Abstract

Drosophila is widely used in connectome studies due to its small brain size, sophisticated genetic tools, and the most complete single-neuron-based anatomical brain map. Surprisingly, even the brain thickness is only 200-μm, common Ti:sapphire-based two-photon excitation cannot penetrate, possibly due to light aberration/scattering of trachea. Here we quantitatively characterized scattering and light distortion of trachea-filled tissues, and found that trachea-induced light distortion dominates at long wavelength by comparing one-photon (488-nm), two-photon (920-nm), and three-photon (1300-nm) excitations. Whole-Drosophila-brain imaging is achieved by reducing tracheal light aberration/scattering via brain-degassing or long-wavelength excitation at 1300-nm. Our work paves the way toward constructing whole-brain connectome in a living Drosophila.

© 2019 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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    [Crossref] [PubMed]
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    [Crossref]
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2018 (1)

Z. Zheng, J. S. Lauritzen, E. Perlman, C. G. Robinson, M. Nichols, D. Milkie, O. Torrens, J. Price, C. B. Fisher, N. Sharifi, S. A. Calle-Schuler, L. Kmecova, I. J. Ali, B. Karsh, E. T. Trautman, J. A. Bogovic, P. Hanslovsky, G. S. X. E. Jefferis, M. Kazhdan, K. Khairy, S. Saalfeld, R. D. Fetter, and D. D. Bock, “A complete electron microscopy volume of the brain of adult Drosophila melanogaster,” Cell 174(3), 730–743 (2018).
[Crossref] [PubMed]

2017 (3)

X. Tao, H.-H. Lin, T. Lam, R. Rodriguez, J. W. Wang, and J. Kubby, “Transcutical imaging with cellular and subcellular resolution,” Biomed. Opt. Express 8(3), 1277–1289 (2017).
[Crossref] [PubMed]

D. G. Ouzounov, T. Wang, M. Wang, D. D. Feng, N. G. Horton, J. C. Cruz-Hernández, Y.-T. Cheng, J. Reimer, A. S. Tolias, N. Nishimura, and C. Xu, “In vivo three-photon imaging of activity of GCaMP6-labeled neurons deep in intact mouse brain,” Nat. Methods 14(4), 388–390 (2017).
[Crossref] [PubMed]

K. Mann, C. L. Gallen, and T. R. Clandinin, “Whole-brain calcium imaging reveals an intrinsic functional network in Drosophila,” Curr. Biol. 27(15), 2389–2396 (2017).
[Crossref] [PubMed]

2016 (2)

C.-C. Lo and A.-S. Chiang, “Toward whole-body connectomics,” J. Neurosci. 36(45), 11375–11383 (2016).
[Crossref] [PubMed]

M. Pedrazzani, V. Loriette, P. Tchenio, S. Benrezzak, D. Nutarelli, and A. Fragola, “Sensorless adaptive optics implementation in widefield optical sectioning microscopy inside in vivo Drosophila brain,” J. Biomed. Opt. 21(3), 036006 (2016).
[Crossref] [PubMed]

2015 (3)

C.-W. Lin, H.-W. Lin, M.-T. Chiu, Y.-H. Shih, T.-Y. Wang, H.-M. Chang, and A.-S. Chiang, “Automated in situ brain imaging for mapping the Drosophila connectome,” J. Neurogenet. 29(4), 157–168 (2015).
[Crossref] [PubMed]

P. R. Rao, L. Lin, H. Huang, A. Guha, S. Roy, and T. B. Kornberg, “Developmental compartments in the larval trachea of Drosophila,” eLife 4, e08666 (2015).
[Crossref] [PubMed]

C.-T. Shih, O. Sporns, S.-L. Yuan, T.-S. Su, Y.-J. Lin, C.-C. Chuang, T.-Y. Wang, C.-C. Lo, R. J. Greenspan, and A. S. Chiang, “Connectomics-based analysis of information flow in the Drosophila brain,” Curr. Biol. 25(10), 1249–1258 (2015).
[Crossref] [PubMed]

2014 (2)

M. J. Booth, “Adaptive optical microscopy: the ongoing quest for a perfect image,” Light Sci. Appl. 3(4), e165 (2014).
[Crossref]

C. Wang, R. Liu, D. E. Milkie, W. Sun, Z. Tan, A. Kerlin, T.-W. Chen, D. S. Kim, and N. Ji, “Multiplexed aberration measurement for deep tissue imaging in vivo,” Nat. Methods 11(10), 1037–1040 (2014).
[Crossref] [PubMed]

2013 (2)

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]

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 (3)

N. Ji, T. R. Sato, and E. Betzig, “Characterization and adaptive optical correction of aberrations during in vivo imaging in the mouse cortex,” Proc. Natl. Acad. Sci. U.S.A. 109(1), 22–27 (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]

L. Wei, Z. Chen, and W. Min, “Stimulated emission reduced fluorescence microscopy: a concept for extending the fundamental depth limit of two-photon fluorescence imaging,” Biomed. Opt. Express 3(6), 1465–1475 (2012).
[Crossref] [PubMed]

2011 (4)

K. S. Honegger, R. A. A. Campbell, and G. C. Turner, “Cellular-resolution population imaging reveals robust sparse coding in the Drosophila mushroom body,” J. Neurosci. 31(33), 11772–11785 (2011).
[Crossref] [PubMed]

A.-S. Chiang, C.-Y. Lin, C.-C. Chuang, H.-M. Chang, C.-H. Hsieh, C.-W. Yeh, C.-T. Shih, J.-J. Wu, G.-T. Wang, Y.-C. Chen, C.-C. Wu, G.-Y. Chen, Y.-T. Ching, P.-C. Lee, C.-Y. Lin, H.-H. Lin, C.-C. Wu, H.-W. Hsu, Y.-A. Huang, J.-Y. Chen, H.-J. Chiang, C.-F. Lu, R.-F. Ni, C.-Y. Yeh, and J.-K. Hwang, “Three-dimensional reconstruction of brain-wide wiring networks in Drosophila at single-cell resolution,” Curr. Biol. 21(1), 1–11 (2011).
[Crossref] [PubMed]

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

E. Chaigneau, A. J. Wright, S. P. Poland, J. M. Girkin, and R. A. Silver, “Impact of wavefront distortion and scattering on 2-photon microscopy in mammalian brain tissue,” Opt. Express 19(23), 22755–22774 (2011).
[Crossref] [PubMed]

2010 (1)

V. Ruta, S. R. Datta, M. L. Vasconcelos, J. Freeland, L. L. Looger, and R. Axel, “A dimorphic pheromone circuit in Drosophila from sensory input to descending output,” Nature 468(7324), 686–690 (2010).
[Crossref] [PubMed]

2009 (3)

R. Ignell, C. M. Root, R. T. Birse, J. W. Wang, D. R. Nässel, and Å. M. E. Winther, “Presynaptic peptidergic modulation of olfactory receptor neurons in Drosophila,” Proc. Natl. Acad. Sci. U.S.A. 106(31), 13070–13075 (2009).
[Crossref] [PubMed]

J. C. Tuthill, “Lessons from a compartmental model of a Drosophila neuron,” J. Neurosci. 29(39), 12033–12034 (2009).
[Crossref] [PubMed]

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]

2007 (1)

C. M. Root, J. L. Semmelhack, A. M. Wong, J. Flores, and J. W. Wang, “Propagation of olfactory information in Drosophila,” Proc. Natl. Acad. Sci. U.S.A. 104(28), 11826–11831 (2007).
[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)

Y. Wang, H. F. Guo, T. A. Pologruto, F. Hannan, I. Hakker, K. Svoboda, and Y. Zhong, “Stereotyped odor-evoked activity in the mushroom body of Drosophila revealed by green fluorescent protein-based Ca2+ imaging,” J. Neurosci. 24(29), 6507–6514 (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. 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]

C.-Y. Dong, K. Koenig, and P. So, “Characterizing point spread functions of two-photon fluorescence microscopy in turbid medium,” J. Biomed. Opt. 8(3), 450–459 (2003).
[Crossref] [PubMed]

S.-W. Chu, S.-Y. Chen, T.-H. Tsai, T.-M. Liu, C.-Y. Lin, H.-J. Tsai, and C.-K. Sun, “In vivo developmental biology study using noninvasive multi-harmonic generation microscopy,” Opt. Express 11(23), 3093–3099 (2003).
[Crossref] [PubMed]

2002 (1)

I. H. Chen, S. W. Chu, C. K. Sun, P. C. Cheng, and B. L. Lin, “Wavelength dependent damage in biological multi-photon confocal microscopy: A micro-spectroscopic comparison between femtosecond Ti:sapphire and Cr:forsterite laser sources,” Opt. Quantum Electron. 34(12), 1251–1266 (2002).
[Crossref]

2000 (1)

G. J. Beitel and M. A. Krasnow, “Genetic control of epithelial tube size in the Drosophila tracheal system,” Development 127(15), 3271–3282 (2000).
[PubMed]

Ali, I. J.

Z. Zheng, J. S. Lauritzen, E. Perlman, C. G. Robinson, M. Nichols, D. Milkie, O. Torrens, J. Price, C. B. Fisher, N. Sharifi, S. A. Calle-Schuler, L. Kmecova, I. J. Ali, B. Karsh, E. T. Trautman, J. A. Bogovic, P. Hanslovsky, G. S. X. E. Jefferis, M. Kazhdan, K. Khairy, S. Saalfeld, R. D. Fetter, and D. D. Bock, “A complete electron microscopy volume of the brain of adult Drosophila melanogaster,” Cell 174(3), 730–743 (2018).
[Crossref] [PubMed]

Axel, R.

V. Ruta, S. R. Datta, M. L. Vasconcelos, J. Freeland, L. L. Looger, and R. Axel, “A dimorphic pheromone circuit in Drosophila from sensory input to descending output,” Nature 468(7324), 686–690 (2010).
[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]

Beitel, G. J.

G. J. Beitel and M. A. Krasnow, “Genetic control of epithelial tube size in the Drosophila tracheal system,” Development 127(15), 3271–3282 (2000).
[PubMed]

Benrezzak, S.

M. Pedrazzani, V. Loriette, P. Tchenio, S. Benrezzak, D. Nutarelli, and A. Fragola, “Sensorless adaptive optics implementation in widefield optical sectioning microscopy inside in vivo Drosophila brain,” J. Biomed. Opt. 21(3), 036006 (2016).
[Crossref] [PubMed]

Betzig, E.

N. Ji, T. R. Sato, and E. Betzig, “Characterization and adaptive optical correction of aberrations during in vivo imaging in the mouse cortex,” Proc. Natl. Acad. Sci. U.S.A. 109(1), 22–27 (2012).
[Crossref] [PubMed]

Birse, R. T.

R. Ignell, C. M. Root, R. T. Birse, J. W. Wang, D. R. Nässel, and Å. M. E. Winther, “Presynaptic peptidergic modulation of olfactory receptor neurons in Drosophila,” Proc. Natl. Acad. Sci. U.S.A. 106(31), 13070–13075 (2009).
[Crossref] [PubMed]

Bock, D. D.

Z. Zheng, J. S. Lauritzen, E. Perlman, C. G. Robinson, M. Nichols, D. Milkie, O. Torrens, J. Price, C. B. Fisher, N. Sharifi, S. A. Calle-Schuler, L. Kmecova, I. J. Ali, B. Karsh, E. T. Trautman, J. A. Bogovic, P. Hanslovsky, G. S. X. E. Jefferis, M. Kazhdan, K. Khairy, S. Saalfeld, R. D. Fetter, and D. D. Bock, “A complete electron microscopy volume of the brain of adult Drosophila melanogaster,” Cell 174(3), 730–743 (2018).
[Crossref] [PubMed]

Bogovic, J. A.

Z. Zheng, J. S. Lauritzen, E. Perlman, C. G. Robinson, M. Nichols, D. Milkie, O. Torrens, J. Price, C. B. Fisher, N. Sharifi, S. A. Calle-Schuler, L. Kmecova, I. J. Ali, B. Karsh, E. T. Trautman, J. A. Bogovic, P. Hanslovsky, G. S. X. E. Jefferis, M. Kazhdan, K. Khairy, S. Saalfeld, R. D. Fetter, and D. D. Bock, “A complete electron microscopy volume of the brain of adult Drosophila melanogaster,” Cell 174(3), 730–743 (2018).
[Crossref] [PubMed]

Booth, M. J.

M. J. Booth, “Adaptive optical microscopy: the ongoing quest for a perfect image,” Light Sci. Appl. 3(4), e165 (2014).
[Crossref]

Calle-Schuler, S. A.

Z. Zheng, J. S. Lauritzen, E. Perlman, C. G. Robinson, M. Nichols, D. Milkie, O. Torrens, J. Price, C. B. Fisher, N. Sharifi, S. A. Calle-Schuler, L. Kmecova, I. J. Ali, B. Karsh, E. T. Trautman, J. A. Bogovic, P. Hanslovsky, G. S. X. E. Jefferis, M. Kazhdan, K. Khairy, S. Saalfeld, R. D. Fetter, and D. D. Bock, “A complete electron microscopy volume of the brain of adult Drosophila melanogaster,” Cell 174(3), 730–743 (2018).
[Crossref] [PubMed]

Campbell, R. A. A.

K. S. Honegger, R. A. A. Campbell, and G. C. Turner, “Cellular-resolution population imaging reveals robust sparse coding in the Drosophila mushroom body,” J. Neurosci. 31(33), 11772–11785 (2011).
[Crossref] [PubMed]

Chaigneau, E.

Chang, H.-M.

C.-W. Lin, H.-W. Lin, M.-T. Chiu, Y.-H. Shih, T.-Y. Wang, H.-M. Chang, and A.-S. Chiang, “Automated in situ brain imaging for mapping the Drosophila connectome,” J. Neurogenet. 29(4), 157–168 (2015).
[Crossref] [PubMed]

A.-S. Chiang, C.-Y. Lin, C.-C. Chuang, H.-M. Chang, C.-H. Hsieh, C.-W. Yeh, C.-T. Shih, J.-J. Wu, G.-T. Wang, Y.-C. Chen, C.-C. Wu, G.-Y. Chen, Y.-T. Ching, P.-C. Lee, C.-Y. Lin, H.-H. Lin, C.-C. Wu, H.-W. Hsu, Y.-A. Huang, J.-Y. Chen, H.-J. Chiang, C.-F. Lu, R.-F. Ni, C.-Y. Yeh, and J.-K. Hwang, “Three-dimensional reconstruction of brain-wide wiring networks in Drosophila at single-cell resolution,” Curr. Biol. 21(1), 1–11 (2011).
[Crossref] [PubMed]

Chen, G.-Y.

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K. Mann, C. L. Gallen, and T. R. Clandinin, “Whole-brain calcium imaging reveals an intrinsic functional network in Drosophila,” Curr. Biol. 27(15), 2389–2396 (2017).
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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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D. Kobat, N. G. Horton, and C. Xu, “In vivo two-photon microscopy to 1.6-mm depth in mouse cortex,” J. Biomed. Opt. 16(10), 106014 (2011).
[Crossref] [PubMed]

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]

Koenig, K.

C.-Y. Dong, K. Koenig, and P. So, “Characterizing point spread functions of two-photon fluorescence microscopy in turbid medium,” J. Biomed. Opt. 8(3), 450–459 (2003).
[Crossref] [PubMed]

Kornberg, T. B.

P. R. Rao, L. Lin, H. Huang, A. Guha, S. Roy, and T. B. Kornberg, “Developmental compartments in the larval trachea of Drosophila,” eLife 4, e08666 (2015).
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Krasnow, M. A.

G. J. Beitel and M. A. Krasnow, “Genetic control of epithelial tube size in the Drosophila tracheal system,” Development 127(15), 3271–3282 (2000).
[PubMed]

Kubby, J.

Lam, T.

Lauritzen, J. S.

Z. Zheng, J. S. Lauritzen, E. Perlman, C. G. Robinson, M. Nichols, D. Milkie, O. Torrens, J. Price, C. B. Fisher, N. Sharifi, S. A. Calle-Schuler, L. Kmecova, I. J. Ali, B. Karsh, E. T. Trautman, J. A. Bogovic, P. Hanslovsky, G. S. X. E. Jefferis, M. Kazhdan, K. Khairy, S. Saalfeld, R. D. Fetter, and D. D. Bock, “A complete electron microscopy volume of the brain of adult Drosophila melanogaster,” Cell 174(3), 730–743 (2018).
[Crossref] [PubMed]

Lee, P.-C.

A.-S. Chiang, C.-Y. Lin, C.-C. Chuang, H.-M. Chang, C.-H. Hsieh, C.-W. Yeh, C.-T. Shih, J.-J. Wu, G.-T. Wang, Y.-C. Chen, C.-C. Wu, G.-Y. Chen, Y.-T. Ching, P.-C. Lee, C.-Y. Lin, H.-H. Lin, C.-C. Wu, H.-W. Hsu, Y.-A. Huang, J.-Y. Chen, H.-J. Chiang, C.-F. Lu, R.-F. Ni, C.-Y. Yeh, and J.-K. Hwang, “Three-dimensional reconstruction of brain-wide wiring networks in Drosophila at single-cell resolution,” Curr. Biol. 21(1), 1–11 (2011).
[Crossref] [PubMed]

Lin, B. L.

I. H. Chen, S. W. Chu, C. K. Sun, P. C. Cheng, and B. L. Lin, “Wavelength dependent damage in biological multi-photon confocal microscopy: A micro-spectroscopic comparison between femtosecond Ti:sapphire and Cr:forsterite laser sources,” Opt. Quantum Electron. 34(12), 1251–1266 (2002).
[Crossref]

Lin, C.-W.

C.-W. Lin, H.-W. Lin, M.-T. Chiu, Y.-H. Shih, T.-Y. Wang, H.-M. Chang, and A.-S. Chiang, “Automated in situ brain imaging for mapping the Drosophila connectome,” J. Neurogenet. 29(4), 157–168 (2015).
[Crossref] [PubMed]

Lin, C.-Y.

A.-S. Chiang, C.-Y. Lin, C.-C. Chuang, H.-M. Chang, C.-H. Hsieh, C.-W. Yeh, C.-T. Shih, J.-J. Wu, G.-T. Wang, Y.-C. Chen, C.-C. Wu, G.-Y. Chen, Y.-T. Ching, P.-C. Lee, C.-Y. Lin, H.-H. Lin, C.-C. Wu, H.-W. Hsu, Y.-A. Huang, J.-Y. Chen, H.-J. Chiang, C.-F. Lu, R.-F. Ni, C.-Y. Yeh, and J.-K. Hwang, “Three-dimensional reconstruction of brain-wide wiring networks in Drosophila at single-cell resolution,” Curr. Biol. 21(1), 1–11 (2011).
[Crossref] [PubMed]

A.-S. Chiang, C.-Y. Lin, C.-C. Chuang, H.-M. Chang, C.-H. Hsieh, C.-W. Yeh, C.-T. Shih, J.-J. Wu, G.-T. Wang, Y.-C. Chen, C.-C. Wu, G.-Y. Chen, Y.-T. Ching, P.-C. Lee, C.-Y. Lin, H.-H. Lin, C.-C. Wu, H.-W. Hsu, Y.-A. Huang, J.-Y. Chen, H.-J. Chiang, C.-F. Lu, R.-F. Ni, C.-Y. Yeh, and J.-K. Hwang, “Three-dimensional reconstruction of brain-wide wiring networks in Drosophila at single-cell resolution,” Curr. Biol. 21(1), 1–11 (2011).
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S.-W. Chu, S.-Y. Chen, T.-H. Tsai, T.-M. Liu, C.-Y. Lin, H.-J. Tsai, and C.-K. Sun, “In vivo developmental biology study using noninvasive multi-harmonic generation microscopy,” Opt. Express 11(23), 3093–3099 (2003).
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Lin, H.-H.

X. Tao, H.-H. Lin, T. Lam, R. Rodriguez, J. W. Wang, and J. Kubby, “Transcutical imaging with cellular and subcellular resolution,” Biomed. Opt. Express 8(3), 1277–1289 (2017).
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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).
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A.-S. Chiang, C.-Y. Lin, C.-C. Chuang, H.-M. Chang, C.-H. Hsieh, C.-W. Yeh, C.-T. Shih, J.-J. Wu, G.-T. Wang, Y.-C. Chen, C.-C. Wu, G.-Y. Chen, Y.-T. Ching, P.-C. Lee, C.-Y. Lin, H.-H. Lin, C.-C. Wu, H.-W. Hsu, Y.-A. Huang, J.-Y. Chen, H.-J. Chiang, C.-F. Lu, R.-F. Ni, C.-Y. Yeh, and J.-K. Hwang, “Three-dimensional reconstruction of brain-wide wiring networks in Drosophila at single-cell resolution,” Curr. Biol. 21(1), 1–11 (2011).
[Crossref] [PubMed]

Lin, H.-W.

C.-W. Lin, H.-W. Lin, M.-T. Chiu, Y.-H. Shih, T.-Y. Wang, H.-M. Chang, and A.-S. Chiang, “Automated in situ brain imaging for mapping the Drosophila connectome,” J. Neurogenet. 29(4), 157–168 (2015).
[Crossref] [PubMed]

Lin, L.

P. R. Rao, L. Lin, H. Huang, A. Guha, S. Roy, and T. B. Kornberg, “Developmental compartments in the larval trachea of Drosophila,” eLife 4, e08666 (2015).
[Crossref] [PubMed]

Lin, Y.-J.

C.-T. Shih, O. Sporns, S.-L. Yuan, T.-S. Su, Y.-J. Lin, C.-C. Chuang, T.-Y. Wang, C.-C. Lo, R. J. Greenspan, and A. S. Chiang, “Connectomics-based analysis of information flow in the Drosophila brain,” Curr. Biol. 25(10), 1249–1258 (2015).
[Crossref] [PubMed]

Liu, R.

C. Wang, R. Liu, D. E. Milkie, W. Sun, Z. Tan, A. Kerlin, T.-W. Chen, D. S. Kim, and N. Ji, “Multiplexed aberration measurement for deep tissue imaging in vivo,” Nat. Methods 11(10), 1037–1040 (2014).
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Liu, T.-M.

Lo, C.-C.

C.-C. Lo and A.-S. Chiang, “Toward whole-body connectomics,” J. Neurosci. 36(45), 11375–11383 (2016).
[Crossref] [PubMed]

C.-T. Shih, O. Sporns, S.-L. Yuan, T.-S. Su, Y.-J. Lin, C.-C. Chuang, T.-Y. Wang, C.-C. Lo, R. J. Greenspan, and A. S. Chiang, “Connectomics-based analysis of information flow in the Drosophila brain,” Curr. Biol. 25(10), 1249–1258 (2015).
[Crossref] [PubMed]

Looger, L. L.

V. Ruta, S. R. Datta, M. L. Vasconcelos, J. Freeland, L. L. Looger, and R. Axel, “A dimorphic pheromone circuit in Drosophila from sensory input to descending output,” Nature 468(7324), 686–690 (2010).
[Crossref] [PubMed]

Loriette, V.

M. Pedrazzani, V. Loriette, P. Tchenio, S. Benrezzak, D. Nutarelli, and A. Fragola, “Sensorless adaptive optics implementation in widefield optical sectioning microscopy inside in vivo Drosophila brain,” J. Biomed. Opt. 21(3), 036006 (2016).
[Crossref] [PubMed]

Lu, C.-F.

A.-S. Chiang, C.-Y. Lin, C.-C. Chuang, H.-M. Chang, C.-H. Hsieh, C.-W. Yeh, C.-T. Shih, J.-J. Wu, G.-T. Wang, Y.-C. Chen, C.-C. Wu, G.-Y. Chen, Y.-T. Ching, P.-C. Lee, C.-Y. Lin, H.-H. Lin, C.-C. Wu, H.-W. Hsu, Y.-A. Huang, J.-Y. Chen, H.-J. Chiang, C.-F. Lu, R.-F. Ni, C.-Y. Yeh, and J.-K. Hwang, “Three-dimensional reconstruction of brain-wide wiring networks in Drosophila at single-cell resolution,” Curr. Biol. 21(1), 1–11 (2011).
[Crossref] [PubMed]

Mann, K.

K. Mann, C. L. Gallen, and T. R. Clandinin, “Whole-brain calcium imaging reveals an intrinsic functional network in Drosophila,” Curr. Biol. 27(15), 2389–2396 (2017).
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Milkie, D.

Z. Zheng, J. S. Lauritzen, E. Perlman, C. G. Robinson, M. Nichols, D. Milkie, O. Torrens, J. Price, C. B. Fisher, N. Sharifi, S. A. Calle-Schuler, L. Kmecova, I. J. Ali, B. Karsh, E. T. Trautman, J. A. Bogovic, P. Hanslovsky, G. S. X. E. Jefferis, M. Kazhdan, K. Khairy, S. Saalfeld, R. D. Fetter, and D. D. Bock, “A complete electron microscopy volume of the brain of adult Drosophila melanogaster,” Cell 174(3), 730–743 (2018).
[Crossref] [PubMed]

Milkie, D. E.

C. Wang, R. Liu, D. E. Milkie, W. Sun, Z. Tan, A. Kerlin, T.-W. Chen, D. S. Kim, and N. Ji, “Multiplexed aberration measurement for deep tissue imaging in vivo,” Nat. Methods 11(10), 1037–1040 (2014).
[Crossref] [PubMed]

Min, W.

Nässel, D. R.

R. Ignell, C. M. Root, R. T. Birse, J. W. Wang, D. R. Nässel, and Å. M. E. Winther, “Presynaptic peptidergic modulation of olfactory receptor neurons in Drosophila,” Proc. Natl. Acad. Sci. U.S.A. 106(31), 13070–13075 (2009).
[Crossref] [PubMed]

Ni, R.-F.

A.-S. Chiang, C.-Y. Lin, C.-C. Chuang, H.-M. Chang, C.-H. Hsieh, C.-W. Yeh, C.-T. Shih, J.-J. Wu, G.-T. Wang, Y.-C. Chen, C.-C. Wu, G.-Y. Chen, Y.-T. Ching, P.-C. Lee, C.-Y. Lin, H.-H. Lin, C.-C. Wu, H.-W. Hsu, Y.-A. Huang, J.-Y. Chen, H.-J. Chiang, C.-F. Lu, R.-F. Ni, C.-Y. Yeh, and J.-K. Hwang, “Three-dimensional reconstruction of brain-wide wiring networks in Drosophila at single-cell resolution,” Curr. Biol. 21(1), 1–11 (2011).
[Crossref] [PubMed]

Nichols, M.

Z. Zheng, J. S. Lauritzen, E. Perlman, C. G. Robinson, M. Nichols, D. Milkie, O. Torrens, J. Price, C. B. Fisher, N. Sharifi, S. A. Calle-Schuler, L. Kmecova, I. J. Ali, B. Karsh, E. T. Trautman, J. A. Bogovic, P. Hanslovsky, G. S. X. E. Jefferis, M. Kazhdan, K. Khairy, S. Saalfeld, R. D. Fetter, and D. D. Bock, “A complete electron microscopy volume of the brain of adult Drosophila melanogaster,” Cell 174(3), 730–743 (2018).
[Crossref] [PubMed]

Nishimura, N.

D. G. Ouzounov, T. Wang, M. Wang, D. D. Feng, N. G. Horton, J. C. Cruz-Hernández, Y.-T. Cheng, J. Reimer, A. S. Tolias, N. Nishimura, and C. Xu, “In vivo three-photon imaging of activity of GCaMP6-labeled neurons deep in intact mouse brain,” Nat. Methods 14(4), 388–390 (2017).
[Crossref] [PubMed]

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]

Nutarelli, D.

M. Pedrazzani, V. Loriette, P. Tchenio, S. Benrezzak, D. Nutarelli, and A. Fragola, “Sensorless adaptive optics implementation in widefield optical sectioning microscopy inside in vivo Drosophila brain,” J. Biomed. Opt. 21(3), 036006 (2016).
[Crossref] [PubMed]

Ouzounov, D. G.

D. G. Ouzounov, T. Wang, M. Wang, D. D. Feng, N. G. Horton, J. C. Cruz-Hernández, Y.-T. Cheng, J. Reimer, A. S. Tolias, N. Nishimura, and C. Xu, “In vivo three-photon imaging of activity of GCaMP6-labeled neurons deep in intact mouse brain,” Nat. Methods 14(4), 388–390 (2017).
[Crossref] [PubMed]

Pedrazzani, M.

M. Pedrazzani, V. Loriette, P. Tchenio, S. Benrezzak, D. Nutarelli, and A. Fragola, “Sensorless adaptive optics implementation in widefield optical sectioning microscopy inside in vivo Drosophila brain,” J. Biomed. Opt. 21(3), 036006 (2016).
[Crossref] [PubMed]

Perlman, E.

Z. Zheng, J. S. Lauritzen, E. Perlman, C. G. Robinson, M. Nichols, D. Milkie, O. Torrens, J. Price, C. B. Fisher, N. Sharifi, S. A. Calle-Schuler, L. Kmecova, I. J. Ali, B. Karsh, E. T. Trautman, J. A. Bogovic, P. Hanslovsky, G. S. X. E. Jefferis, M. Kazhdan, K. Khairy, S. Saalfeld, R. D. Fetter, and D. D. Bock, “A complete electron microscopy volume of the brain of adult Drosophila melanogaster,” Cell 174(3), 730–743 (2018).
[Crossref] [PubMed]

Poland, S. P.

Pologruto, T. A.

Y. Wang, H. F. Guo, T. A. Pologruto, F. Hannan, I. Hakker, K. Svoboda, and Y. Zhong, “Stereotyped odor-evoked activity in the mushroom body of Drosophila revealed by green fluorescent protein-based Ca2+ imaging,” J. Neurosci. 24(29), 6507–6514 (2004).
[Crossref] [PubMed]

Price, J.

Z. Zheng, J. S. Lauritzen, E. Perlman, C. G. Robinson, M. Nichols, D. Milkie, O. Torrens, J. Price, C. B. Fisher, N. Sharifi, S. A. Calle-Schuler, L. Kmecova, I. J. Ali, B. Karsh, E. T. Trautman, J. A. Bogovic, P. Hanslovsky, G. S. X. E. Jefferis, M. Kazhdan, K. Khairy, S. Saalfeld, R. D. Fetter, and D. D. Bock, “A complete electron microscopy volume of the brain of adult Drosophila melanogaster,” Cell 174(3), 730–743 (2018).
[Crossref] [PubMed]

Rao, P. R.

P. R. Rao, L. Lin, H. Huang, A. Guha, S. Roy, and T. B. Kornberg, “Developmental compartments in the larval trachea of Drosophila,” eLife 4, e08666 (2015).
[Crossref] [PubMed]

Reimer, J.

D. G. Ouzounov, T. Wang, M. Wang, D. D. Feng, N. G. Horton, J. C. Cruz-Hernández, Y.-T. Cheng, J. Reimer, A. S. Tolias, N. Nishimura, and C. Xu, “In vivo three-photon imaging of activity of GCaMP6-labeled neurons deep in intact mouse brain,” Nat. Methods 14(4), 388–390 (2017).
[Crossref] [PubMed]

Robinson, C. G.

Z. Zheng, J. S. Lauritzen, E. Perlman, C. G. Robinson, M. Nichols, D. Milkie, O. Torrens, J. Price, C. B. Fisher, N. Sharifi, S. A. Calle-Schuler, L. Kmecova, I. J. Ali, B. Karsh, E. T. Trautman, J. A. Bogovic, P. Hanslovsky, G. S. X. E. Jefferis, M. Kazhdan, K. Khairy, S. Saalfeld, R. D. Fetter, and D. D. Bock, “A complete electron microscopy volume of the brain of adult Drosophila melanogaster,” Cell 174(3), 730–743 (2018).
[Crossref] [PubMed]

Rodriguez, R.

Root, C. M.

R. Ignell, C. M. Root, R. T. Birse, J. W. Wang, D. R. Nässel, and Å. M. E. Winther, “Presynaptic peptidergic modulation of olfactory receptor neurons in Drosophila,” Proc. Natl. Acad. Sci. U.S.A. 106(31), 13070–13075 (2009).
[Crossref] [PubMed]

C. M. Root, J. L. Semmelhack, A. M. Wong, J. Flores, and J. W. Wang, “Propagation of olfactory information in Drosophila,” Proc. Natl. Acad. Sci. U.S.A. 104(28), 11826–11831 (2007).
[Crossref] [PubMed]

Roy, S.

P. R. Rao, L. Lin, H. Huang, A. Guha, S. Roy, and T. B. Kornberg, “Developmental compartments in the larval trachea of Drosophila,” eLife 4, e08666 (2015).
[Crossref] [PubMed]

Ruta, V.

V. Ruta, S. R. Datta, M. L. Vasconcelos, J. Freeland, L. L. Looger, and R. Axel, “A dimorphic pheromone circuit in Drosophila from sensory input to descending output,” Nature 468(7324), 686–690 (2010).
[Crossref] [PubMed]

Saalfeld, S.

Z. Zheng, J. S. Lauritzen, E. Perlman, C. G. Robinson, M. Nichols, D. Milkie, O. Torrens, J. Price, C. B. Fisher, N. Sharifi, S. A. Calle-Schuler, L. Kmecova, I. J. Ali, B. Karsh, E. T. Trautman, J. A. Bogovic, P. Hanslovsky, G. S. X. E. Jefferis, M. Kazhdan, K. Khairy, S. Saalfeld, R. D. Fetter, and D. D. Bock, “A complete electron microscopy volume of the brain of adult Drosophila melanogaster,” Cell 174(3), 730–743 (2018).
[Crossref] [PubMed]

Sato, T. R.

N. Ji, T. R. Sato, and E. Betzig, “Characterization and adaptive optical correction of aberrations during in vivo imaging in the mouse cortex,” Proc. Natl. Acad. Sci. U.S.A. 109(1), 22–27 (2012).
[Crossref] [PubMed]

Schaffer, C. B.

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]

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]

Semmelhack, J. L.

C. M. Root, J. L. Semmelhack, A. M. Wong, J. Flores, and J. W. Wang, “Propagation of olfactory information in Drosophila,” Proc. Natl. Acad. Sci. U.S.A. 104(28), 11826–11831 (2007).
[Crossref] [PubMed]

Sharifi, N.

Z. Zheng, J. S. Lauritzen, E. Perlman, C. G. Robinson, M. Nichols, D. Milkie, O. Torrens, J. Price, C. B. Fisher, N. Sharifi, S. A. Calle-Schuler, L. Kmecova, I. J. Ali, B. Karsh, E. T. Trautman, J. A. Bogovic, P. Hanslovsky, G. S. X. E. Jefferis, M. Kazhdan, K. Khairy, S. Saalfeld, R. D. Fetter, and D. D. Bock, “A complete electron microscopy volume of the brain of adult Drosophila melanogaster,” Cell 174(3), 730–743 (2018).
[Crossref] [PubMed]

Shih, C.-T.

C.-T. Shih, O. Sporns, S.-L. Yuan, T.-S. Su, Y.-J. Lin, C.-C. Chuang, T.-Y. Wang, C.-C. Lo, R. J. Greenspan, and A. S. Chiang, “Connectomics-based analysis of information flow in the Drosophila brain,” Curr. Biol. 25(10), 1249–1258 (2015).
[Crossref] [PubMed]

A.-S. Chiang, C.-Y. Lin, C.-C. Chuang, H.-M. Chang, C.-H. Hsieh, C.-W. Yeh, C.-T. Shih, J.-J. Wu, G.-T. Wang, Y.-C. Chen, C.-C. Wu, G.-Y. Chen, Y.-T. Ching, P.-C. Lee, C.-Y. Lin, H.-H. Lin, C.-C. Wu, H.-W. Hsu, Y.-A. Huang, J.-Y. Chen, H.-J. Chiang, C.-F. Lu, R.-F. Ni, C.-Y. Yeh, and J.-K. Hwang, “Three-dimensional reconstruction of brain-wide wiring networks in Drosophila at single-cell resolution,” Curr. Biol. 21(1), 1–11 (2011).
[Crossref] [PubMed]

Shih, Y.-H.

C.-W. Lin, H.-W. Lin, M.-T. Chiu, Y.-H. Shih, T.-Y. Wang, H.-M. Chang, and A.-S. Chiang, “Automated in situ brain imaging for mapping the Drosophila connectome,” J. Neurogenet. 29(4), 157–168 (2015).
[Crossref] [PubMed]

Silver, R. A.

So, P.

C.-Y. Dong, K. Koenig, and P. So, “Characterizing point spread functions of two-photon fluorescence microscopy in turbid medium,” J. Biomed. Opt. 8(3), 450–459 (2003).
[Crossref] [PubMed]

Sporns, O.

C.-T. Shih, O. Sporns, S.-L. Yuan, T.-S. Su, Y.-J. Lin, C.-C. Chuang, T.-Y. Wang, C.-C. Lo, R. J. Greenspan, and A. S. Chiang, “Connectomics-based analysis of information flow in the Drosophila brain,” Curr. Biol. 25(10), 1249–1258 (2015).
[Crossref] [PubMed]

Su, T.-S.

C.-T. Shih, O. Sporns, S.-L. Yuan, T.-S. Su, Y.-J. Lin, C.-C. Chuang, T.-Y. Wang, C.-C. Lo, R. J. Greenspan, and A. S. Chiang, “Connectomics-based analysis of information flow in the Drosophila brain,” Curr. Biol. 25(10), 1249–1258 (2015).
[Crossref] [PubMed]

Sun, C. K.

I. H. Chen, S. W. Chu, C. K. Sun, P. C. Cheng, and B. L. Lin, “Wavelength dependent damage in biological multi-photon confocal microscopy: A micro-spectroscopic comparison between femtosecond Ti:sapphire and Cr:forsterite laser sources,” Opt. Quantum Electron. 34(12), 1251–1266 (2002).
[Crossref]

Sun, C.-K.

Sun, W.

C. Wang, R. Liu, D. E. Milkie, W. Sun, Z. Tan, A. Kerlin, T.-W. Chen, D. S. Kim, and N. Ji, “Multiplexed aberration measurement for deep tissue imaging in vivo,” Nat. Methods 11(10), 1037–1040 (2014).
[Crossref] [PubMed]

Svoboda, K.

Y. Wang, H. F. Guo, T. A. Pologruto, F. Hannan, I. Hakker, K. Svoboda, and Y. Zhong, “Stereotyped odor-evoked activity in the mushroom body of Drosophila revealed by green fluorescent protein-based Ca2+ imaging,” J. Neurosci. 24(29), 6507–6514 (2004).
[Crossref] [PubMed]

Tan, Z.

C. Wang, R. Liu, D. E. Milkie, W. Sun, Z. Tan, A. Kerlin, T.-W. Chen, D. S. Kim, and N. Ji, “Multiplexed aberration measurement for deep tissue imaging in vivo,” Nat. Methods 11(10), 1037–1040 (2014).
[Crossref] [PubMed]

Tang, J.

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]

Tao, X.

Tchenio, P.

M. Pedrazzani, V. Loriette, P. Tchenio, S. Benrezzak, D. Nutarelli, and A. Fragola, “Sensorless adaptive optics implementation in widefield optical sectioning microscopy inside in vivo Drosophila brain,” J. Biomed. Opt. 21(3), 036006 (2016).
[Crossref] [PubMed]

Theer, P.

Tolias, A. S.

D. G. Ouzounov, T. Wang, M. Wang, D. D. Feng, N. G. Horton, J. C. Cruz-Hernández, Y.-T. Cheng, J. Reimer, A. S. Tolias, N. Nishimura, and C. Xu, “In vivo three-photon imaging of activity of GCaMP6-labeled neurons deep in intact mouse brain,” Nat. Methods 14(4), 388–390 (2017).
[Crossref] [PubMed]

Torrens, O.

Z. Zheng, J. S. Lauritzen, E. Perlman, C. G. Robinson, M. Nichols, D. Milkie, O. Torrens, J. Price, C. B. Fisher, N. Sharifi, S. A. Calle-Schuler, L. Kmecova, I. J. Ali, B. Karsh, E. T. Trautman, J. A. Bogovic, P. Hanslovsky, G. S. X. E. Jefferis, M. Kazhdan, K. Khairy, S. Saalfeld, R. D. Fetter, and D. D. Bock, “A complete electron microscopy volume of the brain of adult Drosophila melanogaster,” Cell 174(3), 730–743 (2018).
[Crossref] [PubMed]

Trautman, E. T.

Z. Zheng, J. S. Lauritzen, E. Perlman, C. G. Robinson, M. Nichols, D. Milkie, O. Torrens, J. Price, C. B. Fisher, N. Sharifi, S. A. Calle-Schuler, L. Kmecova, I. J. Ali, B. Karsh, E. T. Trautman, J. A. Bogovic, P. Hanslovsky, G. S. X. E. Jefferis, M. Kazhdan, K. Khairy, S. Saalfeld, R. D. Fetter, and D. D. Bock, “A complete electron microscopy volume of the brain of adult Drosophila melanogaster,” Cell 174(3), 730–743 (2018).
[Crossref] [PubMed]

Tsai, H.-J.

Tsai, T.-H.

Turner, G. C.

K. S. Honegger, R. A. A. Campbell, and G. C. Turner, “Cellular-resolution population imaging reveals robust sparse coding in the Drosophila mushroom body,” J. Neurosci. 31(33), 11772–11785 (2011).
[Crossref] [PubMed]

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J. C. Tuthill, “Lessons from a compartmental model of a Drosophila neuron,” J. Neurosci. 29(39), 12033–12034 (2009).
[Crossref] [PubMed]

Vasconcelos, M. L.

V. Ruta, S. R. Datta, M. L. Vasconcelos, J. Freeland, L. L. Looger, and R. Axel, “A dimorphic pheromone circuit in Drosophila from sensory input to descending output,” Nature 468(7324), 686–690 (2010).
[Crossref] [PubMed]

Vosshall, L. B.

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]

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C. Wang, R. Liu, D. E. Milkie, W. Sun, Z. Tan, A. Kerlin, T.-W. Chen, D. S. Kim, and N. Ji, “Multiplexed aberration measurement for deep tissue imaging in vivo,” Nat. Methods 11(10), 1037–1040 (2014).
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C. M. Root, J. L. Semmelhack, A. M. Wong, J. Flores, and J. W. Wang, “Propagation of olfactory information in Drosophila,” Proc. Natl. Acad. Sci. U.S.A. 104(28), 11826–11831 (2007).
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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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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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D. G. Ouzounov, T. Wang, M. Wang, D. D. Feng, N. G. Horton, J. C. Cruz-Hernández, Y.-T. Cheng, J. Reimer, A. S. Tolias, N. Nishimura, and C. Xu, “In vivo three-photon imaging of activity of GCaMP6-labeled neurons deep in intact mouse brain,” Nat. Methods 14(4), 388–390 (2017).
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D. G. Ouzounov, T. Wang, M. Wang, D. D. Feng, N. G. Horton, J. C. Cruz-Hernández, Y.-T. Cheng, J. Reimer, A. S. Tolias, N. Nishimura, and C. Xu, “In vivo three-photon imaging of activity of GCaMP6-labeled neurons deep in intact mouse brain,” Nat. Methods 14(4), 388–390 (2017).
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C.-W. Lin, H.-W. Lin, M.-T. Chiu, Y.-H. Shih, T.-Y. Wang, H.-M. Chang, and A.-S. Chiang, “Automated in situ brain imaging for mapping the Drosophila connectome,” J. Neurogenet. 29(4), 157–168 (2015).
[Crossref] [PubMed]

C.-T. Shih, O. Sporns, S.-L. Yuan, T.-S. Su, Y.-J. Lin, C.-C. Chuang, T.-Y. Wang, C.-C. Lo, R. J. Greenspan, and A. S. Chiang, “Connectomics-based analysis of information flow in the Drosophila brain,” Curr. Biol. 25(10), 1249–1258 (2015).
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Winther, Å. M. E.

R. Ignell, C. M. Root, R. T. Birse, J. W. Wang, D. R. Nässel, and Å. M. E. Winther, “Presynaptic peptidergic modulation of olfactory receptor neurons in Drosophila,” Proc. Natl. Acad. Sci. U.S.A. 106(31), 13070–13075 (2009).
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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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C. M. Root, J. L. Semmelhack, A. M. Wong, J. Flores, and J. W. Wang, “Propagation of olfactory information in Drosophila,” Proc. Natl. Acad. Sci. U.S.A. 104(28), 11826–11831 (2007).
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Xu, C.

D. G. Ouzounov, T. Wang, M. Wang, D. D. Feng, N. G. Horton, J. C. Cruz-Hernández, Y.-T. Cheng, J. Reimer, A. S. Tolias, N. Nishimura, and C. Xu, “In vivo three-photon imaging of activity of GCaMP6-labeled neurons deep in intact mouse brain,” Nat. Methods 14(4), 388–390 (2017).
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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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D. Kobat, N. G. Horton, and C. Xu, “In vivo two-photon microscopy to 1.6-mm depth in mouse cortex,” J. Biomed. Opt. 16(10), 106014 (2011).
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A.-S. Chiang, C.-Y. Lin, C.-C. Chuang, H.-M. Chang, C.-H. Hsieh, C.-W. Yeh, C.-T. Shih, J.-J. Wu, G.-T. Wang, Y.-C. Chen, C.-C. Wu, G.-Y. Chen, Y.-T. Ching, P.-C. Lee, C.-Y. Lin, H.-H. Lin, C.-C. Wu, H.-W. Hsu, Y.-A. Huang, J.-Y. Chen, H.-J. Chiang, C.-F. Lu, R.-F. Ni, C.-Y. Yeh, and J.-K. Hwang, “Three-dimensional reconstruction of brain-wide wiring networks in Drosophila at single-cell resolution,” Curr. Biol. 21(1), 1–11 (2011).
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A.-S. Chiang, C.-Y. Lin, C.-C. Chuang, H.-M. Chang, C.-H. Hsieh, C.-W. Yeh, C.-T. Shih, J.-J. Wu, G.-T. Wang, Y.-C. Chen, C.-C. Wu, G.-Y. Chen, Y.-T. Ching, P.-C. Lee, C.-Y. Lin, H.-H. Lin, C.-C. Wu, H.-W. Hsu, Y.-A. Huang, J.-Y. Chen, H.-J. Chiang, C.-F. Lu, R.-F. Ni, C.-Y. Yeh, and J.-K. Hwang, “Three-dimensional reconstruction of brain-wide wiring networks in Drosophila at single-cell resolution,” Curr. Biol. 21(1), 1–11 (2011).
[Crossref] [PubMed]

Yuan, S.-L.

C.-T. Shih, O. Sporns, S.-L. Yuan, T.-S. Su, Y.-J. Lin, C.-C. Chuang, T.-Y. Wang, C.-C. Lo, R. J. Greenspan, and A. S. Chiang, “Connectomics-based analysis of information flow in the Drosophila brain,” Curr. Biol. 25(10), 1249–1258 (2015).
[Crossref] [PubMed]

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Z. Zheng, J. S. Lauritzen, E. Perlman, C. G. Robinson, M. Nichols, D. Milkie, O. Torrens, J. Price, C. B. Fisher, N. Sharifi, S. A. Calle-Schuler, L. Kmecova, I. J. Ali, B. Karsh, E. T. Trautman, J. A. Bogovic, P. Hanslovsky, G. S. X. E. Jefferis, M. Kazhdan, K. Khairy, S. Saalfeld, R. D. Fetter, and D. D. Bock, “A complete electron microscopy volume of the brain of adult Drosophila melanogaster,” Cell 174(3), 730–743 (2018).
[Crossref] [PubMed]

Zhong, Y.

Y. Wang, H. F. Guo, T. A. Pologruto, F. Hannan, I. Hakker, K. Svoboda, and Y. Zhong, “Stereotyped odor-evoked activity in the mushroom body of Drosophila revealed by green fluorescent protein-based Ca2+ imaging,” J. Neurosci. 24(29), 6507–6514 (2004).
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Biomed. Opt. Express (2)

Cell (2)

Z. Zheng, J. S. Lauritzen, E. Perlman, C. G. Robinson, M. Nichols, D. Milkie, O. Torrens, J. Price, C. B. Fisher, N. Sharifi, S. A. Calle-Schuler, L. Kmecova, I. J. Ali, B. Karsh, E. T. Trautman, J. A. Bogovic, P. Hanslovsky, G. S. X. E. Jefferis, M. Kazhdan, K. Khairy, S. Saalfeld, R. D. Fetter, and D. D. Bock, “A complete electron microscopy volume of the brain of adult Drosophila melanogaster,” Cell 174(3), 730–743 (2018).
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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. Biol. (3)

A.-S. Chiang, C.-Y. Lin, C.-C. Chuang, H.-M. Chang, C.-H. Hsieh, C.-W. Yeh, C.-T. Shih, J.-J. Wu, G.-T. Wang, Y.-C. Chen, C.-C. Wu, G.-Y. Chen, Y.-T. Ching, P.-C. Lee, C.-Y. Lin, H.-H. Lin, C.-C. Wu, H.-W. Hsu, Y.-A. Huang, J.-Y. Chen, H.-J. Chiang, C.-F. Lu, R.-F. Ni, C.-Y. Yeh, and J.-K. Hwang, “Three-dimensional reconstruction of brain-wide wiring networks in Drosophila at single-cell resolution,” Curr. Biol. 21(1), 1–11 (2011).
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C.-T. Shih, O. Sporns, S.-L. Yuan, T.-S. Su, Y.-J. Lin, C.-C. Chuang, T.-Y. Wang, C.-C. Lo, R. J. Greenspan, and A. S. Chiang, “Connectomics-based analysis of information flow in the Drosophila brain,” Curr. Biol. 25(10), 1249–1258 (2015).
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D. Kobat, N. G. Horton, and C. Xu, “In vivo two-photon microscopy to 1.6-mm depth in mouse cortex,” J. Biomed. Opt. 16(10), 106014 (2011).
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M. Pedrazzani, V. Loriette, P. Tchenio, S. Benrezzak, D. Nutarelli, and A. Fragola, “Sensorless adaptive optics implementation in widefield optical sectioning microscopy inside in vivo Drosophila brain,” J. Biomed. Opt. 21(3), 036006 (2016).
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C.-W. Lin, H.-W. Lin, M.-T. Chiu, Y.-H. Shih, T.-Y. Wang, H.-M. Chang, and A.-S. Chiang, “Automated in situ brain imaging for mapping the Drosophila connectome,” J. Neurogenet. 29(4), 157–168 (2015).
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Y. Wang, H. F. Guo, T. A. Pologruto, F. Hannan, I. Hakker, K. Svoboda, and Y. Zhong, “Stereotyped odor-evoked activity in the mushroom body of Drosophila revealed by green fluorescent protein-based Ca2+ imaging,” J. Neurosci. 24(29), 6507–6514 (2004).
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K. S. Honegger, R. A. A. Campbell, and G. C. Turner, “Cellular-resolution population imaging reveals robust sparse coding in the Drosophila mushroom body,” J. Neurosci. 31(33), 11772–11785 (2011).
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Nature (1)

V. Ruta, S. R. Datta, M. L. Vasconcelos, J. Freeland, L. L. Looger, and R. Axel, “A dimorphic pheromone circuit in Drosophila from sensory input to descending output,” Nature 468(7324), 686–690 (2010).
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Supplementary Material (3)

NameDescription
» Visualization 1       1PF axial stacks in living and degassed Drosophila brains. With the degassing process, the imaging depth is greatly improved, but does not penetrate the whole-brain.
» Visualization 2       2PF axial stacks in the living and degassed Drosophila brains. With the degassing process, the whole brain can be in situ observed by 2PF.
» Visualization 3       Axial stacks of 3PF signals from GFP-labeled brain structures and THG signals from trachea/tissue interfaces, showing the capability to penetrate the whole brain in vivo.

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Figures (5)

Fig. 1
Fig. 1 Living and degassed Drosophila brain images under different imaging modalities. (A), (C) and (E) are 1PF, 2PF and 3PF images at 0-20, 40-60, 120-140 and 170-190 μm axial projected images of a living brain. (B) and (D) are 1PF and 2PF images of a degassed brain at the same depth ranges. Although brain-edge structures (arrowheads) are still visible at 40-60 μm depth in (A), the image loses contrast in brain center (white arrow). In the degassed brain, the penetration depth of 1PF is significantly improved in (B), but not approaching the bottom of brain. In (C), 2PF penetrates deeper than 1PF, but becomes blurry at depth beyond 100 μm. Whole-brain imaging is achieved in (D) by 2PF in a degassed brain. (E) shows only 3PF maintains contrast and reasonable resolution throughout the whole brain. The insets in the bottommost panels of (D) and (E) show clear cell bodies. (F) THG images, a complementary contrast with 3PF, show clear tracheae distribution. By comparing with structural connectome, several LPUs at corresponding depth ranges are annotated in (A) - (E), including MB: mushroom body, SDFP: superior dorsofrontal protocerebrum, AL: antennal lobe, DLP: dorsolateral protocerebrum, and CAL: calyx. All the images are intensity normalized with individually brightest 0.5% pixels. Scale bar: 50 μm for (A); 1 μm for insets of (D) and (E). Complete depth-images are given in Visualization 1, Visualization 2, and Visualization 3. Genotype: (A), (B) and (D) are Gal4-elav/UAS-mGFP, (C) and (E) are Gal4-elav.L/CyO × UAS-EGFP.
Fig. 2
Fig. 2 1PF, 2PF, and 3PF signal attenuations in living and degassed brains, and quantitative analysis on contributions from scattering and aberration. (A) and (B) show the semi-logarithmic plot of 1PF and 2PF signal attenuations with depth, inside a living (black) and degassed (green) brains, respectively corresponding to Figs. 1(A) - 1(D). The orange curve in (A) (1P che.) is a control experiment of chemically treated brain (paraformaldehyde and triton), but no degassing. (C) 3PF signal attenuation of a living brain in Fig. 1(E). The inset in (A) is a depth color-coded brain image that shows the area (white box) for signal extraction at different depths. The signals are obtained by averaging the brightest 1% pixels at different depths inside the white box. The red and pink lines in (A) - (C) are linear fits of the signals, and their corresponding attenuation coefficients (μatt) are shown in the bottom. (D) Quantitative comparison of μatt in living brains (black squares) and degassed brains (green diamonds) at each wavelength, and that from brain only treated by chemicals (orange circle), together with corresponding attenuations from mouse brains, i.e. neuron scattering (pink circles) and tracheae (red triangles). Scale bar in inset of (A): 50 μm. In the 1P and 2P degassed brain, 2 and 3 replicates are analyzed to confirm the attenuation coefficients. For the in vivo brain imaging of 2P and 3P, it is performed on the same Drosophila. Therefore, it should be beyond doubt that 3P penetrates deeper than 2P, without the need of more replicates.
Fig. 3
Fig. 3 Wavelength dependency of attenuations from neuronal scattering, trachea-induced light distortion and degassed Drosophila brain attenuations. By plotting in a log-log scale, the slope indicates the exponential power of neuronal scattering, which is about λ−2. The result is reasonable since tissue scattering can be considered as a mixture of Mie scattering (λ−1 dependence) and Rayleigh scattering (λ−4 dependence). The slope of blue line points out that the power of trachea-contributed attenuation, which is around λ-0.9.
Fig. 4
Fig. 4 Depth-dependent axial confinement of 2PF and 3PF inside a living Drosophila brain. (A) and (B) show the 3PF image stack projections at shallow (8 - 18 μm) and deep (54 - 74 μm) regions. The white-dashed boxes show the selected area for depth-dependent axial confinement analysis of (C) - (D) 2PF and of (E) - (F) 3PF. Comparing (C) and (E), which are at shallow region, the axial confinement of 2PF and 3PF are comparable, as manifested by the inset images at different depths. On the other hand, for (D) and (F) at deep region, the 3PF axial confinement is similar to that at shallow region, but the 2PF axial confinement is much worse. The underlying reason is the excess light distortion induced by trachea in a living brain, and the result is image blur for 2PF in deep brain region.
Fig. 5
Fig. 5 Signal-to-background ratio (SBR) and resolution analysis. (A) Color-coded depth projection image of 3PF throughout the whole-brain, showing different structures at different depths. The white-dashed box in the center represents the region of background selection. (B) SBR of 2PF and 3PF signals at each depth at the same brain. (C) and (F) show the XY image of 3PF and THG at 182 and 186 μm, and their YZ images are given on the right-hand-side, respectively. The lateral resolutions are ~1.8 μm (D) for 3PF and ~1.2 μm (G) for THG signals. The axial resolutions are ~5.2 μm for 3PF (E) and ~6.5 μm for THG (H), respectively. Scale bars: 50 μm in (A), 5 μm in (C).

Equations (4)

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

I(d)= I 0 e d l a = I 0 e μ att ×d
F (n) (d) (I(d)) n
F (n) (d)=a× e -n× μ att ×d
ln( F (n) (d))=ln(a)-n× μ att ×d

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