Abstract

We demonstrate a remotely located microelectromechanical systems (MEMS) actuator that can translate >400 μm to perform axial beam scanning in a multiphoton microscope. We use a 2-dimensional MEMS mirror for lateral scanning, and collected multiphoton excited fluorescence images in either the horizontal or vertical plane with a field-of-view of either 270 × 270 or 270 × 200 μm2, respectively, at 5 frames per second. Axial resolution varied from 4.5 to 7 μm over the scan range. The compact size of the actuator and scanner allows for use in an endomicroscope to collect images in the vertical plane with >200 μm depth.

© 2017 Optical Society of America

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2016 (2)

2015 (1)

G. Ducourthial, P. Leclerc, T. Mansuryan, M. Fabert, J. Brevier, R. Habert, F. Braud, R. Batrin, C. Vever-Bizet, G. Bourg-Heckly, L. Thiberville, A. Druilhe, A. Kudlinski, and F. Louradour, “Development of a real-time flexible multiphoton microendoscope for label-free imaging in a live animal,” Sci. Rep. 5, 18303 (2015).
[Crossref] [PubMed]

2014 (1)

A. D. Corbett, R. A. B. Burton, G. Bub, P. S. Salter, S. Tuohy, M. J. Booth, and T. Wilson, “Quantifying distortions in two-photon remote focussing microscope images using a volumetric calibration specimen,” Front. Physiol. 5, 384 (2014).
[PubMed]

2013 (1)

H. Clevers, “The intestinal crypt, a prototype stem cell compartment,” Cell 154(2), 274–284 (2013).
[Crossref] [PubMed]

2012 (4)

A. Masedunskas, M. Sramkova, L. Parente, and R. Weigert, “Intravital Microscopy to Image Membrane Trafficking in Live Rats,” Methods Mol. Biol. 931, 153–167 (2012).
[Crossref] [PubMed]

L. Ritsma, E. J. A. Steller, E. Beerling, C. J. M. Loomans, A. Zomer, C. Gerlach, N. Vrisekoop, D. Seinstra, L. van Gurp, R. Schafer, D. A. Raats, A. de Graaff, T. N. Schumacher, E. J. P. de Koning, O. Kranenburg, and J. van Rheenen, “Intravital Microscopy through an Abdominal Imaging Window Reveals Steps during Liver Metastasis,” Sci. Transl. Med. 4(158), 158ra145 (2012).
[Crossref] [PubMed]

E. J. Botcherby, C. W. Smith, M. M. Kohl, D. Débarre, M. J. Booth, R. Juškaitis, O. Paulsen, and T. Wilson, “Aberration-free three-dimensional multiphoton imaging of neuronal activity at kHz rates,” Proc. Natl. Acad. Sci. U.S.A. 109(8), 2919–2924 (2012).
[Crossref] [PubMed]

D. R. Rivera, C. M. Brown, D. G. Ouzounov, W. W. Webb, and C. Xu, “Multifocal multiphoton endoscope,” Opt. Lett. 37(8), 1349–1351 (2012).
[Crossref] [PubMed]

2011 (5)

Y. Zhu, W. Liu, K. Jia, W. Liao, and H. Xie, “A piezoelectric unimorph actuator based tip-tilt-piston micromirror with high fill factor and small tilt and lateral shift,” Sens. Actuators 167(2), 495–501 (2011).
[Crossref]

H. Mansoor, H. Zeng, K. Chen, Y. Yu, J. Zhao, and M. Chiao, “Vertical optical sectioning using a magnetically driven confocal microscanner aimed for in vivo clinical imaging,” Opt. Express 19(25), 25161–25172 (2011).
[Crossref] [PubMed]

E. E. Hoover, M. D. Young, E. V. Chandler, A. Luo, J. J. Field, K. E. Sheetz, A. W. Sylvester, and J. A. Squier, “Remote focusing for programmable multi-layer differential multiphoton microscopy,” Biomed. Opt. Express 2(1), 113–122 (2011).
[Crossref] [PubMed]

S. J. Miller, B. P. Joshi, A. Gaustad, Y. Feng, E. R. Fearon, and T. D. Wang, “In vivo Fluorescence-Based Endoscopic Detection of Colon Dysplasia in the Mouse using a Novel Peptide Probe,” PLoS one 6(3), e17384 (2011).

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]

2010 (3)

L. Madisen, T. A. Zwingman, S. M. Sunkin, S. W. Oh, H. A. Zariwala, H. Gu, L. L. Ng, R. D. Palmiter, M. J. Hawrylycz, A. R. Jones, E. S. Lein, and H. Zeng, “A robust and high-throughput Cre reporting and characterization system for the whole mouse brain,” Nat. Neurosci. 13(1), 133–140 (2010).
[Crossref] [PubMed]

M. J. Koehler, T. Vogel, P. Elsner, K. König, R. Bückle, and M. Kaatz, “In vivo measurement of the human epidermal thickness in different localizations by multiphoton laser tomography,” Skin Res. Technol. 16(3), 259–264 (2010).
[PubMed]

Y. Wu, Y. Zhang, J. Xi, M.-J. Li, and X. Li, “Fiber-optic nonlinear endomicroscopy with focus scanning by using shape memory alloy actuation,” J. Biomed. Opt. 15(6), 060506 (2010).
[Crossref] [PubMed]

2009 (1)

2008 (1)

2007 (3)

L. Fu, A. Jain, C. Cranfield, H. Xie, and M. Gu, “Three-dimensional nonlinear optical endoscopy,” J. Biomed. Opt. 12(4), 040501 (2007).
[Crossref] [PubMed]

W. Göbel, F. Helmchen, and B. M. Kampa, “Imaging cellular network dynamics in three dimensions using fast 3D laser scanning,” Nat. Methods 4(1), 73–79 (2007).
[Crossref] [PubMed]

E. J. Botcherby, R. Juskaitis, M. J. Booth, and T. Wilson, “Aberration-free optical refocusing in high numerical aperture microscopy,” Opt. Lett. 32(14), 2007–2009 (2007).
[Crossref] [PubMed]

2006 (1)

2004 (1)

K. Lee, K. Krisnamoorthy, K. Yu, and O. Solgaard, “Single-crystalline silicon micromirrors actuated by self-aligned vertical electrostatic comb drives with piston-motion and rotational capabilities,” Sens. Actuators A Phys. 114(2–3), 423–428 (2004).
[Crossref]

2003 (2)

E. K. Griffiths, O. Sanchez, P. Mill, C. Krawczyk, C. V. Hojilla, E. Rubin, M. M. Nau, R. Khokha, S. Lipkowitz, C. C. Hui, and J. M. Penninger, “Cbl-3-deficient mice exhibit normal epithelial development,” Mol. Cell. Biol. 23(21), 7708–7718 (2003).
[Crossref] [PubMed]

T. Hinoi, M. Loda, and E. R. Fearon, “Silencing of CDX2 expression in colon cancer via a dominant repression pathway,” J. Biol. Chem. 278(45), 44608–44616 (2003).
[Crossref] [PubMed]

1998 (1)

K. L. Turner, S. A. Miller, P. G. Hartwell, N. C. MacDonald, S. H. Strogatz, and S. G. Adams, “Five parametric resonances in a microelectromechanical system,” Nature 396(6707), 149–152 (1998).
[Crossref]

1995 (1)

1990 (1)

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

Adams, S. G.

K. L. Turner, S. A. Miller, P. G. Hartwell, N. C. MacDonald, S. H. Strogatz, and S. G. Adams, “Five parametric resonances in a microelectromechanical system,” Nature 396(6707), 149–152 (1998).
[Crossref]

Barretto, R. P.

Batrin, R.

G. Ducourthial, P. Leclerc, T. Mansuryan, M. Fabert, J. Brevier, R. Habert, F. Braud, R. Batrin, C. Vever-Bizet, G. Bourg-Heckly, L. Thiberville, A. Druilhe, A. Kudlinski, and F. Louradour, “Development of a real-time flexible multiphoton microendoscope for label-free imaging in a live animal,” Sci. Rep. 5, 18303 (2015).
[Crossref] [PubMed]

Beerling, E.

L. Ritsma, E. J. A. Steller, E. Beerling, C. J. M. Loomans, A. Zomer, C. Gerlach, N. Vrisekoop, D. Seinstra, L. van Gurp, R. Schafer, D. A. Raats, A. de Graaff, T. N. Schumacher, E. J. P. de Koning, O. Kranenburg, and J. van Rheenen, “Intravital Microscopy through an Abdominal Imaging Window Reveals Steps during Liver Metastasis,” Sci. Transl. Med. 4(158), 158ra145 (2012).
[Crossref] [PubMed]

Booth, M. J.

A. D. Corbett, R. A. B. Burton, G. Bub, P. S. Salter, S. Tuohy, M. J. Booth, and T. Wilson, “Quantifying distortions in two-photon remote focussing microscope images using a volumetric calibration specimen,” Front. Physiol. 5, 384 (2014).
[PubMed]

E. J. Botcherby, C. W. Smith, M. M. Kohl, D. Débarre, M. J. Booth, R. Juškaitis, O. Paulsen, and T. Wilson, “Aberration-free three-dimensional multiphoton imaging of neuronal activity at kHz rates,” Proc. Natl. Acad. Sci. U.S.A. 109(8), 2919–2924 (2012).
[Crossref] [PubMed]

E. J. Botcherby, R. Juskaitis, M. J. Booth, and T. Wilson, “Aberration-free optical refocusing in high numerical aperture microscopy,” Opt. Lett. 32(14), 2007–2009 (2007).
[Crossref] [PubMed]

Botcherby, E. J.

E. J. Botcherby, C. W. Smith, M. M. Kohl, D. Débarre, M. J. Booth, R. Juškaitis, O. Paulsen, and T. Wilson, “Aberration-free three-dimensional multiphoton imaging of neuronal activity at kHz rates,” Proc. Natl. Acad. Sci. U.S.A. 109(8), 2919–2924 (2012).
[Crossref] [PubMed]

E. J. Botcherby, R. Juskaitis, M. J. Booth, and T. Wilson, “Aberration-free optical refocusing in high numerical aperture microscopy,” Opt. Lett. 32(14), 2007–2009 (2007).
[Crossref] [PubMed]

Bourg-Heckly, G.

G. Ducourthial, P. Leclerc, T. Mansuryan, M. Fabert, J. Brevier, R. Habert, F. Braud, R. Batrin, C. Vever-Bizet, G. Bourg-Heckly, L. Thiberville, A. Druilhe, A. Kudlinski, and F. Louradour, “Development of a real-time flexible multiphoton microendoscope for label-free imaging in a live animal,” Sci. Rep. 5, 18303 (2015).
[Crossref] [PubMed]

Braud, F.

G. Ducourthial, P. Leclerc, T. Mansuryan, M. Fabert, J. Brevier, R. Habert, F. Braud, R. Batrin, C. Vever-Bizet, G. Bourg-Heckly, L. Thiberville, A. Druilhe, A. Kudlinski, and F. Louradour, “Development of a real-time flexible multiphoton microendoscope for label-free imaging in a live animal,” Sci. Rep. 5, 18303 (2015).
[Crossref] [PubMed]

Brevier, J.

G. Ducourthial, P. Leclerc, T. Mansuryan, M. Fabert, J. Brevier, R. Habert, F. Braud, R. Batrin, C. Vever-Bizet, G. Bourg-Heckly, L. Thiberville, A. Druilhe, A. Kudlinski, and F. Louradour, “Development of a real-time flexible multiphoton microendoscope for label-free imaging in a live animal,” Sci. Rep. 5, 18303 (2015).
[Crossref] [PubMed]

Brown, C. M.

Bub, G.

A. D. Corbett, R. A. B. Burton, G. Bub, P. S. Salter, S. Tuohy, M. J. Booth, and T. Wilson, “Quantifying distortions in two-photon remote focussing microscope images using a volumetric calibration specimen,” Front. Physiol. 5, 384 (2014).
[PubMed]

Bückle, R.

M. J. Koehler, T. Vogel, P. Elsner, K. König, R. Bückle, and M. Kaatz, “In vivo measurement of the human epidermal thickness in different localizations by multiphoton laser tomography,” Skin Res. Technol. 16(3), 259–264 (2010).
[PubMed]

Burton, R. A. B.

A. D. Corbett, R. A. B. Burton, G. Bub, P. S. Salter, S. Tuohy, M. J. Booth, and T. Wilson, “Quantifying distortions in two-photon remote focussing microscope images using a volumetric calibration specimen,” Front. Physiol. 5, 384 (2014).
[PubMed]

Chandler, E. V.

Chen, K.

Chiao, M.

Clevers, H.

H. Clevers, “The intestinal crypt, a prototype stem cell compartment,” Cell 154(2), 274–284 (2013).
[Crossref] [PubMed]

Cocker, E. D.

Corbett, A. D.

A. D. Corbett, R. A. B. Burton, G. Bub, P. S. Salter, S. Tuohy, M. J. Booth, and T. Wilson, “Quantifying distortions in two-photon remote focussing microscope images using a volumetric calibration specimen,” Front. Physiol. 5, 384 (2014).
[PubMed]

Cranfield, C.

L. Fu, A. Jain, C. Cranfield, H. Xie, and M. Gu, “Three-dimensional nonlinear optical endoscopy,” J. Biomed. Opt. 12(4), 040501 (2007).
[Crossref] [PubMed]

de Graaff, A.

L. Ritsma, E. J. A. Steller, E. Beerling, C. J. M. Loomans, A. Zomer, C. Gerlach, N. Vrisekoop, D. Seinstra, L. van Gurp, R. Schafer, D. A. Raats, A. de Graaff, T. N. Schumacher, E. J. P. de Koning, O. Kranenburg, and J. van Rheenen, “Intravital Microscopy through an Abdominal Imaging Window Reveals Steps during Liver Metastasis,” Sci. Transl. Med. 4(158), 158ra145 (2012).
[Crossref] [PubMed]

de Koning, E. J. P.

L. Ritsma, E. J. A. Steller, E. Beerling, C. J. M. Loomans, A. Zomer, C. Gerlach, N. Vrisekoop, D. Seinstra, L. van Gurp, R. Schafer, D. A. Raats, A. de Graaff, T. N. Schumacher, E. J. P. de Koning, O. Kranenburg, and J. van Rheenen, “Intravital Microscopy through an Abdominal Imaging Window Reveals Steps during Liver Metastasis,” Sci. Transl. Med. 4(158), 158ra145 (2012).
[Crossref] [PubMed]

Débarre, D.

E. J. Botcherby, C. W. Smith, M. M. Kohl, D. Débarre, M. J. Booth, R. Juškaitis, O. Paulsen, and T. Wilson, “Aberration-free three-dimensional multiphoton imaging of neuronal activity at kHz rates,” Proc. Natl. Acad. Sci. U.S.A. 109(8), 2919–2924 (2012).
[Crossref] [PubMed]

Denk, W.

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

Druilhe, A.

G. Ducourthial, P. Leclerc, T. Mansuryan, M. Fabert, J. Brevier, R. Habert, F. Braud, R. Batrin, C. Vever-Bizet, G. Bourg-Heckly, L. Thiberville, A. Druilhe, A. Kudlinski, and F. Louradour, “Development of a real-time flexible multiphoton microendoscope for label-free imaging in a live animal,” Sci. Rep. 5, 18303 (2015).
[Crossref] [PubMed]

Duan, X.

Ducourthial, G.

G. Ducourthial, P. Leclerc, T. Mansuryan, M. Fabert, J. Brevier, R. Habert, F. Braud, R. Batrin, C. Vever-Bizet, G. Bourg-Heckly, L. Thiberville, A. Druilhe, A. Kudlinski, and F. Louradour, “Development of a real-time flexible multiphoton microendoscope for label-free imaging in a live animal,” Sci. Rep. 5, 18303 (2015).
[Crossref] [PubMed]

Elsner, P.

M. J. Koehler, T. Vogel, P. Elsner, K. König, R. Bückle, and M. Kaatz, “In vivo measurement of the human epidermal thickness in different localizations by multiphoton laser tomography,” Skin Res. Technol. 16(3), 259–264 (2010).
[PubMed]

Engelbrecht, C. J.

Fabert, M.

G. Ducourthial, P. Leclerc, T. Mansuryan, M. Fabert, J. Brevier, R. Habert, F. Braud, R. Batrin, C. Vever-Bizet, G. Bourg-Heckly, L. Thiberville, A. Druilhe, A. Kudlinski, and F. Louradour, “Development of a real-time flexible multiphoton microendoscope for label-free imaging in a live animal,” Sci. Rep. 5, 18303 (2015).
[Crossref] [PubMed]

Fearon, E. R.

S. J. Miller, B. P. Joshi, A. Gaustad, Y. Feng, E. R. Fearon, and T. D. Wang, “In vivo Fluorescence-Based Endoscopic Detection of Colon Dysplasia in the Mouse using a Novel Peptide Probe,” PLoS one 6(3), e17384 (2011).

T. Hinoi, M. Loda, and E. R. Fearon, “Silencing of CDX2 expression in colon cancer via a dominant repression pathway,” J. Biol. Chem. 278(45), 44608–44616 (2003).
[Crossref] [PubMed]

Feng, Y.

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Fu, L.

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L. Ritsma, E. J. A. Steller, E. Beerling, C. J. M. Loomans, A. Zomer, C. Gerlach, N. Vrisekoop, D. Seinstra, L. van Gurp, R. Schafer, D. A. Raats, A. de Graaff, T. N. Schumacher, E. J. P. de Koning, O. Kranenburg, and J. van Rheenen, “Intravital Microscopy through an Abdominal Imaging Window Reveals Steps during Liver Metastasis,” Sci. Transl. Med. 4(158), 158ra145 (2012).
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L. Fu, A. Jain, C. Cranfield, H. Xie, and M. Gu, “Three-dimensional nonlinear optical endoscopy,” J. Biomed. Opt. 12(4), 040501 (2007).
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E. K. Griffiths, O. Sanchez, P. Mill, C. Krawczyk, C. V. Hojilla, E. Rubin, M. M. Nau, R. Khokha, S. Lipkowitz, C. C. Hui, and J. M. Penninger, “Cbl-3-deficient mice exhibit normal epithelial development,” Mol. Cell. Biol. 23(21), 7708–7718 (2003).
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L. Madisen, T. A. Zwingman, S. M. Sunkin, S. W. Oh, H. A. Zariwala, H. Gu, L. L. Ng, R. D. Palmiter, M. J. Hawrylycz, A. R. Jones, E. S. Lein, and H. Zeng, “A robust and high-throughput Cre reporting and characterization system for the whole mouse brain,” Nat. Neurosci. 13(1), 133–140 (2010).
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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).
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S. J. Miller, B. P. Joshi, A. Gaustad, Y. Feng, E. R. Fearon, and T. D. Wang, “In vivo Fluorescence-Based Endoscopic Detection of Colon Dysplasia in the Mouse using a Novel Peptide Probe,” PLoS one 6(3), e17384 (2011).

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E. K. Griffiths, O. Sanchez, P. Mill, C. Krawczyk, C. V. Hojilla, E. Rubin, M. M. Nau, R. Khokha, S. Lipkowitz, C. C. Hui, and J. M. Penninger, “Cbl-3-deficient mice exhibit normal epithelial development,” Mol. Cell. Biol. 23(21), 7708–7718 (2003).
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L. Madisen, T. A. Zwingman, S. M. Sunkin, S. W. Oh, H. A. Zariwala, H. Gu, L. L. Ng, R. D. Palmiter, M. J. Hawrylycz, A. R. Jones, E. S. Lein, and H. Zeng, “A robust and high-throughput Cre reporting and characterization system for the whole mouse brain,” Nat. Neurosci. 13(1), 133–140 (2010).
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L. Madisen, T. A. Zwingman, S. M. Sunkin, S. W. Oh, H. A. Zariwala, H. Gu, L. L. Ng, R. D. Palmiter, M. J. Hawrylycz, A. R. Jones, E. S. Lein, and H. Zeng, “A robust and high-throughput Cre reporting and characterization system for the whole mouse brain,” Nat. Neurosci. 13(1), 133–140 (2010).
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E. K. Griffiths, O. Sanchez, P. Mill, C. Krawczyk, C. V. Hojilla, E. Rubin, M. M. Nau, R. Khokha, S. Lipkowitz, C. C. Hui, and J. M. Penninger, “Cbl-3-deficient mice exhibit normal epithelial development,” Mol. Cell. Biol. 23(21), 7708–7718 (2003).
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Rebane, A.

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Schumacher, T. N.

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Strogatz, S. H.

K. L. Turner, S. A. Miller, P. G. Hartwell, N. C. MacDonald, S. H. Strogatz, and S. G. Adams, “Five parametric resonances in a microelectromechanical system,” Nature 396(6707), 149–152 (1998).
[Crossref]

Sunkin, S. M.

L. Madisen, T. A. Zwingman, S. M. Sunkin, S. W. Oh, H. A. Zariwala, H. Gu, L. L. Ng, R. D. Palmiter, M. J. Hawrylycz, A. R. Jones, E. S. Lein, and H. Zeng, “A robust and high-throughput Cre reporting and characterization system for the whole mouse brain,” Nat. Neurosci. 13(1), 133–140 (2010).
[Crossref] [PubMed]

Sylvester, A. W.

Thiberville, L.

G. Ducourthial, P. Leclerc, T. Mansuryan, M. Fabert, J. Brevier, R. Habert, F. Braud, R. Batrin, C. Vever-Bizet, G. Bourg-Heckly, L. Thiberville, A. Druilhe, A. Kudlinski, and F. Louradour, “Development of a real-time flexible multiphoton microendoscope for label-free imaging in a live animal,” Sci. Rep. 5, 18303 (2015).
[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]

Tuohy, S.

A. D. Corbett, R. A. B. Burton, G. Bub, P. S. Salter, S. Tuohy, M. J. Booth, and T. Wilson, “Quantifying distortions in two-photon remote focussing microscope images using a volumetric calibration specimen,” Front. Physiol. 5, 384 (2014).
[PubMed]

Turner, K. L.

K. L. Turner, S. A. Miller, P. G. Hartwell, N. C. MacDonald, S. H. Strogatz, and S. G. Adams, “Five parametric resonances in a microelectromechanical system,” Nature 396(6707), 149–152 (1998).
[Crossref]

van Gurp, L.

L. Ritsma, E. J. A. Steller, E. Beerling, C. J. M. Loomans, A. Zomer, C. Gerlach, N. Vrisekoop, D. Seinstra, L. van Gurp, R. Schafer, D. A. Raats, A. de Graaff, T. N. Schumacher, E. J. P. de Koning, O. Kranenburg, and J. van Rheenen, “Intravital Microscopy through an Abdominal Imaging Window Reveals Steps during Liver Metastasis,” Sci. Transl. Med. 4(158), 158ra145 (2012).
[Crossref] [PubMed]

van Rheenen, J.

L. Ritsma, E. J. A. Steller, E. Beerling, C. J. M. Loomans, A. Zomer, C. Gerlach, N. Vrisekoop, D. Seinstra, L. van Gurp, R. Schafer, D. A. Raats, A. de Graaff, T. N. Schumacher, E. J. P. de Koning, O. Kranenburg, and J. van Rheenen, “Intravital Microscopy through an Abdominal Imaging Window Reveals Steps during Liver Metastasis,” Sci. Transl. Med. 4(158), 158ra145 (2012).
[Crossref] [PubMed]

Vever-Bizet, C.

G. Ducourthial, P. Leclerc, T. Mansuryan, M. Fabert, J. Brevier, R. Habert, F. Braud, R. Batrin, C. Vever-Bizet, G. Bourg-Heckly, L. Thiberville, A. Druilhe, A. Kudlinski, and F. Louradour, “Development of a real-time flexible multiphoton microendoscope for label-free imaging in a live animal,” Sci. Rep. 5, 18303 (2015).
[Crossref] [PubMed]

Vogel, T.

M. J. Koehler, T. Vogel, P. Elsner, K. König, R. Bückle, and M. Kaatz, “In vivo measurement of the human epidermal thickness in different localizations by multiphoton laser tomography,” Skin Res. Technol. 16(3), 259–264 (2010).
[PubMed]

Vrisekoop, N.

L. Ritsma, E. J. A. Steller, E. Beerling, C. J. M. Loomans, A. Zomer, C. Gerlach, N. Vrisekoop, D. Seinstra, L. van Gurp, R. Schafer, D. A. Raats, A. de Graaff, T. N. Schumacher, E. J. P. de Koning, O. Kranenburg, and J. van Rheenen, “Intravital Microscopy through an Abdominal Imaging Window Reveals Steps during Liver Metastasis,” Sci. Transl. Med. 4(158), 158ra145 (2012).
[Crossref] [PubMed]

Wang, T. D.

H. Li, X. Duan, Z. Qiu, Q. Zhou, K. Kurabayashi, K. R. Oldham, and T. D. Wang, “Integrated monolithic 3D MEMS scanner for switchable real time vertical/horizontal cross-sectional imaging,” Opt. Express 24(3), 2145–2155 (2016).
[Crossref] [PubMed]

S. J. Miller, B. P. Joshi, A. Gaustad, Y. Feng, E. R. Fearon, and T. D. Wang, “In vivo Fluorescence-Based Endoscopic Detection of Colon Dysplasia in the Mouse using a Novel Peptide Probe,” PLoS one 6(3), e17384 (2011).

Webb, W. W.

D. R. Rivera, C. M. Brown, D. G. Ouzounov, W. W. Webb, and C. Xu, “Multifocal multiphoton endoscope,” Opt. Lett. 37(8), 1349–1351 (2012).
[Crossref] [PubMed]

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

Weigert, R.

A. Masedunskas, M. Sramkova, L. Parente, and R. Weigert, “Intravital Microscopy to Image Membrane Trafficking in Live Rats,” Methods Mol. Biol. 931, 153–167 (2012).
[Crossref] [PubMed]

Wilson, T.

A. D. Corbett, R. A. B. Burton, G. Bub, P. S. Salter, S. Tuohy, M. J. Booth, and T. Wilson, “Quantifying distortions in two-photon remote focussing microscope images using a volumetric calibration specimen,” Front. Physiol. 5, 384 (2014).
[PubMed]

E. J. Botcherby, C. W. Smith, M. M. Kohl, D. Débarre, M. J. Booth, R. Juškaitis, O. Paulsen, and T. Wilson, “Aberration-free three-dimensional multiphoton imaging of neuronal activity at kHz rates,” Proc. Natl. Acad. Sci. U.S.A. 109(8), 2919–2924 (2012).
[Crossref] [PubMed]

E. J. Botcherby, R. Juskaitis, M. J. Booth, and T. Wilson, “Aberration-free optical refocusing in high numerical aperture microscopy,” Opt. Lett. 32(14), 2007–2009 (2007).
[Crossref] [PubMed]

Wu, Y.

Y. Wu, Y. Zhang, J. Xi, M.-J. Li, and X. Li, “Fiber-optic nonlinear endomicroscopy with focus scanning by using shape memory alloy actuation,” J. Biomed. Opt. 15(6), 060506 (2010).
[Crossref] [PubMed]

Wyart, C.

Xi, J.

Y. Wu, Y. Zhang, J. Xi, M.-J. Li, and X. Li, “Fiber-optic nonlinear endomicroscopy with focus scanning by using shape memory alloy actuation,” J. Biomed. Opt. 15(6), 060506 (2010).
[Crossref] [PubMed]

Xie, H.

Y. Zhu, W. Liu, K. Jia, W. Liao, and H. Xie, “A piezoelectric unimorph actuator based tip-tilt-piston micromirror with high fill factor and small tilt and lateral shift,” Sens. Actuators 167(2), 495–501 (2011).
[Crossref]

L. Fu, A. Jain, C. Cranfield, H. Xie, and M. Gu, “Three-dimensional nonlinear optical endoscopy,” J. Biomed. Opt. 12(4), 040501 (2007).
[Crossref] [PubMed]

Xu, C.

Young, M. D.

Yu, K.

K. Lee, K. Krisnamoorthy, K. Yu, and O. Solgaard, “Single-crystalline silicon micromirrors actuated by self-aligned vertical electrostatic comb drives with piston-motion and rotational capabilities,” Sens. Actuators A Phys. 114(2–3), 423–428 (2004).
[Crossref]

Yu, Y.

Zariwala, H. A.

L. Madisen, T. A. Zwingman, S. M. Sunkin, S. W. Oh, H. A. Zariwala, H. Gu, L. L. Ng, R. D. Palmiter, M. J. Hawrylycz, A. R. Jones, E. S. Lein, and H. Zeng, “A robust and high-throughput Cre reporting and characterization system for the whole mouse brain,” Nat. Neurosci. 13(1), 133–140 (2010).
[Crossref] [PubMed]

Zeng, H.

H. Mansoor, H. Zeng, K. Chen, Y. Yu, J. Zhao, and M. Chiao, “Vertical optical sectioning using a magnetically driven confocal microscanner aimed for in vivo clinical imaging,” Opt. Express 19(25), 25161–25172 (2011).
[Crossref] [PubMed]

L. Madisen, T. A. Zwingman, S. M. Sunkin, S. W. Oh, H. A. Zariwala, H. Gu, L. L. Ng, R. D. Palmiter, M. J. Hawrylycz, A. R. Jones, E. S. Lein, and H. Zeng, “A robust and high-throughput Cre reporting and characterization system for the whole mouse brain,” Nat. Neurosci. 13(1), 133–140 (2010).
[Crossref] [PubMed]

Zhang, Y.

Y. Wu, Y. Zhang, J. Xi, M.-J. Li, and X. Li, “Fiber-optic nonlinear endomicroscopy with focus scanning by using shape memory alloy actuation,” J. Biomed. Opt. 15(6), 060506 (2010).
[Crossref] [PubMed]

Zhao, J.

Zhou, Q.

Zhu, Y.

Y. Zhu, W. Liu, K. Jia, W. Liao, and H. Xie, “A piezoelectric unimorph actuator based tip-tilt-piston micromirror with high fill factor and small tilt and lateral shift,” Sens. Actuators 167(2), 495–501 (2011).
[Crossref]

Zomer, A.

L. Ritsma, E. J. A. Steller, E. Beerling, C. J. M. Loomans, A. Zomer, C. Gerlach, N. Vrisekoop, D. Seinstra, L. van Gurp, R. Schafer, D. A. Raats, A. de Graaff, T. N. Schumacher, E. J. P. de Koning, O. Kranenburg, and J. van Rheenen, “Intravital Microscopy through an Abdominal Imaging Window Reveals Steps during Liver Metastasis,” Sci. Transl. Med. 4(158), 158ra145 (2012).
[Crossref] [PubMed]

Zwingman, T. A.

L. Madisen, T. A. Zwingman, S. M. Sunkin, S. W. Oh, H. A. Zariwala, H. Gu, L. L. Ng, R. D. Palmiter, M. J. Hawrylycz, A. R. Jones, E. S. Lein, and H. Zeng, “A robust and high-throughput Cre reporting and characterization system for the whole mouse brain,” Nat. Neurosci. 13(1), 133–140 (2010).
[Crossref] [PubMed]

Appl. Opt. (1)

Biomed. Opt. Express (2)

Cell (1)

H. Clevers, “The intestinal crypt, a prototype stem cell compartment,” Cell 154(2), 274–284 (2013).
[Crossref] [PubMed]

Front. Physiol. (1)

A. D. Corbett, R. A. B. Burton, G. Bub, P. S. Salter, S. Tuohy, M. J. Booth, and T. Wilson, “Quantifying distortions in two-photon remote focussing microscope images using a volumetric calibration specimen,” Front. Physiol. 5, 384 (2014).
[PubMed]

J. Biol. Chem. (1)

T. Hinoi, M. Loda, and E. R. Fearon, “Silencing of CDX2 expression in colon cancer via a dominant repression pathway,” J. Biol. Chem. 278(45), 44608–44616 (2003).
[Crossref] [PubMed]

J. Biomed. Opt. (2)

L. Fu, A. Jain, C. Cranfield, H. Xie, and M. Gu, “Three-dimensional nonlinear optical endoscopy,” J. Biomed. Opt. 12(4), 040501 (2007).
[Crossref] [PubMed]

Y. Wu, Y. Zhang, J. Xi, M.-J. Li, and X. Li, “Fiber-optic nonlinear endomicroscopy with focus scanning by using shape memory alloy actuation,” J. Biomed. Opt. 15(6), 060506 (2010).
[Crossref] [PubMed]

Methods Mol. Biol. (1)

A. Masedunskas, M. Sramkova, L. Parente, and R. Weigert, “Intravital Microscopy to Image Membrane Trafficking in Live Rats,” Methods Mol. Biol. 931, 153–167 (2012).
[Crossref] [PubMed]

Mol. Cell. Biol. (1)

E. K. Griffiths, O. Sanchez, P. Mill, C. Krawczyk, C. V. Hojilla, E. Rubin, M. M. Nau, R. Khokha, S. Lipkowitz, C. C. Hui, and J. M. Penninger, “Cbl-3-deficient mice exhibit normal epithelial development,” Mol. Cell. Biol. 23(21), 7708–7718 (2003).
[Crossref] [PubMed]

Nat. Methods (2)

W. Göbel, F. Helmchen, and B. M. Kampa, “Imaging cellular network dynamics in three dimensions using fast 3D laser scanning,” Nat. Methods 4(1), 73–79 (2007).
[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]

Nat. Neurosci. (1)

L. Madisen, T. A. Zwingman, S. M. Sunkin, S. W. Oh, H. A. Zariwala, H. Gu, L. L. Ng, R. D. Palmiter, M. J. Hawrylycz, A. R. Jones, E. S. Lein, and H. Zeng, “A robust and high-throughput Cre reporting and characterization system for the whole mouse brain,” Nat. Neurosci. 13(1), 133–140 (2010).
[Crossref] [PubMed]

Nature (1)

K. L. Turner, S. A. Miller, P. G. Hartwell, N. C. MacDonald, S. H. Strogatz, and S. G. Adams, “Five parametric resonances in a microelectromechanical system,” Nature 396(6707), 149–152 (1998).
[Crossref]

Opt. Express (3)

Opt. Lett. (4)

PLoS one (1)

S. J. Miller, B. P. Joshi, A. Gaustad, Y. Feng, E. R. Fearon, and T. D. Wang, “In vivo Fluorescence-Based Endoscopic Detection of Colon Dysplasia in the Mouse using a Novel Peptide Probe,” PLoS one 6(3), e17384 (2011).

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

E. J. Botcherby, C. W. Smith, M. M. Kohl, D. Débarre, M. J. Booth, R. Juškaitis, O. Paulsen, and T. Wilson, “Aberration-free three-dimensional multiphoton imaging of neuronal activity at kHz rates,” Proc. Natl. Acad. Sci. U.S.A. 109(8), 2919–2924 (2012).
[Crossref] [PubMed]

Sci. Rep. (1)

G. Ducourthial, P. Leclerc, T. Mansuryan, M. Fabert, J. Brevier, R. Habert, F. Braud, R. Batrin, C. Vever-Bizet, G. Bourg-Heckly, L. Thiberville, A. Druilhe, A. Kudlinski, and F. Louradour, “Development of a real-time flexible multiphoton microendoscope for label-free imaging in a live animal,” Sci. Rep. 5, 18303 (2015).
[Crossref] [PubMed]

Sci. Transl. Med. (1)

L. Ritsma, E. J. A. Steller, E. Beerling, C. J. M. Loomans, A. Zomer, C. Gerlach, N. Vrisekoop, D. Seinstra, L. van Gurp, R. Schafer, D. A. Raats, A. de Graaff, T. N. Schumacher, E. J. P. de Koning, O. Kranenburg, and J. van Rheenen, “Intravital Microscopy through an Abdominal Imaging Window Reveals Steps during Liver Metastasis,” Sci. Transl. Med. 4(158), 158ra145 (2012).
[Crossref] [PubMed]

Science (1)

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

Sens. Actuators (1)

Y. Zhu, W. Liu, K. Jia, W. Liao, and H. Xie, “A piezoelectric unimorph actuator based tip-tilt-piston micromirror with high fill factor and small tilt and lateral shift,” Sens. Actuators 167(2), 495–501 (2011).
[Crossref]

Sens. Actuators A Phys. (1)

K. Lee, K. Krisnamoorthy, K. Yu, and O. Solgaard, “Single-crystalline silicon micromirrors actuated by self-aligned vertical electrostatic comb drives with piston-motion and rotational capabilities,” Sens. Actuators A Phys. 114(2–3), 423–428 (2004).
[Crossref]

Skin Res. Technol. (1)

M. J. Koehler, T. Vogel, P. Elsner, K. König, R. Bückle, and M. Kaatz, “In vivo measurement of the human epidermal thickness in different localizations by multiphoton laser tomography,” Skin Res. Technol. 16(3), 259–264 (2010).
[PubMed]

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Figures (8)

Fig. 1
Fig. 1 (a) Schematic of multiphoton microscope. Compact, lightweight MEMS mirrors M1 and M2 are located remotely and used for lateral scanning and axial actuation, respectively. The mirrors translate the excitation wavefront between two objectives (Obj1 and Obj2) that introduce equal but opposite aberrations to produce axial scanning below the surface of the specimen. Key: HWP: half wave plate, LP: linear polarizer, PBS: polarizing beam splitter, QWP: quarter wave plate, L1-6: lenses, Obj1,2: objectives, M1-3: mirrors, DM: dichroic mirror, BPF: bandpass filter, PMT: photomultiplier tube. (b) Lateral MEMS scanner. Compact 2D device has a chip size of 3 × 3 mm2. The aluminum (Al) coated reflector has dimensions of 1.8 mm, and is mounted on a gimbal frame. Orthogonal electrostatic comb-drive actuators are coupled to inner and outer torsional springs to produce rapid Lissajous scanning.
Fig. 2
Fig. 2 – Performance of lateral MEMS scanner. Frequency response shows mechanical scan angles ≥5° for the (a) inner (X) and (b) outer (Y) axes. For imaging, we applied a sine wave at 60 Vpp in a downsweep (red) at drive frequencies of 8570 and 2100 Hz, respectively. The non-linear response of the scanner results from complex interactions in the springs, including electrostatic softening, mechanical hardening, and structural damping.
Fig. 3
Fig. 3 Axial MEMS actuator. (a) Compact device has a 2 mm diameter circular reflector actuated by two sets of U-shaped levers coupled to serpentine springs to produce large out-of-plane displacement when driven in phase. (b) For imaging, we applied a square wave at 60 Vpp in an upsweep (blue) at a drive frequency of 930 Hz to achieve vertical displacement >400 μm.
Fig. 4
Fig. 4 Axial scan. In the neutral position, the multiphoton excitation wavefront is imaged onto the focal plane at position Z = 0 µm, defined at a distance of 100 µm below the mucosal surface. (a) When the axial MEMS actuator M2 moves away from Obj2, the wavefront converges, and the focal plane moves upward axially to Z = −100 µm. (b) When M2 moves toward Obj2, the wavefront diverges, and the focal plane moves downward axially to Z = 100 µm.
Fig. 5
Fig. 5 Tilt angles of axial MEMS actuator. We measured (a) <0.004° and (b) and <0.19° in the X and Y axes, respectively, while translating a distance >400 μm at a drive frequency of 930 Hz.
Fig. 6
Fig. 6 Axial scan properties. (a) We found the position of M2 and depth of the focus to have a linear relationship with slope of 0.45 and P-value = 2x10−20. Axial resolution defined by FWHM varies from 4.5 to 7 μm over scan range. (b) We found the lateral magnification to range from 0.9 to 1.2 over relevant imaging depths with slope of −0.0016 and P-value = 1.35x10−14.
Fig. 7
Fig. 7 Multiphoton excited fluorescence images of pollen grains. (a) Horizontal (XY) image using lateral MEMS scanner. (b) Vertical (XZ) image was reconstructed from series of horizontal images along plane marked by red line in a). (c) Vertical (XZ) image collected directly using MEMS actuator. Comparing panels b) and c), we calculated a Pearson’s correlation coefficient of 0.897.
Fig. 8
Fig. 8 Imaging of mouse colonic epithelium ex vivo. Representative multiphoton excited fluorescence images in (a) horizontal (XY) and (b) vertical (XZ) planes from specimen expressing tdTomato reveal crypt structures. Key: crypt (arrow), lumen (l), goblet cells (g), cytoplasm (c), inflammatory cells (arrowhead), lamina propria (lp).

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