Abstract

We demonstrate transcutical structural and functional imaging of neurons labeled with genetically encoded red fluorescent proteins and calcium indicators in the living Drosophila brain with cellular and subcellular resolution.

© 2017 Optical Society of America

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References

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    [Crossref] [PubMed]
  3. P. Theer, M. T. Hasan, and W. Denk, “Two-photon imaging to a depth of 1000 microm in living brains by use of a Ti:Al2O3 regenerative amplifier,” Opt. Lett. 28(12), 1022–1024 (2003).
    [Crossref] [PubMed]
  4. D. Kobat, M. E. Durst, N. Nishimura, A. W. Wong, C. B. Schaffer, and C. Xu, “Deep tissue multiphoton microscopy using longer wavelength excitation,” Opt. Express 17(16), 13354–13364 (2009).
    [Crossref] [PubMed]
  5. L. Shi, L. A. Sordillo, A. Rodríguez-Contreras, and R. Alfano, “Transmission in near-infrared optical windows for deep brain imaging,” J. Biophotonics 9(1-2), 38–43 (2016).
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  8. J. Tang, R. N. Germain, and M. Cui, “Superpenetration optical microscopy by iterative multiphoton adaptive compensation technique,” Proc. Natl. Acad. Sci. U.S.A. 109(22), 8434–8439 (2012).
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  9. X. Tao, A. Norton, M. Kissel, O. Azucena, and J. Kubby, “Adaptive optical two-photon microscopy using autofluorescent guide stars,” Opt. Lett. 38(23), 5075–5078 (2013).
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  26. C. M. Root, K. I. Ko, A. Jafari, and J. W. Wang, “Presynaptic facilitation by neuropeptide signaling mediates odor-driven food search,” Cell 145(1), 133–144 (2011).
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  30. D. Grover, T. Katsuki, and R. J. Greenspan, “Flyception: imaging brain activity in freely walking fruit flies,” Nat. Methods 13(7), 569–572 (2016).
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    [Crossref] [PubMed]
  34. A. Facomprez, E. Beaurepaire, and D. Débarre, “Accuracy of correction in modal sensorless adaptive optics,” Opt. Express 20(3), 2598–2612 (2012).
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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
  38. Y. Wang, W. Wen, K. Wang, P. Zhai, P. Qiu, and K. Wang, “Measurement of absorption spectrum of deuterium oxide (D2O) and its application to signal enhancement in multiphoton microscopy at the 1700-nm window,” Appl. Phys. Lett. 108(2), 021112 (2016).
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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
  42. K. Yasuyama, I. A. Meinertzhagen, and F. W. Schuermann, “Synaptic connections of cholinergic antennal lobe relay neurons in the brain of Drosophila melanogaster,” J. Comp. Neurol. 466, 299–315 (2003).
    [Crossref] [PubMed]
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2016 (6)

H.-H. Lin, D.-S. Cao, S. Sethi, Z. Zeng, J. S. R. Chin, T. S. Chakraborty, A. K. Shepherd, C. A. Nguyen, J. Y. Yew, C.-Y. Su, and J. W. Wang, “Hormonal Modulation of Pheromone Detection Enhances Male Courtship Success,” Neuron 90(6), 1272–1285 (2016).
[Crossref] [PubMed]

D. Grover, T. Katsuki, and R. J. Greenspan, “Flyception: imaging brain activity in freely walking fruit flies,” Nat. Methods 13(7), 569–572 (2016).
[Crossref] [PubMed]

L. Shi, L. A. Sordillo, A. Rodríguez-Contreras, and R. Alfano, “Transmission in near-infrared optical windows for deep brain imaging,” J. Biophotonics 9(1-2), 38–43 (2016).
[Crossref] [PubMed]

A. R. Kay, D. Raccuglia, J. Scholte, E. Sivan-Loukianova, C. A. Barwacz, S. R. Armstrong, C. A. Guymon, M. N. Nitabach, and D. F. Eberl, “Goggatomy: A Method for Opening Small Cuticular Compartments in Arthropods for Physiological Experiments,” Front. Physiol. 7, 398 (2016).
[Crossref] [PubMed]

Y. Wang, W. Wen, K. Wang, P. Zhai, P. Qiu, and K. Wang, “Measurement of absorption spectrum of deuterium oxide (D2O) and its application to signal enhancement in multiphoton microscopy at the 1700-nm window,” Appl. Phys. Lett. 108(2), 021112 (2016).
[Crossref]

H. Dana, B. Mohar, Y. Sun, S. Narayan, A. Gordus, J. P. Hasseman, G. Tsegaye, G. T. Holt, A. Hu, D. Walpita, R. Patel, J. J. Macklin, C. I. Bargmann, M. B. Ahrens, E. R. Schreiter, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Sensitive red protein calcium indicators for imaging neural activity,” eLife 5, 1–24 (2016).
[Crossref] [PubMed]

2015 (8)

M. Dus, J. S. Lai, K. M. Gunapala, S. Min, T. D. Tayler, A. C. Hergarden, E. Geraud, C. M. Joseph, and G. S. Suh, “Nutrient sensor in the brain directs the action of the brain-gut axis in Drosophila,” Neuron 87(1), 139–151 (2015).
[Crossref] [PubMed]

R. Cohn, I. Morantte, and V. Ruta, “Coordinated and Compartmentalized Neuromodulation Shapes Sensory Processing in Drosophila,” Cell 163(7), 1742–1755 (2015).
[Crossref] [PubMed]

K. I. Ko, C. M. Root, S. A. Lindsay, O. A. Zaninovich, A. K. Shepherd, S. A. Wasserman, S. M. Kim, and J. W. Wang, “Starvation promotes concerted modulation of appetitive olfactory behavior via parallel neuromodulatory circuits,” eLife 4, 1–17 (2015).
[Crossref] [PubMed]

K. Wang, W. Sun, C. T. Richie, B. K. Harvey, E. Betzig, and N. Ji, “Direct wavefront sensing for high-resolution in vivo imaging in scattering tissue,” Nat. Commun. 6, 7276 (2015).
[Crossref] [PubMed]

M. J. McGinley, M. Vinck, J. Reimer, R. Batista-Brito, E. Zagha, C. R. Cadwell, A. S. Tolias, J. A. Cardin, and D. A. McCormick, “Waking State: Rapid Variations Modulate Neural and Behavioral Responses,” Neuron 87(6), 1143–1161 (2015).
[Crossref] [PubMed]

N. G. Horton and C. Xu, “Dispersion compensation in three-photon fluorescence microscopy at 1,700 nm,” Biomed. Opt. Express 6(4), 1392–1397 (2015).
[Crossref] [PubMed]

P.-Y. Hsiao, C.-L. Tsai, M.-C. Chen, Y.-Y. Lin, S.-D. Yang, and A.-S. Chiang, “Non-invasive manipulation of Drosophila behavior by two-photon excited red-activatable channelrhodopsin,” Biomed. Opt. Express 6(11), 4344–4352 (2015).
[Crossref] [PubMed]

D. Sinefeld, H. P. Paudel, D. G. Ouzounov, T. G. Bifano, and C. Xu, “Adaptive optics in multiphoton microscopy: comparison of two, three and four photon fluorescence,” Opt. Express 23(24), 31472–31483 (2015).
[Crossref] [PubMed]

2014 (2)

K. Wang, N. G. Horton, K. Charan, and C. Xu, “Advanced Fiber Soliton Sources for Nonlinear Deep Tissue Imaging in Biophotonics,” IEEE J. Sel. Top. Quantum Electron. 20(2), 50–60 (2014).
[Crossref]

C. Y. Su and J. W. Wang, “Modulation of neural circuits: How stimulus context shapes innate behavior in Drosophila,” Curr. Opin. Neurobiol. 29, 9–16 (2014).
[Crossref] [PubMed]

2013 (8)

N. J. Strausfeld and F. Hirth, “Deep Homology of Arthropod Central Complex and Vertebrate Basal Ganglia,” Science 340(6129), 157–161 (2013).
[Crossref] [PubMed]

N. G. Horton, K. Wang, D. Kobat, C. G. Clark, F. W. Wise, C. B. Schaffer, and C. Xu, “In vivo three-photon microscopy of subcortical structures within an intact mouse brain,” Nat. Photonics 7(3), 205–209 (2013).
[Crossref] [PubMed]

C. I. Bargmann and E. Marder, “From the connectome to brain function,” Nat. Methods 10(6), 483–490 (2013).
[Crossref] [PubMed]

T. W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
[Crossref] [PubMed]

T.-W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
[Crossref] [PubMed]

S. M. Kim and J. W. Wang, “Calcium Imaging of Pheromone Responses in the Insect Antennal Lobe,” Methods Mol. Biol. 1068, 179–187 (2013).
[Crossref] [PubMed]

J. D. Seelig and V. Jayaraman, “Feature detection and orientation tuning in the Drosophila central complex,” Nature 503(7475), 262–266 (2013).
[PubMed]

X. Tao, A. Norton, M. Kissel, O. Azucena, and J. Kubby, “Adaptive optical two-photon microscopy using autofluorescent guide stars,” Opt. Lett. 38(23), 5075–5078 (2013).
[Crossref] [PubMed]

2012 (2)

A. Facomprez, E. Beaurepaire, and D. Débarre, “Accuracy of correction in modal sensorless adaptive optics,” Opt. Express 20(3), 2598–2612 (2012).
[Crossref] [PubMed]

J. Tang, R. N. Germain, and M. Cui, “Superpenetration optical microscopy by iterative multiphoton adaptive compensation technique,” Proc. Natl. Acad. Sci. U.S.A. 109(22), 8434–8439 (2012).
[Crossref] [PubMed]

2011 (2)

K. J. T. Venken, J. H. Simpson, and H. J. Bellen, “Genetic manipulation of genes and cells in the nervous system of the fruit fly,” Neuron 72(2), 202–230 (2011).
[Crossref] [PubMed]

C. M. Root, K. I. Ko, A. Jafari, and J. W. Wang, “Presynaptic facilitation by neuropeptide signaling mediates odor-driven food search,” Cell 145(1), 133–144 (2011).
[Crossref] [PubMed]

2010 (3)

A. Kamikouchi, R. Wiek, T. Effertz, M. C. Göpfert, and A. Fiala, “Transcuticular optical imaging of stimulus-evoked neural activities in the Drosophila peripheral nervous system,” Nat. Protoc. 5(7), 1229–1235 (2010).
[Crossref] [PubMed]

N. Ji, D. E. Milkie, and E. Betzig, “Adaptive optics via pupil segmentation for high-resolution imaging in biological tissues,” Nat. Methods 7(2), 141–147 (2010).
[Crossref] [PubMed]

O. Azucena, J. Crest, J. Cao, W. Sullivan, P. Kner, D. Gavel, D. Dillon, S. Olivier, and J. Kubby, “Wavefront aberration measurements and corrections through thick tissue using fluorescent microsphere reference beacons,” Opt. Express 18(16), 17521–17532 (2010).
[Crossref] [PubMed]

2009 (2)

2007 (1)

M. J. Booth, “Adaptive optics in microscopy,” Philos Trans A Math Phys Eng Sci 365(1861), 2829–2843 (2007).
[Crossref] [PubMed]

2006 (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]

2005 (1)

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

2004 (1)

G. S. Suh, A. M. Wong, A. C. Hergarden, J. W. Wang, A. F. Simon, S. Benzer, R. Axel, and D. J. Anderson, “A single population of olfactory sensory neurons mediates an innate avoidance behaviour in Drosophila,” Nature 431(7010), 854–859 (2004).
[Crossref] [PubMed]

2003 (4)

J. W. Wang, A. M. Wong, J. Flores, L. B. Vosshall, and R. Axel, “Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain,” Cell 112(2), 271–282 (2003).
[Crossref] [PubMed]

P. Marsh, D. Burns, and J. Girkin, “Practical implementation of adaptive optics in multiphoton microscopy,” Opt. Express 11(10), 1123–1130 (2003).
[Crossref] [PubMed]

P. Theer, M. T. Hasan, and W. Denk, “Two-photon imaging to a depth of 1000 microm in living brains by use of a Ti:Al2O3 regenerative amplifier,” Opt. Lett. 28(12), 1022–1024 (2003).
[Crossref] [PubMed]

K. Yasuyama, I. A. Meinertzhagen, and F. W. Schuermann, “Synaptic connections of cholinergic antennal lobe relay neurons in the brain of Drosophila melanogaster,” J. Comp. Neurol. 466, 299–315 (2003).
[Crossref] [PubMed]

2001 (2)

M. B. Sokolowski, “Drosophila: Genetics meets behaviour,” Nat. Rev. Genet. 2(11), 879–890 (2001).
[Crossref] [PubMed]

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

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]

Ahrens, M. B.

H. Dana, B. Mohar, Y. Sun, S. Narayan, A. Gordus, J. P. Hasseman, G. Tsegaye, G. T. Holt, A. Hu, D. Walpita, R. Patel, J. J. Macklin, C. I. Bargmann, M. B. Ahrens, E. R. Schreiter, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Sensitive red protein calcium indicators for imaging neural activity,” eLife 5, 1–24 (2016).
[Crossref] [PubMed]

Alfano, R.

L. Shi, L. A. Sordillo, A. Rodríguez-Contreras, and R. Alfano, “Transmission in near-infrared optical windows for deep brain imaging,” J. Biophotonics 9(1-2), 38–43 (2016).
[Crossref] [PubMed]

Anderson, D. J.

G. S. Suh, A. M. Wong, A. C. Hergarden, J. W. Wang, A. F. Simon, S. Benzer, R. Axel, and D. J. Anderson, “A single population of olfactory sensory neurons mediates an innate avoidance behaviour in Drosophila,” Nature 431(7010), 854–859 (2004).
[Crossref] [PubMed]

Armstrong, S. R.

A. R. Kay, D. Raccuglia, J. Scholte, E. Sivan-Loukianova, C. A. Barwacz, S. R. Armstrong, C. A. Guymon, M. N. Nitabach, and D. F. Eberl, “Goggatomy: A Method for Opening Small Cuticular Compartments in Arthropods for Physiological Experiments,” Front. Physiol. 7, 398 (2016).
[Crossref] [PubMed]

Axel, R.

G. S. Suh, A. M. Wong, A. C. Hergarden, J. W. Wang, A. F. Simon, S. Benzer, R. Axel, and D. J. Anderson, “A single population of olfactory sensory neurons mediates an innate avoidance behaviour in Drosophila,” Nature 431(7010), 854–859 (2004).
[Crossref] [PubMed]

J. W. Wang, A. M. Wong, J. Flores, L. B. Vosshall, and R. Axel, “Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain,” Cell 112(2), 271–282 (2003).
[Crossref] [PubMed]

Azucena, O.

Baohan, A.

T. W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
[Crossref] [PubMed]

T.-W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
[Crossref] [PubMed]

Bargmann, C. I.

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Y. Wang, W. Wen, K. Wang, P. Zhai, P. Qiu, and K. Wang, “Measurement of absorption spectrum of deuterium oxide (D2O) and its application to signal enhancement in multiphoton microscopy at the 1700-nm window,” Appl. Phys. Lett. 108(2), 021112 (2016).
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T. W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
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T.-W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
[Crossref] [PubMed]

Wasserman, S. A.

K. I. Ko, C. M. Root, S. A. Lindsay, O. A. Zaninovich, A. K. Shepherd, S. A. Wasserman, S. M. Kim, and J. W. Wang, “Starvation promotes concerted modulation of appetitive olfactory behavior via parallel neuromodulatory circuits,” eLife 4, 1–17 (2015).
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Watanabe, T.

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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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Y. Wang, W. Wen, K. Wang, P. Zhai, P. Qiu, and K. Wang, “Measurement of absorption spectrum of deuterium oxide (D2O) and its application to signal enhancement in multiphoton microscopy at the 1700-nm window,” Appl. Phys. Lett. 108(2), 021112 (2016).
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A. Kamikouchi, R. Wiek, T. Effertz, M. C. Göpfert, and A. Fiala, “Transcuticular optical imaging of stimulus-evoked neural activities in the Drosophila peripheral nervous system,” Nat. Protoc. 5(7), 1229–1235 (2010).
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Wilson, T.

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N. G. Horton, K. Wang, D. Kobat, C. G. Clark, F. W. Wise, C. B. Schaffer, and C. Xu, “In vivo three-photon microscopy of subcortical structures within an intact mouse brain,” Nat. Photonics 7(3), 205–209 (2013).
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G. S. Suh, A. M. Wong, A. C. Hergarden, J. W. Wang, A. F. Simon, S. Benzer, R. Axel, and D. J. Anderson, “A single population of olfactory sensory neurons mediates an innate avoidance behaviour in Drosophila,” Nature 431(7010), 854–859 (2004).
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J. W. Wang, A. M. Wong, J. Flores, L. B. Vosshall, and R. Axel, “Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain,” Cell 112(2), 271–282 (2003).
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Wong, A. W.

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K. Svoboda and R. Yasuda, “Principles of two-photon excitation microscopy and its applications to neuroscience,” Neuron 50(6), 823–839 (2006).
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K. Yasuyama, I. A. Meinertzhagen, and F. W. Schuermann, “Synaptic connections of cholinergic antennal lobe relay neurons in the brain of Drosophila melanogaster,” J. Comp. Neurol. 466, 299–315 (2003).
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H.-H. Lin, D.-S. Cao, S. Sethi, Z. Zeng, J. S. R. Chin, T. S. Chakraborty, A. K. Shepherd, C. A. Nguyen, J. Y. Yew, C.-Y. Su, and J. W. Wang, “Hormonal Modulation of Pheromone Detection Enhances Male Courtship Success,” Neuron 90(6), 1272–1285 (2016).
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Zagha, E.

M. J. McGinley, M. Vinck, J. Reimer, R. Batista-Brito, E. Zagha, C. R. Cadwell, A. S. Tolias, J. A. Cardin, and D. A. McCormick, “Waking State: Rapid Variations Modulate Neural and Behavioral Responses,” Neuron 87(6), 1143–1161 (2015).
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Zaninovich, O. A.

K. I. Ko, C. M. Root, S. A. Lindsay, O. A. Zaninovich, A. K. Shepherd, S. A. Wasserman, S. M. Kim, and J. W. Wang, “Starvation promotes concerted modulation of appetitive olfactory behavior via parallel neuromodulatory circuits,” eLife 4, 1–17 (2015).
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Zeng, Z.

H.-H. Lin, D.-S. Cao, S. Sethi, Z. Zeng, J. S. R. Chin, T. S. Chakraborty, A. K. Shepherd, C. A. Nguyen, J. Y. Yew, C.-Y. Su, and J. W. Wang, “Hormonal Modulation of Pheromone Detection Enhances Male Courtship Success,” Neuron 90(6), 1272–1285 (2016).
[Crossref] [PubMed]

Zhai, P.

Y. Wang, W. Wen, K. Wang, P. Zhai, P. Qiu, and K. Wang, “Measurement of absorption spectrum of deuterium oxide (D2O) and its application to signal enhancement in multiphoton microscopy at the 1700-nm window,” Appl. Phys. Lett. 108(2), 021112 (2016).
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Appl. Phys. Lett. (1)

Y. Wang, W. Wen, K. Wang, P. Zhai, P. Qiu, and K. Wang, “Measurement of absorption spectrum of deuterium oxide (D2O) and its application to signal enhancement in multiphoton microscopy at the 1700-nm window,” Appl. Phys. Lett. 108(2), 021112 (2016).
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Biomed. Opt. Express (2)

Cell (3)

R. Cohn, I. Morantte, and V. Ruta, “Coordinated and Compartmentalized Neuromodulation Shapes Sensory Processing in Drosophila,” Cell 163(7), 1742–1755 (2015).
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C. M. Root, K. I. Ko, A. Jafari, and J. W. Wang, “Presynaptic facilitation by neuropeptide signaling mediates odor-driven food search,” Cell 145(1), 133–144 (2011).
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J. W. Wang, A. M. Wong, J. Flores, L. B. Vosshall, and R. Axel, “Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain,” Cell 112(2), 271–282 (2003).
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Curr. Opin. Neurobiol. (1)

C. Y. Su and J. W. Wang, “Modulation of neural circuits: How stimulus context shapes innate behavior in Drosophila,” Curr. Opin. Neurobiol. 29, 9–16 (2014).
[Crossref] [PubMed]

eLife (2)

K. I. Ko, C. M. Root, S. A. Lindsay, O. A. Zaninovich, A. K. Shepherd, S. A. Wasserman, S. M. Kim, and J. W. Wang, “Starvation promotes concerted modulation of appetitive olfactory behavior via parallel neuromodulatory circuits,” eLife 4, 1–17 (2015).
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H. Dana, B. Mohar, Y. Sun, S. Narayan, A. Gordus, J. P. Hasseman, G. Tsegaye, G. T. Holt, A. Hu, D. Walpita, R. Patel, J. J. Macklin, C. I. Bargmann, M. B. Ahrens, E. R. Schreiter, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Sensitive red protein calcium indicators for imaging neural activity,” eLife 5, 1–24 (2016).
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Front. Physiol. (1)

A. R. Kay, D. Raccuglia, J. Scholte, E. Sivan-Loukianova, C. A. Barwacz, S. R. Armstrong, C. A. Guymon, M. N. Nitabach, and D. F. Eberl, “Goggatomy: A Method for Opening Small Cuticular Compartments in Arthropods for Physiological Experiments,” Front. Physiol. 7, 398 (2016).
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IEEE J. Sel. Top. Quantum Electron. (1)

K. Wang, N. G. Horton, K. Charan, and C. Xu, “Advanced Fiber Soliton Sources for Nonlinear Deep Tissue Imaging in Biophotonics,” IEEE J. Sel. Top. Quantum Electron. 20(2), 50–60 (2014).
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J. Biophotonics (1)

L. Shi, L. A. Sordillo, A. Rodríguez-Contreras, and R. Alfano, “Transmission in near-infrared optical windows for deep brain imaging,” J. Biophotonics 9(1-2), 38–43 (2016).
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J. Comp. Neurol. (1)

K. Yasuyama, I. A. Meinertzhagen, and F. W. Schuermann, “Synaptic connections of cholinergic antennal lobe relay neurons in the brain of Drosophila melanogaster,” J. Comp. Neurol. 466, 299–315 (2003).
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Methods Mol. Biol. (1)

S. M. Kim and J. W. Wang, “Calcium Imaging of Pheromone Responses in the Insect Antennal Lobe,” Methods Mol. Biol. 1068, 179–187 (2013).
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Nat. Biotechnol. (1)

J. Nakai, M. Ohkura, and K. Imoto, “A high signal-to-noise Ca(2+) probe composed of a single green fluorescent protein,” Nat. Biotechnol. 19(2), 137–141 (2001).
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Nat. Commun. (1)

K. Wang, W. Sun, C. T. Richie, B. K. Harvey, E. Betzig, and N. Ji, “Direct wavefront sensing for high-resolution in vivo imaging in scattering tissue,” Nat. Commun. 6, 7276 (2015).
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Nat. Methods (4)

F. Helmchen and W. Denk, “Deep tissue two-photon microscopy,” Nat. Methods 2(12), 932–940 (2005).
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N. Ji, D. E. Milkie, and E. Betzig, “Adaptive optics via pupil segmentation for high-resolution imaging in biological tissues,” Nat. Methods 7(2), 141–147 (2010).
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D. Grover, T. Katsuki, and R. J. Greenspan, “Flyception: imaging brain activity in freely walking fruit flies,” Nat. Methods 13(7), 569–572 (2016).
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C. I. Bargmann and E. Marder, “From the connectome to brain function,” Nat. Methods 10(6), 483–490 (2013).
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Nat. Photonics (1)

N. G. Horton, K. Wang, D. Kobat, C. G. Clark, F. W. Wise, C. B. Schaffer, and C. Xu, “In vivo three-photon microscopy of subcortical structures within an intact mouse brain,” Nat. Photonics 7(3), 205–209 (2013).
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Nat. Protoc. (1)

A. Kamikouchi, R. Wiek, T. Effertz, M. C. Göpfert, and A. Fiala, “Transcuticular optical imaging of stimulus-evoked neural activities in the Drosophila peripheral nervous system,” Nat. Protoc. 5(7), 1229–1235 (2010).
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M. B. Sokolowski, “Drosophila: Genetics meets behaviour,” Nat. Rev. Genet. 2(11), 879–890 (2001).
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Nature (4)

J. D. Seelig and V. Jayaraman, “Feature detection and orientation tuning in the Drosophila central complex,” Nature 503(7475), 262–266 (2013).
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G. S. Suh, A. M. Wong, A. C. Hergarden, J. W. Wang, A. F. Simon, S. Benzer, R. Axel, and D. J. Anderson, “A single population of olfactory sensory neurons mediates an innate avoidance behaviour in Drosophila,” Nature 431(7010), 854–859 (2004).
[Crossref] [PubMed]

T. W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
[Crossref] [PubMed]

T.-W. Chen, T. J. Wardill, Y. Sun, S. R. Pulver, S. L. Renninger, A. Baohan, E. R. Schreiter, R. A. Kerr, M. B. Orger, V. Jayaraman, L. L. Looger, K. Svoboda, and D. S. Kim, “Ultrasensitive fluorescent proteins for imaging neuronal activity,” Nature 499(7458), 295–300 (2013).
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Neuron (5)

M. J. McGinley, M. Vinck, J. Reimer, R. Batista-Brito, E. Zagha, C. R. Cadwell, A. S. Tolias, J. A. Cardin, and D. A. McCormick, “Waking State: Rapid Variations Modulate Neural and Behavioral Responses,” Neuron 87(6), 1143–1161 (2015).
[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]

H.-H. Lin, D.-S. Cao, S. Sethi, Z. Zeng, J. S. R. Chin, T. S. Chakraborty, A. K. Shepherd, C. A. Nguyen, J. Y. Yew, C.-Y. Su, and J. W. Wang, “Hormonal Modulation of Pheromone Detection Enhances Male Courtship Success,” Neuron 90(6), 1272–1285 (2016).
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M. Dus, J. S. Lai, K. M. Gunapala, S. Min, T. D. Tayler, A. C. Hergarden, E. Geraud, C. M. Joseph, and G. S. Suh, “Nutrient sensor in the brain directs the action of the brain-gut axis in Drosophila,” Neuron 87(1), 139–151 (2015).
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Opt. Express (5)

Opt. Lett. (3)

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

J. Tang, R. N. Germain, and M. Cui, “Superpenetration optical microscopy by iterative multiphoton adaptive compensation technique,” Proc. Natl. Acad. Sci. U.S.A. 109(22), 8434–8439 (2012).
[Crossref] [PubMed]

Science (2)

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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N. J. Strausfeld and F. Hirth, “Deep Homology of Arthropod Central Complex and Vertebrate Basal Ganglia,” Science 340(6129), 157–161 (2013).
[Crossref] [PubMed]

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J. A. Kubby, ed., Adaptive Optics for Biological Imaging (CRC Press, Taylor & Francis Group, 2013).

J. W. Hardy, Adaptive Optics for Astronomical Telescopes (Oxford University Press, 1998).

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Figures (8)

Fig. 1
Fig. 1 (a) System diagram and (b) setup of the 3P-AO add-on. L, lens; DM, deformable mirror; ST, shutter; ND, variable metallic neutral density filter; LPF, long pass filter; D1, dichroic mirror; PCR, photonic crystal rod.
Fig. 2
Fig. 2 Power spectrum and pulse width measurement of the 3P system. (a) The PCR shifts and broadens the spectrum of the fiber laser. The LPF blocks wavelengths shorter than 1580 nm. (b) Pulse width measured at the output port of the FLCPA, (c) after the PCR, and (d) after the objective lens. All pulse width measurements assume sech2-shaped pulses.
Fig. 3
Fig. 3 Flow chart for sensorless wavefront correction.
Fig. 4
Fig. 4 Logarithmic plots of intensity and excitation power at the objective indicating three-photon excitation. A first order polynomial fit is applied to a log-log plot of the data, as shown by the solid curves. The results for using heavy water (D2O) and regular water (H2O) as the immersion medium are indicted by blue and red data points, respectively.
Fig. 5
Fig. 5 3P-AO imaging of fluorescent microspheres. (a) Fluorescence intensity decreases as spherical aberration increases. Red line: cubic curve fitting. (b) Images of microspheres before and after AO correction, where the aberration was introduced by adjusting the correction collar of the objective lens. (c) The intensity profiles along the lines in (b). (d) The final phase on the DM. Scale bar, 5 µm.
Fig. 6
Fig. 6 Transcutical imaging of Drosophila brain structures. (a) External view of a fly head. Image source: www.sdbonline.org. The four boxes denote imaging regions. The viewing angle may be slightly different for each region. (b) Mushroom body Kenyon cells of a fly bearing the OK107-GAL4 and UAS-jRCaMP1b transgenes. (c) Axon terminals of second-order projection neurons in the lateral horn region. Transgenes: GH146-GAL4 and UAS-mCherry. (e) Cell bodies of the Or47b odorant receptor neurons. Transgenes: Or47b-GAL4 and UAS-mCherry. (b-e) Red color: fluorescence signals from the labeled neurons. Green color: third harmonic signal. Scale bar, 50 µm.
Fig. 7
Fig. 7 Odor-evoked activity in the fly mushroom body. (a) A fly is glued to a cover glass with light curable resin. (b) Fluorescence and third-harmonic signals at different depths from the fly cuticle. (c) Peak olfactory response of the fly mushroom body. Pseudocolor images show ∆F/F measurement. (d) ∆F/F is plotted against time. Odor: isoamyl acetate at 5% saturated vapor pressure. Fly: OK107-GAL4, UAS-jRCaMP1b. Scale bar, 50 µm.
Fig. 8
Fig. 8 Adaptive optics reveals fine neuronal structures. Axon terminals of the second-order olfactory projection neurons in the lateral horn regions are shown in a fly carrying the GH146-GAL4 and UAS-mCherry transgenes. Line profiles were plotted in the inset. Orange arrowheads: boutons of the projection neurons. Green arrowheads: branches of the projection neurons. Scale bar, 20 µm.

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