Abstract

We optimize two-photon imaging of living neurons in brain tissue by temporally gating an incident laser to reduce the photon flux while optimizing the maximum fluorescence signal from the acquired images. Temporal gating produces a bunch of ~10 femtosecond pulses and the fluorescence signal is improved by increasing the bunch-pulse energy. Gating is achieved using an acousto-optic modulator with a variable gating frequency determined as integral multiples of the imaging sampling frequency. We hypothesize that reducing the photon flux minimizes the photo-damage to the cells. Our results, however, show that despite producing a high fluorescence signal, cell viability is compromised when the gating and sampling frequencies are equal (or effectively one bunch-pulse per pixel). We found an optimum gating frequency range that maintains the viability of the cells while preserving a pre-set fluorescence signal of the acquired two-photon images. The neurons are imaged while under whole-cell patch, and the cell viability is monitored as a change in the membrane’s input resistance.

© 2015 Optical Society of America

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2015 (2)

I. A. Ghouri, A. Kelly, F. L. Burton, G. L. Smith, and O. J. Kemi, “2-photon excitation fluorescence microscopy enables deeper high-resolution imaging of voltage and Ca2+ in intact mice, rat, and rabbit hearts,” J. Biophotonics 8(1-2), 112–123 (2015).
[Crossref] [PubMed]

P. Lai, L. Wang, J. W. Tay, and L. V. Wang, “Photoacoustically guided wavefront shaping for enhanced optical focusing in scattering media,” Nat. Photonics 9(2), 126–132 (2015).
[Crossref] [PubMed]

2014 (3)

G. Thériault, M. Cottet, A. Castonguay, N. McCarthy, and Y. De Koninck, “Extended two-photon microscopy in live samples with Bessel beams: steadier focus, faster volume scans, and simpler stereoscopic imaging,” Front. Cell. Neurosci. 8, 139 (2014).
[PubMed]

R. J. Low, Y. Gu, and D. W. Tank, “Cellular resolution optical access to brain regions in fissures: imaging medial prefrontal cortex and grid cells in entorhinal cortex,” Proc. Natl. Acad. Sci. U.S.A. 111(52), 18739–18744 (2014).
[Crossref] [PubMed]

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

2013 (4)

M. A. Go, M. S. To, C. Stricker, S. Redman, H.-A. Bachor, G. J. Stuart, and V. R. Daria, “Four-dimensional multi-site photolysis of caged neurotransmitters,” Front. Cell. Neurosci. 7, 231 (2013).
[Crossref] [PubMed]

N. R. Wilson, J. Schummers, C. A. Runyan, S. X. Yan, R. E. Chen, Y. Deng, and M. Sur, “Two-way communication with neural networks in vivo using focused light,” Nat. Protoc. 8(6), 1184–1203 (2013).
[Crossref] [PubMed]

E. Ronzitti, B. Harke, and A. Diaspro, “Frequency dependent detection in a STED microscope using modulated excitation light,” Opt. Express 21(1), 210–219 (2013).
[Crossref] [PubMed]

M. Yamanaka, K. Saito, N. I. Smith, S. Kawata, T. Nagai, and K. Fujita, “Saturated excitation of fluorescent proteins for subdiffraction-limited imaging of living cells in three dimensions,” Interface Focus 3(5), 20130007 (2013).
[Crossref] [PubMed]

2012 (3)

A. P. Mosk, A. Lagendijk, G. Lerosey, and M. Fink, “Controlling waves in space and time for imaging and focusing in complex media,” Nat. Photonics 6(5), 283–292 (2012).
[Crossref]

X. Chen, U. Leischner, Z. Varga, H. Jia, D. Deca, N. L. Rochefort, and A. Konnerth, “LOTOS-based two-photon calcium imaging of dendritic spines in vivo,” Nat. Protoc. 7(10), 1818–1829 (2012).
[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]

2011 (2)

T. Abraham, J. A. Hirota, S. Wadsworth, and D. A. Knight, “Minimally invasive multiphoton and harmonic generation imaging of extracellular matrix structures in lung airway and related diseases,” Pulm. Pharmacol. Ther. 24(5), 487–496 (2011).
[Crossref] [PubMed]

D. Kobat, N. G. Horton, and C. Xu, “In vivo two-photon microscopy to 1.6-mm depth in mouse cortex,” J. Biomed. Opt. 16(10), 106014 (2011).
[Crossref] [PubMed]

2010 (3)

S. W. Botchway, P. Reynolds, A. W. Parker, and P. O’Neill, “Use of near infrared femtosecond lasers as sub-micron radiation microbeam for cell DNA damage and repair studies,” Mutat. Res. 704(1-3), 38–44 (2010).
[Crossref] [PubMed]

H. Lütcke, M. Murayama, T. Hahn, D. J. Margolis, S. Astori, S. M. Zum Alten Borgloh, W. Göbel, Y. Yang, W. Tang, S. Kügler, R. Sprengel, T. Nagai, A. Miyawaki, M. E. Larkum, F. Helmchen, and M. T. Hasan, “Optical recording of neuronal activity with a genetically-encoded calcium indicator in anesthetized and freely moving mice,” Front. Neural Circuits 4, 9 (2010).
[PubMed]

P. A. Kirkby, K. M. Srinivas Nadella, and R. A. Silver, “A compact Acousto-Optic Lens for 2D and 3D femtosecond based 2-photon microscopy,” Opt. Express 18(13), 13720–13745 (2010).
[Crossref] [PubMed]

2009 (4)

N. Olivier, A. Mermillod-Blondin, C. B. Arnold, and E. Beaurepaire, “Two-photon microscopy with simultaneous standard and extended depth of field using a tunable acoustic gradient-index lens,” Opt. Lett. 34(11), 1684–1686 (2009).
[Crossref] [PubMed]

B. E. Losavio, V. Iyer, and P. Saggau, “Two-photon microscope for multisite microphotolysis of caged neurotransmitters in acute brain slices,” J. Biomed. Opt. 14(6), 064033 (2009).
[Crossref] [PubMed]

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]

H. He, K. T. Chan, S. K. Kong, and R. K. Y. Lee, “Mechanism of oxidative stress generation in cells by localized near-infrared femtosecond laser excitation,” Appl. Phys. Lett. 95(23), 233702 (2009).
[Crossref]

2008 (2)

N. Ji, J. C. Magee, and E. Betzig, “High-speed, low-photodamage nonlinear imaging using passive pulse splitters,” Nat. Methods 5(2), 197–202 (2008).
[Crossref] [PubMed]

D. J. Wallace, S. Meyer zum Alten Borgloh, S. Astori, Y. Yang, M. Bausen, S. Kügler, A. E. Palmer, R. Y. Tsien, R. Sprengel, J. N. Kerr, W. Denk, and M. T. Hasan, “Single-spike detection in vitro and in vivo with a genetic Ca2+ sensor,” Nat. Methods 5(9), 797–804 (2008).
[Crossref] [PubMed]

2007 (3)

V. Nikolenko, K. E. Poskanzer, and R. Yuste, “Two-photon photostimulation and imaging of neural circuits,” Nat. Methods 4(11), 943–950 (2007).
[Crossref] [PubMed]

K. Fujita, M. Kobayashi, S. Kawano, M. Yamanaka, and S. Kawata, “High-resolution confocal microscopy by saturated excitation of fluorescence,” Phys. Rev. Lett. 99(22), 228105 (2007).
[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]

2006 (2)

S. Tang, T. B. Krasieva, Z. Chen, G. Tempea, and B. J. Tromberg, “Effect of pulse duration on two-photon excited fluorescence and second harmonic generation in nonlinear optical microscopy,” J. Biomed. Opt. 11(2), 020501 (2006).
[Crossref] [PubMed]

K. Svoboda and R. Yasuda, “Principles of two-photon excitation microscopy and its applications to neuroscience,” Neuron 50(6), 823–839 (2006).
[Crossref] [PubMed]

2005 (1)

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

2004 (1)

G. McConnell and E. Riis, “Two-photon laser scanning fluorescence microscopy using photonic crystal fiber,” J. Biomed. Opt. 9(5), 922–927 (2004).
[Crossref] [PubMed]

2003 (1)

C. Stosiek, O. Garaschuk, K. Holthoff, and A. Konnerth, “In vivo two-photon calcium imaging of neuronal networks,” Proc. Natl. Acad. Sci. U.S.A. 100(12), 7319–7324 (2003).
[Crossref] [PubMed]

2001 (3)

A. Hopt and E. Neher, “Highly nonlinear photodamage in two-photon fluorescence microscopy,” Biophys. J. 80(4), 2029–2036 (2001).
[Crossref] [PubMed]

E. Beaurepaire, M. Oheim, and J. Mertz, “Ultra-deep two-photon fluorescence excitation in turbid media,” Opt. Commun. 188(1-4), 25–29 (2001).
[Crossref]

U. K. Tirlapur, K. König, C. Peuckert, R. Krieg, and K.-J. Halbhuber, “Femtosecond near-infrared laser pulses elicit generation of reactive oxygen species in mammalian cells leading to apoptosis-like death,” Exp. Cell Res. 263(1), 88–97 (2001).
[Crossref] [PubMed]

1997 (1)

1996 (1)

1990 (1)

W. Denk, J. H. Strickler, and W. W. Webb, “Two-photon laser scanning fluorescence microscopy,” Science 248(4951), 73–76 (1990).
[Crossref] [PubMed]

Abraham, T.

T. Abraham, J. A. Hirota, S. Wadsworth, and D. A. Knight, “Minimally invasive multiphoton and harmonic generation imaging of extracellular matrix structures in lung airway and related diseases,” Pulm. Pharmacol. Ther. 24(5), 487–496 (2011).
[Crossref] [PubMed]

Arnold, C. B.

Astori, S.

H. Lütcke, M. Murayama, T. Hahn, D. J. Margolis, S. Astori, S. M. Zum Alten Borgloh, W. Göbel, Y. Yang, W. Tang, S. Kügler, R. Sprengel, T. Nagai, A. Miyawaki, M. E. Larkum, F. Helmchen, and M. T. Hasan, “Optical recording of neuronal activity with a genetically-encoded calcium indicator in anesthetized and freely moving mice,” Front. Neural Circuits 4, 9 (2010).
[PubMed]

D. J. Wallace, S. Meyer zum Alten Borgloh, S. Astori, Y. Yang, M. Bausen, S. Kügler, A. E. Palmer, R. Y. Tsien, R. Sprengel, J. N. Kerr, W. Denk, and M. T. Hasan, “Single-spike detection in vitro and in vivo with a genetic Ca2+ sensor,” Nat. Methods 5(9), 797–804 (2008).
[Crossref] [PubMed]

Bachor, H.-A.

M. A. Go, M. S. To, C. Stricker, S. Redman, H.-A. Bachor, G. J. Stuart, and V. R. Daria, “Four-dimensional multi-site photolysis of caged neurotransmitters,” Front. Cell. Neurosci. 7, 231 (2013).
[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]

Bausen, M.

D. J. Wallace, S. Meyer zum Alten Borgloh, S. Astori, Y. Yang, M. Bausen, S. Kügler, A. E. Palmer, R. Y. Tsien, R. Sprengel, J. N. Kerr, W. Denk, and M. T. Hasan, “Single-spike detection in vitro and in vivo with a genetic Ca2+ sensor,” Nat. Methods 5(9), 797–804 (2008).
[Crossref] [PubMed]

Beaurepaire, E.

Betzig, E.

N. Ji, J. C. Magee, and E. Betzig, “High-speed, low-photodamage nonlinear imaging using passive pulse splitters,” Nat. Methods 5(2), 197–202 (2008).
[Crossref] [PubMed]

Botchway, S. W.

S. W. Botchway, P. Reynolds, A. W. Parker, and P. O’Neill, “Use of near infrared femtosecond lasers as sub-micron radiation microbeam for cell DNA damage and repair studies,” Mutat. Res. 704(1-3), 38–44 (2010).
[Crossref] [PubMed]

Burton, F. L.

I. A. Ghouri, A. Kelly, F. L. Burton, G. L. Smith, and O. J. Kemi, “2-photon excitation fluorescence microscopy enables deeper high-resolution imaging of voltage and Ca2+ in intact mice, rat, and rabbit hearts,” J. Biophotonics 8(1-2), 112–123 (2015).
[Crossref] [PubMed]

Castonguay, A.

G. Thériault, M. Cottet, A. Castonguay, N. McCarthy, and Y. De Koninck, “Extended two-photon microscopy in live samples with Bessel beams: steadier focus, faster volume scans, and simpler stereoscopic imaging,” Front. Cell. Neurosci. 8, 139 (2014).
[PubMed]

Chan, K. T.

H. He, K. T. Chan, S. K. Kong, and R. K. Y. Lee, “Mechanism of oxidative stress generation in cells by localized near-infrared femtosecond laser excitation,” Appl. Phys. Lett. 95(23), 233702 (2009).
[Crossref]

Chen, R. E.

N. R. Wilson, J. Schummers, C. A. Runyan, S. X. Yan, R. E. Chen, Y. Deng, and M. Sur, “Two-way communication with neural networks in vivo using focused light,” Nat. Protoc. 8(6), 1184–1203 (2013).
[Crossref] [PubMed]

Chen, X.

X. Chen, U. Leischner, Z. Varga, H. Jia, D. Deca, N. L. Rochefort, and A. Konnerth, “LOTOS-based two-photon calcium imaging of dendritic spines in vivo,” Nat. Protoc. 7(10), 1818–1829 (2012).
[Crossref] [PubMed]

Chen, Z.

S. Tang, T. B. Krasieva, Z. Chen, G. Tempea, and B. J. Tromberg, “Effect of pulse duration on two-photon excited fluorescence and second harmonic generation in nonlinear optical microscopy,” J. Biomed. Opt. 11(2), 020501 (2006).
[Crossref] [PubMed]

Cottet, M.

G. Thériault, M. Cottet, A. Castonguay, N. McCarthy, and Y. De Koninck, “Extended two-photon microscopy in live samples with Bessel beams: steadier focus, faster volume scans, and simpler stereoscopic imaging,” Front. Cell. Neurosci. 8, 139 (2014).
[PubMed]

Dalgleish, H. W. P.

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

Daria, V. R.

M. A. Go, M. S. To, C. Stricker, S. Redman, H.-A. Bachor, G. J. Stuart, and V. R. Daria, “Four-dimensional multi-site photolysis of caged neurotransmitters,” Front. Cell. Neurosci. 7, 231 (2013).
[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]

De Koninck, Y.

G. Thériault, M. Cottet, A. Castonguay, N. McCarthy, and Y. De Koninck, “Extended two-photon microscopy in live samples with Bessel beams: steadier focus, faster volume scans, and simpler stereoscopic imaging,” Front. Cell. Neurosci. 8, 139 (2014).
[PubMed]

Deca, D.

X. Chen, U. Leischner, Z. Varga, H. Jia, D. Deca, N. L. Rochefort, and A. Konnerth, “LOTOS-based two-photon calcium imaging of dendritic spines in vivo,” Nat. Protoc. 7(10), 1818–1829 (2012).
[Crossref] [PubMed]

Deng, Y.

N. R. Wilson, J. Schummers, C. A. Runyan, S. X. Yan, R. E. Chen, Y. Deng, and M. Sur, “Two-way communication with neural networks in vivo using focused light,” Nat. Protoc. 8(6), 1184–1203 (2013).
[Crossref] [PubMed]

Denk, W.

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G. Donnert, C. Eggeling, and S. W. Hell, “Triplet-relaxation microscopy with bunched pulsed excitation,” Photochem. Photobiol. Sci. 8(4), 481–485 (2009).
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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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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).
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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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A. P. Mosk, A. Lagendijk, G. Lerosey, and M. Fink, “Controlling waves in space and time for imaging and focusing in complex media,” Nat. Photonics 6(5), 283–292 (2012).
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M. Yamanaka, K. Saito, N. I. Smith, S. Kawata, T. Nagai, and K. Fujita, “Saturated excitation of fluorescent proteins for subdiffraction-limited imaging of living cells in three dimensions,” Interface Focus 3(5), 20130007 (2013).
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K. Fujita, M. Kobayashi, S. Kawano, M. Yamanaka, and S. Kawata, “High-resolution confocal microscopy by saturated excitation of fluorescence,” Phys. Rev. Lett. 99(22), 228105 (2007).
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Garaschuk, O.

C. Stosiek, O. Garaschuk, K. Holthoff, and A. Konnerth, “In vivo two-photon calcium imaging of neuronal networks,” Proc. Natl. Acad. Sci. U.S.A. 100(12), 7319–7324 (2003).
[Crossref] [PubMed]

Ghouri, I. A.

I. A. Ghouri, A. Kelly, F. L. Burton, G. L. Smith, and O. J. Kemi, “2-photon excitation fluorescence microscopy enables deeper high-resolution imaging of voltage and Ca2+ in intact mice, rat, and rabbit hearts,” J. Biophotonics 8(1-2), 112–123 (2015).
[Crossref] [PubMed]

Go, M. A.

M. A. Go, M. S. To, C. Stricker, S. Redman, H.-A. Bachor, G. J. Stuart, and V. R. Daria, “Four-dimensional multi-site photolysis of caged neurotransmitters,” Front. Cell. Neurosci. 7, 231 (2013).
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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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H. Lütcke, M. Murayama, T. Hahn, D. J. Margolis, S. Astori, S. M. Zum Alten Borgloh, W. Göbel, Y. Yang, W. Tang, S. Kügler, R. Sprengel, T. Nagai, A. Miyawaki, M. E. Larkum, F. Helmchen, and M. T. Hasan, “Optical recording of neuronal activity with a genetically-encoded calcium indicator in anesthetized and freely moving mice,” Front. Neural Circuits 4, 9 (2010).
[PubMed]

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Gu, Y.

R. J. Low, Y. Gu, and D. W. Tank, “Cellular resolution optical access to brain regions in fissures: imaging medial prefrontal cortex and grid cells in entorhinal cortex,” Proc. Natl. Acad. Sci. U.S.A. 111(52), 18739–18744 (2014).
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H. Lütcke, M. Murayama, T. Hahn, D. J. Margolis, S. Astori, S. M. Zum Alten Borgloh, W. Göbel, Y. Yang, W. Tang, S. Kügler, R. Sprengel, T. Nagai, A. Miyawaki, M. E. Larkum, F. Helmchen, and M. T. Hasan, “Optical recording of neuronal activity with a genetically-encoded calcium indicator in anesthetized and freely moving mice,” Front. Neural Circuits 4, 9 (2010).
[PubMed]

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U. K. Tirlapur, K. König, C. Peuckert, R. Krieg, and K.-J. Halbhuber, “Femtosecond near-infrared laser pulses elicit generation of reactive oxygen species in mammalian cells leading to apoptosis-like death,” Exp. Cell Res. 263(1), 88–97 (2001).
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Hasan, M. T.

H. Lütcke, M. Murayama, T. Hahn, D. J. Margolis, S. Astori, S. M. Zum Alten Borgloh, W. Göbel, Y. Yang, W. Tang, S. Kügler, R. Sprengel, T. Nagai, A. Miyawaki, M. E. Larkum, F. Helmchen, and M. T. Hasan, “Optical recording of neuronal activity with a genetically-encoded calcium indicator in anesthetized and freely moving mice,” Front. Neural Circuits 4, 9 (2010).
[PubMed]

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A. M. Packer, L. E. Russell, H. W. P. Dalgleish, and M. Häusser, “Simultaneous all-optical manipulation and recording of neural circuit activity with cellular resolution in vivo,” Nat. Methods 12(2), 140–146 (2014).
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H. He, K. T. Chan, S. K. Kong, and R. K. Y. Lee, “Mechanism of oxidative stress generation in cells by localized near-infrared femtosecond laser excitation,” Appl. Phys. Lett. 95(23), 233702 (2009).
[Crossref]

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.

H. Lütcke, M. Murayama, T. Hahn, D. J. Margolis, S. Astori, S. M. Zum Alten Borgloh, W. Göbel, Y. Yang, W. Tang, S. Kügler, R. Sprengel, T. Nagai, A. Miyawaki, M. E. Larkum, F. Helmchen, and M. T. Hasan, “Optical recording of neuronal activity with a genetically-encoded calcium indicator in anesthetized and freely moving mice,” Front. Neural Circuits 4, 9 (2010).
[PubMed]

F. Helmchen and W. Denk, “Deep tissue two-photon microscopy,” Nat. Methods 2(12), 932–940 (2005).
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T. Abraham, J. A. Hirota, S. Wadsworth, and D. A. Knight, “Minimally invasive multiphoton and harmonic generation imaging of extracellular matrix structures in lung airway and related diseases,” Pulm. Pharmacol. Ther. 24(5), 487–496 (2011).
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C. Stosiek, O. Garaschuk, K. Holthoff, and A. Konnerth, “In vivo two-photon calcium imaging of neuronal networks,” Proc. Natl. Acad. Sci. U.S.A. 100(12), 7319–7324 (2003).
[Crossref] [PubMed]

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A. Hopt and E. Neher, “Highly nonlinear photodamage in two-photon fluorescence microscopy,” Biophys. J. 80(4), 2029–2036 (2001).
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D. Kobat, N. G. Horton, and C. Xu, “In vivo two-photon microscopy to 1.6-mm depth in mouse cortex,” J. Biomed. Opt. 16(10), 106014 (2011).
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B. E. Losavio, V. Iyer, and P. Saggau, “Two-photon microscope for multisite microphotolysis of caged neurotransmitters in acute brain slices,” J. Biomed. Opt. 14(6), 064033 (2009).
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N. Ji, J. C. Magee, and E. Betzig, “High-speed, low-photodamage nonlinear imaging using passive pulse splitters,” Nat. Methods 5(2), 197–202 (2008).
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X. Chen, U. Leischner, Z. Varga, H. Jia, D. Deca, N. L. Rochefort, and A. Konnerth, “LOTOS-based two-photon calcium imaging of dendritic spines in vivo,” Nat. Protoc. 7(10), 1818–1829 (2012).
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K. Fujita, M. Kobayashi, S. Kawano, M. Yamanaka, and S. Kawata, “High-resolution confocal microscopy by saturated excitation of fluorescence,” Phys. Rev. Lett. 99(22), 228105 (2007).
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M. Yamanaka, K. Saito, N. I. Smith, S. Kawata, T. Nagai, and K. Fujita, “Saturated excitation of fluorescent proteins for subdiffraction-limited imaging of living cells in three dimensions,” Interface Focus 3(5), 20130007 (2013).
[Crossref] [PubMed]

K. Fujita, M. Kobayashi, S. Kawano, M. Yamanaka, and S. Kawata, “High-resolution confocal microscopy by saturated excitation of fluorescence,” Phys. Rev. Lett. 99(22), 228105 (2007).
[Crossref] [PubMed]

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I. A. Ghouri, A. Kelly, F. L. Burton, G. L. Smith, and O. J. Kemi, “2-photon excitation fluorescence microscopy enables deeper high-resolution imaging of voltage and Ca2+ in intact mice, rat, and rabbit hearts,” J. Biophotonics 8(1-2), 112–123 (2015).
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I. A. Ghouri, A. Kelly, F. L. Burton, G. L. Smith, and O. J. Kemi, “2-photon excitation fluorescence microscopy enables deeper high-resolution imaging of voltage and Ca2+ in intact mice, rat, and rabbit hearts,” J. Biophotonics 8(1-2), 112–123 (2015).
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D. J. Wallace, S. Meyer zum Alten Borgloh, S. Astori, Y. Yang, M. Bausen, S. Kügler, A. E. Palmer, R. Y. Tsien, R. Sprengel, J. N. Kerr, W. Denk, and M. T. Hasan, “Single-spike detection in vitro and in vivo with a genetic Ca2+ sensor,” Nat. Methods 5(9), 797–804 (2008).
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Knight, D. A.

T. Abraham, J. A. Hirota, S. Wadsworth, and D. A. Knight, “Minimally invasive multiphoton and harmonic generation imaging of extracellular matrix structures in lung airway and related diseases,” Pulm. Pharmacol. Ther. 24(5), 487–496 (2011).
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D. Kobat, N. G. Horton, and C. Xu, “In vivo two-photon microscopy to 1.6-mm depth in mouse cortex,” J. Biomed. Opt. 16(10), 106014 (2011).
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K. Fujita, M. Kobayashi, S. Kawano, M. Yamanaka, and S. Kawata, “High-resolution confocal microscopy by saturated excitation of fluorescence,” Phys. Rev. Lett. 99(22), 228105 (2007).
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H. He, K. T. Chan, S. K. Kong, and R. K. Y. Lee, “Mechanism of oxidative stress generation in cells by localized near-infrared femtosecond laser excitation,” Appl. Phys. Lett. 95(23), 233702 (2009).
[Crossref]

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U. K. Tirlapur, K. König, C. Peuckert, R. Krieg, and K.-J. Halbhuber, “Femtosecond near-infrared laser pulses elicit generation of reactive oxygen species in mammalian cells leading to apoptosis-like death,” Exp. Cell Res. 263(1), 88–97 (2001).
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X. Chen, U. Leischner, Z. Varga, H. Jia, D. Deca, N. L. Rochefort, and A. Konnerth, “LOTOS-based two-photon calcium imaging of dendritic spines in vivo,” Nat. Protoc. 7(10), 1818–1829 (2012).
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C. Stosiek, O. Garaschuk, K. Holthoff, and A. Konnerth, “In vivo two-photon calcium imaging of neuronal networks,” Proc. Natl. Acad. Sci. U.S.A. 100(12), 7319–7324 (2003).
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S. Tang, T. B. Krasieva, Z. Chen, G. Tempea, and B. J. Tromberg, “Effect of pulse duration on two-photon excited fluorescence and second harmonic generation in nonlinear optical microscopy,” J. Biomed. Opt. 11(2), 020501 (2006).
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U. K. Tirlapur, K. König, C. Peuckert, R. Krieg, and K.-J. Halbhuber, “Femtosecond near-infrared laser pulses elicit generation of reactive oxygen species in mammalian cells leading to apoptosis-like death,” Exp. Cell Res. 263(1), 88–97 (2001).
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H. Lütcke, M. Murayama, T. Hahn, D. J. Margolis, S. Astori, S. M. Zum Alten Borgloh, W. Göbel, Y. Yang, W. Tang, S. Kügler, R. Sprengel, T. Nagai, A. Miyawaki, M. E. Larkum, F. Helmchen, and M. T. Hasan, “Optical recording of neuronal activity with a genetically-encoded calcium indicator in anesthetized and freely moving mice,” Front. Neural Circuits 4, 9 (2010).
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D. J. Wallace, S. Meyer zum Alten Borgloh, S. Astori, Y. Yang, M. Bausen, S. Kügler, A. E. Palmer, R. Y. Tsien, R. Sprengel, J. N. Kerr, W. Denk, and M. T. Hasan, “Single-spike detection in vitro and in vivo with a genetic Ca2+ sensor,” Nat. Methods 5(9), 797–804 (2008).
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A. P. Mosk, A. Lagendijk, G. Lerosey, and M. Fink, “Controlling waves in space and time for imaging and focusing in complex media,” Nat. Photonics 6(5), 283–292 (2012).
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P. Lai, L. Wang, J. W. Tay, and L. V. Wang, “Photoacoustically guided wavefront shaping for enhanced optical focusing in scattering media,” Nat. Photonics 9(2), 126–132 (2015).
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H. Lütcke, M. Murayama, T. Hahn, D. J. Margolis, S. Astori, S. M. Zum Alten Borgloh, W. Göbel, Y. Yang, W. Tang, S. Kügler, R. Sprengel, T. Nagai, A. Miyawaki, M. E. Larkum, F. Helmchen, and M. T. Hasan, “Optical recording of neuronal activity with a genetically-encoded calcium indicator in anesthetized and freely moving mice,” Front. Neural Circuits 4, 9 (2010).
[PubMed]

Lee, R. K. Y.

H. He, K. T. Chan, S. K. Kong, and R. K. Y. Lee, “Mechanism of oxidative stress generation in cells by localized near-infrared femtosecond laser excitation,” Appl. Phys. Lett. 95(23), 233702 (2009).
[Crossref]

Leischner, U.

X. Chen, U. Leischner, Z. Varga, H. Jia, D. Deca, N. L. Rochefort, and A. Konnerth, “LOTOS-based two-photon calcium imaging of dendritic spines in vivo,” Nat. Protoc. 7(10), 1818–1829 (2012).
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A. P. Mosk, A. Lagendijk, G. Lerosey, and M. Fink, “Controlling waves in space and time for imaging and focusing in complex media,” Nat. Photonics 6(5), 283–292 (2012).
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Losavio, B. E.

B. E. Losavio, V. Iyer, and P. Saggau, “Two-photon microscope for multisite microphotolysis of caged neurotransmitters in acute brain slices,” J. Biomed. Opt. 14(6), 064033 (2009).
[Crossref] [PubMed]

Low, R. J.

R. J. Low, Y. Gu, and D. W. Tank, “Cellular resolution optical access to brain regions in fissures: imaging medial prefrontal cortex and grid cells in entorhinal cortex,” Proc. Natl. Acad. Sci. U.S.A. 111(52), 18739–18744 (2014).
[Crossref] [PubMed]

Lütcke, H.

H. Lütcke, M. Murayama, T. Hahn, D. J. Margolis, S. Astori, S. M. Zum Alten Borgloh, W. Göbel, Y. Yang, W. Tang, S. Kügler, R. Sprengel, T. Nagai, A. Miyawaki, M. E. Larkum, F. Helmchen, and M. T. Hasan, “Optical recording of neuronal activity with a genetically-encoded calcium indicator in anesthetized and freely moving mice,” Front. Neural Circuits 4, 9 (2010).
[PubMed]

Magee, J. C.

N. Ji, J. C. Magee, and E. Betzig, “High-speed, low-photodamage nonlinear imaging using passive pulse splitters,” Nat. Methods 5(2), 197–202 (2008).
[Crossref] [PubMed]

Mantulin, W. W.

Margolis, D. J.

H. Lütcke, M. Murayama, T. Hahn, D. J. Margolis, S. Astori, S. M. Zum Alten Borgloh, W. Göbel, Y. Yang, W. Tang, S. Kügler, R. Sprengel, T. Nagai, A. Miyawaki, M. E. Larkum, F. Helmchen, and M. T. Hasan, “Optical recording of neuronal activity with a genetically-encoded calcium indicator in anesthetized and freely moving mice,” Front. Neural Circuits 4, 9 (2010).
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G. Thériault, M. Cottet, A. Castonguay, N. McCarthy, and Y. De Koninck, “Extended two-photon microscopy in live samples with Bessel beams: steadier focus, faster volume scans, and simpler stereoscopic imaging,” Front. Cell. Neurosci. 8, 139 (2014).
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McConnell, G.

G. McConnell and E. Riis, “Two-photon laser scanning fluorescence microscopy using photonic crystal fiber,” J. Biomed. Opt. 9(5), 922–927 (2004).
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Mermillod-Blondin, A.

Mertz, J.

E. Beaurepaire, M. Oheim, and J. Mertz, “Ultra-deep two-photon fluorescence excitation in turbid media,” Opt. Commun. 188(1-4), 25–29 (2001).
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Meyer zum Alten Borgloh, S.

D. J. Wallace, S. Meyer zum Alten Borgloh, S. Astori, Y. Yang, M. Bausen, S. Kügler, A. E. Palmer, R. Y. Tsien, R. Sprengel, J. N. Kerr, W. Denk, and M. T. Hasan, “Single-spike detection in vitro and in vivo with a genetic Ca2+ sensor,” Nat. Methods 5(9), 797–804 (2008).
[Crossref] [PubMed]

Miyawaki, A.

H. Lütcke, M. Murayama, T. Hahn, D. J. Margolis, S. Astori, S. M. Zum Alten Borgloh, W. Göbel, Y. Yang, W. Tang, S. Kügler, R. Sprengel, T. Nagai, A. Miyawaki, M. E. Larkum, F. Helmchen, and M. T. Hasan, “Optical recording of neuronal activity with a genetically-encoded calcium indicator in anesthetized and freely moving mice,” Front. Neural Circuits 4, 9 (2010).
[PubMed]

Mosk, A. P.

A. P. Mosk, A. Lagendijk, G. Lerosey, and M. Fink, “Controlling waves in space and time for imaging and focusing in complex media,” Nat. Photonics 6(5), 283–292 (2012).
[Crossref]

Murayama, M.

H. Lütcke, M. Murayama, T. Hahn, D. J. Margolis, S. Astori, S. M. Zum Alten Borgloh, W. Göbel, Y. Yang, W. Tang, S. Kügler, R. Sprengel, T. Nagai, A. Miyawaki, M. E. Larkum, F. Helmchen, and M. T. Hasan, “Optical recording of neuronal activity with a genetically-encoded calcium indicator in anesthetized and freely moving mice,” Front. Neural Circuits 4, 9 (2010).
[PubMed]

Nagai, T.

M. Yamanaka, K. Saito, N. I. Smith, S. Kawata, T. Nagai, and K. Fujita, “Saturated excitation of fluorescent proteins for subdiffraction-limited imaging of living cells in three dimensions,” Interface Focus 3(5), 20130007 (2013).
[Crossref] [PubMed]

H. Lütcke, M. Murayama, T. Hahn, D. J. Margolis, S. Astori, S. M. Zum Alten Borgloh, W. Göbel, Y. Yang, W. Tang, S. Kügler, R. Sprengel, T. Nagai, A. Miyawaki, M. E. Larkum, F. Helmchen, and M. T. Hasan, “Optical recording of neuronal activity with a genetically-encoded calcium indicator in anesthetized and freely moving mice,” Front. Neural Circuits 4, 9 (2010).
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A. Hopt and E. Neher, “Highly nonlinear photodamage in two-photon fluorescence microscopy,” Biophys. J. 80(4), 2029–2036 (2001).
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V. Nikolenko, K. E. Poskanzer, and R. Yuste, “Two-photon photostimulation and imaging of neural circuits,” Nat. Methods 4(11), 943–950 (2007).
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S. W. Botchway, P. Reynolds, A. W. Parker, and P. O’Neill, “Use of near infrared femtosecond lasers as sub-micron radiation microbeam for cell DNA damage and repair studies,” Mutat. Res. 704(1-3), 38–44 (2010).
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E. Beaurepaire, M. Oheim, and J. Mertz, “Ultra-deep two-photon fluorescence excitation in turbid media,” Opt. Commun. 188(1-4), 25–29 (2001).
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Olivier, N.

Packer, A. M.

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

D. J. Wallace, S. Meyer zum Alten Borgloh, S. Astori, Y. Yang, M. Bausen, S. Kügler, A. E. Palmer, R. Y. Tsien, R. Sprengel, J. N. Kerr, W. Denk, and M. T. Hasan, “Single-spike detection in vitro and in vivo with a genetic Ca2+ sensor,” Nat. Methods 5(9), 797–804 (2008).
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S. W. Botchway, P. Reynolds, A. W. Parker, and P. O’Neill, “Use of near infrared femtosecond lasers as sub-micron radiation microbeam for cell DNA damage and repair studies,” Mutat. Res. 704(1-3), 38–44 (2010).
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U. K. Tirlapur, K. König, C. Peuckert, R. Krieg, and K.-J. Halbhuber, “Femtosecond near-infrared laser pulses elicit generation of reactive oxygen species in mammalian cells leading to apoptosis-like death,” Exp. Cell Res. 263(1), 88–97 (2001).
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V. Nikolenko, K. E. Poskanzer, and R. Yuste, “Two-photon photostimulation and imaging of neural circuits,” Nat. Methods 4(11), 943–950 (2007).
[Crossref] [PubMed]

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M. A. Go, M. S. To, C. Stricker, S. Redman, H.-A. Bachor, G. J. Stuart, and V. R. Daria, “Four-dimensional multi-site photolysis of caged neurotransmitters,” Front. Cell. Neurosci. 7, 231 (2013).
[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).
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S. W. Botchway, P. Reynolds, A. W. Parker, and P. O’Neill, “Use of near infrared femtosecond lasers as sub-micron radiation microbeam for cell DNA damage and repair studies,” Mutat. Res. 704(1-3), 38–44 (2010).
[Crossref] [PubMed]

Riis, E.

G. McConnell and E. Riis, “Two-photon laser scanning fluorescence microscopy using photonic crystal fiber,” J. Biomed. Opt. 9(5), 922–927 (2004).
[Crossref] [PubMed]

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X. Chen, U. Leischner, Z. Varga, H. Jia, D. Deca, N. L. Rochefort, and A. Konnerth, “LOTOS-based two-photon calcium imaging of dendritic spines in vivo,” Nat. Protoc. 7(10), 1818–1829 (2012).
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A. M. Packer, L. E. Russell, H. W. P. Dalgleish, and M. Häusser, “Simultaneous all-optical manipulation and recording of neural circuit activity with cellular resolution in vivo,” Nat. Methods 12(2), 140–146 (2014).
[Crossref] [PubMed]

Saggau, P.

B. E. Losavio, V. Iyer, and P. Saggau, “Two-photon microscope for multisite microphotolysis of caged neurotransmitters in acute brain slices,” J. Biomed. Opt. 14(6), 064033 (2009).
[Crossref] [PubMed]

Saito, K.

M. Yamanaka, K. Saito, N. I. Smith, S. Kawata, T. Nagai, and K. Fujita, “Saturated excitation of fluorescent proteins for subdiffraction-limited imaging of living cells in three dimensions,” Interface Focus 3(5), 20130007 (2013).
[Crossref] [PubMed]

Schummers, J.

N. R. Wilson, J. Schummers, C. A. Runyan, S. X. Yan, R. E. Chen, Y. Deng, and M. Sur, “Two-way communication with neural networks in vivo using focused light,” Nat. Protoc. 8(6), 1184–1203 (2013).
[Crossref] [PubMed]

Silver, R. A.

Smith, G. L.

I. A. Ghouri, A. Kelly, F. L. Burton, G. L. Smith, and O. J. Kemi, “2-photon excitation fluorescence microscopy enables deeper high-resolution imaging of voltage and Ca2+ in intact mice, rat, and rabbit hearts,” J. Biophotonics 8(1-2), 112–123 (2015).
[Crossref] [PubMed]

Smith, N. I.

M. Yamanaka, K. Saito, N. I. Smith, S. Kawata, T. Nagai, and K. Fujita, “Saturated excitation of fluorescent proteins for subdiffraction-limited imaging of living cells in three dimensions,” Interface Focus 3(5), 20130007 (2013).
[Crossref] [PubMed]

So, P. T. C.

Sprengel, R.

H. Lütcke, M. Murayama, T. Hahn, D. J. Margolis, S. Astori, S. M. Zum Alten Borgloh, W. Göbel, Y. Yang, W. Tang, S. Kügler, R. Sprengel, T. Nagai, A. Miyawaki, M. E. Larkum, F. Helmchen, and M. T. Hasan, “Optical recording of neuronal activity with a genetically-encoded calcium indicator in anesthetized and freely moving mice,” Front. Neural Circuits 4, 9 (2010).
[PubMed]

D. J. Wallace, S. Meyer zum Alten Borgloh, S. Astori, Y. Yang, M. Bausen, S. Kügler, A. E. Palmer, R. Y. Tsien, R. Sprengel, J. N. Kerr, W. Denk, and M. T. Hasan, “Single-spike detection in vitro and in vivo with a genetic Ca2+ sensor,” Nat. Methods 5(9), 797–804 (2008).
[Crossref] [PubMed]

Srinivas Nadella, K. M.

Stosiek, C.

C. Stosiek, O. Garaschuk, K. Holthoff, and A. Konnerth, “In vivo two-photon calcium imaging of neuronal networks,” Proc. Natl. Acad. Sci. U.S.A. 100(12), 7319–7324 (2003).
[Crossref] [PubMed]

Stricker, C.

M. A. Go, M. S. To, C. Stricker, S. Redman, H.-A. Bachor, G. J. Stuart, and V. R. Daria, “Four-dimensional multi-site photolysis of caged neurotransmitters,” Front. Cell. Neurosci. 7, 231 (2013).
[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]

Strickler, J. H.

W. Denk, J. H. Strickler, and W. W. Webb, “Two-photon laser scanning fluorescence microscopy,” Science 248(4951), 73–76 (1990).
[Crossref] [PubMed]

Stuart, G. J.

M. A. Go, M. S. To, C. Stricker, S. Redman, H.-A. Bachor, G. J. Stuart, and V. R. Daria, “Four-dimensional multi-site photolysis of caged neurotransmitters,” Front. Cell. Neurosci. 7, 231 (2013).
[Crossref] [PubMed]

Sur, M.

N. R. Wilson, J. Schummers, C. A. Runyan, S. X. Yan, R. E. Chen, Y. Deng, and M. Sur, “Two-way communication with neural networks in vivo using focused light,” Nat. Protoc. 8(6), 1184–1203 (2013).
[Crossref] [PubMed]

Svoboda, K.

K. Svoboda and R. Yasuda, “Principles of two-photon excitation microscopy and its applications to neuroscience,” Neuron 50(6), 823–839 (2006).
[Crossref] [PubMed]

Tang, S.

S. Tang, T. B. Krasieva, Z. Chen, G. Tempea, and B. J. Tromberg, “Effect of pulse duration on two-photon excited fluorescence and second harmonic generation in nonlinear optical microscopy,” J. Biomed. Opt. 11(2), 020501 (2006).
[Crossref] [PubMed]

Tang, W.

H. Lütcke, M. Murayama, T. Hahn, D. J. Margolis, S. Astori, S. M. Zum Alten Borgloh, W. Göbel, Y. Yang, W. Tang, S. Kügler, R. Sprengel, T. Nagai, A. Miyawaki, M. E. Larkum, F. Helmchen, and M. T. Hasan, “Optical recording of neuronal activity with a genetically-encoded calcium indicator in anesthetized and freely moving mice,” Front. Neural Circuits 4, 9 (2010).
[PubMed]

Tank, D. W.

R. J. Low, Y. Gu, and D. W. Tank, “Cellular resolution optical access to brain regions in fissures: imaging medial prefrontal cortex and grid cells in entorhinal cortex,” Proc. Natl. Acad. Sci. U.S.A. 111(52), 18739–18744 (2014).
[Crossref] [PubMed]

Tay, J. W.

P. Lai, L. Wang, J. W. Tay, and L. V. Wang, “Photoacoustically guided wavefront shaping for enhanced optical focusing in scattering media,” Nat. Photonics 9(2), 126–132 (2015).
[Crossref] [PubMed]

Tempea, G.

S. Tang, T. B. Krasieva, Z. Chen, G. Tempea, and B. J. Tromberg, “Effect of pulse duration on two-photon excited fluorescence and second harmonic generation in nonlinear optical microscopy,” J. Biomed. Opt. 11(2), 020501 (2006).
[Crossref] [PubMed]

Thériault, G.

G. Thériault, M. Cottet, A. Castonguay, N. McCarthy, and Y. De Koninck, “Extended two-photon microscopy in live samples with Bessel beams: steadier focus, faster volume scans, and simpler stereoscopic imaging,” Front. Cell. Neurosci. 8, 139 (2014).
[PubMed]

Tirlapur, U. K.

U. K. Tirlapur, K. König, C. Peuckert, R. Krieg, and K.-J. Halbhuber, “Femtosecond near-infrared laser pulses elicit generation of reactive oxygen species in mammalian cells leading to apoptosis-like death,” Exp. Cell Res. 263(1), 88–97 (2001).
[Crossref] [PubMed]

To, M. S.

M. A. Go, M. S. To, C. Stricker, S. Redman, H.-A. Bachor, G. J. Stuart, and V. R. Daria, “Four-dimensional multi-site photolysis of caged neurotransmitters,” Front. Cell. Neurosci. 7, 231 (2013).
[Crossref] [PubMed]

Tromberg, B. J.

S. Tang, T. B. Krasieva, Z. Chen, G. Tempea, and B. J. Tromberg, “Effect of pulse duration on two-photon excited fluorescence and second harmonic generation in nonlinear optical microscopy,” J. Biomed. Opt. 11(2), 020501 (2006).
[Crossref] [PubMed]

Tsien, R. Y.

D. J. Wallace, S. Meyer zum Alten Borgloh, S. Astori, Y. Yang, M. Bausen, S. Kügler, A. E. Palmer, R. Y. Tsien, R. Sprengel, J. N. Kerr, W. Denk, and M. T. Hasan, “Single-spike detection in vitro and in vivo with a genetic Ca2+ sensor,” Nat. Methods 5(9), 797–804 (2008).
[Crossref] [PubMed]

Varga, Z.

X. Chen, U. Leischner, Z. Varga, H. Jia, D. Deca, N. L. Rochefort, and A. Konnerth, “LOTOS-based two-photon calcium imaging of dendritic spines in vivo,” Nat. Protoc. 7(10), 1818–1829 (2012).
[Crossref] [PubMed]

Wadsworth, S.

T. Abraham, J. A. Hirota, S. Wadsworth, and D. A. Knight, “Minimally invasive multiphoton and harmonic generation imaging of extracellular matrix structures in lung airway and related diseases,” Pulm. Pharmacol. Ther. 24(5), 487–496 (2011).
[Crossref] [PubMed]

Wallace, D. J.

D. J. Wallace, S. Meyer zum Alten Borgloh, S. Astori, Y. Yang, M. Bausen, S. Kügler, A. E. Palmer, R. Y. Tsien, R. Sprengel, J. N. Kerr, W. Denk, and M. T. Hasan, “Single-spike detection in vitro and in vivo with a genetic Ca2+ sensor,” Nat. Methods 5(9), 797–804 (2008).
[Crossref] [PubMed]

Wang, L.

P. Lai, L. Wang, J. W. Tay, and L. V. Wang, “Photoacoustically guided wavefront shaping for enhanced optical focusing in scattering media,” Nat. Photonics 9(2), 126–132 (2015).
[Crossref] [PubMed]

Wang, L. V.

P. Lai, L. Wang, J. W. Tay, and L. V. Wang, “Photoacoustically guided wavefront shaping for enhanced optical focusing in scattering media,” Nat. Photonics 9(2), 126–132 (2015).
[Crossref] [PubMed]

Webb, W. W.

Wilson, N. R.

N. R. Wilson, J. Schummers, C. A. Runyan, S. X. Yan, R. E. Chen, Y. Deng, and M. Sur, “Two-way communication with neural networks in vivo using focused light,” Nat. Protoc. 8(6), 1184–1203 (2013).
[Crossref] [PubMed]

Xu, C.

D. Kobat, N. G. Horton, and C. Xu, “In vivo two-photon microscopy to 1.6-mm depth in mouse cortex,” J. Biomed. Opt. 16(10), 106014 (2011).
[Crossref] [PubMed]

C. Xu and W. W. Webb, “Measurement of two-photon excitation cross sections of molecular fluorophores with data from 690 to 1050 nm,” J. Opt. Soc. Am. B 13(3), 481–491 (1996).
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Yamanaka, M.

M. Yamanaka, K. Saito, N. I. Smith, S. Kawata, T. Nagai, and K. Fujita, “Saturated excitation of fluorescent proteins for subdiffraction-limited imaging of living cells in three dimensions,” Interface Focus 3(5), 20130007 (2013).
[Crossref] [PubMed]

K. Fujita, M. Kobayashi, S. Kawano, M. Yamanaka, and S. Kawata, “High-resolution confocal microscopy by saturated excitation of fluorescence,” Phys. Rev. Lett. 99(22), 228105 (2007).
[Crossref] [PubMed]

Yan, S. X.

N. R. Wilson, J. Schummers, C. A. Runyan, S. X. Yan, R. E. Chen, Y. Deng, and M. Sur, “Two-way communication with neural networks in vivo using focused light,” Nat. Protoc. 8(6), 1184–1203 (2013).
[Crossref] [PubMed]

Yang, Y.

H. Lütcke, M. Murayama, T. Hahn, D. J. Margolis, S. Astori, S. M. Zum Alten Borgloh, W. Göbel, Y. Yang, W. Tang, S. Kügler, R. Sprengel, T. Nagai, A. Miyawaki, M. E. Larkum, F. Helmchen, and M. T. Hasan, “Optical recording of neuronal activity with a genetically-encoded calcium indicator in anesthetized and freely moving mice,” Front. Neural Circuits 4, 9 (2010).
[PubMed]

D. J. Wallace, S. Meyer zum Alten Borgloh, S. Astori, Y. Yang, M. Bausen, S. Kügler, A. E. Palmer, R. Y. Tsien, R. Sprengel, J. N. Kerr, W. Denk, and M. T. Hasan, “Single-spike detection in vitro and in vivo with a genetic Ca2+ sensor,” Nat. Methods 5(9), 797–804 (2008).
[Crossref] [PubMed]

Yasuda, R.

K. Svoboda and R. Yasuda, “Principles of two-photon excitation microscopy and its applications to neuroscience,” Neuron 50(6), 823–839 (2006).
[Crossref] [PubMed]

Yuste, R.

V. Nikolenko, K. E. Poskanzer, and R. Yuste, “Two-photon photostimulation and imaging of neural circuits,” Nat. Methods 4(11), 943–950 (2007).
[Crossref] [PubMed]

Zum Alten Borgloh, S. M.

H. Lütcke, M. Murayama, T. Hahn, D. J. Margolis, S. Astori, S. M. Zum Alten Borgloh, W. Göbel, Y. Yang, W. Tang, S. Kügler, R. Sprengel, T. Nagai, A. Miyawaki, M. E. Larkum, F. Helmchen, and M. T. Hasan, “Optical recording of neuronal activity with a genetically-encoded calcium indicator in anesthetized and freely moving mice,” Front. Neural Circuits 4, 9 (2010).
[PubMed]

Appl. Phys. Lett. (1)

H. He, K. T. Chan, S. K. Kong, and R. K. Y. Lee, “Mechanism of oxidative stress generation in cells by localized near-infrared femtosecond laser excitation,” Appl. Phys. Lett. 95(23), 233702 (2009).
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Biophys. J. (1)

A. Hopt and E. Neher, “Highly nonlinear photodamage in two-photon fluorescence microscopy,” Biophys. J. 80(4), 2029–2036 (2001).
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Exp. Cell Res. (1)

U. K. Tirlapur, K. König, C. Peuckert, R. Krieg, and K.-J. Halbhuber, “Femtosecond near-infrared laser pulses elicit generation of reactive oxygen species in mammalian cells leading to apoptosis-like death,” Exp. Cell Res. 263(1), 88–97 (2001).
[Crossref] [PubMed]

Front. Cell. Neurosci. (2)

G. Thériault, M. Cottet, A. Castonguay, N. McCarthy, and Y. De Koninck, “Extended two-photon microscopy in live samples with Bessel beams: steadier focus, faster volume scans, and simpler stereoscopic imaging,” Front. Cell. Neurosci. 8, 139 (2014).
[PubMed]

M. A. Go, M. S. To, C. Stricker, S. Redman, H.-A. Bachor, G. J. Stuart, and V. R. Daria, “Four-dimensional multi-site photolysis of caged neurotransmitters,” Front. Cell. Neurosci. 7, 231 (2013).
[Crossref] [PubMed]

Front. Neural Circuits (1)

H. Lütcke, M. Murayama, T. Hahn, D. J. Margolis, S. Astori, S. M. Zum Alten Borgloh, W. Göbel, Y. Yang, W. Tang, S. Kügler, R. Sprengel, T. Nagai, A. Miyawaki, M. E. Larkum, F. Helmchen, and M. T. Hasan, “Optical recording of neuronal activity with a genetically-encoded calcium indicator in anesthetized and freely moving mice,” Front. Neural Circuits 4, 9 (2010).
[PubMed]

Interface Focus (1)

M. Yamanaka, K. Saito, N. I. Smith, S. Kawata, T. Nagai, and K. Fujita, “Saturated excitation of fluorescent proteins for subdiffraction-limited imaging of living cells in three dimensions,” Interface Focus 3(5), 20130007 (2013).
[Crossref] [PubMed]

J. Biomed. Opt. (4)

D. Kobat, N. G. Horton, and C. Xu, “In vivo two-photon microscopy to 1.6-mm depth in mouse cortex,” J. Biomed. Opt. 16(10), 106014 (2011).
[Crossref] [PubMed]

B. E. Losavio, V. Iyer, and P. Saggau, “Two-photon microscope for multisite microphotolysis of caged neurotransmitters in acute brain slices,” J. Biomed. Opt. 14(6), 064033 (2009).
[Crossref] [PubMed]

S. Tang, T. B. Krasieva, Z. Chen, G. Tempea, and B. J. Tromberg, “Effect of pulse duration on two-photon excited fluorescence and second harmonic generation in nonlinear optical microscopy,” J. Biomed. Opt. 11(2), 020501 (2006).
[Crossref] [PubMed]

G. McConnell and E. Riis, “Two-photon laser scanning fluorescence microscopy using photonic crystal fiber,” J. Biomed. Opt. 9(5), 922–927 (2004).
[Crossref] [PubMed]

J. Biophotonics (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]

I. A. Ghouri, A. Kelly, F. L. Burton, G. L. Smith, and O. J. Kemi, “2-photon excitation fluorescence microscopy enables deeper high-resolution imaging of voltage and Ca2+ in intact mice, rat, and rabbit hearts,” J. Biophotonics 8(1-2), 112–123 (2015).
[Crossref] [PubMed]

J. Opt. Soc. Am. B (1)

Mutat. Res. (1)

S. W. Botchway, P. Reynolds, A. W. Parker, and P. O’Neill, “Use of near infrared femtosecond lasers as sub-micron radiation microbeam for cell DNA damage and repair studies,” Mutat. Res. 704(1-3), 38–44 (2010).
[Crossref] [PubMed]

Nat. Methods (6)

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]

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

V. Nikolenko, K. E. Poskanzer, and R. Yuste, “Two-photon photostimulation and imaging of neural circuits,” Nat. Methods 4(11), 943–950 (2007).
[Crossref] [PubMed]

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

D. J. Wallace, S. Meyer zum Alten Borgloh, S. Astori, Y. Yang, M. Bausen, S. Kügler, A. E. Palmer, R. Y. Tsien, R. Sprengel, J. N. Kerr, W. Denk, and M. T. Hasan, “Single-spike detection in vitro and in vivo with a genetic Ca2+ sensor,” Nat. Methods 5(9), 797–804 (2008).
[Crossref] [PubMed]

N. Ji, J. C. Magee, and E. Betzig, “High-speed, low-photodamage nonlinear imaging using passive pulse splitters,” Nat. Methods 5(2), 197–202 (2008).
[Crossref] [PubMed]

Nat. Photonics (2)

P. Lai, L. Wang, J. W. Tay, and L. V. Wang, “Photoacoustically guided wavefront shaping for enhanced optical focusing in scattering media,” Nat. Photonics 9(2), 126–132 (2015).
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A. P. Mosk, A. Lagendijk, G. Lerosey, and M. Fink, “Controlling waves in space and time for imaging and focusing in complex media,” Nat. Photonics 6(5), 283–292 (2012).
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Nat. Protoc. (2)

X. Chen, U. Leischner, Z. Varga, H. Jia, D. Deca, N. L. Rochefort, and A. Konnerth, “LOTOS-based two-photon calcium imaging of dendritic spines in vivo,” Nat. Protoc. 7(10), 1818–1829 (2012).
[Crossref] [PubMed]

N. R. Wilson, J. Schummers, C. A. Runyan, S. X. Yan, R. E. Chen, Y. Deng, and M. Sur, “Two-way communication with neural networks in vivo using focused light,” Nat. Protoc. 8(6), 1184–1203 (2013).
[Crossref] [PubMed]

Neuron (1)

K. Svoboda and R. Yasuda, “Principles of two-photon excitation microscopy and its applications to neuroscience,” Neuron 50(6), 823–839 (2006).
[Crossref] [PubMed]

Opt. Commun. (1)

E. Beaurepaire, M. Oheim, and J. Mertz, “Ultra-deep two-photon fluorescence excitation in turbid media,” Opt. Commun. 188(1-4), 25–29 (2001).
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Opt. Express (2)

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G. Donnert, C. Eggeling, and S. W. Hell, “Triplet-relaxation microscopy with bunched pulsed excitation,” Photochem. Photobiol. Sci. 8(4), 481–485 (2009).
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Phys. Rev. Lett. (1)

K. Fujita, M. Kobayashi, S. Kawano, M. Yamanaka, and S. Kawata, “High-resolution confocal microscopy by saturated excitation of fluorescence,” Phys. Rev. Lett. 99(22), 228105 (2007).
[Crossref] [PubMed]

Proc. Natl. Acad. Sci. U.S.A. (2)

C. Stosiek, O. Garaschuk, K. Holthoff, and A. Konnerth, “In vivo two-photon calcium imaging of neuronal networks,” Proc. Natl. Acad. Sci. U.S.A. 100(12), 7319–7324 (2003).
[Crossref] [PubMed]

R. J. Low, Y. Gu, and D. W. Tank, “Cellular resolution optical access to brain regions in fissures: imaging medial prefrontal cortex and grid cells in entorhinal cortex,” Proc. Natl. Acad. Sci. U.S.A. 111(52), 18739–18744 (2014).
[Crossref] [PubMed]

Pulm. Pharmacol. Ther. (1)

T. Abraham, J. A. Hirota, S. Wadsworth, and D. A. Knight, “Minimally invasive multiphoton and harmonic generation imaging of extracellular matrix structures in lung airway and related diseases,” Pulm. Pharmacol. Ther. 24(5), 487–496 (2011).
[Crossref] [PubMed]

Science (1)

W. Denk, J. H. Strickler, and W. W. Webb, “Two-photon laser scanning fluorescence microscopy,” Science 248(4951), 73–76 (1990).
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Other (1)

V. Magidson and A. Khodjakov, “Circumventing photodamage in live-cell microscopy”, in Methods in Cell Biology, S. Greenfield and E. W. David eds. (Vol. 114, 2013).

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Figures (6)

Fig. 1
Fig. 1 (a) Schematic showing the experimental set-up with temporal gating using an acousto-optic modulator (AOM). (b) Schematic showing a bunch of femtosecond pulses gated with a bunch pulse width, σ~140ns, period of 1/fR (where fR is the gating frequency) and average power <Pin> before and <Pout> after the AOM. The top trace depicts the un-gated femtosecond laser. Bottom trace shows temporal gating where <Pout> is less than <Pin>. (c) Schematic depicting a constant energy in one pixel (pixel dwell time To = 2.5 μs) with varying gating frequencies. Note that a low fR requires a high <Pin>. Here fs is the sampling frequency and n = fR/fs is the number of bunches per pixel.
Fig. 2
Fig. 2 (a) Relation between gating frequency, fR and <Pin> for a constant <Pout> = 0.5 mW, shown on a log-log plot. The data fit has a slope of −0.94. (b) Relation between gating frequency, fR and fluorescence, F for a constant <Pout> = 1 mW, shown on a log-log plot. The data fit has a slope of −1.02. Inset shows an image of the fluorescent microspheres used to perform these experiments.
Fig. 3
Fig. 3 Images of a layer V cortical pyramidal neuron obtained (a) without and with temporal gating with frequencies set at: (b) 2.4 MHz; (c) 1.2 MHz and (d) 0.4 MHz. All the images were taken at <Pout> = 0.5 mW. Scale bar = 20 μm.
Fig. 4
Fig. 4 Projected 3-D images of active neurons in a brain slice, imaged (a) without temporal gating (b) at 2.4 MHz gating frequency, for a constant <Pout> = 2.5 mW. Scale bar = 20 μm. Panels (c), (d) show a selected dendritic area from the neuron for the two modes in (a) and (b) respectively. Panel (e) compares the relative fluorescence intensity profiles measured for the selected areas in (a) and (b), and panel (d) shows the fluorescence profiles along the highlighted line in (c) and (d) respectively.
Fig. 5
Fig. 5 Fluorescence intensity measured as a function of depth of the neurons within the brain tissue, shown for 1.2 MHz and 2.4 MHz frequencies, and compared with those obtained without gating. The data corresponding to each depth on the x-axis is from the same cell.
Fig. 6
Fig. 6 (a) Representative profile of membrane voltage across a neuronal cell in response to input current steps. The membrane voltage value is calculated at the arrows marked. (b) An example of the membrane-voltage-current response curve from which Rin values are calculated. (c) A typical behavior of change in a cell’s input resistance (ΔRin) as a function of gating frequency, fR and corresponding <Pout>. Here, Normalized |ΔRin| = |Rin(before imaging)-Rin(after imaging)|/Rin(before imaging). The error bars in |ΔRin| are calculated from the standard deviation of membrane voltage in panel (a). Solid lines have been used to show discontinuity between gated and un-gated modes of imaging.

Equations (3)

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

< P out > f R 1 =< P in >σ
<F> n< P in 2 >
<F> T o < P out 2 > σ 2 1 f R

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