Abstract

Two-photon imaging using high-speed multi-channel detectors is a promising approach for optical recording of cellular membrane dynamics at multiple sites. A main bottleneck of this technique is the limited number of photons captured within a short exposure time (~1ms). Here, we implement temporal gating to improve the two-photon fluorescence yield from holographically projected multiple foci whilst maintaining a biologically safe incident average power. We observed up to 6x improvement in the signal-to-noise ratio (SNR) in Fluorescein and cultured hippocampal neurons showing evoked calcium transients. With improved SNR, we could pave the way to achieving multi-site optical recording of fluorogenic probes with response times in the order of ~1ms.

© 2016 Optical Society of America

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References

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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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2016 (1)

W. Yang, J. E. K. 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 (5)

V. Gautam, J. Drury, J. M. C. Choy, C. Stricker, H.-A. Bachor, and V. R. Daria, “Improved two-photon imaging of living neurons in brain tissue through temporal gating,” Biomed. Opt. Express 6(10), 4027–4036 (2015).
[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]

Y. Gong, C. Huang, J. Z. Li, B. F. Grewe, Y. Zhang, S. Eismann, and M. J. Schnitzer, “High-speed recording of neural spikes in awake mice and flies with a fluorescent voltage sensor,” Science 350(6266), 1361–1366 (2015).
[Crossref] [PubMed]

M. Popovic, K. Vogt, K. Holthoff, A. Konnerth, B. M. Salzberg, A. Grinvald, S. D. Antic, M. Canepari, and D. Zecevic, “Imaging Submillisecond Membrane Potential Changes from Individual Regions of Single Axons, Dendrites and Spines,” Adv. Exp. Med. Biol. 859, 57–101 (2015).
[Crossref] [PubMed]

A. J. Foust, V. Zampini, D. Tanese, E. Papagiakoumou, and V. Emiliani, “Computer-generated holography enhances voltage dye fluorescence discrimination in adjacent neuronal structures,” Neurophotonics 2(2), 021007 (2015).
[Crossref] [PubMed]

2014 (2)

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]

M. Tada, A. Takeuchi, M. Hashizume, K. Kitamura, and M. Kano, “A highly sensitive fluorescent indicator dye for calcium imaging of neural activity in vitro and in vivo,” Eur. J. Neurosci. 39(11), 1720–1728 (2014).
[Crossref] [PubMed]

2013 (2)

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]

M. Ducros, Y. Goulam Houssen, J. Bradley, V. de Sars, and S. Charpak, “Encoded multisite two-photon microscopy,” Proc. Natl. Acad. Sci. U.S.A. 110(32), 13138–13143 (2013).
[Crossref] [PubMed]

2012 (2)

M. A. Go, C. Stricker, S. Redman, H. A. Bachor, and V. R. Daria, “Simultaneous multi-site two-photon photostimulation in three dimensions,” J. Biophotonics 5(10), 745–753 (2012).
[Crossref] [PubMed]

P. Yan, C. D. Acker, W. L. Zhou, P. Lee, C. Bollensdorff, A. Negrean, J. Lotti, L. Sacconi, S. D. Antic, P. Kohl, H. D. Mansvelder, F. S. Pavone, and L. M. Loew, “Palette of fluorinated voltage-sensitive hemicyanine dyes,” Proc. Natl. Acad. Sci. U.S.A. 109(50), 20443–20448 (2012).
[Crossref] [PubMed]

2011 (1)

C. D. Acker, P. Yan, and L. M. Loew, “Single-voxel recording of voltage transients in dendritic spines,” Biophys. J. 101(2), L11–L13 (2011).
[Crossref] [PubMed]

2010 (2)

B. F. Grewe, D. Langer, H. Kasper, B. M. Kampa, and F. Helmchen, “High-speed in vivo calcium imaging reveals neuronal network activity with near-millisecond precision,” Nat. Methods 7(5), 399–405 (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]

2009 (2)

G. Donnert, C. Eggeling, and S. W. Hell, “Triplet-relaxation microscopy with bunched pulsed excitation,” Photochem. Photobiol. Sci. 8(4), 481–485 (2009).
[Crossref] [PubMed]

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(9), 093701 (2009).
[Crossref]

2008 (3)

W. L. Zhou, P. Yan, J. P. Wuskell, L. M. Loew, and S. D. Antic, “Dynamics of action potential backpropagation in basal dendrites of prefrontal cortical pyramidal neurons,” Eur. J. Neurosci. 27(4), 923–936 (2008).
[Crossref] [PubMed]

C. Lutz, T. S. Otis, V. DeSars, S. Charpak, D. A. DiGregorio, and V. Emiliani, “Holographic photolysis of caged neurotransmitters,” Nat. Methods 5(9), 821–827 (2008).
[Crossref] [PubMed]

V. Poher, N. Grossman, G. T. Kennedy, K. Nikolic, H. X. Zhang, Z. Gong, E. M. Drakakis, E. Gu, M. D. Dawson, P. M. W. French, P. Degenaar, and M. A. A. Neil, “Micro-LED arrays: a tool for two-dimensional neuron stimulation,” J. Phys. D Appl. Phys. 41(9), 094014 (2008).
[Crossref]

2007 (1)

G. Donnert, C. Eggeling, and S. W. Hell, “Major signal increase in fluorescence microscopy through dark-state relaxation,” Nat. Methods 4(1), 81–86 (2007).
[Crossref] [PubMed]

2006 (1)

G. J. Stuart and L. M. Palmer, “Imaging membrane potential in dendrites and axons of single neurons,” Pflugers Arch. 453(3), 403–410 (2006).
[Crossref] [PubMed]

2005 (1)

K. Ohki, S. Chung, Y. H. Ch’ng, P. Kara, and R. C. Reid, “Functional imaging with cellular resolution reveals precise micro-architecture in visual cortex,” Nature 433(7026), 597–603 (2005).
[Crossref] [PubMed]

2003 (1)

2001 (1)

J. Nakai, M. Ohkura, and K. Imoto, “A high signal-to-noise Ca2+ probe composed of a single green fluorescent protein,” Nat. Biotechnol. 19(2), 137–141 (2001).
[Crossref] [PubMed]

2000 (1)

J. Liesener, M. Reicherter, T. Haist, and H. J. Tiziani, “Multi-functional optical tweezers using computer-generated holograms,” Opt. Commun. 185(1-3), 77–82 (2000).
[Crossref]

1997 (1)

A. Bullen, S. S. Patel, and P. Saggau, “High-speed, random-access fluorescence microscopy: I. High-resolution optical recording with voltage-sensitive dyes and ion indicators,” Biophys. J. 73(1), 477–491 (1997).
[Crossref] [PubMed]

1996 (1)

Acker, C. D.

P. Yan, C. D. Acker, W. L. Zhou, P. Lee, C. Bollensdorff, A. Negrean, J. Lotti, L. Sacconi, S. D. Antic, P. Kohl, H. D. Mansvelder, F. S. Pavone, and L. M. Loew, “Palette of fluorinated voltage-sensitive hemicyanine dyes,” Proc. Natl. Acad. Sci. U.S.A. 109(50), 20443–20448 (2012).
[Crossref] [PubMed]

C. D. Acker, P. Yan, and L. M. Loew, “Single-voxel recording of voltage transients in dendritic spines,” Biophys. J. 101(2), L11–L13 (2011).
[Crossref] [PubMed]

Allen, W. E.

Andalman, A. S.

Antic, S. D.

M. Popovic, K. Vogt, K. Holthoff, A. Konnerth, B. M. Salzberg, A. Grinvald, S. D. Antic, M. Canepari, and D. Zecevic, “Imaging Submillisecond Membrane Potential Changes from Individual Regions of Single Axons, Dendrites and Spines,” Adv. Exp. Med. Biol. 859, 57–101 (2015).
[Crossref] [PubMed]

P. Yan, C. D. Acker, W. L. Zhou, P. Lee, C. Bollensdorff, A. Negrean, J. Lotti, L. Sacconi, S. D. Antic, P. Kohl, H. D. Mansvelder, F. S. Pavone, and L. M. Loew, “Palette of fluorinated voltage-sensitive hemicyanine dyes,” Proc. Natl. Acad. Sci. U.S.A. 109(50), 20443–20448 (2012).
[Crossref] [PubMed]

W. L. Zhou, P. Yan, J. P. Wuskell, L. M. Loew, and S. D. Antic, “Dynamics of action potential backpropagation in basal dendrites of prefrontal cortical pyramidal neurons,” Eur. J. Neurosci. 27(4), 923–936 (2008).
[Crossref] [PubMed]

Bachor, H. A.

M. A. Go, C. Stricker, S. Redman, H. A. Bachor, and V. R. Daria, “Simultaneous multi-site two-photon photostimulation in three dimensions,” J. Biophotonics 5(10), 745–753 (2012).
[Crossref] [PubMed]

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(9), 093701 (2009).
[Crossref]

Bachor, H.-A.

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]

Beltramo, R.

Benfenati, F.

Blau, A.

Bollensdorff, C.

P. Yan, C. D. Acker, W. L. Zhou, P. Lee, C. Bollensdorff, A. Negrean, J. Lotti, L. Sacconi, S. D. Antic, P. Kohl, H. D. Mansvelder, F. S. Pavone, and L. M. Loew, “Palette of fluorinated voltage-sensitive hemicyanine dyes,” Proc. Natl. Acad. Sci. U.S.A. 109(50), 20443–20448 (2012).
[Crossref] [PubMed]

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(9), 093701 (2009).
[Crossref]

Bradley, J.

M. Ducros, Y. Goulam Houssen, J. Bradley, V. de Sars, and S. Charpak, “Encoded multisite two-photon microscopy,” Proc. Natl. Acad. Sci. U.S.A. 110(32), 13138–13143 (2013).
[Crossref] [PubMed]

Bullen, A.

A. Bullen, S. S. Patel, and P. Saggau, “High-speed, random-access fluorescence microscopy: I. High-resolution optical recording with voltage-sensitive dyes and ion indicators,” Biophys. J. 73(1), 477–491 (1997).
[Crossref] [PubMed]

Canepari, M.

M. Popovic, K. Vogt, K. Holthoff, A. Konnerth, B. M. Salzberg, A. Grinvald, S. D. Antic, M. Canepari, and D. Zecevic, “Imaging Submillisecond Membrane Potential Changes from Individual Regions of Single Axons, Dendrites and Spines,” Adv. Exp. Med. Biol. 859, 57–101 (2015).
[Crossref] [PubMed]

Carrillo-Reid, L.

W. Yang, J. E. K. 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]

Ch’ng, Y. H.

K. Ohki, S. Chung, Y. H. Ch’ng, P. Kara, and R. C. Reid, “Functional imaging with cellular resolution reveals precise micro-architecture in visual cortex,” Nature 433(7026), 597–603 (2005).
[Crossref] [PubMed]

Charpak, S.

M. Ducros, Y. Goulam Houssen, J. Bradley, V. de Sars, and S. Charpak, “Encoded multisite two-photon microscopy,” Proc. Natl. Acad. Sci. U.S.A. 110(32), 13138–13143 (2013).
[Crossref] [PubMed]

C. Lutz, T. S. Otis, V. DeSars, S. Charpak, D. A. DiGregorio, and V. Emiliani, “Holographic photolysis of caged neurotransmitters,” Nat. Methods 5(9), 821–827 (2008).
[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]

Choy, J. M. C.

Chung, S.

K. Ohki, S. Chung, Y. H. Ch’ng, P. Kara, and R. C. Reid, “Functional imaging with cellular resolution reveals precise micro-architecture in visual cortex,” Nature 433(7026), 597–603 (2005).
[Crossref] [PubMed]

Dal Maschio, M.

Daria, V. R.

V. Gautam, J. Drury, J. M. C. Choy, C. Stricker, H.-A. Bachor, and V. R. Daria, “Improved two-photon imaging of living neurons in brain tissue through temporal gating,” Biomed. Opt. Express 6(10), 4027–4036 (2015).
[Crossref] [PubMed]

M. A. Go, C. Stricker, S. Redman, H. A. Bachor, and V. R. Daria, “Simultaneous multi-site two-photon photostimulation in three dimensions,” J. Biophotonics 5(10), 745–753 (2012).
[Crossref] [PubMed]

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(9), 093701 (2009).
[Crossref]

Dawson, M. D.

V. Poher, N. Grossman, G. T. Kennedy, K. Nikolic, H. X. Zhang, Z. Gong, E. M. Drakakis, E. Gu, M. D. Dawson, P. M. W. French, P. Degenaar, and M. A. A. Neil, “Micro-LED arrays: a tool for two-dimensional neuron stimulation,” J. Phys. D Appl. Phys. 41(9), 094014 (2008).
[Crossref]

de Sars, V.

M. Ducros, Y. Goulam Houssen, J. Bradley, V. de Sars, and S. Charpak, “Encoded multisite two-photon microscopy,” Proc. Natl. Acad. Sci. U.S.A. 110(32), 13138–13143 (2013).
[Crossref] [PubMed]

Degenaar, P.

V. Poher, N. Grossman, G. T. Kennedy, K. Nikolic, H. X. Zhang, Z. Gong, E. M. Drakakis, E. Gu, M. D. Dawson, P. M. W. French, P. Degenaar, and M. A. A. Neil, “Micro-LED arrays: a tool for two-dimensional neuron stimulation,” J. Phys. D Appl. Phys. 41(9), 094014 (2008).
[Crossref]

Deisseroth, K.

Denk, W.

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(9), 821–827 (2008).
[Crossref] [PubMed]

Difato, F.

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(9), 821–827 (2008).
[Crossref] [PubMed]

Donnert, G.

G. Donnert, C. Eggeling, and S. W. Hell, “Triplet-relaxation microscopy with bunched pulsed excitation,” Photochem. Photobiol. Sci. 8(4), 481–485 (2009).
[Crossref] [PubMed]

G. Donnert, C. Eggeling, and S. W. Hell, “Major signal increase in fluorescence microscopy through dark-state relaxation,” Nat. Methods 4(1), 81–86 (2007).
[Crossref] [PubMed]

Drakakis, E. M.

V. Poher, N. Grossman, G. T. Kennedy, K. Nikolic, H. X. Zhang, Z. Gong, E. M. Drakakis, E. Gu, M. D. Dawson, P. M. W. French, P. Degenaar, and M. A. A. Neil, “Micro-LED arrays: a tool for two-dimensional neuron stimulation,” J. Phys. D Appl. Phys. 41(9), 094014 (2008).
[Crossref]

Drury, J.

Ducros, M.

M. Ducros, Y. Goulam Houssen, J. Bradley, V. de Sars, and S. Charpak, “Encoded multisite two-photon microscopy,” Proc. Natl. Acad. Sci. U.S.A. 110(32), 13138–13143 (2013).
[Crossref] [PubMed]

Eggeling, C.

G. Donnert, C. Eggeling, and S. W. Hell, “Triplet-relaxation microscopy with bunched pulsed excitation,” Photochem. Photobiol. Sci. 8(4), 481–485 (2009).
[Crossref] [PubMed]

G. Donnert, C. Eggeling, and S. W. Hell, “Major signal increase in fluorescence microscopy through dark-state relaxation,” Nat. Methods 4(1), 81–86 (2007).
[Crossref] [PubMed]

Eismann, S.

Y. Gong, C. Huang, J. Z. Li, B. F. Grewe, Y. Zhang, S. Eismann, and M. J. Schnitzer, “High-speed recording of neural spikes in awake mice and flies with a fluorescent voltage sensor,” Science 350(6266), 1361–1366 (2015).
[Crossref] [PubMed]

Emiliani, V.

A. J. Foust, V. Zampini, D. Tanese, E. Papagiakoumou, and V. Emiliani, “Computer-generated holography enhances voltage dye fluorescence discrimination in adjacent neuronal structures,” Neurophotonics 2(2), 021007 (2015).
[Crossref] [PubMed]

C. Lutz, T. S. Otis, V. DeSars, S. Charpak, D. A. DiGregorio, and V. Emiliani, “Holographic photolysis of caged neurotransmitters,” Nat. Methods 5(9), 821–827 (2008).
[Crossref] [PubMed]

Fellin, T.

Foust, A. J.

A. J. Foust, V. Zampini, D. Tanese, E. Papagiakoumou, and V. Emiliani, “Computer-generated holography enhances voltage dye fluorescence discrimination in adjacent neuronal structures,” Neurophotonics 2(2), 021007 (2015).
[Crossref] [PubMed]

French, P. M. W.

V. Poher, N. Grossman, G. T. Kennedy, K. Nikolic, H. X. Zhang, Z. Gong, E. M. Drakakis, E. Gu, M. D. Dawson, P. M. W. French, P. Degenaar, and M. A. A. Neil, “Micro-LED arrays: a tool for two-dimensional neuron stimulation,” J. Phys. D Appl. Phys. 41(9), 094014 (2008).
[Crossref]

Gautam, V.

Go, M. A.

M. A. Go, C. Stricker, S. Redman, H. A. Bachor, and V. R. Daria, “Simultaneous multi-site two-photon photostimulation in three dimensions,” J. Biophotonics 5(10), 745–753 (2012).
[Crossref] [PubMed]

Gong, Y.

Y. Gong, C. Huang, J. Z. Li, B. F. Grewe, Y. Zhang, S. Eismann, and M. J. Schnitzer, “High-speed recording of neural spikes in awake mice and flies with a fluorescent voltage sensor,” Science 350(6266), 1361–1366 (2015).
[Crossref] [PubMed]

Gong, Z.

V. Poher, N. Grossman, G. T. Kennedy, K. Nikolic, H. X. Zhang, Z. Gong, E. M. Drakakis, E. Gu, M. D. Dawson, P. M. W. French, P. Degenaar, and M. A. A. Neil, “Micro-LED arrays: a tool for two-dimensional neuron stimulation,” J. Phys. D Appl. Phys. 41(9), 094014 (2008).
[Crossref]

Goulam Houssen, Y.

M. Ducros, Y. Goulam Houssen, J. Bradley, V. de Sars, and S. Charpak, “Encoded multisite two-photon microscopy,” Proc. Natl. Acad. Sci. U.S.A. 110(32), 13138–13143 (2013).
[Crossref] [PubMed]

Grewe, B. F.

Y. Gong, C. Huang, J. Z. Li, B. F. Grewe, Y. Zhang, S. Eismann, and M. J. Schnitzer, “High-speed recording of neural spikes in awake mice and flies with a fluorescent voltage sensor,” Science 350(6266), 1361–1366 (2015).
[Crossref] [PubMed]

B. F. Grewe, D. Langer, H. Kasper, B. M. Kampa, and F. Helmchen, “High-speed in vivo calcium imaging reveals neuronal network activity with near-millisecond precision,” Nat. Methods 7(5), 399–405 (2010).
[Crossref] [PubMed]

Grinvald, A.

M. Popovic, K. Vogt, K. Holthoff, A. Konnerth, B. M. Salzberg, A. Grinvald, S. D. Antic, M. Canepari, and D. Zecevic, “Imaging Submillisecond Membrane Potential Changes from Individual Regions of Single Axons, Dendrites and Spines,” Adv. Exp. Med. Biol. 859, 57–101 (2015).
[Crossref] [PubMed]

Grossman, N.

V. Poher, N. Grossman, G. T. Kennedy, K. Nikolic, H. X. Zhang, Z. Gong, E. M. Drakakis, E. Gu, M. D. Dawson, P. M. W. French, P. Degenaar, and M. A. A. Neil, “Micro-LED arrays: a tool for two-dimensional neuron stimulation,” J. Phys. D Appl. Phys. 41(9), 094014 (2008).
[Crossref]

Gu, E.

V. Poher, N. Grossman, G. T. Kennedy, K. Nikolic, H. X. Zhang, Z. Gong, E. M. Drakakis, E. Gu, M. D. Dawson, P. M. W. French, P. Degenaar, and M. A. A. Neil, “Micro-LED arrays: a tool for two-dimensional neuron stimulation,” J. Phys. D Appl. Phys. 41(9), 094014 (2008).
[Crossref]

Haist, T.

J. Liesener, M. Reicherter, T. Haist, and H. J. Tiziani, “Multi-functional optical tweezers using computer-generated holograms,” Opt. Commun. 185(1-3), 77–82 (2000).
[Crossref]

Hasan, M. T.

Hashizume, M.

M. Tada, A. Takeuchi, M. Hashizume, K. Kitamura, and M. Kano, “A highly sensitive fluorescent indicator dye for calcium imaging of neural activity in vitro and in vivo,” Eur. J. Neurosci. 39(11), 1720–1728 (2014).
[Crossref] [PubMed]

Hell, S. W.

G. Donnert, C. Eggeling, and S. W. Hell, “Triplet-relaxation microscopy with bunched pulsed excitation,” Photochem. Photobiol. Sci. 8(4), 481–485 (2009).
[Crossref] [PubMed]

G. Donnert, C. Eggeling, and S. W. Hell, “Major signal increase in fluorescence microscopy through dark-state relaxation,” Nat. Methods 4(1), 81–86 (2007).
[Crossref] [PubMed]

Helmchen, F.

B. F. Grewe, D. Langer, H. Kasper, B. M. Kampa, and F. Helmchen, “High-speed in vivo calcium imaging reveals neuronal network activity with near-millisecond precision,” Nat. Methods 7(5), 399–405 (2010).
[Crossref] [PubMed]

Holthoff, K.

M. Popovic, K. Vogt, K. Holthoff, A. Konnerth, B. M. Salzberg, A. Grinvald, S. D. Antic, M. Canepari, and D. Zecevic, “Imaging Submillisecond Membrane Potential Changes from Individual Regions of Single Axons, Dendrites and Spines,” Adv. Exp. Med. Biol. 859, 57–101 (2015).
[Crossref] [PubMed]

Huang, C.

Y. Gong, C. Huang, J. Z. Li, B. F. Grewe, Y. Zhang, S. Eismann, and M. J. Schnitzer, “High-speed recording of neural spikes in awake mice and flies with a fluorescent voltage sensor,” Science 350(6266), 1361–1366 (2015).
[Crossref] [PubMed]

Imoto, K.

J. Nakai, M. Ohkura, and K. Imoto, “A high signal-to-noise Ca2+ probe composed of a single green fluorescent protein,” Nat. Biotechnol. 19(2), 137–141 (2001).
[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]

Kampa, B. M.

B. F. Grewe, D. Langer, H. Kasper, B. M. Kampa, and F. Helmchen, “High-speed in vivo calcium imaging reveals neuronal network activity with near-millisecond precision,” Nat. Methods 7(5), 399–405 (2010).
[Crossref] [PubMed]

Kano, M.

M. Tada, A. Takeuchi, M. Hashizume, K. Kitamura, and M. Kano, “A highly sensitive fluorescent indicator dye for calcium imaging of neural activity in vitro and in vivo,” Eur. J. Neurosci. 39(11), 1720–1728 (2014).
[Crossref] [PubMed]

Kara, P.

K. Ohki, S. Chung, Y. H. Ch’ng, P. Kara, and R. C. Reid, “Functional imaging with cellular resolution reveals precise micro-architecture in visual cortex,” Nature 433(7026), 597–603 (2005).
[Crossref] [PubMed]

Kasper, H.

B. F. Grewe, D. Langer, H. Kasper, B. M. Kampa, and F. Helmchen, “High-speed in vivo calcium imaging reveals neuronal network activity with near-millisecond precision,” Nat. Methods 7(5), 399–405 (2010).
[Crossref] [PubMed]

Kauvar, I.

Kennedy, G. T.

V. Poher, N. Grossman, G. T. Kennedy, K. Nikolic, H. X. Zhang, Z. Gong, E. M. Drakakis, E. Gu, M. D. Dawson, P. M. W. French, P. Degenaar, and M. A. A. Neil, “Micro-LED arrays: a tool for two-dimensional neuron stimulation,” J. Phys. D Appl. Phys. 41(9), 094014 (2008).
[Crossref]

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]

Kitamura, K.

M. Tada, A. Takeuchi, M. Hashizume, K. Kitamura, and M. Kano, “A highly sensitive fluorescent indicator dye for calcium imaging of neural activity in vitro and in vivo,” Eur. J. Neurosci. 39(11), 1720–1728 (2014).
[Crossref] [PubMed]

Kohl, P.

P. Yan, C. D. Acker, W. L. Zhou, P. Lee, C. Bollensdorff, A. Negrean, J. Lotti, L. Sacconi, S. D. Antic, P. Kohl, H. D. Mansvelder, F. S. Pavone, and L. M. Loew, “Palette of fluorinated voltage-sensitive hemicyanine dyes,” Proc. Natl. Acad. Sci. U.S.A. 109(50), 20443–20448 (2012).
[Crossref] [PubMed]

Konnerth, A.

M. Popovic, K. Vogt, K. Holthoff, A. Konnerth, B. M. Salzberg, A. Grinvald, S. D. Antic, M. Canepari, and D. Zecevic, “Imaging Submillisecond Membrane Potential Changes from Individual Regions of Single Axons, Dendrites and Spines,” Adv. Exp. Med. Biol. 859, 57–101 (2015).
[Crossref] [PubMed]

Langer, D.

B. F. Grewe, D. Langer, H. Kasper, B. M. Kampa, and F. Helmchen, “High-speed in vivo calcium imaging reveals neuronal network activity with near-millisecond precision,” Nat. Methods 7(5), 399–405 (2010).
[Crossref] [PubMed]

Lee, P.

P. Yan, C. D. Acker, W. L. Zhou, P. Lee, C. Bollensdorff, A. Negrean, J. Lotti, L. Sacconi, S. D. Antic, P. Kohl, H. D. Mansvelder, F. S. Pavone, and L. M. Loew, “Palette of fluorinated voltage-sensitive hemicyanine dyes,” Proc. Natl. Acad. Sci. U.S.A. 109(50), 20443–20448 (2012).
[Crossref] [PubMed]

Li, J. Z.

Y. Gong, C. Huang, J. Z. Li, B. F. Grewe, Y. Zhang, S. Eismann, and M. J. Schnitzer, “High-speed recording of neural spikes in awake mice and flies with a fluorescent voltage sensor,” Science 350(6266), 1361–1366 (2015).
[Crossref] [PubMed]

Liesener, J.

J. Liesener, M. Reicherter, T. Haist, and H. J. Tiziani, “Multi-functional optical tweezers using computer-generated holograms,” Opt. Commun. 185(1-3), 77–82 (2000).
[Crossref]

Loew, L. M.

P. Yan, C. D. Acker, W. L. Zhou, P. Lee, C. Bollensdorff, A. Negrean, J. Lotti, L. Sacconi, S. D. Antic, P. Kohl, H. D. Mansvelder, F. S. Pavone, and L. M. Loew, “Palette of fluorinated voltage-sensitive hemicyanine dyes,” Proc. Natl. Acad. Sci. U.S.A. 109(50), 20443–20448 (2012).
[Crossref] [PubMed]

C. D. Acker, P. Yan, and L. M. Loew, “Single-voxel recording of voltage transients in dendritic spines,” Biophys. J. 101(2), L11–L13 (2011).
[Crossref] [PubMed]

W. L. Zhou, P. Yan, J. P. Wuskell, L. M. Loew, and S. D. Antic, “Dynamics of action potential backpropagation in basal dendrites of prefrontal cortical pyramidal neurons,” Eur. J. Neurosci. 27(4), 923–936 (2008).
[Crossref] [PubMed]

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]

Lotti, J.

P. Yan, C. D. Acker, W. L. Zhou, P. Lee, C. Bollensdorff, A. Negrean, J. Lotti, L. Sacconi, S. D. Antic, P. Kohl, H. D. Mansvelder, F. S. Pavone, and L. M. Loew, “Palette of fluorinated voltage-sensitive hemicyanine dyes,” Proc. Natl. Acad. Sci. U.S.A. 109(50), 20443–20448 (2012).
[Crossref] [PubMed]

Lutz, C.

C. Lutz, T. S. Otis, V. DeSars, S. Charpak, D. A. DiGregorio, and V. Emiliani, “Holographic photolysis of caged neurotransmitters,” Nat. Methods 5(9), 821–827 (2008).
[Crossref] [PubMed]

Mansvelder, H. D.

P. Yan, C. D. Acker, W. L. Zhou, P. Lee, C. Bollensdorff, A. Negrean, J. Lotti, L. Sacconi, S. D. Antic, P. Kohl, H. D. Mansvelder, F. S. Pavone, and L. M. Loew, “Palette of fluorinated voltage-sensitive hemicyanine dyes,” Proc. Natl. Acad. Sci. U.S.A. 109(50), 20443–20448 (2012).
[Crossref] [PubMed]

Marshel, J. H.

Miller, J. E. K.

W. Yang, J. E. K. 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]

Nakai, J.

J. Nakai, M. Ohkura, and K. Imoto, “A high signal-to-noise Ca2+ probe composed of a single green fluorescent protein,” Nat. Biotechnol. 19(2), 137–141 (2001).
[Crossref] [PubMed]

Negrean, A.

P. Yan, C. D. Acker, W. L. Zhou, P. Lee, C. Bollensdorff, A. Negrean, J. Lotti, L. Sacconi, S. D. Antic, P. Kohl, H. D. Mansvelder, F. S. Pavone, and L. M. Loew, “Palette of fluorinated voltage-sensitive hemicyanine dyes,” Proc. Natl. Acad. Sci. U.S.A. 109(50), 20443–20448 (2012).
[Crossref] [PubMed]

Neil, M. A. A.

V. Poher, N. Grossman, G. T. Kennedy, K. Nikolic, H. X. Zhang, Z. Gong, E. M. Drakakis, E. Gu, M. D. Dawson, P. M. W. French, P. Degenaar, and M. A. A. Neil, “Micro-LED arrays: a tool for two-dimensional neuron stimulation,” J. Phys. D Appl. Phys. 41(9), 094014 (2008).
[Crossref]

Nikolic, K.

V. Poher, N. Grossman, G. T. Kennedy, K. Nikolic, H. X. Zhang, Z. Gong, E. M. Drakakis, E. Gu, M. D. Dawson, P. M. W. French, P. Degenaar, and M. A. A. Neil, “Micro-LED arrays: a tool for two-dimensional neuron stimulation,” J. Phys. D Appl. Phys. 41(9), 094014 (2008).
[Crossref]

Ohki, K.

K. Ohki, S. Chung, Y. H. Ch’ng, P. Kara, and R. C. Reid, “Functional imaging with cellular resolution reveals precise micro-architecture in visual cortex,” Nature 433(7026), 597–603 (2005).
[Crossref] [PubMed]

Ohkura, M.

J. Nakai, M. Ohkura, and K. Imoto, “A high signal-to-noise Ca2+ probe composed of a single green fluorescent protein,” Nat. Biotechnol. 19(2), 137–141 (2001).
[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]

Otis, T. S.

C. Lutz, T. S. Otis, V. DeSars, S. Charpak, D. A. DiGregorio, and V. Emiliani, “Holographic photolysis of caged neurotransmitters,” Nat. Methods 5(9), 821–827 (2008).
[Crossref] [PubMed]

Palmer, L. M.

G. J. Stuart and L. M. Palmer, “Imaging membrane potential in dendrites and axons of single neurons,” Pflugers Arch. 453(3), 403–410 (2006).
[Crossref] [PubMed]

Paninski, L.

W. Yang, J. E. K. 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.

A. J. Foust, V. Zampini, D. Tanese, E. Papagiakoumou, and V. Emiliani, “Computer-generated holography enhances voltage dye fluorescence discrimination in adjacent neuronal structures,” Neurophotonics 2(2), 021007 (2015).
[Crossref] [PubMed]

Patel, S. S.

A. Bullen, S. S. Patel, and P. Saggau, “High-speed, random-access fluorescence microscopy: I. High-resolution optical recording with voltage-sensitive dyes and ion indicators,” Biophys. J. 73(1), 477–491 (1997).
[Crossref] [PubMed]

Pavone, F. S.

P. Yan, C. D. Acker, W. L. Zhou, P. Lee, C. Bollensdorff, A. Negrean, J. Lotti, L. Sacconi, S. D. Antic, P. Kohl, H. D. Mansvelder, F. S. Pavone, and L. M. Loew, “Palette of fluorinated voltage-sensitive hemicyanine dyes,” Proc. Natl. Acad. Sci. U.S.A. 109(50), 20443–20448 (2012).
[Crossref] [PubMed]

Peterka, D. S.

W. Yang, J. E. K. 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]

Pnevmatikakis, E.

W. Yang, J. E. K. 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]

Poher, V.

V. Poher, N. Grossman, G. T. Kennedy, K. Nikolic, H. X. Zhang, Z. Gong, E. M. Drakakis, E. Gu, M. D. Dawson, P. M. W. French, P. Degenaar, and M. A. A. Neil, “Micro-LED arrays: a tool for two-dimensional neuron stimulation,” J. Phys. D Appl. Phys. 41(9), 094014 (2008).
[Crossref]

Popovic, M.

M. Popovic, K. Vogt, K. Holthoff, A. Konnerth, B. M. Salzberg, A. Grinvald, S. D. Antic, M. Canepari, and D. Zecevic, “Imaging Submillisecond Membrane Potential Changes from Individual Regions of Single Axons, Dendrites and Spines,” Adv. Exp. Med. Biol. 859, 57–101 (2015).
[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.

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]

Redman, S.

M. A. Go, C. Stricker, S. Redman, H. A. Bachor, and V. R. Daria, “Simultaneous multi-site two-photon photostimulation in three dimensions,” J. Biophotonics 5(10), 745–753 (2012).
[Crossref] [PubMed]

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(9), 093701 (2009).
[Crossref]

Reicherter, M.

J. Liesener, M. Reicherter, T. Haist, and H. J. Tiziani, “Multi-functional optical tweezers using computer-generated holograms,” Opt. Commun. 185(1-3), 77–82 (2000).
[Crossref]

Reid, R. C.

K. Ohki, S. Chung, Y. H. Ch’ng, P. Kara, and R. C. Reid, “Functional imaging with cellular resolution reveals precise micro-architecture in visual cortex,” Nature 433(7026), 597–603 (2005).
[Crossref] [PubMed]

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]

Sacconi, L.

P. Yan, C. D. Acker, W. L. Zhou, P. Lee, C. Bollensdorff, A. Negrean, J. Lotti, L. Sacconi, S. D. Antic, P. Kohl, H. D. Mansvelder, F. S. Pavone, and L. M. Loew, “Palette of fluorinated voltage-sensitive hemicyanine dyes,” Proc. Natl. Acad. Sci. U.S.A. 109(50), 20443–20448 (2012).
[Crossref] [PubMed]

Saggau, P.

A. Bullen, S. S. Patel, and P. Saggau, “High-speed, random-access fluorescence microscopy: I. High-resolution optical recording with voltage-sensitive dyes and ion indicators,” Biophys. J. 73(1), 477–491 (1997).
[Crossref] [PubMed]

Salzberg, B. M.

M. Popovic, K. Vogt, K. Holthoff, A. Konnerth, B. M. Salzberg, A. Grinvald, S. D. Antic, M. Canepari, and D. Zecevic, “Imaging Submillisecond Membrane Potential Changes from Individual Regions of Single Axons, Dendrites and Spines,” Adv. Exp. Med. Biol. 859, 57–101 (2015).
[Crossref] [PubMed]

Schnitzer, M. J.

Y. Gong, C. Huang, J. Z. Li, B. F. Grewe, Y. Zhang, S. Eismann, and M. J. Schnitzer, “High-speed recording of neural spikes in awake mice and flies with a fluorescent voltage sensor,” Science 350(6266), 1361–1366 (2015).
[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]

Stricker, C.

V. Gautam, J. Drury, J. M. C. Choy, C. Stricker, H.-A. Bachor, and V. R. Daria, “Improved two-photon imaging of living neurons in brain tissue through temporal gating,” Biomed. Opt. Express 6(10), 4027–4036 (2015).
[Crossref] [PubMed]

M. A. Go, C. Stricker, S. Redman, H. A. Bachor, and V. R. Daria, “Simultaneous multi-site two-photon photostimulation in three dimensions,” J. Biophotonics 5(10), 745–753 (2012).
[Crossref] [PubMed]

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(9), 093701 (2009).
[Crossref]

Stuart, G. J.

G. J. Stuart and L. M. Palmer, “Imaging membrane potential in dendrites and axons of single neurons,” Pflugers Arch. 453(3), 403–410 (2006).
[Crossref] [PubMed]

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]

Tada, M.

M. Tada, A. Takeuchi, M. Hashizume, K. Kitamura, and M. Kano, “A highly sensitive fluorescent indicator dye for calcium imaging of neural activity in vitro and in vivo,” Eur. J. Neurosci. 39(11), 1720–1728 (2014).
[Crossref] [PubMed]

Takeuchi, A.

M. Tada, A. Takeuchi, M. Hashizume, K. Kitamura, and M. Kano, “A highly sensitive fluorescent indicator dye for calcium imaging of neural activity in vitro and in vivo,” Eur. J. Neurosci. 39(11), 1720–1728 (2014).
[Crossref] [PubMed]

Tanese, D.

A. J. Foust, V. Zampini, D. Tanese, E. Papagiakoumou, and V. Emiliani, “Computer-generated holography enhances voltage dye fluorescence discrimination in adjacent neuronal structures,” Neurophotonics 2(2), 021007 (2015).
[Crossref] [PubMed]

Theer, P.

Tiziani, H. J.

J. Liesener, M. Reicherter, T. Haist, and H. J. Tiziani, “Multi-functional optical tweezers using computer-generated holograms,” Opt. Commun. 185(1-3), 77–82 (2000).
[Crossref]

Vogt, K.

M. Popovic, K. Vogt, K. Holthoff, A. Konnerth, B. M. Salzberg, A. Grinvald, S. D. Antic, M. Canepari, and D. Zecevic, “Imaging Submillisecond Membrane Potential Changes from Individual Regions of Single Axons, Dendrites and Spines,” Adv. Exp. Med. Biol. 859, 57–101 (2015).
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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).
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Wetzstein, G.

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W. L. Zhou, P. Yan, J. P. Wuskell, L. M. Loew, and S. D. Antic, “Dynamics of action potential backpropagation in basal dendrites of prefrontal cortical pyramidal neurons,” Eur. J. Neurosci. 27(4), 923–936 (2008).
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C. D. Acker, P. Yan, and L. M. Loew, “Single-voxel recording of voltage transients in dendritic spines,” Biophys. J. 101(2), L11–L13 (2011).
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W. L. Zhou, P. Yan, J. P. Wuskell, L. M. Loew, and S. D. Antic, “Dynamics of action potential backpropagation in basal dendrites of prefrontal cortical pyramidal neurons,” Eur. J. Neurosci. 27(4), 923–936 (2008).
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Yang, W.

W. Yang, J. E. K. 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).
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W. Yang, J. E. K. 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).
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S. Quirin, J. Jackson, D. S. Peterka, and R. Yuste, “Simultaneous imaging of neural activity in three dimensions,” Front. Neural Circuits 8, 29 (2014).
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Zampini, V.

A. J. Foust, V. Zampini, D. Tanese, E. Papagiakoumou, and V. Emiliani, “Computer-generated holography enhances voltage dye fluorescence discrimination in adjacent neuronal structures,” Neurophotonics 2(2), 021007 (2015).
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M. Popovic, K. Vogt, K. Holthoff, A. Konnerth, B. M. Salzberg, A. Grinvald, S. D. Antic, M. Canepari, and D. Zecevic, “Imaging Submillisecond Membrane Potential Changes from Individual Regions of Single Axons, Dendrites and Spines,” Adv. Exp. Med. Biol. 859, 57–101 (2015).
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Zhang, H. X.

V. Poher, N. Grossman, G. T. Kennedy, K. Nikolic, H. X. Zhang, Z. Gong, E. M. Drakakis, E. Gu, M. D. Dawson, P. M. W. French, P. Degenaar, and M. A. A. Neil, “Micro-LED arrays: a tool for two-dimensional neuron stimulation,” J. Phys. D Appl. Phys. 41(9), 094014 (2008).
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Y. Gong, C. Huang, J. Z. Li, B. F. Grewe, Y. Zhang, S. Eismann, and M. J. Schnitzer, “High-speed recording of neural spikes in awake mice and flies with a fluorescent voltage sensor,” Science 350(6266), 1361–1366 (2015).
[Crossref] [PubMed]

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P. Yan, C. D. Acker, W. L. Zhou, P. Lee, C. Bollensdorff, A. Negrean, J. Lotti, L. Sacconi, S. D. Antic, P. Kohl, H. D. Mansvelder, F. S. Pavone, and L. M. Loew, “Palette of fluorinated voltage-sensitive hemicyanine dyes,” Proc. Natl. Acad. Sci. U.S.A. 109(50), 20443–20448 (2012).
[Crossref] [PubMed]

W. L. Zhou, P. Yan, J. P. Wuskell, L. M. Loew, and S. D. Antic, “Dynamics of action potential backpropagation in basal dendrites of prefrontal cortical pyramidal neurons,” Eur. J. Neurosci. 27(4), 923–936 (2008).
[Crossref] [PubMed]

Adv. Exp. Med. Biol. (1)

M. Popovic, K. Vogt, K. Holthoff, A. Konnerth, B. M. Salzberg, A. Grinvald, S. D. Antic, M. Canepari, and D. Zecevic, “Imaging Submillisecond Membrane Potential Changes from Individual Regions of Single Axons, Dendrites and Spines,” Adv. Exp. Med. Biol. 859, 57–101 (2015).
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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(9), 093701 (2009).
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Biomed. Opt. Express (1)

Biophys. J. (2)

C. D. Acker, P. Yan, and L. M. Loew, “Single-voxel recording of voltage transients in dendritic spines,” Biophys. J. 101(2), L11–L13 (2011).
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[Crossref] [PubMed]

M. Tada, A. Takeuchi, M. Hashizume, K. Kitamura, and M. Kano, “A highly sensitive fluorescent indicator dye for calcium imaging of neural activity in vitro and in vivo,” Eur. J. Neurosci. 39(11), 1720–1728 (2014).
[Crossref] [PubMed]

Front. Neural Circuits (1)

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)

M. A. Go, C. Stricker, S. Redman, H. A. Bachor, and V. R. Daria, “Simultaneous multi-site two-photon photostimulation in three dimensions,” J. Biophotonics 5(10), 745–753 (2012).
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J. Opt. Soc. Am. B (1)

J. Phys. D Appl. Phys. (1)

V. Poher, N. Grossman, G. T. Kennedy, K. Nikolic, H. X. Zhang, Z. Gong, E. M. Drakakis, E. Gu, M. D. Dawson, P. M. W. French, P. Degenaar, and M. A. A. Neil, “Micro-LED arrays: a tool for two-dimensional neuron stimulation,” J. Phys. D Appl. Phys. 41(9), 094014 (2008).
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Nat. Biotechnol. (1)

J. Nakai, M. Ohkura, and K. Imoto, “A high signal-to-noise Ca2+ probe composed of a single green fluorescent protein,” Nat. Biotechnol. 19(2), 137–141 (2001).
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Nat. Methods (3)

B. F. Grewe, D. Langer, H. Kasper, B. M. Kampa, and F. Helmchen, “High-speed in vivo calcium imaging reveals neuronal network activity with near-millisecond precision,” Nat. Methods 7(5), 399–405 (2010).
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C. Lutz, T. S. Otis, V. DeSars, S. Charpak, D. A. DiGregorio, and V. Emiliani, “Holographic photolysis of caged neurotransmitters,” Nat. Methods 5(9), 821–827 (2008).
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G. Donnert, C. Eggeling, and S. W. Hell, “Major signal increase in fluorescence microscopy through dark-state relaxation,” Nat. Methods 4(1), 81–86 (2007).
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Nature (2)

K. Ohki, S. Chung, Y. H. Ch’ng, P. Kara, and R. C. Reid, “Functional imaging with cellular resolution reveals precise micro-architecture in visual cortex,” Nature 433(7026), 597–603 (2005).
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T. W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
[Crossref] [PubMed]

Neuron (1)

W. Yang, J. E. K. 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]

Neurophotonics (1)

A. J. Foust, V. Zampini, D. Tanese, E. Papagiakoumou, and V. Emiliani, “Computer-generated holography enhances voltage dye fluorescence discrimination in adjacent neuronal structures,” Neurophotonics 2(2), 021007 (2015).
[Crossref] [PubMed]

Opt. Commun. (1)

J. Liesener, M. Reicherter, T. Haist, and H. J. Tiziani, “Multi-functional optical tweezers using computer-generated holograms,” Opt. Commun. 185(1-3), 77–82 (2000).
[Crossref]

Opt. Express (2)

Opt. Lett. (1)

Pflugers Arch. (1)

G. J. Stuart and L. M. Palmer, “Imaging membrane potential in dendrites and axons of single neurons,” Pflugers Arch. 453(3), 403–410 (2006).
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Proc. Natl. Acad. Sci. U.S.A. (2)

P. Yan, C. D. Acker, W. L. Zhou, P. Lee, C. Bollensdorff, A. Negrean, J. Lotti, L. Sacconi, S. D. Antic, P. Kohl, H. D. Mansvelder, F. S. Pavone, and L. M. Loew, “Palette of fluorinated voltage-sensitive hemicyanine dyes,” Proc. Natl. Acad. Sci. U.S.A. 109(50), 20443–20448 (2012).
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M. Ducros, Y. Goulam Houssen, J. Bradley, V. de Sars, and S. Charpak, “Encoded multisite two-photon microscopy,” Proc. Natl. Acad. Sci. U.S.A. 110(32), 13138–13143 (2013).
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Science (1)

Y. Gong, C. Huang, J. Z. Li, B. F. Grewe, Y. Zhang, S. Eismann, and M. J. Schnitzer, “High-speed recording of neural spikes in awake mice and flies with a fluorescent voltage sensor,” Science 350(6266), 1361–1366 (2015).
[Crossref] [PubMed]

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Figures (4)

Fig. 1
Fig. 1 The holographic two-photon microscope for multisite fluorescence monitoring using a CMOS camera. Multi-site fluorescence imaging is achieved by holographically splitting the laser into multi-foci using a spatial light modulator (SLM). The laser is temporally gated with an acousto-optic modulator (AOM), to enhance the fluorescence yield from the multi-foci.
Fig. 2
Fig. 2 (a) Sample time-series across <Pout>/N ~2 to 6mW for ungated and temporally gated beam and sample negative images of the fluorescence from the holographic sites at <P>/N = 4mW, (b) The plot of fluorescence of each site with power, (c) The fluctuations of the fluorescence with power (d) The pooled SNR of each site for gated beam (fR = 0.8 and 1.6 MHz) relative to the SNR of the ungated beam (U).
Fig. 3
Fig. 3 (a) Epifluorescence image of the neuronal cultures loaded with Cal-520 dye with the positions of the eight holographically projected two-photon sites. (b) A sample time-series plot of the fluorescence of each site for ungated and temporally gated beam at 4mW average power (c) The relative change in the fluorescence under 0.8 MHz and 4 mW temporally gated beam (d) The pooled SNR ratio of the temporally gated beam relative to the ungated beam. The scale bar is 50µm.
Fig. 4
Fig. 4 Diagram of the relative number of photoelectrons with exposure time for 0.8 MHz (red line) temporally gated and ungated beam (black line) captured by the CMOS camera, and for 0.8 MHz temporally gated beam using an EMCCD(blue line). The exposure time can be reduced down to 7.58 ms (red broken line) with 0.8 MHz temporally gated beam for collecting the same number of photo-electrons (N0.8MHz/Nungated = 1, horizontal broken line) as that of the ungated beam at 50ms exposure. Using an EMCCD with temporal gating, the exposure time can be further reduced to ~0.28 ms (blue broken line).

Equations (7)

Equations on this page are rendered with MathJax. Learn more.

P(r)=δ(r) P in N
F(r)=αP (r) 2
F(r) = 1 T o 0 T o F(r) dt =k= 1 T o ( 0 T o F(r) dt+ τ f R 1 F(r) dt ) = f R (τF(r))+0
P out f R 1 =τ P in
F(r) =α( 1 τ f R ) [ δ(r) P out N ] 2 .
SNR(r)= F(r) /σ
ΔF F = F(t) F b F b max

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