Abstract

Scattering and absorption limit light penetration through inhomogeneous tissue. To reduce scattering, biochemists have shifted the wavelengths of excitation light for optogenetic actuators and fluorescent proteins to the orange-red range, while physicists have developed multiphoton technologies for deep tissue stimulation. We have built a rapid multiphoton spectroscopic screening system of genetically encoded red-activatable channelrhodopsin (ReaChR), and considered specific behaviors in transgenic Drosophila melanogaster as readouts to optimize the laser parameters for two-photon optogenetic activation. A wavelength-tunable optical parametric amplifier was adopted as the major light source for widefield two-photon excitation (TPE) of ReaChR. Our assays suggest that the optimized TPE wavelength of ReaChR is 1250 nm. Exploiting its capacity for optogenetic manipulation to induce macroscopic behavioral change, we realized rapid spectroscopic screening of genetically encoded effectors or indicators in vivo, and used modulation of ReaChR in the fly as a successful demonstration of such a system.

© 2015 Optical Society of America

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  1. C. Schroll, T. Riemensperger, D. Bucher, J. Ehmer, T. Völler, K. Erbguth, B. Gerber, T. Hendel, G. Nagel, E. Buchner, and A. Fiala, “Light-induced activation of distinct modulatory neurons triggers appetitive or aversive learning in Drosophila larvae,” Curr. Biol. 16(17), 1741–1747 (2006).
    [Crossref] [PubMed]
  2. G. S. Suh, S. Ben-Tabou de Leon, H. Tanimoto, A. Fiala, S. Benzer, and D. J. Anderson, “Light activation of an innate olfactory avoidance response in Drosophila,” Curr. Biol. 17(10), 905–908 (2007).
    [Crossref] [PubMed]
  3. M. C. Wu, L. A. Chu, P. Y. Hsiao, Y. Y. Lin, C. C. Chi, T. H. Liu, C. C. Fu, and A. S. Chiang, “Optogenetic control of selective neural activity in multiple freely moving Drosophila adults,” Proc. Natl. Acad. Sci. U.S.A. 111(14), 5367–5372 (2014).
    [Crossref] [PubMed]
  4. Y. Y. Lin, M. C. Wu, P. Y. Hsiao, L. A. Chu, M. M. Yang, C. C. Fu, and A. S. Chiang, “Three-wavelength light control of freely moving Drosophila Melanogaster for less perturbation and efficient social-behavioral studies,” Biomed. Opt. Express 6(2), 514–523 (2015).
    [Crossref] [PubMed]
  5. H. H. Lin, L. A. Chu, T. F. Fu, B. J. Dickson, and A. S. Chiang, “Parallel neural pathways mediate CO2 avoidance responses in Drosophila,” Science 340(6138), 1338–1341 (2013).
    [Crossref] [PubMed]
  6. G. Nagel, T. Szellas, W. Huhn, S. Kateriya, N. Adeishvili, P. Berthold, D. Ollig, P. Hegemann, and E. Bamberg, “Channelrhodopsin-2, a directly light-gated cation-selective membrane channel,” Proc. Natl. Acad. Sci. U.S.A. 100(24), 13940–13945 (2003).
    [Crossref] [PubMed]
  7. F. Zhang, L. P. Wang, E. S. Boyden, and K. Deisseroth, “Channelrhodopsin-2 and optical control of excitable cells,” Nat. Methods 3(10), 785–792 (2006).
    [Crossref] [PubMed]
  8. F. Zhang, M. Prigge, F. Beyrière, S. P. Tsunoda, J. Mattis, O. Yizhar, P. Hegemann, and K. Deisseroth, “Red-shifted optogenetic excitation: a tool for fast neural control derived from Volvox carteri,” Nat. Neurosci. 11(6), 631–633 (2008).
    [Crossref] [PubMed]
  9. A. Berndt, O. Yizhar, L. A. Gunaydin, P. Hegemann, and K. Deisseroth, “Bi-stable neural state switches,” Nat. Neurosci. 12(2), 229–234 (2009).
    [Crossref] [PubMed]
  10. J. Y. Lin, P. M. Knutsen, A. Muller, D. Kleinfeld, and R. Y. Tsien, “ReaChR: a red-shifted variant of channelrhodopsin enables deep transcranial optogenetic excitation,” Nat. Neurosci. 16(10), 1499–1508 (2013).
    [Crossref] [PubMed]
  11. N. C. Klapoetke, Y. Murata, S. S. Kim, S. R. Pulver, A. Birdsey-Benson, Y. K. Cho, T. K. Morimoto, A. S. Chuong, E. J. Carpenter, Z. Tian, J. Wang, Y. Xie, Z. Yan, Y. Zhang, B. Y. Chow, B. Surek, M. Melkonian, V. Jayaraman, M. Constantine-Paton, G. K. Wong, and E. S. Boyden, “Independent optical excitation of distinct neural populations,” Nat. Methods 11(3), 338–346 (2014).
    [Crossref] [PubMed]
  12. H. K. Inagaki, Y. Jung, E. D. Hoopfer, A. M. Wong, N. Mishra, J. Y. Lin, R. Y. Tsien, and D. J. Anderson, “Optogenetic control of Drosophila using a red-shifted channelrhodopsin reveals experience-dependent influences on courtship,” Nat. Methods 11(3), 325–332 (2013).
    [Crossref] [PubMed]
  13. A. S. Chuong, M. L. Miri, V. Busskamp, G. A. Matthews, L. C. Acker, A. T. Sørensen, A. Young, N. C. Klapoetke, M. A. Henninger, S. B. Kodandaramaiah, M. Ogawa, S. B. Ramanlal, R. C. Bandler, B. D. Allen, C. R. Forest, B. Y. Chow, X. Han, Y. Lin, K. M. Tye, B. Roska, J. A. Cardin, and E. S. Boyden, “Noninvasive optical inhibition with a red-shifted microbial rhodopsin,” Nat. Neurosci. 17(8), 1123–1129 (2014).
    [Crossref] [PubMed]
  14. A. M. Packer, L. E. Russell, H. W. 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]
  15. E. Papagiakoumou, F. Anselmi, A. Bègue, V. de Sars, J. Glückstad, E. Y. Isacoff, and V. Emiliani, “Scanless two-photon excitation of channelrhodopsin-2,” Nat. Methods 7(10), 848–854 (2010).
    [Crossref] [PubMed]
  16. J. P. Rickgauer and D. W. Tank, “Two-photon excitation of channelrhodopsin-2 at saturation,” Proc. Natl. Acad. Sci. U.S.A. 106(35), 15025–15030 (2009).
    [Crossref] [PubMed]
  17. C. Xu, W. Zipfel, J. B. Shear, R. M. Williams, and W. W. Webb, “Multiphoton fluorescence excitation: new spectral windows for biological nonlinear microscopy,” Proc. Natl. Acad. Sci. U.S.A. 93(20), 10763–10768 (1996).
    [Crossref] [PubMed]
  18. J. B. Guild, C. Xu, and W. W. Webb, “Measurement of group delay dispersion of high numerical aperture objective lenses using two-photon excited fluorescence,” Appl. Opt. 36(1), 397–401 (1997).
    [Crossref] [PubMed]
  19. M. Drobizhev, N. S. Makarov, S. E. Tillo, T. E. Hughes, and A. Rebane, “Two-photon absorption properties of fluorescent proteins,” Nat. Methods 8(5), 393–399 (2011).
    [Crossref] [PubMed]
  20. C. Li, D. Wang, L. Song, J. Liu, P. Liu, C. Xu, Y. Leng, R. Li, and Z. Xu, “Generation of carrier-envelope phase stabilized intense 1.5 cycle pulses at 1.75 μm,” Opt. Express 19(7), 6783–6789 (2011).
    [Crossref] [PubMed]
  21. G. Andriukaitis, T. Balčiūnas, S. Ališauskas, A. Pugžlys, A. Baltuška, T. Popmintchev, M. C. Chen, M. M. Murnane, and H. C. Kapteyn, “90 GW peak power few-cycle mid-infrared pulses from an optical parametric amplifier,” Opt. Lett. 36(15), 2755–2757 (2011).
    [Crossref] [PubMed]
  22. N. Ishii, K. Kaneshima, K. Kitano, T. Kanai, S. Watanabe, and J. Itatani, “Sub-two-cycle, carrier-envelope phase-stable, intense optical pulses at 1.6 μm from a BiB3O6 optical parametric chirped-pulse amplifier,” Opt. Lett. 37(20), 4182–4184 (2012).
    [Crossref] [PubMed]
  23. T. D. Tayler, D. A. Pacheco, A. C. Hergarden, M. Murthy, and D. J. Anderson, “A neuropeptide circuit that coordinates sperm transfer and copulation duration in Drosophila,” Proc. Natl. Acad. Sci. U.S.A. 109(50), 20697–20702 (2012).
    [Crossref] [PubMed]
  24. Z. Wang, A. Singhvi, P. Kong, and K. Scott, “Taste representations in the Drosophila brain,” Cell 117(7), 981–991 (2004).
    [Crossref] [PubMed]
  25. M. Chakir, H. Negoua, B. Moreteau, and J. R. David, “Quantitative morphometrical analysis of a North African population of Drosophila melanogaster: sexual dimorphism, and comparison with European populations,” J. Genet. 87(4), 373–382 (2008).
    [Crossref] [PubMed]
  26. Y. R. Shen, “Two-photon absorption,” in The Principle of Nonlinear Optics, Y. R. Shen, ed. (Wiley-Interscience 1984) pp. 202–210.
  27. S. Yamaguchi, C. Desplan, and M. Heisenberg, “Contribution of photoreceptor subtypes to spectral wavelength preference in Drosophila,” Proc. Natl. Acad. Sci. U.S.A. 107(12), 5634–5639 (2010).
    [Crossref] [PubMed]

2015 (1)

2014 (4)

M. C. Wu, L. A. Chu, P. Y. Hsiao, Y. Y. Lin, C. C. Chi, T. H. Liu, C. C. Fu, and A. S. Chiang, “Optogenetic control of selective neural activity in multiple freely moving Drosophila adults,” Proc. Natl. Acad. Sci. U.S.A. 111(14), 5367–5372 (2014).
[Crossref] [PubMed]

A. S. Chuong, M. L. Miri, V. Busskamp, G. A. Matthews, L. C. Acker, A. T. Sørensen, A. Young, N. C. Klapoetke, M. A. Henninger, S. B. Kodandaramaiah, M. Ogawa, S. B. Ramanlal, R. C. Bandler, B. D. Allen, C. R. Forest, B. Y. Chow, X. Han, Y. Lin, K. M. Tye, B. Roska, J. A. Cardin, and E. S. Boyden, “Noninvasive optical inhibition with a red-shifted microbial rhodopsin,” Nat. Neurosci. 17(8), 1123–1129 (2014).
[Crossref] [PubMed]

A. M. Packer, L. E. Russell, H. W. 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]

N. C. Klapoetke, Y. Murata, S. S. Kim, S. R. Pulver, A. Birdsey-Benson, Y. K. Cho, T. K. Morimoto, A. S. Chuong, E. J. Carpenter, Z. Tian, J. Wang, Y. Xie, Z. Yan, Y. Zhang, B. Y. Chow, B. Surek, M. Melkonian, V. Jayaraman, M. Constantine-Paton, G. K. Wong, and E. S. Boyden, “Independent optical excitation of distinct neural populations,” Nat. Methods 11(3), 338–346 (2014).
[Crossref] [PubMed]

2013 (3)

H. K. Inagaki, Y. Jung, E. D. Hoopfer, A. M. Wong, N. Mishra, J. Y. Lin, R. Y. Tsien, and D. J. Anderson, “Optogenetic control of Drosophila using a red-shifted channelrhodopsin reveals experience-dependent influences on courtship,” Nat. Methods 11(3), 325–332 (2013).
[Crossref] [PubMed]

J. Y. Lin, P. M. Knutsen, A. Muller, D. Kleinfeld, and R. Y. Tsien, “ReaChR: a red-shifted variant of channelrhodopsin enables deep transcranial optogenetic excitation,” Nat. Neurosci. 16(10), 1499–1508 (2013).
[Crossref] [PubMed]

H. H. Lin, L. A. Chu, T. F. Fu, B. J. Dickson, and A. S. Chiang, “Parallel neural pathways mediate CO2 avoidance responses in Drosophila,” Science 340(6138), 1338–1341 (2013).
[Crossref] [PubMed]

2012 (2)

N. Ishii, K. Kaneshima, K. Kitano, T. Kanai, S. Watanabe, and J. Itatani, “Sub-two-cycle, carrier-envelope phase-stable, intense optical pulses at 1.6 μm from a BiB3O6 optical parametric chirped-pulse amplifier,” Opt. Lett. 37(20), 4182–4184 (2012).
[Crossref] [PubMed]

T. D. Tayler, D. A. Pacheco, A. C. Hergarden, M. Murthy, and D. J. Anderson, “A neuropeptide circuit that coordinates sperm transfer and copulation duration in Drosophila,” Proc. Natl. Acad. Sci. U.S.A. 109(50), 20697–20702 (2012).
[Crossref] [PubMed]

2011 (3)

2010 (2)

S. Yamaguchi, C. Desplan, and M. Heisenberg, “Contribution of photoreceptor subtypes to spectral wavelength preference in Drosophila,” Proc. Natl. Acad. Sci. U.S.A. 107(12), 5634–5639 (2010).
[Crossref] [PubMed]

E. Papagiakoumou, F. Anselmi, A. Bègue, V. de Sars, J. Glückstad, E. Y. Isacoff, and V. Emiliani, “Scanless two-photon excitation of channelrhodopsin-2,” Nat. Methods 7(10), 848–854 (2010).
[Crossref] [PubMed]

2009 (2)

J. P. Rickgauer and D. W. Tank, “Two-photon excitation of channelrhodopsin-2 at saturation,” Proc. Natl. Acad. Sci. U.S.A. 106(35), 15025–15030 (2009).
[Crossref] [PubMed]

A. Berndt, O. Yizhar, L. A. Gunaydin, P. Hegemann, and K. Deisseroth, “Bi-stable neural state switches,” Nat. Neurosci. 12(2), 229–234 (2009).
[Crossref] [PubMed]

2008 (2)

F. Zhang, M. Prigge, F. Beyrière, S. P. Tsunoda, J. Mattis, O. Yizhar, P. Hegemann, and K. Deisseroth, “Red-shifted optogenetic excitation: a tool for fast neural control derived from Volvox carteri,” Nat. Neurosci. 11(6), 631–633 (2008).
[Crossref] [PubMed]

M. Chakir, H. Negoua, B. Moreteau, and J. R. David, “Quantitative morphometrical analysis of a North African population of Drosophila melanogaster: sexual dimorphism, and comparison with European populations,” J. Genet. 87(4), 373–382 (2008).
[Crossref] [PubMed]

2007 (1)

G. S. Suh, S. Ben-Tabou de Leon, H. Tanimoto, A. Fiala, S. Benzer, and D. J. Anderson, “Light activation of an innate olfactory avoidance response in Drosophila,” Curr. Biol. 17(10), 905–908 (2007).
[Crossref] [PubMed]

2006 (2)

C. Schroll, T. Riemensperger, D. Bucher, J. Ehmer, T. Völler, K. Erbguth, B. Gerber, T. Hendel, G. Nagel, E. Buchner, and A. Fiala, “Light-induced activation of distinct modulatory neurons triggers appetitive or aversive learning in Drosophila larvae,” Curr. Biol. 16(17), 1741–1747 (2006).
[Crossref] [PubMed]

F. Zhang, L. P. Wang, E. S. Boyden, and K. Deisseroth, “Channelrhodopsin-2 and optical control of excitable cells,” Nat. Methods 3(10), 785–792 (2006).
[Crossref] [PubMed]

2004 (1)

Z. Wang, A. Singhvi, P. Kong, and K. Scott, “Taste representations in the Drosophila brain,” Cell 117(7), 981–991 (2004).
[Crossref] [PubMed]

2003 (1)

G. Nagel, T. Szellas, W. Huhn, S. Kateriya, N. Adeishvili, P. Berthold, D. Ollig, P. Hegemann, and E. Bamberg, “Channelrhodopsin-2, a directly light-gated cation-selective membrane channel,” Proc. Natl. Acad. Sci. U.S.A. 100(24), 13940–13945 (2003).
[Crossref] [PubMed]

1997 (1)

1996 (1)

C. Xu, W. Zipfel, J. B. Shear, R. M. Williams, and W. W. Webb, “Multiphoton fluorescence excitation: new spectral windows for biological nonlinear microscopy,” Proc. Natl. Acad. Sci. U.S.A. 93(20), 10763–10768 (1996).
[Crossref] [PubMed]

Acker, L. C.

A. S. Chuong, M. L. Miri, V. Busskamp, G. A. Matthews, L. C. Acker, A. T. Sørensen, A. Young, N. C. Klapoetke, M. A. Henninger, S. B. Kodandaramaiah, M. Ogawa, S. B. Ramanlal, R. C. Bandler, B. D. Allen, C. R. Forest, B. Y. Chow, X. Han, Y. Lin, K. M. Tye, B. Roska, J. A. Cardin, and E. S. Boyden, “Noninvasive optical inhibition with a red-shifted microbial rhodopsin,” Nat. Neurosci. 17(8), 1123–1129 (2014).
[Crossref] [PubMed]

Adeishvili, N.

G. Nagel, T. Szellas, W. Huhn, S. Kateriya, N. Adeishvili, P. Berthold, D. Ollig, P. Hegemann, and E. Bamberg, “Channelrhodopsin-2, a directly light-gated cation-selective membrane channel,” Proc. Natl. Acad. Sci. U.S.A. 100(24), 13940–13945 (2003).
[Crossref] [PubMed]

Ališauskas, S.

Allen, B. D.

A. S. Chuong, M. L. Miri, V. Busskamp, G. A. Matthews, L. C. Acker, A. T. Sørensen, A. Young, N. C. Klapoetke, M. A. Henninger, S. B. Kodandaramaiah, M. Ogawa, S. B. Ramanlal, R. C. Bandler, B. D. Allen, C. R. Forest, B. Y. Chow, X. Han, Y. Lin, K. M. Tye, B. Roska, J. A. Cardin, and E. S. Boyden, “Noninvasive optical inhibition with a red-shifted microbial rhodopsin,” Nat. Neurosci. 17(8), 1123–1129 (2014).
[Crossref] [PubMed]

Anderson, D. J.

H. K. Inagaki, Y. Jung, E. D. Hoopfer, A. M. Wong, N. Mishra, J. Y. Lin, R. Y. Tsien, and D. J. Anderson, “Optogenetic control of Drosophila using a red-shifted channelrhodopsin reveals experience-dependent influences on courtship,” Nat. Methods 11(3), 325–332 (2013).
[Crossref] [PubMed]

T. D. Tayler, D. A. Pacheco, A. C. Hergarden, M. Murthy, and D. J. Anderson, “A neuropeptide circuit that coordinates sperm transfer and copulation duration in Drosophila,” Proc. Natl. Acad. Sci. U.S.A. 109(50), 20697–20702 (2012).
[Crossref] [PubMed]

G. S. Suh, S. Ben-Tabou de Leon, H. Tanimoto, A. Fiala, S. Benzer, and D. J. Anderson, “Light activation of an innate olfactory avoidance response in Drosophila,” Curr. Biol. 17(10), 905–908 (2007).
[Crossref] [PubMed]

Andriukaitis, G.

Anselmi, F.

E. Papagiakoumou, F. Anselmi, A. Bègue, V. de Sars, J. Glückstad, E. Y. Isacoff, and V. Emiliani, “Scanless two-photon excitation of channelrhodopsin-2,” Nat. Methods 7(10), 848–854 (2010).
[Crossref] [PubMed]

Balciunas, T.

Baltuška, A.

Bamberg, E.

G. Nagel, T. Szellas, W. Huhn, S. Kateriya, N. Adeishvili, P. Berthold, D. Ollig, P. Hegemann, and E. Bamberg, “Channelrhodopsin-2, a directly light-gated cation-selective membrane channel,” Proc. Natl. Acad. Sci. U.S.A. 100(24), 13940–13945 (2003).
[Crossref] [PubMed]

Bandler, R. C.

A. S. Chuong, M. L. Miri, V. Busskamp, G. A. Matthews, L. C. Acker, A. T. Sørensen, A. Young, N. C. Klapoetke, M. A. Henninger, S. B. Kodandaramaiah, M. Ogawa, S. B. Ramanlal, R. C. Bandler, B. D. Allen, C. R. Forest, B. Y. Chow, X. Han, Y. Lin, K. M. Tye, B. Roska, J. A. Cardin, and E. S. Boyden, “Noninvasive optical inhibition with a red-shifted microbial rhodopsin,” Nat. Neurosci. 17(8), 1123–1129 (2014).
[Crossref] [PubMed]

Bègue, A.

E. Papagiakoumou, F. Anselmi, A. Bègue, V. de Sars, J. Glückstad, E. Y. Isacoff, and V. Emiliani, “Scanless two-photon excitation of channelrhodopsin-2,” Nat. Methods 7(10), 848–854 (2010).
[Crossref] [PubMed]

Ben-Tabou de Leon, S.

G. S. Suh, S. Ben-Tabou de Leon, H. Tanimoto, A. Fiala, S. Benzer, and D. J. Anderson, “Light activation of an innate olfactory avoidance response in Drosophila,” Curr. Biol. 17(10), 905–908 (2007).
[Crossref] [PubMed]

Benzer, S.

G. S. Suh, S. Ben-Tabou de Leon, H. Tanimoto, A. Fiala, S. Benzer, and D. J. Anderson, “Light activation of an innate olfactory avoidance response in Drosophila,” Curr. Biol. 17(10), 905–908 (2007).
[Crossref] [PubMed]

Berndt, A.

A. Berndt, O. Yizhar, L. A. Gunaydin, P. Hegemann, and K. Deisseroth, “Bi-stable neural state switches,” Nat. Neurosci. 12(2), 229–234 (2009).
[Crossref] [PubMed]

Berthold, P.

G. Nagel, T. Szellas, W. Huhn, S. Kateriya, N. Adeishvili, P. Berthold, D. Ollig, P. Hegemann, and E. Bamberg, “Channelrhodopsin-2, a directly light-gated cation-selective membrane channel,” Proc. Natl. Acad. Sci. U.S.A. 100(24), 13940–13945 (2003).
[Crossref] [PubMed]

Beyrière, F.

F. Zhang, M. Prigge, F. Beyrière, S. P. Tsunoda, J. Mattis, O. Yizhar, P. Hegemann, and K. Deisseroth, “Red-shifted optogenetic excitation: a tool for fast neural control derived from Volvox carteri,” Nat. Neurosci. 11(6), 631–633 (2008).
[Crossref] [PubMed]

Birdsey-Benson, A.

N. C. Klapoetke, Y. Murata, S. S. Kim, S. R. Pulver, A. Birdsey-Benson, Y. K. Cho, T. K. Morimoto, A. S. Chuong, E. J. Carpenter, Z. Tian, J. Wang, Y. Xie, Z. Yan, Y. Zhang, B. Y. Chow, B. Surek, M. Melkonian, V. Jayaraman, M. Constantine-Paton, G. K. Wong, and E. S. Boyden, “Independent optical excitation of distinct neural populations,” Nat. Methods 11(3), 338–346 (2014).
[Crossref] [PubMed]

Boyden, E. S.

N. C. Klapoetke, Y. Murata, S. S. Kim, S. R. Pulver, A. Birdsey-Benson, Y. K. Cho, T. K. Morimoto, A. S. Chuong, E. J. Carpenter, Z. Tian, J. Wang, Y. Xie, Z. Yan, Y. Zhang, B. Y. Chow, B. Surek, M. Melkonian, V. Jayaraman, M. Constantine-Paton, G. K. Wong, and E. S. Boyden, “Independent optical excitation of distinct neural populations,” Nat. Methods 11(3), 338–346 (2014).
[Crossref] [PubMed]

A. S. Chuong, M. L. Miri, V. Busskamp, G. A. Matthews, L. C. Acker, A. T. Sørensen, A. Young, N. C. Klapoetke, M. A. Henninger, S. B. Kodandaramaiah, M. Ogawa, S. B. Ramanlal, R. C. Bandler, B. D. Allen, C. R. Forest, B. Y. Chow, X. Han, Y. Lin, K. M. Tye, B. Roska, J. A. Cardin, and E. S. Boyden, “Noninvasive optical inhibition with a red-shifted microbial rhodopsin,” Nat. Neurosci. 17(8), 1123–1129 (2014).
[Crossref] [PubMed]

F. Zhang, L. P. Wang, E. S. Boyden, and K. Deisseroth, “Channelrhodopsin-2 and optical control of excitable cells,” Nat. Methods 3(10), 785–792 (2006).
[Crossref] [PubMed]

Bucher, D.

C. Schroll, T. Riemensperger, D. Bucher, J. Ehmer, T. Völler, K. Erbguth, B. Gerber, T. Hendel, G. Nagel, E. Buchner, and A. Fiala, “Light-induced activation of distinct modulatory neurons triggers appetitive or aversive learning in Drosophila larvae,” Curr. Biol. 16(17), 1741–1747 (2006).
[Crossref] [PubMed]

Buchner, E.

C. Schroll, T. Riemensperger, D. Bucher, J. Ehmer, T. Völler, K. Erbguth, B. Gerber, T. Hendel, G. Nagel, E. Buchner, and A. Fiala, “Light-induced activation of distinct modulatory neurons triggers appetitive or aversive learning in Drosophila larvae,” Curr. Biol. 16(17), 1741–1747 (2006).
[Crossref] [PubMed]

Busskamp, V.

A. S. Chuong, M. L. Miri, V. Busskamp, G. A. Matthews, L. C. Acker, A. T. Sørensen, A. Young, N. C. Klapoetke, M. A. Henninger, S. B. Kodandaramaiah, M. Ogawa, S. B. Ramanlal, R. C. Bandler, B. D. Allen, C. R. Forest, B. Y. Chow, X. Han, Y. Lin, K. M. Tye, B. Roska, J. A. Cardin, and E. S. Boyden, “Noninvasive optical inhibition with a red-shifted microbial rhodopsin,” Nat. Neurosci. 17(8), 1123–1129 (2014).
[Crossref] [PubMed]

Cardin, J. A.

A. S. Chuong, M. L. Miri, V. Busskamp, G. A. Matthews, L. C. Acker, A. T. Sørensen, A. Young, N. C. Klapoetke, M. A. Henninger, S. B. Kodandaramaiah, M. Ogawa, S. B. Ramanlal, R. C. Bandler, B. D. Allen, C. R. Forest, B. Y. Chow, X. Han, Y. Lin, K. M. Tye, B. Roska, J. A. Cardin, and E. S. Boyden, “Noninvasive optical inhibition with a red-shifted microbial rhodopsin,” Nat. Neurosci. 17(8), 1123–1129 (2014).
[Crossref] [PubMed]

Carpenter, E. J.

N. C. Klapoetke, Y. Murata, S. S. Kim, S. R. Pulver, A. Birdsey-Benson, Y. K. Cho, T. K. Morimoto, A. S. Chuong, E. J. Carpenter, Z. Tian, J. Wang, Y. Xie, Z. Yan, Y. Zhang, B. Y. Chow, B. Surek, M. Melkonian, V. Jayaraman, M. Constantine-Paton, G. K. Wong, and E. S. Boyden, “Independent optical excitation of distinct neural populations,” Nat. Methods 11(3), 338–346 (2014).
[Crossref] [PubMed]

Chakir, M.

M. Chakir, H. Negoua, B. Moreteau, and J. R. David, “Quantitative morphometrical analysis of a North African population of Drosophila melanogaster: sexual dimorphism, and comparison with European populations,” J. Genet. 87(4), 373–382 (2008).
[Crossref] [PubMed]

Chen, M. C.

Chi, C. C.

M. C. Wu, L. A. Chu, P. Y. Hsiao, Y. Y. Lin, C. C. Chi, T. H. Liu, C. C. Fu, and A. S. Chiang, “Optogenetic control of selective neural activity in multiple freely moving Drosophila adults,” Proc. Natl. Acad. Sci. U.S.A. 111(14), 5367–5372 (2014).
[Crossref] [PubMed]

Chiang, A. S.

Y. Y. Lin, M. C. Wu, P. Y. Hsiao, L. A. Chu, M. M. Yang, C. C. Fu, and A. S. Chiang, “Three-wavelength light control of freely moving Drosophila Melanogaster for less perturbation and efficient social-behavioral studies,” Biomed. Opt. Express 6(2), 514–523 (2015).
[Crossref] [PubMed]

M. C. Wu, L. A. Chu, P. Y. Hsiao, Y. Y. Lin, C. C. Chi, T. H. Liu, C. C. Fu, and A. S. Chiang, “Optogenetic control of selective neural activity in multiple freely moving Drosophila adults,” Proc. Natl. Acad. Sci. U.S.A. 111(14), 5367–5372 (2014).
[Crossref] [PubMed]

H. H. Lin, L. A. Chu, T. F. Fu, B. J. Dickson, and A. S. Chiang, “Parallel neural pathways mediate CO2 avoidance responses in Drosophila,” Science 340(6138), 1338–1341 (2013).
[Crossref] [PubMed]

Cho, Y. K.

N. C. Klapoetke, Y. Murata, S. S. Kim, S. R. Pulver, A. Birdsey-Benson, Y. K. Cho, T. K. Morimoto, A. S. Chuong, E. J. Carpenter, Z. Tian, J. Wang, Y. Xie, Z. Yan, Y. Zhang, B. Y. Chow, B. Surek, M. Melkonian, V. Jayaraman, M. Constantine-Paton, G. K. Wong, and E. S. Boyden, “Independent optical excitation of distinct neural populations,” Nat. Methods 11(3), 338–346 (2014).
[Crossref] [PubMed]

Chow, B. Y.

N. C. Klapoetke, Y. Murata, S. S. Kim, S. R. Pulver, A. Birdsey-Benson, Y. K. Cho, T. K. Morimoto, A. S. Chuong, E. J. Carpenter, Z. Tian, J. Wang, Y. Xie, Z. Yan, Y. Zhang, B. Y. Chow, B. Surek, M. Melkonian, V. Jayaraman, M. Constantine-Paton, G. K. Wong, and E. S. Boyden, “Independent optical excitation of distinct neural populations,” Nat. Methods 11(3), 338–346 (2014).
[Crossref] [PubMed]

A. S. Chuong, M. L. Miri, V. Busskamp, G. A. Matthews, L. C. Acker, A. T. Sørensen, A. Young, N. C. Klapoetke, M. A. Henninger, S. B. Kodandaramaiah, M. Ogawa, S. B. Ramanlal, R. C. Bandler, B. D. Allen, C. R. Forest, B. Y. Chow, X. Han, Y. Lin, K. M. Tye, B. Roska, J. A. Cardin, and E. S. Boyden, “Noninvasive optical inhibition with a red-shifted microbial rhodopsin,” Nat. Neurosci. 17(8), 1123–1129 (2014).
[Crossref] [PubMed]

Chu, L. A.

Y. Y. Lin, M. C. Wu, P. Y. Hsiao, L. A. Chu, M. M. Yang, C. C. Fu, and A. S. Chiang, “Three-wavelength light control of freely moving Drosophila Melanogaster for less perturbation and efficient social-behavioral studies,” Biomed. Opt. Express 6(2), 514–523 (2015).
[Crossref] [PubMed]

M. C. Wu, L. A. Chu, P. Y. Hsiao, Y. Y. Lin, C. C. Chi, T. H. Liu, C. C. Fu, and A. S. Chiang, “Optogenetic control of selective neural activity in multiple freely moving Drosophila adults,” Proc. Natl. Acad. Sci. U.S.A. 111(14), 5367–5372 (2014).
[Crossref] [PubMed]

H. H. Lin, L. A. Chu, T. F. Fu, B. J. Dickson, and A. S. Chiang, “Parallel neural pathways mediate CO2 avoidance responses in Drosophila,” Science 340(6138), 1338–1341 (2013).
[Crossref] [PubMed]

Chuong, A. S.

N. C. Klapoetke, Y. Murata, S. S. Kim, S. R. Pulver, A. Birdsey-Benson, Y. K. Cho, T. K. Morimoto, A. S. Chuong, E. J. Carpenter, Z. Tian, J. Wang, Y. Xie, Z. Yan, Y. Zhang, B. Y. Chow, B. Surek, M. Melkonian, V. Jayaraman, M. Constantine-Paton, G. K. Wong, and E. S. Boyden, “Independent optical excitation of distinct neural populations,” Nat. Methods 11(3), 338–346 (2014).
[Crossref] [PubMed]

A. S. Chuong, M. L. Miri, V. Busskamp, G. A. Matthews, L. C. Acker, A. T. Sørensen, A. Young, N. C. Klapoetke, M. A. Henninger, S. B. Kodandaramaiah, M. Ogawa, S. B. Ramanlal, R. C. Bandler, B. D. Allen, C. R. Forest, B. Y. Chow, X. Han, Y. Lin, K. M. Tye, B. Roska, J. A. Cardin, and E. S. Boyden, “Noninvasive optical inhibition with a red-shifted microbial rhodopsin,” Nat. Neurosci. 17(8), 1123–1129 (2014).
[Crossref] [PubMed]

Constantine-Paton, M.

N. C. Klapoetke, Y. Murata, S. S. Kim, S. R. Pulver, A. Birdsey-Benson, Y. K. Cho, T. K. Morimoto, A. S. Chuong, E. J. Carpenter, Z. Tian, J. Wang, Y. Xie, Z. Yan, Y. Zhang, B. Y. Chow, B. Surek, M. Melkonian, V. Jayaraman, M. Constantine-Paton, G. K. Wong, and E. S. Boyden, “Independent optical excitation of distinct neural populations,” Nat. Methods 11(3), 338–346 (2014).
[Crossref] [PubMed]

Dalgleish, H. W.

A. M. Packer, L. E. Russell, H. W. 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]

David, J. R.

M. Chakir, H. Negoua, B. Moreteau, and J. R. David, “Quantitative morphometrical analysis of a North African population of Drosophila melanogaster: sexual dimorphism, and comparison with European populations,” J. Genet. 87(4), 373–382 (2008).
[Crossref] [PubMed]

de Sars, V.

E. Papagiakoumou, F. Anselmi, A. Bègue, V. de Sars, J. Glückstad, E. Y. Isacoff, and V. Emiliani, “Scanless two-photon excitation of channelrhodopsin-2,” Nat. Methods 7(10), 848–854 (2010).
[Crossref] [PubMed]

Deisseroth, K.

A. Berndt, O. Yizhar, L. A. Gunaydin, P. Hegemann, and K. Deisseroth, “Bi-stable neural state switches,” Nat. Neurosci. 12(2), 229–234 (2009).
[Crossref] [PubMed]

F. Zhang, M. Prigge, F. Beyrière, S. P. Tsunoda, J. Mattis, O. Yizhar, P. Hegemann, and K. Deisseroth, “Red-shifted optogenetic excitation: a tool for fast neural control derived from Volvox carteri,” Nat. Neurosci. 11(6), 631–633 (2008).
[Crossref] [PubMed]

F. Zhang, L. P. Wang, E. S. Boyden, and K. Deisseroth, “Channelrhodopsin-2 and optical control of excitable cells,” Nat. Methods 3(10), 785–792 (2006).
[Crossref] [PubMed]

Desplan, C.

S. Yamaguchi, C. Desplan, and M. Heisenberg, “Contribution of photoreceptor subtypes to spectral wavelength preference in Drosophila,” Proc. Natl. Acad. Sci. U.S.A. 107(12), 5634–5639 (2010).
[Crossref] [PubMed]

Dickson, B. J.

H. H. Lin, L. A. Chu, T. F. Fu, B. J. Dickson, and A. S. Chiang, “Parallel neural pathways mediate CO2 avoidance responses in Drosophila,” Science 340(6138), 1338–1341 (2013).
[Crossref] [PubMed]

Drobizhev, M.

M. Drobizhev, N. S. Makarov, S. E. Tillo, T. E. Hughes, and A. Rebane, “Two-photon absorption properties of fluorescent proteins,” Nat. Methods 8(5), 393–399 (2011).
[Crossref] [PubMed]

Ehmer, J.

C. Schroll, T. Riemensperger, D. Bucher, J. Ehmer, T. Völler, K. Erbguth, B. Gerber, T. Hendel, G. Nagel, E. Buchner, and A. Fiala, “Light-induced activation of distinct modulatory neurons triggers appetitive or aversive learning in Drosophila larvae,” Curr. Biol. 16(17), 1741–1747 (2006).
[Crossref] [PubMed]

Emiliani, V.

E. Papagiakoumou, F. Anselmi, A. Bègue, V. de Sars, J. Glückstad, E. Y. Isacoff, and V. Emiliani, “Scanless two-photon excitation of channelrhodopsin-2,” Nat. Methods 7(10), 848–854 (2010).
[Crossref] [PubMed]

Erbguth, K.

C. Schroll, T. Riemensperger, D. Bucher, J. Ehmer, T. Völler, K. Erbguth, B. Gerber, T. Hendel, G. Nagel, E. Buchner, and A. Fiala, “Light-induced activation of distinct modulatory neurons triggers appetitive or aversive learning in Drosophila larvae,” Curr. Biol. 16(17), 1741–1747 (2006).
[Crossref] [PubMed]

Fiala, A.

G. S. Suh, S. Ben-Tabou de Leon, H. Tanimoto, A. Fiala, S. Benzer, and D. J. Anderson, “Light activation of an innate olfactory avoidance response in Drosophila,” Curr. Biol. 17(10), 905–908 (2007).
[Crossref] [PubMed]

C. Schroll, T. Riemensperger, D. Bucher, J. Ehmer, T. Völler, K. Erbguth, B. Gerber, T. Hendel, G. Nagel, E. Buchner, and A. Fiala, “Light-induced activation of distinct modulatory neurons triggers appetitive or aversive learning in Drosophila larvae,” Curr. Biol. 16(17), 1741–1747 (2006).
[Crossref] [PubMed]

Forest, C. R.

A. S. Chuong, M. L. Miri, V. Busskamp, G. A. Matthews, L. C. Acker, A. T. Sørensen, A. Young, N. C. Klapoetke, M. A. Henninger, S. B. Kodandaramaiah, M. Ogawa, S. B. Ramanlal, R. C. Bandler, B. D. Allen, C. R. Forest, B. Y. Chow, X. Han, Y. Lin, K. M. Tye, B. Roska, J. A. Cardin, and E. S. Boyden, “Noninvasive optical inhibition with a red-shifted microbial rhodopsin,” Nat. Neurosci. 17(8), 1123–1129 (2014).
[Crossref] [PubMed]

Fu, C. C.

Y. Y. Lin, M. C. Wu, P. Y. Hsiao, L. A. Chu, M. M. Yang, C. C. Fu, and A. S. Chiang, “Three-wavelength light control of freely moving Drosophila Melanogaster for less perturbation and efficient social-behavioral studies,” Biomed. Opt. Express 6(2), 514–523 (2015).
[Crossref] [PubMed]

M. C. Wu, L. A. Chu, P. Y. Hsiao, Y. Y. Lin, C. C. Chi, T. H. Liu, C. C. Fu, and A. S. Chiang, “Optogenetic control of selective neural activity in multiple freely moving Drosophila adults,” Proc. Natl. Acad. Sci. U.S.A. 111(14), 5367–5372 (2014).
[Crossref] [PubMed]

Fu, T. F.

H. H. Lin, L. A. Chu, T. F. Fu, B. J. Dickson, and A. S. Chiang, “Parallel neural pathways mediate CO2 avoidance responses in Drosophila,” Science 340(6138), 1338–1341 (2013).
[Crossref] [PubMed]

Gerber, B.

C. Schroll, T. Riemensperger, D. Bucher, J. Ehmer, T. Völler, K. Erbguth, B. Gerber, T. Hendel, G. Nagel, E. Buchner, and A. Fiala, “Light-induced activation of distinct modulatory neurons triggers appetitive or aversive learning in Drosophila larvae,” Curr. Biol. 16(17), 1741–1747 (2006).
[Crossref] [PubMed]

Glückstad, J.

E. Papagiakoumou, F. Anselmi, A. Bègue, V. de Sars, J. Glückstad, E. Y. Isacoff, and V. Emiliani, “Scanless two-photon excitation of channelrhodopsin-2,” Nat. Methods 7(10), 848–854 (2010).
[Crossref] [PubMed]

Guild, J. B.

Gunaydin, L. A.

A. Berndt, O. Yizhar, L. A. Gunaydin, P. Hegemann, and K. Deisseroth, “Bi-stable neural state switches,” Nat. Neurosci. 12(2), 229–234 (2009).
[Crossref] [PubMed]

Han, X.

A. S. Chuong, M. L. Miri, V. Busskamp, G. A. Matthews, L. C. Acker, A. T. Sørensen, A. Young, N. C. Klapoetke, M. A. Henninger, S. B. Kodandaramaiah, M. Ogawa, S. B. Ramanlal, R. C. Bandler, B. D. Allen, C. R. Forest, B. Y. Chow, X. Han, Y. Lin, K. M. Tye, B. Roska, J. A. Cardin, and E. S. Boyden, “Noninvasive optical inhibition with a red-shifted microbial rhodopsin,” Nat. Neurosci. 17(8), 1123–1129 (2014).
[Crossref] [PubMed]

Häusser, M.

A. M. Packer, L. E. Russell, H. W. 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]

Hegemann, P.

A. Berndt, O. Yizhar, L. A. Gunaydin, P. Hegemann, and K. Deisseroth, “Bi-stable neural state switches,” Nat. Neurosci. 12(2), 229–234 (2009).
[Crossref] [PubMed]

F. Zhang, M. Prigge, F. Beyrière, S. P. Tsunoda, J. Mattis, O. Yizhar, P. Hegemann, and K. Deisseroth, “Red-shifted optogenetic excitation: a tool for fast neural control derived from Volvox carteri,” Nat. Neurosci. 11(6), 631–633 (2008).
[Crossref] [PubMed]

G. Nagel, T. Szellas, W. Huhn, S. Kateriya, N. Adeishvili, P. Berthold, D. Ollig, P. Hegemann, and E. Bamberg, “Channelrhodopsin-2, a directly light-gated cation-selective membrane channel,” Proc. Natl. Acad. Sci. U.S.A. 100(24), 13940–13945 (2003).
[Crossref] [PubMed]

Heisenberg, M.

S. Yamaguchi, C. Desplan, and M. Heisenberg, “Contribution of photoreceptor subtypes to spectral wavelength preference in Drosophila,” Proc. Natl. Acad. Sci. U.S.A. 107(12), 5634–5639 (2010).
[Crossref] [PubMed]

Hendel, T.

C. Schroll, T. Riemensperger, D. Bucher, J. Ehmer, T. Völler, K. Erbguth, B. Gerber, T. Hendel, G. Nagel, E. Buchner, and A. Fiala, “Light-induced activation of distinct modulatory neurons triggers appetitive or aversive learning in Drosophila larvae,” Curr. Biol. 16(17), 1741–1747 (2006).
[Crossref] [PubMed]

Henninger, M. A.

A. S. Chuong, M. L. Miri, V. Busskamp, G. A. Matthews, L. C. Acker, A. T. Sørensen, A. Young, N. C. Klapoetke, M. A. Henninger, S. B. Kodandaramaiah, M. Ogawa, S. B. Ramanlal, R. C. Bandler, B. D. Allen, C. R. Forest, B. Y. Chow, X. Han, Y. Lin, K. M. Tye, B. Roska, J. A. Cardin, and E. S. Boyden, “Noninvasive optical inhibition with a red-shifted microbial rhodopsin,” Nat. Neurosci. 17(8), 1123–1129 (2014).
[Crossref] [PubMed]

Hergarden, A. C.

T. D. Tayler, D. A. Pacheco, A. C. Hergarden, M. Murthy, and D. J. Anderson, “A neuropeptide circuit that coordinates sperm transfer and copulation duration in Drosophila,” Proc. Natl. Acad. Sci. U.S.A. 109(50), 20697–20702 (2012).
[Crossref] [PubMed]

Hoopfer, E. D.

H. K. Inagaki, Y. Jung, E. D. Hoopfer, A. M. Wong, N. Mishra, J. Y. Lin, R. Y. Tsien, and D. J. Anderson, “Optogenetic control of Drosophila using a red-shifted channelrhodopsin reveals experience-dependent influences on courtship,” Nat. Methods 11(3), 325–332 (2013).
[Crossref] [PubMed]

Hsiao, P. Y.

Y. Y. Lin, M. C. Wu, P. Y. Hsiao, L. A. Chu, M. M. Yang, C. C. Fu, and A. S. Chiang, “Three-wavelength light control of freely moving Drosophila Melanogaster for less perturbation and efficient social-behavioral studies,” Biomed. Opt. Express 6(2), 514–523 (2015).
[Crossref] [PubMed]

M. C. Wu, L. A. Chu, P. Y. Hsiao, Y. Y. Lin, C. C. Chi, T. H. Liu, C. C. Fu, and A. S. Chiang, “Optogenetic control of selective neural activity in multiple freely moving Drosophila adults,” Proc. Natl. Acad. Sci. U.S.A. 111(14), 5367–5372 (2014).
[Crossref] [PubMed]

Hughes, T. E.

M. Drobizhev, N. S. Makarov, S. E. Tillo, T. E. Hughes, and A. Rebane, “Two-photon absorption properties of fluorescent proteins,” Nat. Methods 8(5), 393–399 (2011).
[Crossref] [PubMed]

Huhn, W.

G. Nagel, T. Szellas, W. Huhn, S. Kateriya, N. Adeishvili, P. Berthold, D. Ollig, P. Hegemann, and E. Bamberg, “Channelrhodopsin-2, a directly light-gated cation-selective membrane channel,” Proc. Natl. Acad. Sci. U.S.A. 100(24), 13940–13945 (2003).
[Crossref] [PubMed]

Inagaki, H. K.

H. K. Inagaki, Y. Jung, E. D. Hoopfer, A. M. Wong, N. Mishra, J. Y. Lin, R. Y. Tsien, and D. J. Anderson, “Optogenetic control of Drosophila using a red-shifted channelrhodopsin reveals experience-dependent influences on courtship,” Nat. Methods 11(3), 325–332 (2013).
[Crossref] [PubMed]

Isacoff, E. Y.

E. Papagiakoumou, F. Anselmi, A. Bègue, V. de Sars, J. Glückstad, E. Y. Isacoff, and V. Emiliani, “Scanless two-photon excitation of channelrhodopsin-2,” Nat. Methods 7(10), 848–854 (2010).
[Crossref] [PubMed]

Ishii, N.

Itatani, J.

Jayaraman, V.

N. C. Klapoetke, Y. Murata, S. S. Kim, S. R. Pulver, A. Birdsey-Benson, Y. K. Cho, T. K. Morimoto, A. S. Chuong, E. J. Carpenter, Z. Tian, J. Wang, Y. Xie, Z. Yan, Y. Zhang, B. Y. Chow, B. Surek, M. Melkonian, V. Jayaraman, M. Constantine-Paton, G. K. Wong, and E. S. Boyden, “Independent optical excitation of distinct neural populations,” Nat. Methods 11(3), 338–346 (2014).
[Crossref] [PubMed]

Jung, Y.

H. K. Inagaki, Y. Jung, E. D. Hoopfer, A. M. Wong, N. Mishra, J. Y. Lin, R. Y. Tsien, and D. J. Anderson, “Optogenetic control of Drosophila using a red-shifted channelrhodopsin reveals experience-dependent influences on courtship,” Nat. Methods 11(3), 325–332 (2013).
[Crossref] [PubMed]

Kanai, T.

Kaneshima, K.

Kapteyn, H. C.

Kateriya, S.

G. Nagel, T. Szellas, W. Huhn, S. Kateriya, N. Adeishvili, P. Berthold, D. Ollig, P. Hegemann, and E. Bamberg, “Channelrhodopsin-2, a directly light-gated cation-selective membrane channel,” Proc. Natl. Acad. Sci. U.S.A. 100(24), 13940–13945 (2003).
[Crossref] [PubMed]

Kim, S. S.

N. C. Klapoetke, Y. Murata, S. S. Kim, S. R. Pulver, A. Birdsey-Benson, Y. K. Cho, T. K. Morimoto, A. S. Chuong, E. J. Carpenter, Z. Tian, J. Wang, Y. Xie, Z. Yan, Y. Zhang, B. Y. Chow, B. Surek, M. Melkonian, V. Jayaraman, M. Constantine-Paton, G. K. Wong, and E. S. Boyden, “Independent optical excitation of distinct neural populations,” Nat. Methods 11(3), 338–346 (2014).
[Crossref] [PubMed]

Kitano, K.

Klapoetke, N. C.

N. C. Klapoetke, Y. Murata, S. S. Kim, S. R. Pulver, A. Birdsey-Benson, Y. K. Cho, T. K. Morimoto, A. S. Chuong, E. J. Carpenter, Z. Tian, J. Wang, Y. Xie, Z. Yan, Y. Zhang, B. Y. Chow, B. Surek, M. Melkonian, V. Jayaraman, M. Constantine-Paton, G. K. Wong, and E. S. Boyden, “Independent optical excitation of distinct neural populations,” Nat. Methods 11(3), 338–346 (2014).
[Crossref] [PubMed]

A. S. Chuong, M. L. Miri, V. Busskamp, G. A. Matthews, L. C. Acker, A. T. Sørensen, A. Young, N. C. Klapoetke, M. A. Henninger, S. B. Kodandaramaiah, M. Ogawa, S. B. Ramanlal, R. C. Bandler, B. D. Allen, C. R. Forest, B. Y. Chow, X. Han, Y. Lin, K. M. Tye, B. Roska, J. A. Cardin, and E. S. Boyden, “Noninvasive optical inhibition with a red-shifted microbial rhodopsin,” Nat. Neurosci. 17(8), 1123–1129 (2014).
[Crossref] [PubMed]

Kleinfeld, D.

J. Y. Lin, P. M. Knutsen, A. Muller, D. Kleinfeld, and R. Y. Tsien, “ReaChR: a red-shifted variant of channelrhodopsin enables deep transcranial optogenetic excitation,” Nat. Neurosci. 16(10), 1499–1508 (2013).
[Crossref] [PubMed]

Knutsen, P. M.

J. Y. Lin, P. M. Knutsen, A. Muller, D. Kleinfeld, and R. Y. Tsien, “ReaChR: a red-shifted variant of channelrhodopsin enables deep transcranial optogenetic excitation,” Nat. Neurosci. 16(10), 1499–1508 (2013).
[Crossref] [PubMed]

Kodandaramaiah, S. B.

A. S. Chuong, M. L. Miri, V. Busskamp, G. A. Matthews, L. C. Acker, A. T. Sørensen, A. Young, N. C. Klapoetke, M. A. Henninger, S. B. Kodandaramaiah, M. Ogawa, S. B. Ramanlal, R. C. Bandler, B. D. Allen, C. R. Forest, B. Y. Chow, X. Han, Y. Lin, K. M. Tye, B. Roska, J. A. Cardin, and E. S. Boyden, “Noninvasive optical inhibition with a red-shifted microbial rhodopsin,” Nat. Neurosci. 17(8), 1123–1129 (2014).
[Crossref] [PubMed]

Kong, P.

Z. Wang, A. Singhvi, P. Kong, and K. Scott, “Taste representations in the Drosophila brain,” Cell 117(7), 981–991 (2004).
[Crossref] [PubMed]

Leng, Y.

Li, C.

Li, R.

Lin, H. H.

H. H. Lin, L. A. Chu, T. F. Fu, B. J. Dickson, and A. S. Chiang, “Parallel neural pathways mediate CO2 avoidance responses in Drosophila,” Science 340(6138), 1338–1341 (2013).
[Crossref] [PubMed]

Lin, J. Y.

J. Y. Lin, P. M. Knutsen, A. Muller, D. Kleinfeld, and R. Y. Tsien, “ReaChR: a red-shifted variant of channelrhodopsin enables deep transcranial optogenetic excitation,” Nat. Neurosci. 16(10), 1499–1508 (2013).
[Crossref] [PubMed]

H. K. Inagaki, Y. Jung, E. D. Hoopfer, A. M. Wong, N. Mishra, J. Y. Lin, R. Y. Tsien, and D. J. Anderson, “Optogenetic control of Drosophila using a red-shifted channelrhodopsin reveals experience-dependent influences on courtship,” Nat. Methods 11(3), 325–332 (2013).
[Crossref] [PubMed]

Lin, Y.

A. S. Chuong, M. L. Miri, V. Busskamp, G. A. Matthews, L. C. Acker, A. T. Sørensen, A. Young, N. C. Klapoetke, M. A. Henninger, S. B. Kodandaramaiah, M. Ogawa, S. B. Ramanlal, R. C. Bandler, B. D. Allen, C. R. Forest, B. Y. Chow, X. Han, Y. Lin, K. M. Tye, B. Roska, J. A. Cardin, and E. S. Boyden, “Noninvasive optical inhibition with a red-shifted microbial rhodopsin,” Nat. Neurosci. 17(8), 1123–1129 (2014).
[Crossref] [PubMed]

Lin, Y. Y.

Y. Y. Lin, M. C. Wu, P. Y. Hsiao, L. A. Chu, M. M. Yang, C. C. Fu, and A. S. Chiang, “Three-wavelength light control of freely moving Drosophila Melanogaster for less perturbation and efficient social-behavioral studies,” Biomed. Opt. Express 6(2), 514–523 (2015).
[Crossref] [PubMed]

M. C. Wu, L. A. Chu, P. Y. Hsiao, Y. Y. Lin, C. C. Chi, T. H. Liu, C. C. Fu, and A. S. Chiang, “Optogenetic control of selective neural activity in multiple freely moving Drosophila adults,” Proc. Natl. Acad. Sci. U.S.A. 111(14), 5367–5372 (2014).
[Crossref] [PubMed]

Liu, J.

Liu, P.

Liu, T. H.

M. C. Wu, L. A. Chu, P. Y. Hsiao, Y. Y. Lin, C. C. Chi, T. H. Liu, C. C. Fu, and A. S. Chiang, “Optogenetic control of selective neural activity in multiple freely moving Drosophila adults,” Proc. Natl. Acad. Sci. U.S.A. 111(14), 5367–5372 (2014).
[Crossref] [PubMed]

Makarov, N. S.

M. Drobizhev, N. S. Makarov, S. E. Tillo, T. E. Hughes, and A. Rebane, “Two-photon absorption properties of fluorescent proteins,” Nat. Methods 8(5), 393–399 (2011).
[Crossref] [PubMed]

Matthews, G. A.

A. S. Chuong, M. L. Miri, V. Busskamp, G. A. Matthews, L. C. Acker, A. T. Sørensen, A. Young, N. C. Klapoetke, M. A. Henninger, S. B. Kodandaramaiah, M. Ogawa, S. B. Ramanlal, R. C. Bandler, B. D. Allen, C. R. Forest, B. Y. Chow, X. Han, Y. Lin, K. M. Tye, B. Roska, J. A. Cardin, and E. S. Boyden, “Noninvasive optical inhibition with a red-shifted microbial rhodopsin,” Nat. Neurosci. 17(8), 1123–1129 (2014).
[Crossref] [PubMed]

Mattis, J.

F. Zhang, M. Prigge, F. Beyrière, S. P. Tsunoda, J. Mattis, O. Yizhar, P. Hegemann, and K. Deisseroth, “Red-shifted optogenetic excitation: a tool for fast neural control derived from Volvox carteri,” Nat. Neurosci. 11(6), 631–633 (2008).
[Crossref] [PubMed]

Melkonian, M.

N. C. Klapoetke, Y. Murata, S. S. Kim, S. R. Pulver, A. Birdsey-Benson, Y. K. Cho, T. K. Morimoto, A. S. Chuong, E. J. Carpenter, Z. Tian, J. Wang, Y. Xie, Z. Yan, Y. Zhang, B. Y. Chow, B. Surek, M. Melkonian, V. Jayaraman, M. Constantine-Paton, G. K. Wong, and E. S. Boyden, “Independent optical excitation of distinct neural populations,” Nat. Methods 11(3), 338–346 (2014).
[Crossref] [PubMed]

Miri, M. L.

A. S. Chuong, M. L. Miri, V. Busskamp, G. A. Matthews, L. C. Acker, A. T. Sørensen, A. Young, N. C. Klapoetke, M. A. Henninger, S. B. Kodandaramaiah, M. Ogawa, S. B. Ramanlal, R. C. Bandler, B. D. Allen, C. R. Forest, B. Y. Chow, X. Han, Y. Lin, K. M. Tye, B. Roska, J. A. Cardin, and E. S. Boyden, “Noninvasive optical inhibition with a red-shifted microbial rhodopsin,” Nat. Neurosci. 17(8), 1123–1129 (2014).
[Crossref] [PubMed]

Mishra, N.

H. K. Inagaki, Y. Jung, E. D. Hoopfer, A. M. Wong, N. Mishra, J. Y. Lin, R. Y. Tsien, and D. J. Anderson, “Optogenetic control of Drosophila using a red-shifted channelrhodopsin reveals experience-dependent influences on courtship,” Nat. Methods 11(3), 325–332 (2013).
[Crossref] [PubMed]

Moreteau, B.

M. Chakir, H. Negoua, B. Moreteau, and J. R. David, “Quantitative morphometrical analysis of a North African population of Drosophila melanogaster: sexual dimorphism, and comparison with European populations,” J. Genet. 87(4), 373–382 (2008).
[Crossref] [PubMed]

Morimoto, T. K.

N. C. Klapoetke, Y. Murata, S. S. Kim, S. R. Pulver, A. Birdsey-Benson, Y. K. Cho, T. K. Morimoto, A. S. Chuong, E. J. Carpenter, Z. Tian, J. Wang, Y. Xie, Z. Yan, Y. Zhang, B. Y. Chow, B. Surek, M. Melkonian, V. Jayaraman, M. Constantine-Paton, G. K. Wong, and E. S. Boyden, “Independent optical excitation of distinct neural populations,” Nat. Methods 11(3), 338–346 (2014).
[Crossref] [PubMed]

Muller, A.

J. Y. Lin, P. M. Knutsen, A. Muller, D. Kleinfeld, and R. Y. Tsien, “ReaChR: a red-shifted variant of channelrhodopsin enables deep transcranial optogenetic excitation,” Nat. Neurosci. 16(10), 1499–1508 (2013).
[Crossref] [PubMed]

Murata, Y.

N. C. Klapoetke, Y. Murata, S. S. Kim, S. R. Pulver, A. Birdsey-Benson, Y. K. Cho, T. K. Morimoto, A. S. Chuong, E. J. Carpenter, Z. Tian, J. Wang, Y. Xie, Z. Yan, Y. Zhang, B. Y. Chow, B. Surek, M. Melkonian, V. Jayaraman, M. Constantine-Paton, G. K. Wong, and E. S. Boyden, “Independent optical excitation of distinct neural populations,” Nat. Methods 11(3), 338–346 (2014).
[Crossref] [PubMed]

Murnane, M. M.

Murthy, M.

T. D. Tayler, D. A. Pacheco, A. C. Hergarden, M. Murthy, and D. J. Anderson, “A neuropeptide circuit that coordinates sperm transfer and copulation duration in Drosophila,” Proc. Natl. Acad. Sci. U.S.A. 109(50), 20697–20702 (2012).
[Crossref] [PubMed]

Nagel, G.

C. Schroll, T. Riemensperger, D. Bucher, J. Ehmer, T. Völler, K. Erbguth, B. Gerber, T. Hendel, G. Nagel, E. Buchner, and A. Fiala, “Light-induced activation of distinct modulatory neurons triggers appetitive or aversive learning in Drosophila larvae,” Curr. Biol. 16(17), 1741–1747 (2006).
[Crossref] [PubMed]

G. Nagel, T. Szellas, W. Huhn, S. Kateriya, N. Adeishvili, P. Berthold, D. Ollig, P. Hegemann, and E. Bamberg, “Channelrhodopsin-2, a directly light-gated cation-selective membrane channel,” Proc. Natl. Acad. Sci. U.S.A. 100(24), 13940–13945 (2003).
[Crossref] [PubMed]

Negoua, H.

M. Chakir, H. Negoua, B. Moreteau, and J. R. David, “Quantitative morphometrical analysis of a North African population of Drosophila melanogaster: sexual dimorphism, and comparison with European populations,” J. Genet. 87(4), 373–382 (2008).
[Crossref] [PubMed]

Ogawa, M.

A. S. Chuong, M. L. Miri, V. Busskamp, G. A. Matthews, L. C. Acker, A. T. Sørensen, A. Young, N. C. Klapoetke, M. A. Henninger, S. B. Kodandaramaiah, M. Ogawa, S. B. Ramanlal, R. C. Bandler, B. D. Allen, C. R. Forest, B. Y. Chow, X. Han, Y. Lin, K. M. Tye, B. Roska, J. A. Cardin, and E. S. Boyden, “Noninvasive optical inhibition with a red-shifted microbial rhodopsin,” Nat. Neurosci. 17(8), 1123–1129 (2014).
[Crossref] [PubMed]

Ollig, D.

G. Nagel, T. Szellas, W. Huhn, S. Kateriya, N. Adeishvili, P. Berthold, D. Ollig, P. Hegemann, and E. Bamberg, “Channelrhodopsin-2, a directly light-gated cation-selective membrane channel,” Proc. Natl. Acad. Sci. U.S.A. 100(24), 13940–13945 (2003).
[Crossref] [PubMed]

Pacheco, D. A.

T. D. Tayler, D. A. Pacheco, A. C. Hergarden, M. Murthy, and D. J. Anderson, “A neuropeptide circuit that coordinates sperm transfer and copulation duration in Drosophila,” Proc. Natl. Acad. Sci. U.S.A. 109(50), 20697–20702 (2012).
[Crossref] [PubMed]

Packer, A. M.

A. M. Packer, L. E. Russell, H. W. 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]

Papagiakoumou, E.

E. Papagiakoumou, F. Anselmi, A. Bègue, V. de Sars, J. Glückstad, E. Y. Isacoff, and V. Emiliani, “Scanless two-photon excitation of channelrhodopsin-2,” Nat. Methods 7(10), 848–854 (2010).
[Crossref] [PubMed]

Popmintchev, T.

Prigge, M.

F. Zhang, M. Prigge, F. Beyrière, S. P. Tsunoda, J. Mattis, O. Yizhar, P. Hegemann, and K. Deisseroth, “Red-shifted optogenetic excitation: a tool for fast neural control derived from Volvox carteri,” Nat. Neurosci. 11(6), 631–633 (2008).
[Crossref] [PubMed]

Pugžlys, A.

Pulver, S. R.

N. C. Klapoetke, Y. Murata, S. S. Kim, S. R. Pulver, A. Birdsey-Benson, Y. K. Cho, T. K. Morimoto, A. S. Chuong, E. J. Carpenter, Z. Tian, J. Wang, Y. Xie, Z. Yan, Y. Zhang, B. Y. Chow, B. Surek, M. Melkonian, V. Jayaraman, M. Constantine-Paton, G. K. Wong, and E. S. Boyden, “Independent optical excitation of distinct neural populations,” Nat. Methods 11(3), 338–346 (2014).
[Crossref] [PubMed]

Ramanlal, S. B.

A. S. Chuong, M. L. Miri, V. Busskamp, G. A. Matthews, L. C. Acker, A. T. Sørensen, A. Young, N. C. Klapoetke, M. A. Henninger, S. B. Kodandaramaiah, M. Ogawa, S. B. Ramanlal, R. C. Bandler, B. D. Allen, C. R. Forest, B. Y. Chow, X. Han, Y. Lin, K. M. Tye, B. Roska, J. A. Cardin, and E. S. Boyden, “Noninvasive optical inhibition with a red-shifted microbial rhodopsin,” Nat. Neurosci. 17(8), 1123–1129 (2014).
[Crossref] [PubMed]

Rebane, A.

M. Drobizhev, N. S. Makarov, S. E. Tillo, T. E. Hughes, and A. Rebane, “Two-photon absorption properties of fluorescent proteins,” Nat. Methods 8(5), 393–399 (2011).
[Crossref] [PubMed]

Rickgauer, J. P.

J. P. Rickgauer and D. W. Tank, “Two-photon excitation of channelrhodopsin-2 at saturation,” Proc. Natl. Acad. Sci. U.S.A. 106(35), 15025–15030 (2009).
[Crossref] [PubMed]

Riemensperger, T.

C. Schroll, T. Riemensperger, D. Bucher, J. Ehmer, T. Völler, K. Erbguth, B. Gerber, T. Hendel, G. Nagel, E. Buchner, and A. Fiala, “Light-induced activation of distinct modulatory neurons triggers appetitive or aversive learning in Drosophila larvae,” Curr. Biol. 16(17), 1741–1747 (2006).
[Crossref] [PubMed]

Roska, B.

A. S. Chuong, M. L. Miri, V. Busskamp, G. A. Matthews, L. C. Acker, A. T. Sørensen, A. Young, N. C. Klapoetke, M. A. Henninger, S. B. Kodandaramaiah, M. Ogawa, S. B. Ramanlal, R. C. Bandler, B. D. Allen, C. R. Forest, B. Y. Chow, X. Han, Y. Lin, K. M. Tye, B. Roska, J. A. Cardin, and E. S. Boyden, “Noninvasive optical inhibition with a red-shifted microbial rhodopsin,” Nat. Neurosci. 17(8), 1123–1129 (2014).
[Crossref] [PubMed]

Russell, L. E.

A. M. Packer, L. E. Russell, H. W. 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]

Schroll, C.

C. Schroll, T. Riemensperger, D. Bucher, J. Ehmer, T. Völler, K. Erbguth, B. Gerber, T. Hendel, G. Nagel, E. Buchner, and A. Fiala, “Light-induced activation of distinct modulatory neurons triggers appetitive or aversive learning in Drosophila larvae,” Curr. Biol. 16(17), 1741–1747 (2006).
[Crossref] [PubMed]

Scott, K.

Z. Wang, A. Singhvi, P. Kong, and K. Scott, “Taste representations in the Drosophila brain,” Cell 117(7), 981–991 (2004).
[Crossref] [PubMed]

Shear, J. B.

C. Xu, W. Zipfel, J. B. Shear, R. M. Williams, and W. W. Webb, “Multiphoton fluorescence excitation: new spectral windows for biological nonlinear microscopy,” Proc. Natl. Acad. Sci. U.S.A. 93(20), 10763–10768 (1996).
[Crossref] [PubMed]

Singhvi, A.

Z. Wang, A. Singhvi, P. Kong, and K. Scott, “Taste representations in the Drosophila brain,” Cell 117(7), 981–991 (2004).
[Crossref] [PubMed]

Song, L.

Sørensen, A. T.

A. S. Chuong, M. L. Miri, V. Busskamp, G. A. Matthews, L. C. Acker, A. T. Sørensen, A. Young, N. C. Klapoetke, M. A. Henninger, S. B. Kodandaramaiah, M. Ogawa, S. B. Ramanlal, R. C. Bandler, B. D. Allen, C. R. Forest, B. Y. Chow, X. Han, Y. Lin, K. M. Tye, B. Roska, J. A. Cardin, and E. S. Boyden, “Noninvasive optical inhibition with a red-shifted microbial rhodopsin,” Nat. Neurosci. 17(8), 1123–1129 (2014).
[Crossref] [PubMed]

Suh, G. S.

G. S. Suh, S. Ben-Tabou de Leon, H. Tanimoto, A. Fiala, S. Benzer, and D. J. Anderson, “Light activation of an innate olfactory avoidance response in Drosophila,” Curr. Biol. 17(10), 905–908 (2007).
[Crossref] [PubMed]

Surek, B.

N. C. Klapoetke, Y. Murata, S. S. Kim, S. R. Pulver, A. Birdsey-Benson, Y. K. Cho, T. K. Morimoto, A. S. Chuong, E. J. Carpenter, Z. Tian, J. Wang, Y. Xie, Z. Yan, Y. Zhang, B. Y. Chow, B. Surek, M. Melkonian, V. Jayaraman, M. Constantine-Paton, G. K. Wong, and E. S. Boyden, “Independent optical excitation of distinct neural populations,” Nat. Methods 11(3), 338–346 (2014).
[Crossref] [PubMed]

Szellas, T.

G. Nagel, T. Szellas, W. Huhn, S. Kateriya, N. Adeishvili, P. Berthold, D. Ollig, P. Hegemann, and E. Bamberg, “Channelrhodopsin-2, a directly light-gated cation-selective membrane channel,” Proc. Natl. Acad. Sci. U.S.A. 100(24), 13940–13945 (2003).
[Crossref] [PubMed]

Tanimoto, H.

G. S. Suh, S. Ben-Tabou de Leon, H. Tanimoto, A. Fiala, S. Benzer, and D. J. Anderson, “Light activation of an innate olfactory avoidance response in Drosophila,” Curr. Biol. 17(10), 905–908 (2007).
[Crossref] [PubMed]

Tank, D. W.

J. P. Rickgauer and D. W. Tank, “Two-photon excitation of channelrhodopsin-2 at saturation,” Proc. Natl. Acad. Sci. U.S.A. 106(35), 15025–15030 (2009).
[Crossref] [PubMed]

Tayler, T. D.

T. D. Tayler, D. A. Pacheco, A. C. Hergarden, M. Murthy, and D. J. Anderson, “A neuropeptide circuit that coordinates sperm transfer and copulation duration in Drosophila,” Proc. Natl. Acad. Sci. U.S.A. 109(50), 20697–20702 (2012).
[Crossref] [PubMed]

Tian, Z.

N. C. Klapoetke, Y. Murata, S. S. Kim, S. R. Pulver, A. Birdsey-Benson, Y. K. Cho, T. K. Morimoto, A. S. Chuong, E. J. Carpenter, Z. Tian, J. Wang, Y. Xie, Z. Yan, Y. Zhang, B. Y. Chow, B. Surek, M. Melkonian, V. Jayaraman, M. Constantine-Paton, G. K. Wong, and E. S. Boyden, “Independent optical excitation of distinct neural populations,” Nat. Methods 11(3), 338–346 (2014).
[Crossref] [PubMed]

Tillo, S. E.

M. Drobizhev, N. S. Makarov, S. E. Tillo, T. E. Hughes, and A. Rebane, “Two-photon absorption properties of fluorescent proteins,” Nat. Methods 8(5), 393–399 (2011).
[Crossref] [PubMed]

Tsien, R. Y.

H. K. Inagaki, Y. Jung, E. D. Hoopfer, A. M. Wong, N. Mishra, J. Y. Lin, R. Y. Tsien, and D. J. Anderson, “Optogenetic control of Drosophila using a red-shifted channelrhodopsin reveals experience-dependent influences on courtship,” Nat. Methods 11(3), 325–332 (2013).
[Crossref] [PubMed]

J. Y. Lin, P. M. Knutsen, A. Muller, D. Kleinfeld, and R. Y. Tsien, “ReaChR: a red-shifted variant of channelrhodopsin enables deep transcranial optogenetic excitation,” Nat. Neurosci. 16(10), 1499–1508 (2013).
[Crossref] [PubMed]

Tsunoda, S. P.

F. Zhang, M. Prigge, F. Beyrière, S. P. Tsunoda, J. Mattis, O. Yizhar, P. Hegemann, and K. Deisseroth, “Red-shifted optogenetic excitation: a tool for fast neural control derived from Volvox carteri,” Nat. Neurosci. 11(6), 631–633 (2008).
[Crossref] [PubMed]

Tye, K. M.

A. S. Chuong, M. L. Miri, V. Busskamp, G. A. Matthews, L. C. Acker, A. T. Sørensen, A. Young, N. C. Klapoetke, M. A. Henninger, S. B. Kodandaramaiah, M. Ogawa, S. B. Ramanlal, R. C. Bandler, B. D. Allen, C. R. Forest, B. Y. Chow, X. Han, Y. Lin, K. M. Tye, B. Roska, J. A. Cardin, and E. S. Boyden, “Noninvasive optical inhibition with a red-shifted microbial rhodopsin,” Nat. Neurosci. 17(8), 1123–1129 (2014).
[Crossref] [PubMed]

Völler, T.

C. Schroll, T. Riemensperger, D. Bucher, J. Ehmer, T. Völler, K. Erbguth, B. Gerber, T. Hendel, G. Nagel, E. Buchner, and A. Fiala, “Light-induced activation of distinct modulatory neurons triggers appetitive or aversive learning in Drosophila larvae,” Curr. Biol. 16(17), 1741–1747 (2006).
[Crossref] [PubMed]

Wang, D.

Wang, J.

N. C. Klapoetke, Y. Murata, S. S. Kim, S. R. Pulver, A. Birdsey-Benson, Y. K. Cho, T. K. Morimoto, A. S. Chuong, E. J. Carpenter, Z. Tian, J. Wang, Y. Xie, Z. Yan, Y. Zhang, B. Y. Chow, B. Surek, M. Melkonian, V. Jayaraman, M. Constantine-Paton, G. K. Wong, and E. S. Boyden, “Independent optical excitation of distinct neural populations,” Nat. Methods 11(3), 338–346 (2014).
[Crossref] [PubMed]

Wang, L. P.

F. Zhang, L. P. Wang, E. S. Boyden, and K. Deisseroth, “Channelrhodopsin-2 and optical control of excitable cells,” Nat. Methods 3(10), 785–792 (2006).
[Crossref] [PubMed]

Wang, Z.

Z. Wang, A. Singhvi, P. Kong, and K. Scott, “Taste representations in the Drosophila brain,” Cell 117(7), 981–991 (2004).
[Crossref] [PubMed]

Watanabe, S.

Webb, W. W.

J. B. Guild, C. Xu, and W. W. Webb, “Measurement of group delay dispersion of high numerical aperture objective lenses using two-photon excited fluorescence,” Appl. Opt. 36(1), 397–401 (1997).
[Crossref] [PubMed]

C. Xu, W. Zipfel, J. B. Shear, R. M. Williams, and W. W. Webb, “Multiphoton fluorescence excitation: new spectral windows for biological nonlinear microscopy,” Proc. Natl. Acad. Sci. U.S.A. 93(20), 10763–10768 (1996).
[Crossref] [PubMed]

Williams, R. M.

C. Xu, W. Zipfel, J. B. Shear, R. M. Williams, and W. W. Webb, “Multiphoton fluorescence excitation: new spectral windows for biological nonlinear microscopy,” Proc. Natl. Acad. Sci. U.S.A. 93(20), 10763–10768 (1996).
[Crossref] [PubMed]

Wong, A. M.

H. K. Inagaki, Y. Jung, E. D. Hoopfer, A. M. Wong, N. Mishra, J. Y. Lin, R. Y. Tsien, and D. J. Anderson, “Optogenetic control of Drosophila using a red-shifted channelrhodopsin reveals experience-dependent influences on courtship,” Nat. Methods 11(3), 325–332 (2013).
[Crossref] [PubMed]

Wong, G. K.

N. C. Klapoetke, Y. Murata, S. S. Kim, S. R. Pulver, A. Birdsey-Benson, Y. K. Cho, T. K. Morimoto, A. S. Chuong, E. J. Carpenter, Z. Tian, J. Wang, Y. Xie, Z. Yan, Y. Zhang, B. Y. Chow, B. Surek, M. Melkonian, V. Jayaraman, M. Constantine-Paton, G. K. Wong, and E. S. Boyden, “Independent optical excitation of distinct neural populations,” Nat. Methods 11(3), 338–346 (2014).
[Crossref] [PubMed]

Wu, M. C.

Y. Y. Lin, M. C. Wu, P. Y. Hsiao, L. A. Chu, M. M. Yang, C. C. Fu, and A. S. Chiang, “Three-wavelength light control of freely moving Drosophila Melanogaster for less perturbation and efficient social-behavioral studies,” Biomed. Opt. Express 6(2), 514–523 (2015).
[Crossref] [PubMed]

M. C. Wu, L. A. Chu, P. Y. Hsiao, Y. Y. Lin, C. C. Chi, T. H. Liu, C. C. Fu, and A. S. Chiang, “Optogenetic control of selective neural activity in multiple freely moving Drosophila adults,” Proc. Natl. Acad. Sci. U.S.A. 111(14), 5367–5372 (2014).
[Crossref] [PubMed]

Xie, Y.

N. C. Klapoetke, Y. Murata, S. S. Kim, S. R. Pulver, A. Birdsey-Benson, Y. K. Cho, T. K. Morimoto, A. S. Chuong, E. J. Carpenter, Z. Tian, J. Wang, Y. Xie, Z. Yan, Y. Zhang, B. Y. Chow, B. Surek, M. Melkonian, V. Jayaraman, M. Constantine-Paton, G. K. Wong, and E. S. Boyden, “Independent optical excitation of distinct neural populations,” Nat. Methods 11(3), 338–346 (2014).
[Crossref] [PubMed]

Xu, C.

Xu, Z.

Yamaguchi, S.

S. Yamaguchi, C. Desplan, and M. Heisenberg, “Contribution of photoreceptor subtypes to spectral wavelength preference in Drosophila,” Proc. Natl. Acad. Sci. U.S.A. 107(12), 5634–5639 (2010).
[Crossref] [PubMed]

Yan, Z.

N. C. Klapoetke, Y. Murata, S. S. Kim, S. R. Pulver, A. Birdsey-Benson, Y. K. Cho, T. K. Morimoto, A. S. Chuong, E. J. Carpenter, Z. Tian, J. Wang, Y. Xie, Z. Yan, Y. Zhang, B. Y. Chow, B. Surek, M. Melkonian, V. Jayaraman, M. Constantine-Paton, G. K. Wong, and E. S. Boyden, “Independent optical excitation of distinct neural populations,” Nat. Methods 11(3), 338–346 (2014).
[Crossref] [PubMed]

Yang, M. M.

Yizhar, O.

A. Berndt, O. Yizhar, L. A. Gunaydin, P. Hegemann, and K. Deisseroth, “Bi-stable neural state switches,” Nat. Neurosci. 12(2), 229–234 (2009).
[Crossref] [PubMed]

F. Zhang, M. Prigge, F. Beyrière, S. P. Tsunoda, J. Mattis, O. Yizhar, P. Hegemann, and K. Deisseroth, “Red-shifted optogenetic excitation: a tool for fast neural control derived from Volvox carteri,” Nat. Neurosci. 11(6), 631–633 (2008).
[Crossref] [PubMed]

Young, A.

A. S. Chuong, M. L. Miri, V. Busskamp, G. A. Matthews, L. C. Acker, A. T. Sørensen, A. Young, N. C. Klapoetke, M. A. Henninger, S. B. Kodandaramaiah, M. Ogawa, S. B. Ramanlal, R. C. Bandler, B. D. Allen, C. R. Forest, B. Y. Chow, X. Han, Y. Lin, K. M. Tye, B. Roska, J. A. Cardin, and E. S. Boyden, “Noninvasive optical inhibition with a red-shifted microbial rhodopsin,” Nat. Neurosci. 17(8), 1123–1129 (2014).
[Crossref] [PubMed]

Zhang, F.

F. Zhang, M. Prigge, F. Beyrière, S. P. Tsunoda, J. Mattis, O. Yizhar, P. Hegemann, and K. Deisseroth, “Red-shifted optogenetic excitation: a tool for fast neural control derived from Volvox carteri,” Nat. Neurosci. 11(6), 631–633 (2008).
[Crossref] [PubMed]

F. Zhang, L. P. Wang, E. S. Boyden, and K. Deisseroth, “Channelrhodopsin-2 and optical control of excitable cells,” Nat. Methods 3(10), 785–792 (2006).
[Crossref] [PubMed]

Zhang, Y.

N. C. Klapoetke, Y. Murata, S. S. Kim, S. R. Pulver, A. Birdsey-Benson, Y. K. Cho, T. K. Morimoto, A. S. Chuong, E. J. Carpenter, Z. Tian, J. Wang, Y. Xie, Z. Yan, Y. Zhang, B. Y. Chow, B. Surek, M. Melkonian, V. Jayaraman, M. Constantine-Paton, G. K. Wong, and E. S. Boyden, “Independent optical excitation of distinct neural populations,” Nat. Methods 11(3), 338–346 (2014).
[Crossref] [PubMed]

Zipfel, W.

C. Xu, W. Zipfel, J. B. Shear, R. M. Williams, and W. W. Webb, “Multiphoton fluorescence excitation: new spectral windows for biological nonlinear microscopy,” Proc. Natl. Acad. Sci. U.S.A. 93(20), 10763–10768 (1996).
[Crossref] [PubMed]

Appl. Opt. (1)

Biomed. Opt. Express (1)

Cell (1)

Z. Wang, A. Singhvi, P. Kong, and K. Scott, “Taste representations in the Drosophila brain,” Cell 117(7), 981–991 (2004).
[Crossref] [PubMed]

Curr. Biol. (2)

C. Schroll, T. Riemensperger, D. Bucher, J. Ehmer, T. Völler, K. Erbguth, B. Gerber, T. Hendel, G. Nagel, E. Buchner, and A. Fiala, “Light-induced activation of distinct modulatory neurons triggers appetitive or aversive learning in Drosophila larvae,” Curr. Biol. 16(17), 1741–1747 (2006).
[Crossref] [PubMed]

G. S. Suh, S. Ben-Tabou de Leon, H. Tanimoto, A. Fiala, S. Benzer, and D. J. Anderson, “Light activation of an innate olfactory avoidance response in Drosophila,” Curr. Biol. 17(10), 905–908 (2007).
[Crossref] [PubMed]

J. Genet. (1)

M. Chakir, H. Negoua, B. Moreteau, and J. R. David, “Quantitative morphometrical analysis of a North African population of Drosophila melanogaster: sexual dimorphism, and comparison with European populations,” J. Genet. 87(4), 373–382 (2008).
[Crossref] [PubMed]

Nat. Methods (6)

N. C. Klapoetke, Y. Murata, S. S. Kim, S. R. Pulver, A. Birdsey-Benson, Y. K. Cho, T. K. Morimoto, A. S. Chuong, E. J. Carpenter, Z. Tian, J. Wang, Y. Xie, Z. Yan, Y. Zhang, B. Y. Chow, B. Surek, M. Melkonian, V. Jayaraman, M. Constantine-Paton, G. K. Wong, and E. S. Boyden, “Independent optical excitation of distinct neural populations,” Nat. Methods 11(3), 338–346 (2014).
[Crossref] [PubMed]

H. K. Inagaki, Y. Jung, E. D. Hoopfer, A. M. Wong, N. Mishra, J. Y. Lin, R. Y. Tsien, and D. J. Anderson, “Optogenetic control of Drosophila using a red-shifted channelrhodopsin reveals experience-dependent influences on courtship,” Nat. Methods 11(3), 325–332 (2013).
[Crossref] [PubMed]

F. Zhang, L. P. Wang, E. S. Boyden, and K. Deisseroth, “Channelrhodopsin-2 and optical control of excitable cells,” Nat. Methods 3(10), 785–792 (2006).
[Crossref] [PubMed]

M. Drobizhev, N. S. Makarov, S. E. Tillo, T. E. Hughes, and A. Rebane, “Two-photon absorption properties of fluorescent proteins,” Nat. Methods 8(5), 393–399 (2011).
[Crossref] [PubMed]

A. M. Packer, L. E. Russell, H. W. 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]

E. Papagiakoumou, F. Anselmi, A. Bègue, V. de Sars, J. Glückstad, E. Y. Isacoff, and V. Emiliani, “Scanless two-photon excitation of channelrhodopsin-2,” Nat. Methods 7(10), 848–854 (2010).
[Crossref] [PubMed]

Nat. Neurosci. (4)

F. Zhang, M. Prigge, F. Beyrière, S. P. Tsunoda, J. Mattis, O. Yizhar, P. Hegemann, and K. Deisseroth, “Red-shifted optogenetic excitation: a tool for fast neural control derived from Volvox carteri,” Nat. Neurosci. 11(6), 631–633 (2008).
[Crossref] [PubMed]

A. Berndt, O. Yizhar, L. A. Gunaydin, P. Hegemann, and K. Deisseroth, “Bi-stable neural state switches,” Nat. Neurosci. 12(2), 229–234 (2009).
[Crossref] [PubMed]

J. Y. Lin, P. M. Knutsen, A. Muller, D. Kleinfeld, and R. Y. Tsien, “ReaChR: a red-shifted variant of channelrhodopsin enables deep transcranial optogenetic excitation,” Nat. Neurosci. 16(10), 1499–1508 (2013).
[Crossref] [PubMed]

A. S. Chuong, M. L. Miri, V. Busskamp, G. A. Matthews, L. C. Acker, A. T. Sørensen, A. Young, N. C. Klapoetke, M. A. Henninger, S. B. Kodandaramaiah, M. Ogawa, S. B. Ramanlal, R. C. Bandler, B. D. Allen, C. R. Forest, B. Y. Chow, X. Han, Y. Lin, K. M. Tye, B. Roska, J. A. Cardin, and E. S. Boyden, “Noninvasive optical inhibition with a red-shifted microbial rhodopsin,” Nat. Neurosci. 17(8), 1123–1129 (2014).
[Crossref] [PubMed]

Opt. Express (1)

Opt. Lett. (2)

Proc. Natl. Acad. Sci. U.S.A. (6)

T. D. Tayler, D. A. Pacheco, A. C. Hergarden, M. Murthy, and D. J. Anderson, “A neuropeptide circuit that coordinates sperm transfer and copulation duration in Drosophila,” Proc. Natl. Acad. Sci. U.S.A. 109(50), 20697–20702 (2012).
[Crossref] [PubMed]

J. P. Rickgauer and D. W. Tank, “Two-photon excitation of channelrhodopsin-2 at saturation,” Proc. Natl. Acad. Sci. U.S.A. 106(35), 15025–15030 (2009).
[Crossref] [PubMed]

C. Xu, W. Zipfel, J. B. Shear, R. M. Williams, and W. W. Webb, “Multiphoton fluorescence excitation: new spectral windows for biological nonlinear microscopy,” Proc. Natl. Acad. Sci. U.S.A. 93(20), 10763–10768 (1996).
[Crossref] [PubMed]

M. C. Wu, L. A. Chu, P. Y. Hsiao, Y. Y. Lin, C. C. Chi, T. H. Liu, C. C. Fu, and A. S. Chiang, “Optogenetic control of selective neural activity in multiple freely moving Drosophila adults,” Proc. Natl. Acad. Sci. U.S.A. 111(14), 5367–5372 (2014).
[Crossref] [PubMed]

G. Nagel, T. Szellas, W. Huhn, S. Kateriya, N. Adeishvili, P. Berthold, D. Ollig, P. Hegemann, and E. Bamberg, “Channelrhodopsin-2, a directly light-gated cation-selective membrane channel,” Proc. Natl. Acad. Sci. U.S.A. 100(24), 13940–13945 (2003).
[Crossref] [PubMed]

S. Yamaguchi, C. Desplan, and M. Heisenberg, “Contribution of photoreceptor subtypes to spectral wavelength preference in Drosophila,” Proc. Natl. Acad. Sci. U.S.A. 107(12), 5634–5639 (2010).
[Crossref] [PubMed]

Science (1)

H. H. Lin, L. A. Chu, T. F. Fu, B. J. Dickson, and A. S. Chiang, “Parallel neural pathways mediate CO2 avoidance responses in Drosophila,” Science 340(6138), 1338–1341 (2013).
[Crossref] [PubMed]

Other (1)

Y. R. Shen, “Two-photon absorption,” in The Principle of Nonlinear Optics, Y. R. Shen, ed. (Wiley-Interscience 1984) pp. 202–210.

Supplementary Material (2)

NameDescription
» Visualization 1: AVI (3979 KB)      This visualization shows the abdominal bending of a fly (Crz-Gal4 > UAS-ReaChR) fed 100 µM of all-trans-retinal illuminated by an effective peak power of 0.98 GW at 1250 nm.
» Visualization 2: AVI (3565 KB)      This visualization shows the proboscis extension response of a fly (Gr5a-Gal4 > UAS-ReaChR) fed 100 µM of all-trans-retinal illuminated by an effective peak power of 0.98 GW at 1250 nm.

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Figures (4)

Fig. 1
Fig. 1 Schematic of the experimental setup. OPA, optical parametric amplifier; BBO, beta barium borate; WLG, white-light generation.
Fig. 2
Fig. 2 Characteristics of femtosecond three-stage OPA system. (a). Signal power spectra, centered at seven wavelengths from 1150−1565 nm, generated by our three-stage OPA system. (b). Calculated signal and idler wavelengths at different phase-matching angles. (c). White-light spectrum seeded to the first-stage OPA.
Fig. 3
Fig. 3 Fruit fly neuron map and bending rate as a function of wavelength. (a) Corazonin (Crz) neurons (green) were labeled in the Crz-GAL4> UAS-ReaChR transgenic fly. The brain and thoracic ganglia were immunostained with anti-discs large antibody (magenta). The scale bar represents 100 μm. (b) Bending rates at different wavelengths of the femtosecond three-stage OPA laser with an effective peak power of 0.98 GW. The optimized TPE wavelength of ReaChR is 1250 nm. Crz-Gal4>UAS-ReaChR and UAS-ReaChR/W flies were fed standard food with ( + ) or without (–) 100-μM all-trans-retinal, respectively, for 7 days before the experiment. The bending rates at wavelengths of 1150, 1200, and 1300 nm show no significant difference. The data represent mean ± SEM (N = 16). *, P < 0.05; ***, P < 0.005; NS, not significant.
Fig. 4
Fig. 4 Optical transmission spectrum of fly cuticle and laser effective peak power manipulations. (a) Optical transmission of a dissected fly cuticle in the dorsal abdomen. The optical transmission of 1250 nm is 10.8% and the optical transmissions of the other wavelengths were normalized to 1250 nm. The transmission at longer wavelengths is higher because of reduced scattering. (b) Bending rate as a function of effective peak power (0.16, 0.33, 0.54, 0.98, 1.20, and 1.53 GW) at different central wavelengths. Because the required effective peak power of the 1250-nm (red) laser is lower, its efficiency is higher than that of the 1150-nm (blue) and 1300-nm (black) lasers. The solid lines (filled triangle, filled round, and filled square) are the real measured curves, and the dotted lines (unfilled triangle, and unfilled square) are the curves which were adjusted relative to 1250 nm based on the optical transmission through the cuticles. (c) Bending rates for two-photon (effective peak power of 0.98 GW) and one-photon (effective peak power of 0.07 GW) excitations at the same effective average power, using a femtosecond three-stage OPA laser at a central wavelength of 1250 nm. In both panels, Crz-Gal4>UAS-ReaChR flies were fed standard food with 100 μM of all-trans-retinal for 7 days before the experiment. The data represent mean ± SEM (N = 8). ***, P < 0.005.

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