ogden, and V. Emiliani, “Three-dimensional imaging and photostimulation by remote-focusing and holographic light patterning,” Proc. Natl. Acad. Sci. U.S.A. 108(49), 19504–19509 (2011).
[Crossref] [PubMed]

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(10), 848–854 (2010).
[Crossref] [PubMed]

Beltramo, R.

Benfenati, F.

Blau, A.

Bocarsly, M. E.

Bovetti, S.

S. Bovetti and T. Fellin, “Optical dissection of brain circuits with patterned illumination through the phase modulation of light,” J. Neurosci. Methods 241, 66–77 (2015).
[Crossref] [PubMed]

Bradley, J.

V. Szabo, C. Ventalon, V. De Sars, J. Bradley, and V. Emiliani, “Spatially selective holographic photoactivation and functional fluorescence imaging in freely behaving mice with a fiberscope,” Neuron 84(6), 1157–1169 (2014).
[Crossref] [PubMed]

E. Papagiakoumou, A. Bégue, B. Leshem, O. Schwartz, B. M. Stell, J. Bradley, D. Oron, and V. Emiliani, “Funtional patterned multiphoton excitation deep inside scattering tissue,” Nat. Photonics 7(4), 274–278 (2013).
[Crossref]

Bückle, R.

K. König, M. Weinigel, D. Hoppert, R. Bückle, H. Schubert, M. J. Köhler, M. Kaatz, and P. Elsner, “Multiphoton tissue imaging using high-NA microendoscopes and flexible scan heads for clinical studies and small animal research,” J. Biophotonics 1(6), 506–513 (2008).
[Crossref] [PubMed]

Carrillo-Reid, L.

W. Yang, J. E. Miller, L. Carrillo-Reid, E. Pnevmatikakis, L. Paninski, R. Yuste, and D. S. Peterka, “Simultaneous Multi-plane Imaging of Neural Circuits,” Neuron 89(2), 269–284 (2016).
[Crossref] [PubMed]

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(7458), 295–300 (2013).
[Crossref] [PubMed]

Chirico, G.

D. Gandolfi, P. Pozzi, M. Tognolina, G. Chirico, J. Mapelli, and E. D’Angelo, “The spatiotemporal organization of cerebellar network activity resolved by two-photon imaging of multiple single neurons,” Front. Cell. Neurosci. 8, 92 (2014).
[Crossref] [PubMed]

Conti, R.

D’Angelo, E.

D. Gandolfi, P. Pozzi, M. Tognolina, G. Chirico, J. Mapelli, and E. D’Angelo, “The spatiotemporal organization of cerebellar network activity resolved by two-photon imaging of multiple single neurons,” Front. Cell. Neurosci. 8, 92 (2014).
[Crossref] [PubMed]

Dal Maschio, M.

Dalgleish, H. W.

A. M. Packer, L. E. Russell, H. W. Dalgleish, and M. Hausser, “Simultaneous all-optical manipulation and recording of neural circuit activity with cellular resolution in vivo,” Nat. Methods 12(2), 140–146 (2014).
[Crossref] [PubMed]

de Lecea, L.

F. Zhang, V. Gradinaru, A. R. Adamantidis, R. Durand, R. D. Airan, L. de Lecea, and K. Deisseroth, “Optogenetic interrogation of neural circuits: technology for probing mammalian brain structures,” Nat. Protoc. 5(3), 439–456 (2010).
[Crossref] [PubMed]

F. Zhang, A. M. Aravanis, A. Adamantidis, L. de Lecea, and K. Deisseroth, “Circuit-breakers: optical technologies for probing neural signals and systems,” Nat. Rev. Neurosci. 8(8), 577–581 (2007).
[Crossref] [PubMed]

De Sars, V.

V. Szabo, C. Ventalon, V. De Sars, J. Bradley, and V. Emiliani, “Spatially selective holographic photoactivation and functional fluorescence imaging in freely behaving mice with a fiberscope,” Neuron 84(6), 1157–1169 (2014).
[Crossref] [PubMed]

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(10), 848–854 (2010).
[Crossref] [PubMed]

E. Papagiakoumou, V. de Sars, V. Emiliani, and D. Oron, “Temporal focusing with spatially modulated excitation,” Opt. Express 17(7), 5391–5401 (2009).
[Crossref] [PubMed]

E. Papagiakoumou, V. de Sars, D. Oron, and V. Emiliani, “Patterned two-photon illumination by spatiotemporal shaping of ultrashort pulses,” Opt. Express 16(26), 22039–22047 (2008).
[Crossref] [PubMed]

De Stasi, A. M.

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(25), 32573–32581 (2015).
[Crossref] [PubMed]

J. P. Rickgauer, K. Deisseroth, and D. W. Tank, “Simultaneous cellular-resolution optical perturbation and imaging of place cell firing fields,” Nat. Neurosci. 17(12), 1816–1824 (2014).
[Crossref] [PubMed]

F. Zhang, V. Gradinaru, A. R. Adamantidis, R. Durand, R. D. Airan, L. de Lecea, and K. Deisseroth, “Optogenetic interrogation of neural circuits: technology for probing mammalian brain structures,” Nat. Protoc. 5(3), 439–456 (2010).
[Crossref] [PubMed]

F. Zhang, A. M. Aravanis, A. Adamantidis, L. de Lecea, and K. Deisseroth, “Circuit-breakers: optical technologies for probing neural signals and systems,” Nat. Rev. Neurosci. 8(8), 577–581 (2007).
[Crossref] [PubMed]

Denk, W.

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

Di Leonardo, R.

Difato, F.

Dudman, J. T.

Durand, R.

F. Zhang, V. Gradinaru, A. R. Adamantidis, R. Durand, R. D. Airan, L. de Lecea, and K. Deisseroth, “Optogenetic interrogation of neural circuits: technology for probing mammalian brain structures,” Nat. Protoc. 5(3), 439–456 (2010).
[Crossref] [PubMed]

Elsner, P.

K. König, M. Weinigel, D. Hoppert, R. Bückle, H. Schubert, M. J. Köhler, M. Kaatz, and P. Elsner, “Multiphoton tissue imaging using high-NA microendoscopes and flexible scan heads for clinical studies and small animal research,” J. Biophotonics 1(6), 506–513 (2008).
[Crossref] [PubMed]

Emiliani, V.

V. Szabo, C. Ventalon, V. De Sars, J. Bradley, and V. Emiliani, “Spatially selective holographic photoactivation and functional fluorescence imaging in freely behaving mice with a fiberscope,” Neuron 84(6), 1157–1169 (2014).
[Crossref] [PubMed]

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(12), 2869–2879 (2013).
[Crossref] [PubMed]

E. Papagiakoumou, A. Bégue, B. Leshem, O. Schwartz, B. M. Stell, J. Bradley, D. Oron, and V. Emiliani, “Funtional patterned multiphoton excitation deep inside scattering tissue,” Nat. Photonics 7(4), 274–278 (2013).
[Crossref]

F. Anselmi, C. Ventalon, A. Bègue, D. Ogden, and V. Emiliani, “Three-dimensional imaging and photostimulation by remote-focusing and holographic light patterning,” Proc. Natl. Acad. Sci. U.S.A. 108(49), 19504–19509 (2011).
[Crossref] [PubMed]

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(10), 848–854 (2010).
[Crossref] [PubMed]

E. Papagiakoumou, V. de Sars, V. Emiliani, and D. Oron, “Temporal focusing with spatially modulated excitation,” Opt. Express 17(7), 5391–5401 (2009).
[Crossref] [PubMed]

E. Papagiakoumou, V. de Sars, D. Oron, and V. Emiliani, “Patterned two-photon illumination by spatiotemporal shaping of ultrashort pulses,” Opt. Express 16(26), 22039–22047 (2008).
[Crossref] [PubMed]

Enke, L.

Fellin, T.

Gandolfi, D.

D. Gandolfi, P. Pozzi, M. Tognolina, G. Chirico, J. Mapelli, and E. D’Angelo, “The spatiotemporal organization of cerebellar network activity resolved by two-photon imaging of multiple single neurons,” Front. Cell. Neurosci. 8, 92 (2014).
[Crossref] [PubMed]

Glückstad, J.

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(10), 848–854 (2010).
[Crossref] [PubMed]

Gradinaru, V.

F. Zhang, V. Gradinaru, A. R. Adamantidis, R. Durand, R. D. Airan, L. de Lecea, and K. Deisseroth, “Optogenetic interrogation of neural circuits: technology for probing mammalian brain structures,” Nat. Protoc. 5(3), 439–456 (2010).
[Crossref] [PubMed]

Gu, M.

C. J. R. Sheppard and M. Gu, “Image formation in two-photon fluroescence microscopy,” Optik (Stuttg.) 86, 104–106 (1990).

Hausser, M.

A. M. Packer, L. E. Russell, H. W. Dalgleish, and M. Hausser, “Simultaneous all-optical manipulation and recording of neural circuit activity with cellular resolution in vivo,” Nat. Methods 12(2), 140–146 (2014).
[Crossref] [PubMed]

Helmchen, F.

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

Hoppert, D.

K. König, M. Weinigel, D. Hoppert, R. Bückle, H. Schubert, M. J. Köhler, M. Kaatz, and P. Elsner, “Multiphoton tissue imaging using high-NA microendoscopes and flexible scan heads for clinical studies and small animal research,” J. Biophotonics 1(6), 506–513 (2008).
[Crossref] [PubMed]

Ianni, F.

Isacoff, E. Y.

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(10), 848–854 (2010).
[Crossref] [PubMed]

Jackson, J.

S. Quirin, J. Jackson, D. S. Peterka, and R. Yuste, “Simultaneous imaging of neural activity in three dimensions,” Front. Neural Circuits 8, 29 (2014).
[Crossref] [PubMed]

Jayaraman, V.

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(7458), 295–300 (2013).
[Crossref] [PubMed]

Ji, N.

Jiang, W. C.

Kaatz, M.

K. König, M. Weinigel, D. Hoppert, R. Bückle, H. Schubert, M. J. Köhler, M. Kaatz, and P. Elsner, “Multiphoton tissue imaging using high-NA microendoscopes and flexible scan heads for clinical studies and small animal research,” J. Biophotonics 1(6), 506–513 (2008).
[Crossref] [PubMed]

Kauvar, I.

Kerr, R. A.

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(7458), 295–300 (2013).
[Crossref] [PubMed]

Kim, C. K.

Kim, D. S.

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(7458), 295–300 (2013).
[Crossref] [PubMed]

Knöpfel, T.

T. Knöpfel, “Genetically encoded optical indicators for the analysis of neuronal circuits,” Nat. Rev. Neurosci. 13(10), 687–700 (2012).
[PubMed]

Köhler, M. J.

K. König, M. Weinigel, D. Hoppert, R. Bückle, H. Schubert, M. J. Köhler, M. Kaatz, and P. Elsner, “Multiphoton tissue imaging using high-NA microendoscopes and flexible scan heads for clinical studies and small animal research,” J. Biophotonics 1(6), 506–513 (2008).
[Crossref] [PubMed]

König, K.

K. König, M. Weinigel, D. Hoppert, R. Bückle, H. Schubert, M. J. Köhler, M. Kaatz, and P. Elsner, “Multiphoton tissue imaging using high-NA microendoscopes and flexible scan heads for clinical studies and small animal research,” J. Biophotonics 1(6), 506–513 (2008).
[Crossref] [PubMed]

Leshem, B.

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(12), 2869–2879 (2013).
[Crossref] [PubMed]

E. Papagiakoumou, A. Bégue, B. Leshem, O. Schwartz, B. M. Stell, J. Bradley, D. Oron, and V. Emiliani, “Funtional patterned multiphoton excitation deep inside scattering tissue,” Nat. Photonics 7(4), 274–278 (2013).
[Crossref]

Liberale, C.

Looger, L. L.

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(7458), 295–300 (2013).
[Crossref] [PubMed]

Mapelli, J.

D. Gandolfi, P. Pozzi, M. Tognolina, G. Chirico, J. Mapelli, and E. D’Angelo, “The spatiotemporal organization of cerebellar network activity resolved by two-photon imaging of multiple single neurons,” Front. Cell. Neurosci. 8, 92 (2014).
[Crossref] [PubMed]

Marshel, J. H.

Messerschmidt, B.

R. P. Barretto, B. Messerschmidt, and M. J. Schnitzer, “In vivo fluorescence imaging with high-resolution microlenses,” Nat. Methods 6(7), 511–512 (2009).
[Crossref] [PubMed]

Miller, J. E.

W. Yang, J. E. Miller, L. Carrillo-Reid, E. Pnevmatikakis, L. Paninski, R. Yuste, and D. S. Peterka, “Simultaneous Multi-plane Imaging of Neural Circuits,” Neuron 89(2), 269–284 (2016).
[Crossref] [PubMed]

Nikolenko, V.

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, 5–19 (2008).
[Crossref] [PubMed]

Ogden, D.

F. Anselmi, C. Ventalon, A. Bègue, D. Ogden, and V. Emiliani, “Three-dimensional imaging and photostimulation by remote-focusing and holographic light patterning,” Proc. Natl. Acad. Sci. U.S.A. 108(49), 19504–19509 (2011).
[Crossref] [PubMed]

Orger, M. B.

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(7458), 295–300 (2013).
[Crossref] [PubMed]

Oron, D.

Packer, A. M.

A. M. Packer, L. E. Russell, H. W. Dalgleish, and M. Hausser, “Simultaneous all-optical manipulation and recording of neural circuit activity with cellular resolution in vivo,” Nat. Methods 12(2), 140–146 (2014).
[Crossref] [PubMed]

Paninski, L.

W. Yang, J. E. Miller, L. Carrillo-Reid, E. Pnevmatikakis, L. Paninski, R. Yuste, and D. S. Peterka, “Simultaneous Multi-plane Imaging of Neural Circuits,” Neuron 89(2), 269–284 (2016).
[Crossref] [PubMed]

Papagiakoumou, E.

Peterka, D. S.

W. Yang, J. E. Miller, L. Carrillo-Reid, E. Pnevmatikakis, L. Paninski, R. Yuste, and D. S. Peterka, “Simultaneous Multi-plane Imaging of Neural Circuits,” Neuron 89(2), 269–284 (2016).
[Crossref] [PubMed]

S. Quirin, J. Jackson, D. S. Peterka, and R. Yuste, “Simultaneous imaging of neural activity in three dimensions,” Front. Neural Circuits 8, 29 (2014).
[Crossref] [PubMed]

S. Quirin, D. S. Peterka, and R. Yuste, “Instantaneous three-dimensional sensing using spatial light modulator illumination with extended depth of field imaging,” Opt. Express 21(13), 16007–16021 (2013).
[Crossref] [PubMed]

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, 5–19 (2008).
[Crossref] [PubMed]

Pnevmatikakis, E.

W. Yang, J. E. Miller, L. Carrillo-Reid, E. Pnevmatikakis, L. Paninski, R. Yuste, and D. S. Peterka, “Simultaneous Multi-plane Imaging of Neural Circuits,” Neuron 89(2), 269–284 (2016).
[Crossref] [PubMed]

Pozzi, P.

D. Gandolfi, P. Pozzi, M. Tognolina, G. Chirico, J. Mapelli, and E. D’Angelo, “The spatiotemporal organization of cerebellar network activity resolved by two-photon imaging of multiple single neurons,” Front. Cell. Neurosci. 8, 92 (2014).
[Crossref] [PubMed]

Pulver, S. R.

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(7458), 295–300 (2013).
[Crossref] [PubMed]

Quirin, S.

Renninger, S. L.

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(7458), 295–300 (2013).
[Crossref] [PubMed]

Rickgauer, J. P.

J. P. Rickgauer, K. Deisseroth, and D. W. Tank, “Simultaneous cellular-resolution optical perturbation and imaging of place cell firing fields,” Nat. Neurosci. 17(12), 1816–1824 (2014).
[Crossref] [PubMed]

Ruocco, G.

Russell, L. E.

A. M. Packer, L. E. Russell, H. W. Dalgleish, and M. Hausser, “Simultaneous all-optical manipulation and recording of neural circuit activity with cellular resolution in vivo,” Nat. Methods 12(2), 140–146 (2014).
[Crossref] [PubMed]

Schnitzer, M. J.

R. P. Barretto, B. Messerschmidt, and M. J. Schnitzer, “In vivo fluorescence imaging with high-resolution microlenses,” Nat. Methods 6(7), 511–512 (2009).
[Crossref] [PubMed]

Schreiter, E. R.

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(7458), 295–300 (2013).
[Crossref] [PubMed]

Schubert, H.

K. König, M. Weinigel, D. Hoppert, R. Bückle, H. Schubert, M. J. Köhler, M. Kaatz, and P. Elsner, “Multiphoton tissue imaging using high-NA microendoscopes and flexible scan heads for clinical studies and small animal research,” J. Biophotonics 1(6), 506–513 (2008).
[Crossref] [PubMed]

Schwartz, O.

E. Papagiakoumou, A. Bégue, B. Leshem, O. Schwartz, B. M. Stell, J. Bradley, D. Oron, and V. Emiliani, “Funtional patterned multiphoton excitation deep inside scattering tissue,” Nat. Photonics 7(4), 274–278 (2013).
[Crossref]

Sheppard, C. J. R.

C. J. R. Sheppard and M. Gu, “Image formation in two-photon fluroescence microscopy,” Optik (Stuttg.) 86, 104–106 (1990).

Stell, B. M.

E. Papagiakoumou, A. Bégue, B. Leshem, O. Schwartz, B. M. Stell, J. Bradley, D. Oron, and V. Emiliani, “Funtional patterned multiphoton excitation deep inside scattering tissue,” Nat. Photonics 7(4), 274–278 (2013).
[Crossref]

Sun, Y.

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(7458), 295–300 (2013).
[Crossref] [PubMed]

Svoboda, K.

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(7458), 295–300 (2013).
[Crossref] [PubMed]

Szabo, V.

V. Szabo, C. Ventalon, V. De Sars, J. Bradley, and V. Emiliani, “Spatially selective holographic photoactivation and functional fluorescence imaging in freely behaving mice with a fiberscope,” Neuron 84(6), 1157–1169 (2014).
[Crossref] [PubMed]

Tank, D. W.

J. P. Rickgauer, K. Deisseroth, and D. W. Tank, “Simultaneous cellular-resolution optical perturbation and imaging of place cell firing fields,” Nat. Neurosci. 17(12), 1816–1824 (2014).
[Crossref] [PubMed]

Tognolina, M.

D. Gandolfi, P. Pozzi, M. Tognolina, G. Chirico, J. Mapelli, and E. D’Angelo, “The spatiotemporal organization of cerebellar network activity resolved by two-photon imaging of multiple single neurons,” Front. Cell. Neurosci. 8, 92 (2014).
[Crossref] [PubMed]

Ventalon, C.

V. Szabo, C. Ventalon, V. De Sars, J. Bradley, and V. Emiliani, “Spatially selective holographic photoactivation and functional fluorescence imaging in freely behaving mice with a fiberscope,” Neuron 84(6), 1157–1169 (2014).
[Crossref] [PubMed]

F. Anselmi, C. Ventalon, A. Bègue, D. Ogden, and V. Emiliani, “Three-dimensional imaging and photostimulation by remote-focusing and holographic light patterning,” Proc. Natl. Acad. Sci. U.S.A. 108(49), 19504–19509 (2011).
[Crossref] [PubMed]

Wang, C.

Wardill, T. J.

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(7458), 295–300 (2013).
[Crossref] [PubMed]

Watson, B. O.

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, 5–19 (2008).
[Crossref] [PubMed]

Weinigel, M.

K. König, M. Weinigel, D. Hoppert, R. Bückle, H. Schubert, M. J. Köhler, M. Kaatz, and P. Elsner, “Multiphoton tissue imaging using high-NA microendoscopes and flexible scan heads for clinical studies and small animal research,” J. Biophotonics 1(6), 506–513 (2008).
[Crossref] [PubMed]

Wetzstein, G.

Woodruff, A.

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, 5–19 (2008).
[Crossref] [PubMed]

Yang, S. J.

Yang, W.

W. Yang, J. E. Miller, L. Carrillo-Reid, E. Pnevmatikakis, L. Paninski, R. Yuste, and D. S. Peterka, “Simultaneous Multi-plane Imaging of Neural Circuits,” Neuron 89(2), 269–284 (2016).
[Crossref] [PubMed]

Young, N. P.

Yuste, R.

W. Yang, J. E. Miller, L. Carrillo-Reid, E. Pnevmatikakis, L. Paninski, R. Yuste, and D. S. Peterka, “Simultaneous Multi-plane Imaging of Neural Circuits,” Neuron 89(2), 269–284 (2016).
[Crossref] [PubMed]

S. Quirin, J. Jackson, D. S. Peterka, and R. Yuste, “Simultaneous imaging of neural activity in three dimensions,” Front. Neural Circuits 8, 29 (2014).
[Crossref] [PubMed]

S. Quirin, D. S. Peterka, and R. Yuste, “Instantaneous three-dimensional sensing using spatial light modulator illumination with extended depth of field imaging,” Opt. Express 21(13), 16007–16021 (2013).
[Crossref] [PubMed]

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, 5–19 (2008).
[Crossref] [PubMed]

Zhang, F.

F. Zhang, V. Gradinaru, A. R. Adamantidis, R. Durand, R. D. Airan, L. de Lecea, and K. Deisseroth, “Optogenetic interrogation of neural circuits: technology for probing mammalian brain structures,” Nat. Protoc. 5(3), 439–456 (2010).
[Crossref] [PubMed]

F. Zhang, A. M. Aravanis, A. Adamantidis, L. de Lecea, and K. Deisseroth, “Circuit-breakers: optical technologies for probing neural signals and systems,” Nat. Rev. Neurosci. 8(8), 577–581 (2007).
[Crossref] [PubMed]

Biomed. Opt. Express (2)

Front. Cell. Neurosci. (1)

D. Gandolfi, P. Pozzi, M. Tognolina, G. Chirico, J. Mapelli, and E. D’Angelo, “The spatiotemporal organization of cerebellar network activity resolved by two-photon imaging of multiple single neurons,” Front. Cell. Neurosci. 8, 92 (2014).
[Crossref] [PubMed]

Front. Neural Circuits (2)

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, 5–19 (2008).
[Crossref] [PubMed]

S. Quirin, J. Jackson, D. S. Peterka, and R. Yuste, “Simultaneous imaging of neural activity in three dimensions,” Front. Neural Circuits 8, 29 (2014).
[Crossref] [PubMed]

J. Biophotonics (1)

K. König, M. Weinigel, D. Hoppert, R. Bückle, H. Schubert, M. J. Köhler, M. Kaatz, and P. Elsner, “Multiphoton tissue imaging using high-NA microendoscopes and flexible scan heads for clinical studies and small animal research,” J. Biophotonics 1(6), 506–513 (2008).
[Crossref] [PubMed]

J. Neurosci. Methods (1)

S. Bovetti and T. Fellin, “Optical dissection of brain circuits with patterned illumination through the phase modulation of light,” J. Neurosci. Methods 241, 66–77 (2015).
[Crossref] [PubMed]

Nat. Methods (4)

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(10), 848–854 (2010).
[Crossref] [PubMed]

R. P. Barretto, B. Messerschmidt, and M. J. Schnitzer, “In vivo fluorescence imaging with high-resolution microlenses,” Nat. Methods 6(7), 511–512 (2009).
[Crossref] [PubMed]

A. M. Packer, L. E. Russell, H. W. Dalgleish, and M. Hausser, “Simultaneous all-optical manipulation and recording of neural circuit activity with cellular resolution in vivo,” Nat. Methods 12(2), 140–146 (2014).
[Crossref] [PubMed]

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

Nat. Neurosci. (1)

J. P. Rickgauer, K. Deisseroth, and D. W. Tank, “Simultaneous cellular-resolution optical perturbation and imaging of place cell firing fields,” Nat. Neurosci. 17(12), 1816–1824 (2014).
[Crossref] [PubMed]

Nat. Photonics (1)

E. Papagiakoumou, A. Bégue, B. Leshem, O. Schwartz, B. M. Stell, J. Bradley, D. Oron, and V. Emiliani, “Funtional patterned multiphoton excitation deep inside scattering tissue,” Nat. Photonics 7(4), 274–278 (2013).
[Crossref]

Nat. Protoc. (1)

F. Zhang, V. Gradinaru, A. R. Adamantidis, R. Durand, R. D. Airan, L. de Lecea, and K. Deisseroth, “Optogenetic interrogation of neural circuits: technology for probing mammalian brain structures,” Nat. Protoc. 5(3), 439–456 (2010).
[Crossref] [PubMed]

Nat. Rev. Neurosci. (2)

T. Knöpfel, “Genetically encoded optical indicators for the analysis of neuronal circuits,” Nat. Rev. Neurosci. 13(10), 687–700 (2012).
[PubMed]

F. Zhang, A. M. Aravanis, A. Adamantidis, L. de Lecea, and K. Deisseroth, “Circuit-breakers: optical technologies for probing neural signals and systems,” Nat. Rev. Neurosci. 8(8), 577–581 (2007).
[Crossref] [PubMed]

Nature (1)

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(7458), 295–300 (2013).
[Crossref] [PubMed]

Neuron (2)

W. Yang, J. E. Miller, L. Carrillo-Reid, E. Pnevmatikakis, L. Paninski, R. Yuste, and D. S. Peterka, “Simultaneous Multi-plane Imaging of Neural Circuits,” Neuron 89(2), 269–284 (2016).
[Crossref] [PubMed]

V. Szabo, C. Ventalon, V. De Sars, J. Bradley, and V. Emiliani, “Spatially selective holographic photoactivation and functional fluorescence imaging in freely behaving mice with a fiberscope,” Neuron 84(6), 1157–1169 (2014).
[Crossref] [PubMed]

Opt. Express (7)

A. Antonini, C. Liberale, and T. Fellin, “Fluorescent layers for characterization of sectioning microscopy with coverslip-uncorrected and water immersion objectives,” Opt. Express 22(12), 14293–14304 (2014).
[Crossref] [PubMed]

R. Di Leonardo, F. Ianni, and G. Ruocco, “Computer generation of optimal holograms for optical trap arrays,” Opt. Express 15(4), 1913–1922 (2007).
[Crossref] [PubMed]

M. Dal Maschio, F. Difato, R. Beltramo, A. Blau, F. Benfenati, and T. Fellin, “Simultaneous two-photon imaging and photo-stimulation with structured light illumination,” Opt. Express 18(18), 18720–18731 (2010).
[Crossref] [PubMed]

S. Quirin, D. S. Peterka, and R. Yuste, “Instantaneous three-dimensional sensing using spatial light modulator illumination with extended depth of field imaging,” Opt. Express 21(13), 16007–16021 (2013).
[Crossref] [PubMed]

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(25), 32573–32581 (2015).
[Crossref] [PubMed]

E. Papagiakoumou, V. de Sars, D. Oron, and V. Emiliani, “Patterned two-photon illumination by spatiotemporal shaping of ultrashort pulses,” Opt. Express 16(26), 22039–22047 (2008).
[Crossref] [PubMed]

E. Papagiakoumou, V. de Sars, V. Emiliani, and D. Oron, “Temporal focusing with spatially modulated excitation,” Opt. Express 17(7), 5391–5401 (2009).
[Crossref] [PubMed]

Opt. Lett. (1)

Optik (Stuttg.) (1)

C. J. R. Sheppard and M. Gu, “Image formation in two-photon fluroescence microscopy,” Optik (Stuttg.) 86, 104–106 (1990).

Proc. Natl. Acad. Sci. U.S.A. (1)

F. Anselmi, C. Ventalon, A. Bègue, D. Ogden, and V. Emiliani, “Three-dimensional imaging and photostimulation by remote-focusing and holographic light patterning,” Proc. Natl. Acad. Sci. U.S.A. 108(49), 19504–19509 (2011).
[Crossref] [PubMed]

Other (3)

V. A. Soifer, Methods for Computer Design of Diffractive Optical Elements, (John Wiley & Sons, Inc., 2002).

G. Paxinos and K. B. J. Franklin, The Mouse Brain in Stereotaxic Coordinates (Academic Press, ed., 2012).

Grintech product datasheet, “High-NA Endomicroscopic Imaging Objective for 2-Photon Microscopy” (Grintech, 2016). http://www.grintech.de/grin-lens-systems-for-medical-applications.html

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Figures (5)

Fig. 1
Fig. 1 a) Schematic of the optical system. LWP, half-lambda waveplate; L1-L2, beam expander lenses; SLM, phase only spatial light modulator; L3-L4, relay lenses; GM, galvo-mirror system; SL, scan lens; TL, tube lens; OBJ, microscope objective; GRIN, GRIN rod or GRIN microobjective; DIC, dichroic mirror; PMT, photomultiplier tube; L5-L6, image relay lenses; BF, barrier filter; IRF, near-infrared low-pass filter; camera, camera detector. b) Customized GRIN mounting system composed of a z translational mount (SM1Z, Thorlabs, Newton, NJ) which held the microscope objective. Proper positioning of the GRIN lens in the objective focal plane was obtained using a positioner (SPT1, Thorlabs, Newton, NJ).
Fig. 2
Fig. 2 a) Schematic of the experimental configuration. Subresolved fluorescent beads and a single excitation point, which was scanned using the galvanometric mirrors, were used for the measurement of the PSF. b-c) Images of a sub-resolution fluorescent bead in the x, y (left) and x, z (right) plane using the scanning system and the PMT as fluorescence detector for the GRIN rod (b) and the GRIN microobjective (c). Scale bars in b-c: 1 µm in the x,y projection (left image); 5 µm, in the x,z projection (right image). d) Schematic of the experimental configuration. A thin fluorescent layer was used as sample and an array of 17 diffraction- limited spots was projected on the sample. The camera was used as fluorescence detector. e-f) Fluorescence images showing the intensity profiles of a thin fluorescent layer along the z-axis for a spot in the central (left) and distal (right) part of the FOV during simultaneous projection of multiple spots using the GRIN rod (e) and the GRIN microobjective (f). Scale bars: 5 µm. g-h) FWHMz values as a function of the radial displacement for recordings performed in the optical configuration displayed in e-f for the GRIN rod (g) and the GRIN microobjective (h).
Fig. 3
Fig. 3 a) Fluorescence uniformity for the projection of an array of points onto a thick fluorescent slide under the different experimental conditions. ***, p < 0.001; ns, non-significant, p > 0.05, one-way ANOVA, Bonferroni post hoc test (N = 11).The GRIN microobjective was used for experiments displayed in this figure. b) Top: fluorescence image acquired with a camera of a two-photon extended shape projected onto a thick fluorescent slide. Scale bar: 10 µm. Bottom: intensity profile along the direction indicated by the white dashed line in the top panel. c) Fluorescence uniformity for extended shapes illumination under the different experimental conditions. p > 0.05, paired Student’s t-test (N = 10).
Fig. 4
Fig. 4 a-d) Two-photon scanning image of a group of neurons expressing the Green Fluorescent Protein- (GFP) based calcium indicator GCaMP6s (a). The desired pattern of illumination (six diffraction-limited points, b) was identified based on the location of the cells observed in a. The corresponding phase mask (c) was generated and imposed to the SLM. The fluorescence image acquired with the camera and obtained applying the phase mask displayed in c is shown in d. Scale bar: 40 µm. e-h) Same as in a-d for a different field of view and illumination with two extended shapes. Scale bar: 40 µm.
Fig. 5
Fig. 5 a) Two-photon laser scanning image showing GCaMP6 expressing cells in the CA1 hyppocampus in vivo. Red crosses indicate the neurons that were imaged in the scanless configuration and that are numbered from 1 to 10. Scale bar: 100 μm. b) Fluorescence signals over time for the neurons displayed in the left panel recorded in scanless modality.

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u=1 σ I I ¯
ξ m ( I ¯ I m ) ρ
w m k ξ m w m k

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