Abstract

Two-photon excitation fluorescence microscopy has revolutionized our understanding of brain structure and function through the high resolution and large penetration depth it offers. Investigating neural structures in vivo requires gaining optical access to the brain, which is typically achieved by replacing a part of the skull with one or several layers of cover glass windows. To compensate for the spherical aberrations caused by the presence of these layers of glass, collar-correction objectives are typically used. However, the efficiency of this correction has been shown to depend significantly on the tilt angle between the glass window surface and the optical axis of the imaging system. Here, we first expand these observations and characterize the effect of the tilt angle on the collected fluorescence signal with thicker windows (double cover slide) and compare these results with an objective devoid of collar-correction. Second, we present a simple optical alignment device designed to rapidly minimize the tilt angle in vivo and align the optical axis of the microscope perpendicularly to the glass window to an angle below 0.25°, thereby significantly improving the imaging quality. Finally, we describe a tilt-correction procedure for users in an in vivo setting, enabling the accurate alignment with a resolution of <0.2° in only few iterations.

© 2018 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

Full Article  |  PDF Article
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References

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    [Crossref] [PubMed]

2018 (2)

T. Ebina, Y. Masamizu, Y. R. Tanaka, A. Watakabe, R. Hirakawa, Y. Hirayama, R. Hira, S.-I. Terada, D. Koketsu, K. Hikosaka, H. Mizukami, A. Nambu, E. Sasaki, T. Yamamori, and M. Matsuzaki, “Two-photon imaging of neuronal activity in motor cortex of marmosets during upper-limb movement tasks,” Nat. Commun. 9, 1879 (2018).
[Crossref] [PubMed]

G. L. Galiñanes, C. Bonardi, and D. Huber, “Directional Reaching for Water as a Cortex-Dependent Behavioral Framework for Mice,” Cell Reports 22, 2601–2614 (2018).
[Crossref]

2017 (2)

2016 (1)

N. J. Sofroniew, D. Flickinger, J. King, and K. Svoboda, “A large field of view two-photon mesoscope with subcellular resolution for in vivo imaging,” eLife 5, 1–20 (2016).
[Crossref]

2015 (3)

2014 (1)

D. A. Boas and A. K. Dunn, “Laser speckle contrast imaging in biomedical optics,” J. Biomed. Opt. 15, 011109 (2014).
[Crossref]

2013 (1)

R. K. P. Benninger and D. W. Piston, “Two-Photon Excitation Microscopy for the Study of Living Cells and Tissues,” Current Protocols in Cell Biology 59, 1–24 (2013).
[Crossref]

2012 (2)

D. Huber, D. A. Gutnisky, S. Peron, D. H. O’Connor, J. S. Wiegert, L. Tian, T. G. Oertner, L. L. Looger, and K. Svoboda, “Multiple dynamic representations in the motor cortex during sensorimotor learning,” Nature 484, 473–478 (2012).
[Crossref] [PubMed]

T. Bolmont, A. Bouwens, C. Pache, M. Dimitrov, C. Berclaz, M. Villiger, B. M. Wegenast-Braun, T. Lasser, and P. C. Fraering, “Label-free imaging of cerebral β-amyloidosis with extended-focus optical coherence microscopy,” J. Neurosci. 32, 14548–14556 (2012).
[Crossref] [PubMed]

2011 (4)

S. Witte, A. Negrean, J. C. Lodder, C. P. J. de Kock, G. Testa Silva, H. D. Mansvelder, and M. L. Groota, “Label-free live brain imaging and targeted patching with third-harmonic generation microscopy,” Proc. Natl. Acad. Sci. U.S.A 108, 5970–5975 (2011).
[Crossref] [PubMed]

J. Binding, J. Ben Arous, J.-F. Léger, S. Gigan, C. Boccara, and L. Bourdieu, “Brain refractive index measured in vivo with high-NA defocus-corrected full-field OCT and consequences for two-photon microscopy,” Opt. Express 19, 4833 (2011).
[Crossref] [PubMed]

M. L. Andermann, A. M. Kerlin, D. K. Roumis, L. L. Glickfeld, and R. C. Reid, “Functional specialization of mouse higher visual cortical areas,” Neuron 72, 1025–1039 (2011).
[Crossref] [PubMed]

M. R. Looney, E. E. Thornton, D. Sen, W. J. Lamm, R. W. Glenny, and M. F. Krummel, “Stabilized imaging of immune surveillance in the mouse lung,” Nat. Methods 8, 91–96 (2011).
[Crossref]

2010 (3)

N. Olivier, M. A. Luengo-Oroz, L. Duloquin, E. Faure, T. Savy, I. Veilleux, X. Solinas, D. Débarre, P. Bourgine, A. Santos, N. Peyriéras, and E. Beaurepaire, “Cell Lineage Reconstruction of Early zebrafish embryos using label-free nonlinear microscopy,” Science 329, 967–971 (2010).
[Crossref] [PubMed]

R. Imamura, Y. Isaka, R. M. Sandoval, A. Ori, S. Adamsky, E. Feinstein, B. A. Molitoris, and S. Takahara, “Intravital two-photon microscopy assessment of renal protection efficacy of siRNA for p53 in experimental rat kidney transplantation models,” Cell Transplantation 19, 1659–1670 (2010).
[Crossref] [PubMed]

R. S. Friedman, P. Beemiller, C. M. Sorensen, J. Jacobelli, and M. F. Krummel, “Real-time analysis of T cell receptors in naive cells in vitro and in vivo reveals flexibility in synapse and signaling dynamics,” J. Exp. Med. 207, 2733–2749 (2010).
[Crossref] [PubMed]

2009 (2)

A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W. A. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, and L. Wilbrecht, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4, 19–22 (2009).
[Crossref]

M. B. Bouchard, B. R. Chen, S. A. Burgess, and E. M. C. Hillman, “Ultra-fast multispectral optical imaging of cortical oxygenation, blood flow, and intracellular calcium dynamics,” Opt. Express 17, 15670–15678 (2009).
[Crossref] [PubMed]

2008 (1)

P. A. Muriello and K. W. Dunn, “Improving signal levels in intravital multiphoton microscopy using an objective correction collar,” Opt. Commun. 281, 1806–1812 (2008).
[Crossref]

2006 (1)

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

1998 (1)

D. Kleinfeld, P. P. Mitra, F. Helmchen, and W. Denk, “Fluctuations and stimulus-induced changes in blood flow observed in individual capillaries in layers 2 through 4 of rat neocortex,” Proc. Natl. Acad. Sci. U.S.A 95, 15741–15746 (1998).
[Crossref] [PubMed]

1994 (1)

H. Jacobsen, P. Hanninen, E. Soini, and S. W. Hell, “Refractive-index-induced aberrations in two-photon confocal fluorescence microscopy,” J. Microsc. 176, 226–230 (1994).
[Crossref]

1993 (1)

S. Hell, G. Reiner, C. Cremer, and E. H. K. Stelzer, “Aberrations in confocal fluorescence microscopy induced by mismatches in refractive index,” J. Microsc. 169, 391–405 (1993).
[Crossref]

1990 (1)

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

Adamsky, S.

R. Imamura, Y. Isaka, R. M. Sandoval, A. Ori, S. Adamsky, E. Feinstein, B. A. Molitoris, and S. Takahara, “Intravital two-photon microscopy assessment of renal protection efficacy of siRNA for p53 in experimental rat kidney transplantation models,” Cell Transplantation 19, 1659–1670 (2010).
[Crossref] [PubMed]

Andermann, M. L.

M. L. Andermann, A. M. Kerlin, D. K. Roumis, L. L. Glickfeld, and R. C. Reid, “Functional specialization of mouse higher visual cortical areas,” Neuron 72, 1025–1039 (2011).
[Crossref] [PubMed]

Barrett, M. J. P.

Beaurepaire, E.

N. Olivier, M. A. Luengo-Oroz, L. Duloquin, E. Faure, T. Savy, I. Veilleux, X. Solinas, D. Débarre, P. Bourgine, A. Santos, N. Peyriéras, and E. Beaurepaire, “Cell Lineage Reconstruction of Early zebrafish embryos using label-free nonlinear microscopy,” Science 329, 967–971 (2010).
[Crossref] [PubMed]

Beemiller, P.

R. S. Friedman, P. Beemiller, C. M. Sorensen, J. Jacobelli, and M. F. Krummel, “Real-time analysis of T cell receptors in naive cells in vitro and in vivo reveals flexibility in synapse and signaling dynamics,” J. Exp. Med. 207, 2733–2749 (2010).
[Crossref] [PubMed]

Ben Arous, J.

Benninger, R. K. P.

R. K. P. Benninger and D. W. Piston, “Two-Photon Excitation Microscopy for the Study of Living Cells and Tissues,” Current Protocols in Cell Biology 59, 1–24 (2013).
[Crossref]

Berclaz, C.

T. Bolmont, A. Bouwens, C. Pache, M. Dimitrov, C. Berclaz, M. Villiger, B. M. Wegenast-Braun, T. Lasser, and P. C. Fraering, “Label-free imaging of cerebral β-amyloidosis with extended-focus optical coherence microscopy,” J. Neurosci. 32, 14548–14556 (2012).
[Crossref] [PubMed]

Binding, J.

Boas, D. A.

D. A. Boas and A. K. Dunn, “Laser speckle contrast imaging in biomedical optics,” J. Biomed. Opt. 15, 011109 (2014).
[Crossref]

Boccara, C.

Bolmont, T.

T. Bolmont, A. Bouwens, C. Pache, M. Dimitrov, C. Berclaz, M. Villiger, B. M. Wegenast-Braun, T. Lasser, and P. C. Fraering, “Label-free imaging of cerebral β-amyloidosis with extended-focus optical coherence microscopy,” J. Neurosci. 32, 14548–14556 (2012).
[Crossref] [PubMed]

Bonardi, C.

G. L. Galiñanes, C. Bonardi, and D. Huber, “Directional Reaching for Water as a Cortex-Dependent Behavioral Framework for Mice,” Cell Reports 22, 2601–2614 (2018).
[Crossref]

Bonhoeffer, T.

A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W. A. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, and L. Wilbrecht, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4, 19–22 (2009).
[Crossref]

Bouchard, M. B.

Bourdieu, L.

Bourgine, P.

N. Olivier, M. A. Luengo-Oroz, L. Duloquin, E. Faure, T. Savy, I. Veilleux, X. Solinas, D. Débarre, P. Bourgine, A. Santos, N. Peyriéras, and E. Beaurepaire, “Cell Lineage Reconstruction of Early zebrafish embryos using label-free nonlinear microscopy,” Science 329, 967–971 (2010).
[Crossref] [PubMed]

Bouwens, A.

T. Bolmont, A. Bouwens, C. Pache, M. Dimitrov, C. Berclaz, M. Villiger, B. M. Wegenast-Braun, T. Lasser, and P. C. Fraering, “Label-free imaging of cerebral β-amyloidosis with extended-focus optical coherence microscopy,” J. Neurosci. 32, 14548–14556 (2012).
[Crossref] [PubMed]

Burgess, S. A.

Chen, B. R.

Chow, D. K.

A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W. A. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, and L. Wilbrecht, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4, 19–22 (2009).
[Crossref]

Chuckowree, J.

A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W. A. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, and L. Wilbrecht, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4, 19–22 (2009).
[Crossref]

Cremer, C.

S. Hell, G. Reiner, C. Cremer, and E. H. K. Stelzer, “Aberrations in confocal fluorescence microscopy induced by mismatches in refractive index,” J. Microsc. 169, 391–405 (1993).
[Crossref]

de Kock, C. P. J.

S. Witte, A. Negrean, J. C. Lodder, C. P. J. de Kock, G. Testa Silva, H. D. Mansvelder, and M. L. Groota, “Label-free live brain imaging and targeted patching with third-harmonic generation microscopy,” Proc. Natl. Acad. Sci. U.S.A 108, 5970–5975 (2011).
[Crossref] [PubMed]

De Paola, V.

A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W. A. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, and L. Wilbrecht, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4, 19–22 (2009).
[Crossref]

Débarre, D.

N. Olivier, M. A. Luengo-Oroz, L. Duloquin, E. Faure, T. Savy, I. Veilleux, X. Solinas, D. Débarre, P. Bourgine, A. Santos, N. Peyriéras, and E. Beaurepaire, “Cell Lineage Reconstruction of Early zebrafish embryos using label-free nonlinear microscopy,” Science 329, 967–971 (2010).
[Crossref] [PubMed]

Denk, W.

D. Kleinfeld, P. P. Mitra, F. Helmchen, and W. Denk, “Fluctuations and stimulus-induced changes in blood flow observed in individual capillaries in layers 2 through 4 of rat neocortex,” Proc. Natl. Acad. Sci. U.S.A 95, 15741–15746 (1998).
[Crossref] [PubMed]

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

Dimitrov, M.

T. Bolmont, A. Bouwens, C. Pache, M. Dimitrov, C. Berclaz, M. Villiger, B. M. Wegenast-Braun, T. Lasser, and P. C. Fraering, “Label-free imaging of cerebral β-amyloidosis with extended-focus optical coherence microscopy,” J. Neurosci. 32, 14548–14556 (2012).
[Crossref] [PubMed]

Duloquin, L.

N. Olivier, M. A. Luengo-Oroz, L. Duloquin, E. Faure, T. Savy, I. Veilleux, X. Solinas, D. Débarre, P. Bourgine, A. Santos, N. Peyriéras, and E. Beaurepaire, “Cell Lineage Reconstruction of Early zebrafish embryos using label-free nonlinear microscopy,” Science 329, 967–971 (2010).
[Crossref] [PubMed]

Dunn, A. K.

D. A. Boas and A. K. Dunn, “Laser speckle contrast imaging in biomedical optics,” J. Biomed. Opt. 15, 011109 (2014).
[Crossref]

Dunn, K. W.

P. A. Muriello and K. W. Dunn, “Improving signal levels in intravital multiphoton microscopy using an objective correction collar,” Opt. Commun. 281, 1806–1812 (2008).
[Crossref]

Ebina, T.

T. Ebina, Y. Masamizu, Y. R. Tanaka, A. Watakabe, R. Hirakawa, Y. Hirayama, R. Hira, S.-I. Terada, D. Koketsu, K. Hikosaka, H. Mizukami, A. Nambu, E. Sasaki, T. Yamamori, and M. Matsuzaki, “Two-photon imaging of neuronal activity in motor cortex of marmosets during upper-limb movement tasks,” Nat. Commun. 9, 1879 (2018).
[Crossref] [PubMed]

Fang, Y.

Faure, E.

N. Olivier, M. A. Luengo-Oroz, L. Duloquin, E. Faure, T. Savy, I. Veilleux, X. Solinas, D. Débarre, P. Bourgine, A. Santos, N. Peyriéras, and E. Beaurepaire, “Cell Lineage Reconstruction of Early zebrafish embryos using label-free nonlinear microscopy,” Science 329, 967–971 (2010).
[Crossref] [PubMed]

Feinstein, E.

R. Imamura, Y. Isaka, R. M. Sandoval, A. Ori, S. Adamsky, E. Feinstein, B. A. Molitoris, and S. Takahara, “Intravital two-photon microscopy assessment of renal protection efficacy of siRNA for p53 in experimental rat kidney transplantation models,” Cell Transplantation 19, 1659–1670 (2010).
[Crossref] [PubMed]

Ferrari, K. D.

Flickinger, D.

N. J. Sofroniew, D. Flickinger, J. King, and K. Svoboda, “A large field of view two-photon mesoscope with subcellular resolution for in vivo imaging,” eLife 5, 1–20 (2016).
[Crossref]

Fraering, P. C.

T. Bolmont, A. Bouwens, C. Pache, M. Dimitrov, C. Berclaz, M. Villiger, B. M. Wegenast-Braun, T. Lasser, and P. C. Fraering, “Label-free imaging of cerebral β-amyloidosis with extended-focus optical coherence microscopy,” J. Neurosci. 32, 14548–14556 (2012).
[Crossref] [PubMed]

Friedman, R. S.

R. S. Friedman, P. Beemiller, C. M. Sorensen, J. Jacobelli, and M. F. Krummel, “Real-time analysis of T cell receptors in naive cells in vitro and in vivo reveals flexibility in synapse and signaling dynamics,” J. Exp. Med. 207, 2733–2749 (2010).
[Crossref] [PubMed]

Galiñanes, G. L.

G. L. Galiñanes, C. Bonardi, and D. Huber, “Directional Reaching for Water as a Cortex-Dependent Behavioral Framework for Mice,” Cell Reports 22, 2601–2614 (2018).
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Glenny, R. W.

M. R. Looney, E. E. Thornton, D. Sen, W. J. Lamm, R. W. Glenny, and M. F. Krummel, “Stabilized imaging of immune surveillance in the mouse lung,” Nat. Methods 8, 91–96 (2011).
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M. L. Andermann, A. M. Kerlin, D. K. Roumis, L. L. Glickfeld, and R. C. Reid, “Functional specialization of mouse higher visual cortical areas,” Neuron 72, 1025–1039 (2011).
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S. Witte, A. Negrean, J. C. Lodder, C. P. J. de Kock, G. Testa Silva, H. D. Mansvelder, and M. L. Groota, “Label-free live brain imaging and targeted patching with third-harmonic generation microscopy,” Proc. Natl. Acad. Sci. U.S.A 108, 5970–5975 (2011).
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D. Huber, D. A. Gutnisky, S. Peron, D. H. O’Connor, J. S. Wiegert, L. Tian, T. G. Oertner, L. L. Looger, and K. Svoboda, “Multiple dynamic representations in the motor cortex during sensorimotor learning,” Nature 484, 473–478 (2012).
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Haiss, F.

Hall, A.

Hanninen, P.

H. Jacobsen, P. Hanninen, E. Soini, and S. W. Hell, “Refractive-index-induced aberrations in two-photon confocal fluorescence microscopy,” J. Microsc. 176, 226–230 (1994).
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S. Hell, G. Reiner, C. Cremer, and E. H. K. Stelzer, “Aberrations in confocal fluorescence microscopy induced by mismatches in refractive index,” J. Microsc. 169, 391–405 (1993).
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Hell, S. W.

H. Jacobsen, P. Hanninen, E. Soini, and S. W. Hell, “Refractive-index-induced aberrations in two-photon confocal fluorescence microscopy,” J. Microsc. 176, 226–230 (1994).
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Helmchen, F.

D. Kleinfeld, P. P. Mitra, F. Helmchen, and W. Denk, “Fluctuations and stimulus-induced changes in blood flow observed in individual capillaries in layers 2 through 4 of rat neocortex,” Proc. Natl. Acad. Sci. U.S.A 95, 15741–15746 (1998).
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Hikosaka, K.

T. Ebina, Y. Masamizu, Y. R. Tanaka, A. Watakabe, R. Hirakawa, Y. Hirayama, R. Hira, S.-I. Terada, D. Koketsu, K. Hikosaka, H. Mizukami, A. Nambu, E. Sasaki, T. Yamamori, and M. Matsuzaki, “Two-photon imaging of neuronal activity in motor cortex of marmosets during upper-limb movement tasks,” Nat. Commun. 9, 1879 (2018).
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Hillman, E. M. C.

Hira, R.

T. Ebina, Y. Masamizu, Y. R. Tanaka, A. Watakabe, R. Hirakawa, Y. Hirayama, R. Hira, S.-I. Terada, D. Koketsu, K. Hikosaka, H. Mizukami, A. Nambu, E. Sasaki, T. Yamamori, and M. Matsuzaki, “Two-photon imaging of neuronal activity in motor cortex of marmosets during upper-limb movement tasks,” Nat. Commun. 9, 1879 (2018).
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Hirakawa, R.

T. Ebina, Y. Masamizu, Y. R. Tanaka, A. Watakabe, R. Hirakawa, Y. Hirayama, R. Hira, S.-I. Terada, D. Koketsu, K. Hikosaka, H. Mizukami, A. Nambu, E. Sasaki, T. Yamamori, and M. Matsuzaki, “Two-photon imaging of neuronal activity in motor cortex of marmosets during upper-limb movement tasks,” Nat. Commun. 9, 1879 (2018).
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T. Ebina, Y. Masamizu, Y. R. Tanaka, A. Watakabe, R. Hirakawa, Y. Hirayama, R. Hira, S.-I. Terada, D. Koketsu, K. Hikosaka, H. Mizukami, A. Nambu, E. Sasaki, T. Yamamori, and M. Matsuzaki, “Two-photon imaging of neuronal activity in motor cortex of marmosets during upper-limb movement tasks,” Nat. Commun. 9, 1879 (2018).
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A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W. A. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, and L. Wilbrecht, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4, 19–22 (2009).
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A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W. A. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, and L. Wilbrecht, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4, 19–22 (2009).
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A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W. A. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, and L. Wilbrecht, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4, 19–22 (2009).
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Huber, D.

G. L. Galiñanes, C. Bonardi, and D. Huber, “Directional Reaching for Water as a Cortex-Dependent Behavioral Framework for Mice,” Cell Reports 22, 2601–2614 (2018).
[Crossref]

D. Huber, D. A. Gutnisky, S. Peron, D. H. O’Connor, J. S. Wiegert, L. Tian, T. G. Oertner, L. L. Looger, and K. Svoboda, “Multiple dynamic representations in the motor cortex during sensorimotor learning,” Nature 484, 473–478 (2012).
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Imamura, R.

R. Imamura, Y. Isaka, R. M. Sandoval, A. Ori, S. Adamsky, E. Feinstein, B. A. Molitoris, and S. Takahara, “Intravital two-photon microscopy assessment of renal protection efficacy of siRNA for p53 in experimental rat kidney transplantation models,” Cell Transplantation 19, 1659–1670 (2010).
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Isaka, Y.

R. Imamura, Y. Isaka, R. M. Sandoval, A. Ori, S. Adamsky, E. Feinstein, B. A. Molitoris, and S. Takahara, “Intravital two-photon microscopy assessment of renal protection efficacy of siRNA for p53 in experimental rat kidney transplantation models,” Cell Transplantation 19, 1659–1670 (2010).
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Jacobelli, J.

R. S. Friedman, P. Beemiller, C. M. Sorensen, J. Jacobelli, and M. F. Krummel, “Real-time analysis of T cell receptors in naive cells in vitro and in vivo reveals flexibility in synapse and signaling dynamics,” J. Exp. Med. 207, 2733–2749 (2010).
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Jacobsen, H.

H. Jacobsen, P. Hanninen, E. Soini, and S. W. Hell, “Refractive-index-induced aberrations in two-photon confocal fluorescence microscopy,” J. Microsc. 176, 226–230 (1994).
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Johannssen, H.

Kanazawa, S.

Kawakami, R.

Kawasaki, H.

O. Sadakane, Y. Masamizu, A. Watakabe, S. I. Terada, M. Ohtsuka, M. Takaji, H. Mizukami, K. Ozawa, H. Kawasaki, M. Matsuzaki, and T. Yamamori, “Long-Term Two-Photon Calcium Imaging of Neuronal Populations with Subcellular Resolution in Adult Non-human Primates,” Cell Reports 13, 1989–1999 (2015).
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A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W. A. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, and L. Wilbrecht, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4, 19–22 (2009).
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Kerlin, A. M.

M. L. Andermann, A. M. Kerlin, D. K. Roumis, L. L. Glickfeld, and R. C. Reid, “Functional specialization of mouse higher visual cortical areas,” Neuron 72, 1025–1039 (2011).
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King, J.

N. J. Sofroniew, D. Flickinger, J. King, and K. Svoboda, “A large field of view two-photon mesoscope with subcellular resolution for in vivo imaging,” eLife 5, 1–20 (2016).
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Kleinfeld, D.

D. Kleinfeld, P. P. Mitra, F. Helmchen, and W. Denk, “Fluctuations and stimulus-induced changes in blood flow observed in individual capillaries in layers 2 through 4 of rat neocortex,” Proc. Natl. Acad. Sci. U.S.A 95, 15741–15746 (1998).
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Knott, G.

A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W. A. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, and L. Wilbrecht, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4, 19–22 (2009).
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Koketsu, D.

T. Ebina, Y. Masamizu, Y. R. Tanaka, A. Watakabe, R. Hirakawa, Y. Hirayama, R. Hira, S.-I. Terada, D. Koketsu, K. Hikosaka, H. Mizukami, A. Nambu, E. Sasaki, T. Yamamori, and M. Matsuzaki, “Two-photon imaging of neuronal activity in motor cortex of marmosets during upper-limb movement tasks,” Nat. Commun. 9, 1879 (2018).
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Kozawa, Y.

Krummel, M. F.

M. R. Looney, E. E. Thornton, D. Sen, W. J. Lamm, R. W. Glenny, and M. F. Krummel, “Stabilized imaging of immune surveillance in the mouse lung,” Nat. Methods 8, 91–96 (2011).
[Crossref]

R. S. Friedman, P. Beemiller, C. M. Sorensen, J. Jacobelli, and M. F. Krummel, “Real-time analysis of T cell receptors in naive cells in vitro and in vivo reveals flexibility in synapse and signaling dynamics,” J. Exp. Med. 207, 2733–2749 (2010).
[Crossref] [PubMed]

Kusama, Y.

Lamm, W. J.

M. R. Looney, E. E. Thornton, D. Sen, W. J. Lamm, R. W. Glenny, and M. F. Krummel, “Stabilized imaging of immune surveillance in the mouse lung,” Nat. Methods 8, 91–96 (2011).
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Larkum, M. E.

Lasser, T.

T. Bolmont, A. Bouwens, C. Pache, M. Dimitrov, C. Berclaz, M. Villiger, B. M. Wegenast-Braun, T. Lasser, and P. C. Fraering, “Label-free imaging of cerebral β-amyloidosis with extended-focus optical coherence microscopy,” J. Neurosci. 32, 14548–14556 (2012).
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Lee, W. A.

A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W. A. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, and L. Wilbrecht, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4, 19–22 (2009).
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Léger, J.-F.

Liang, Y.

Lodder, J. C.

S. Witte, A. Negrean, J. C. Lodder, C. P. J. de Kock, G. Testa Silva, H. D. Mansvelder, and M. L. Groota, “Label-free live brain imaging and targeted patching with third-harmonic generation microscopy,” Proc. Natl. Acad. Sci. U.S.A 108, 5970–5975 (2011).
[Crossref] [PubMed]

Looger, L. L.

D. Huber, D. A. Gutnisky, S. Peron, D. H. O’Connor, J. S. Wiegert, L. Tian, T. G. Oertner, L. L. Looger, and K. Svoboda, “Multiple dynamic representations in the motor cortex during sensorimotor learning,” Nature 484, 473–478 (2012).
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Looney, M. R.

M. R. Looney, E. E. Thornton, D. Sen, W. J. Lamm, R. W. Glenny, and M. F. Krummel, “Stabilized imaging of immune surveillance in the mouse lung,” Nat. Methods 8, 91–96 (2011).
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Luengo-Oroz, M. A.

N. Olivier, M. A. Luengo-Oroz, L. Duloquin, E. Faure, T. Savy, I. Veilleux, X. Solinas, D. Débarre, P. Bourgine, A. Santos, N. Peyriéras, and E. Beaurepaire, “Cell Lineage Reconstruction of Early zebrafish embryos using label-free nonlinear microscopy,” Science 329, 967–971 (2010).
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Maechler, P.

Mansvelder, H. D.

S. Witte, A. Negrean, J. C. Lodder, C. P. J. de Kock, G. Testa Silva, H. D. Mansvelder, and M. L. Groota, “Label-free live brain imaging and targeted patching with third-harmonic generation microscopy,” Proc. Natl. Acad. Sci. U.S.A 108, 5970–5975 (2011).
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T. Ebina, Y. Masamizu, Y. R. Tanaka, A. Watakabe, R. Hirakawa, Y. Hirayama, R. Hira, S.-I. Terada, D. Koketsu, K. Hikosaka, H. Mizukami, A. Nambu, E. Sasaki, T. Yamamori, and M. Matsuzaki, “Two-photon imaging of neuronal activity in motor cortex of marmosets during upper-limb movement tasks,” Nat. Commun. 9, 1879 (2018).
[Crossref] [PubMed]

O. Sadakane, Y. Masamizu, A. Watakabe, S. I. Terada, M. Ohtsuka, M. Takaji, H. Mizukami, K. Ozawa, H. Kawasaki, M. Matsuzaki, and T. Yamamori, “Long-Term Two-Photon Calcium Imaging of Neuronal Populations with Subcellular Resolution in Adult Non-human Primates,” Cell Reports 13, 1989–1999 (2015).
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Matsuzaki, M.

T. Ebina, Y. Masamizu, Y. R. Tanaka, A. Watakabe, R. Hirakawa, Y. Hirayama, R. Hira, S.-I. Terada, D. Koketsu, K. Hikosaka, H. Mizukami, A. Nambu, E. Sasaki, T. Yamamori, and M. Matsuzaki, “Two-photon imaging of neuronal activity in motor cortex of marmosets during upper-limb movement tasks,” Nat. Commun. 9, 1879 (2018).
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O. Sadakane, Y. Masamizu, A. Watakabe, S. I. Terada, M. Ohtsuka, M. Takaji, H. Mizukami, K. Ozawa, H. Kawasaki, M. Matsuzaki, and T. Yamamori, “Long-Term Two-Photon Calcium Imaging of Neuronal Populations with Subcellular Resolution in Adult Non-human Primates,” Cell Reports 13, 1989–1999 (2015).
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Mayrhofer, J. M.

Mitra, P. P.

D. Kleinfeld, P. P. Mitra, F. Helmchen, and W. Denk, “Fluctuations and stimulus-induced changes in blood flow observed in individual capillaries in layers 2 through 4 of rat neocortex,” Proc. Natl. Acad. Sci. U.S.A 95, 15741–15746 (1998).
[Crossref] [PubMed]

Mizukami, H.

T. Ebina, Y. Masamizu, Y. R. Tanaka, A. Watakabe, R. Hirakawa, Y. Hirayama, R. Hira, S.-I. Terada, D. Koketsu, K. Hikosaka, H. Mizukami, A. Nambu, E. Sasaki, T. Yamamori, and M. Matsuzaki, “Two-photon imaging of neuronal activity in motor cortex of marmosets during upper-limb movement tasks,” Nat. Commun. 9, 1879 (2018).
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O. Sadakane, Y. Masamizu, A. Watakabe, S. I. Terada, M. Ohtsuka, M. Takaji, H. Mizukami, K. Ozawa, H. Kawasaki, M. Matsuzaki, and T. Yamamori, “Long-Term Two-Photon Calcium Imaging of Neuronal Populations with Subcellular Resolution in Adult Non-human Primates,” Cell Reports 13, 1989–1999 (2015).
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Molitoris, B. A.

R. Imamura, Y. Isaka, R. M. Sandoval, A. Ori, S. Adamsky, E. Feinstein, B. A. Molitoris, and S. Takahara, “Intravital two-photon microscopy assessment of renal protection efficacy of siRNA for p53 in experimental rat kidney transplantation models,” Cell Transplantation 19, 1659–1670 (2010).
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Mostany, R.

A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W. A. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, and L. Wilbrecht, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4, 19–22 (2009).
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Mrsic-Flogel, T. D.

A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W. A. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, and L. Wilbrecht, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4, 19–22 (2009).
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P. A. Muriello and K. W. Dunn, “Improving signal levels in intravital multiphoton microscopy using an objective correction collar,” Opt. Commun. 281, 1806–1812 (2008).
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Nambu, A.

T. Ebina, Y. Masamizu, Y. R. Tanaka, A. Watakabe, R. Hirakawa, Y. Hirayama, R. Hira, S.-I. Terada, D. Koketsu, K. Hikosaka, H. Mizukami, A. Nambu, E. Sasaki, T. Yamamori, and M. Matsuzaki, “Two-photon imaging of neuronal activity in motor cortex of marmosets during upper-limb movement tasks,” Nat. Commun. 9, 1879 (2018).
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Nedivi, E.

A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W. A. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, and L. Wilbrecht, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4, 19–22 (2009).
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Negrean, A.

S. Witte, A. Negrean, J. C. Lodder, C. P. J. de Kock, G. Testa Silva, H. D. Mansvelder, and M. L. Groota, “Label-free live brain imaging and targeted patching with third-harmonic generation microscopy,” Proc. Natl. Acad. Sci. U.S.A 108, 5970–5975 (2011).
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Nemoto, T.

O’Connor, D. H.

D. Huber, D. A. Gutnisky, S. Peron, D. H. O’Connor, J. S. Wiegert, L. Tian, T. G. Oertner, L. L. Looger, and K. Svoboda, “Multiple dynamic representations in the motor cortex during sensorimotor learning,” Nature 484, 473–478 (2012).
[Crossref] [PubMed]

Oertner, T. G.

D. Huber, D. A. Gutnisky, S. Peron, D. H. O’Connor, J. S. Wiegert, L. Tian, T. G. Oertner, L. L. Looger, and K. Svoboda, “Multiple dynamic representations in the motor cortex during sensorimotor learning,” Nature 484, 473–478 (2012).
[Crossref] [PubMed]

Ohtsuka, M.

O. Sadakane, Y. Masamizu, A. Watakabe, S. I. Terada, M. Ohtsuka, M. Takaji, H. Mizukami, K. Ozawa, H. Kawasaki, M. Matsuzaki, and T. Yamamori, “Long-Term Two-Photon Calcium Imaging of Neuronal Populations with Subcellular Resolution in Adult Non-human Primates,” Cell Reports 13, 1989–1999 (2015).
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Olivier, N.

N. Olivier, M. A. Luengo-Oroz, L. Duloquin, E. Faure, T. Savy, I. Veilleux, X. Solinas, D. Débarre, P. Bourgine, A. Santos, N. Peyriéras, and E. Beaurepaire, “Cell Lineage Reconstruction of Early zebrafish embryos using label-free nonlinear microscopy,” Science 329, 967–971 (2010).
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Ori, A.

R. Imamura, Y. Isaka, R. M. Sandoval, A. Ori, S. Adamsky, E. Feinstein, B. A. Molitoris, and S. Takahara, “Intravital two-photon microscopy assessment of renal protection efficacy of siRNA for p53 in experimental rat kidney transplantation models,” Cell Transplantation 19, 1659–1670 (2010).
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Osswald, H.

Ozawa, K.

O. Sadakane, Y. Masamizu, A. Watakabe, S. I. Terada, M. Ohtsuka, M. Takaji, H. Mizukami, K. Ozawa, H. Kawasaki, M. Matsuzaki, and T. Yamamori, “Long-Term Two-Photon Calcium Imaging of Neuronal Populations with Subcellular Resolution in Adult Non-human Primates,” Cell Reports 13, 1989–1999 (2015).
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Pache, C.

T. Bolmont, A. Bouwens, C. Pache, M. Dimitrov, C. Berclaz, M. Villiger, B. M. Wegenast-Braun, T. Lasser, and P. C. Fraering, “Label-free imaging of cerebral β-amyloidosis with extended-focus optical coherence microscopy,” J. Neurosci. 32, 14548–14556 (2012).
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Palmer, L. M.

Peron, S.

D. Huber, D. A. Gutnisky, S. Peron, D. H. O’Connor, J. S. Wiegert, L. Tian, T. G. Oertner, L. L. Looger, and K. Svoboda, “Multiple dynamic representations in the motor cortex during sensorimotor learning,” Nature 484, 473–478 (2012).
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Peyriéras, N.

N. Olivier, M. A. Luengo-Oroz, L. Duloquin, E. Faure, T. Savy, I. Veilleux, X. Solinas, D. Débarre, P. Bourgine, A. Santos, N. Peyriéras, and E. Beaurepaire, “Cell Lineage Reconstruction of Early zebrafish embryos using label-free nonlinear microscopy,” Science 329, 967–971 (2010).
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R. K. P. Benninger and D. W. Piston, “Two-Photon Excitation Microscopy for the Study of Living Cells and Tissues,” Current Protocols in Cell Biology 59, 1–24 (2013).
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Portera-Cailliau, C.

A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W. A. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, and L. Wilbrecht, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4, 19–22 (2009).
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Reid, R. C.

M. L. Andermann, A. M. Kerlin, D. K. Roumis, L. L. Glickfeld, and R. C. Reid, “Functional specialization of mouse higher visual cortical areas,” Neuron 72, 1025–1039 (2011).
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Reiner, G.

S. Hell, G. Reiner, C. Cremer, and E. H. K. Stelzer, “Aberrations in confocal fluorescence microscopy induced by mismatches in refractive index,” J. Microsc. 169, 391–405 (1993).
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Revol, V.

Roumis, D. K.

M. L. Andermann, A. M. Kerlin, D. K. Roumis, L. L. Glickfeld, and R. C. Reid, “Functional specialization of mouse higher visual cortical areas,” Neuron 72, 1025–1039 (2011).
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Rutz-Innerhofer, E.

Saab, A. S.

Sadakane, O.

O. Sadakane, Y. Masamizu, A. Watakabe, S. I. Terada, M. Ohtsuka, M. Takaji, H. Mizukami, K. Ozawa, H. Kawasaki, M. Matsuzaki, and T. Yamamori, “Long-Term Two-Photon Calcium Imaging of Neuronal Populations with Subcellular Resolution in Adult Non-human Primates,” Cell Reports 13, 1989–1999 (2015).
[Crossref] [PubMed]

Sandoval, R. M.

R. Imamura, Y. Isaka, R. M. Sandoval, A. Ori, S. Adamsky, E. Feinstein, B. A. Molitoris, and S. Takahara, “Intravital two-photon microscopy assessment of renal protection efficacy of siRNA for p53 in experimental rat kidney transplantation models,” Cell Transplantation 19, 1659–1670 (2010).
[Crossref] [PubMed]

Santos, A.

N. Olivier, M. A. Luengo-Oroz, L. Duloquin, E. Faure, T. Savy, I. Veilleux, X. Solinas, D. Débarre, P. Bourgine, A. Santos, N. Peyriéras, and E. Beaurepaire, “Cell Lineage Reconstruction of Early zebrafish embryos using label-free nonlinear microscopy,” Science 329, 967–971 (2010).
[Crossref] [PubMed]

Sasaki, E.

T. Ebina, Y. Masamizu, Y. R. Tanaka, A. Watakabe, R. Hirakawa, Y. Hirayama, R. Hira, S.-I. Terada, D. Koketsu, K. Hikosaka, H. Mizukami, A. Nambu, E. Sasaki, T. Yamamori, and M. Matsuzaki, “Two-photon imaging of neuronal activity in motor cortex of marmosets during upper-limb movement tasks,” Nat. Commun. 9, 1879 (2018).
[Crossref] [PubMed]

Sato, S.

Savy, T.

N. Olivier, M. A. Luengo-Oroz, L. Duloquin, E. Faure, T. Savy, I. Veilleux, X. Solinas, D. Débarre, P. Bourgine, A. Santos, N. Peyriéras, and E. Beaurepaire, “Cell Lineage Reconstruction of Early zebrafish embryos using label-free nonlinear microscopy,” Science 329, 967–971 (2010).
[Crossref] [PubMed]

Sawada, K.

Schuh, C.-D.

Sen, D.

M. R. Looney, E. E. Thornton, D. Sen, W. J. Lamm, R. W. Glenny, and M. F. Krummel, “Stabilized imaging of immune surveillance in the mouse lung,” Nat. Methods 8, 91–96 (2011).
[Crossref]

Sofroniew, N. J.

N. J. Sofroniew, D. Flickinger, J. King, and K. Svoboda, “A large field of view two-photon mesoscope with subcellular resolution for in vivo imaging,” eLife 5, 1–20 (2016).
[Crossref]

Soini, E.

H. Jacobsen, P. Hanninen, E. Soini, and S. W. Hell, “Refractive-index-induced aberrations in two-photon confocal fluorescence microscopy,” J. Microsc. 176, 226–230 (1994).
[Crossref]

Solinas, X.

N. Olivier, M. A. Luengo-Oroz, L. Duloquin, E. Faure, T. Savy, I. Veilleux, X. Solinas, D. Débarre, P. Bourgine, A. Santos, N. Peyriéras, and E. Beaurepaire, “Cell Lineage Reconstruction of Early zebrafish embryos using label-free nonlinear microscopy,” Science 329, 967–971 (2010).
[Crossref] [PubMed]

Sorensen, C. M.

R. S. Friedman, P. Beemiller, C. M. Sorensen, J. Jacobelli, and M. F. Krummel, “Real-time analysis of T cell receptors in naive cells in vitro and in vivo reveals flexibility in synapse and signaling dynamics,” J. Exp. Med. 207, 2733–2749 (2010).
[Crossref] [PubMed]

Stelzer, E. H. K.

S. Hell, G. Reiner, C. Cremer, and E. H. K. Stelzer, “Aberrations in confocal fluorescence microscopy induced by mismatches in refractive index,” J. Microsc. 169, 391–405 (1993).
[Crossref]

Stobart, J. L.

Strickler, J.

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

Svoboda, K.

N. J. Sofroniew, D. Flickinger, J. King, and K. Svoboda, “A large field of view two-photon mesoscope with subcellular resolution for in vivo imaging,” eLife 5, 1–20 (2016).
[Crossref]

D. Huber, D. A. Gutnisky, S. Peron, D. H. O’Connor, J. S. Wiegert, L. Tian, T. G. Oertner, L. L. Looger, and K. Svoboda, “Multiple dynamic representations in the motor cortex during sensorimotor learning,” Nature 484, 473–478 (2012).
[Crossref] [PubMed]

A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W. A. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, and L. Wilbrecht, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4, 19–22 (2009).
[Crossref]

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

Takahara, S.

R. Imamura, Y. Isaka, R. M. Sandoval, A. Ori, S. Adamsky, E. Feinstein, B. A. Molitoris, and S. Takahara, “Intravital two-photon microscopy assessment of renal protection efficacy of siRNA for p53 in experimental rat kidney transplantation models,” Cell Transplantation 19, 1659–1670 (2010).
[Crossref] [PubMed]

Takaji, M.

O. Sadakane, Y. Masamizu, A. Watakabe, S. I. Terada, M. Ohtsuka, M. Takaji, H. Mizukami, K. Ozawa, H. Kawasaki, M. Matsuzaki, and T. Yamamori, “Long-Term Two-Photon Calcium Imaging of Neuronal Populations with Subcellular Resolution in Adult Non-human Primates,” Cell Reports 13, 1989–1999 (2015).
[Crossref] [PubMed]

Tanaka, Y. R.

T. Ebina, Y. Masamizu, Y. R. Tanaka, A. Watakabe, R. Hirakawa, Y. Hirayama, R. Hira, S.-I. Terada, D. Koketsu, K. Hikosaka, H. Mizukami, A. Nambu, E. Sasaki, T. Yamamori, and M. Matsuzaki, “Two-photon imaging of neuronal activity in motor cortex of marmosets during upper-limb movement tasks,” Nat. Commun. 9, 1879 (2018).
[Crossref] [PubMed]

Terada, S. I.

O. Sadakane, Y. Masamizu, A. Watakabe, S. I. Terada, M. Ohtsuka, M. Takaji, H. Mizukami, K. Ozawa, H. Kawasaki, M. Matsuzaki, and T. Yamamori, “Long-Term Two-Photon Calcium Imaging of Neuronal Populations with Subcellular Resolution in Adult Non-human Primates,” Cell Reports 13, 1989–1999 (2015).
[Crossref] [PubMed]

Terada, S.-I.

T. Ebina, Y. Masamizu, Y. R. Tanaka, A. Watakabe, R. Hirakawa, Y. Hirayama, R. Hira, S.-I. Terada, D. Koketsu, K. Hikosaka, H. Mizukami, A. Nambu, E. Sasaki, T. Yamamori, and M. Matsuzaki, “Two-photon imaging of neuronal activity in motor cortex of marmosets during upper-limb movement tasks,” Nat. Commun. 9, 1879 (2018).
[Crossref] [PubMed]

Testa Silva, G.

S. Witte, A. Negrean, J. C. Lodder, C. P. J. de Kock, G. Testa Silva, H. D. Mansvelder, and M. L. Groota, “Label-free live brain imaging and targeted patching with third-harmonic generation microscopy,” Proc. Natl. Acad. Sci. U.S.A 108, 5970–5975 (2011).
[Crossref] [PubMed]

Thornton, E. E.

M. R. Looney, E. E. Thornton, D. Sen, W. J. Lamm, R. W. Glenny, and M. F. Krummel, “Stabilized imaging of immune surveillance in the mouse lung,” Nat. Methods 8, 91–96 (2011).
[Crossref]

Tian, L.

D. Huber, D. A. Gutnisky, S. Peron, D. H. O’Connor, J. S. Wiegert, L. Tian, T. G. Oertner, L. L. Looger, and K. Svoboda, “Multiple dynamic representations in the motor cortex during sensorimotor learning,” Nature 484, 473–478 (2012).
[Crossref] [PubMed]

Trachtenberg, J. T.

A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W. A. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, and L. Wilbrecht, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4, 19–22 (2009).
[Crossref]

Turcotte, R.

Urban, C.

Veilleux, I.

N. Olivier, M. A. Luengo-Oroz, L. Duloquin, E. Faure, T. Savy, I. Veilleux, X. Solinas, D. Débarre, P. Bourgine, A. Santos, N. Peyriéras, and E. Beaurepaire, “Cell Lineage Reconstruction of Early zebrafish embryos using label-free nonlinear microscopy,” Science 329, 967–971 (2010).
[Crossref] [PubMed]

Villiger, M.

T. Bolmont, A. Bouwens, C. Pache, M. Dimitrov, C. Berclaz, M. Villiger, B. M. Wegenast-Braun, T. Lasser, and P. C. Fraering, “Label-free imaging of cerebral β-amyloidosis with extended-focus optical coherence microscopy,” J. Neurosci. 32, 14548–14556 (2012).
[Crossref] [PubMed]

Watakabe, A.

T. Ebina, Y. Masamizu, Y. R. Tanaka, A. Watakabe, R. Hirakawa, Y. Hirayama, R. Hira, S.-I. Terada, D. Koketsu, K. Hikosaka, H. Mizukami, A. Nambu, E. Sasaki, T. Yamamori, and M. Matsuzaki, “Two-photon imaging of neuronal activity in motor cortex of marmosets during upper-limb movement tasks,” Nat. Commun. 9, 1879 (2018).
[Crossref] [PubMed]

O. Sadakane, Y. Masamizu, A. Watakabe, S. I. Terada, M. Ohtsuka, M. Takaji, H. Mizukami, K. Ozawa, H. Kawasaki, M. Matsuzaki, and T. Yamamori, “Long-Term Two-Photon Calcium Imaging of Neuronal Populations with Subcellular Resolution in Adult Non-human Primates,” Cell Reports 13, 1989–1999 (2015).
[Crossref] [PubMed]

Webb, W.

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

Weber, B.

Weber, S.

Wegenast-Braun, B. M.

T. Bolmont, A. Bouwens, C. Pache, M. Dimitrov, C. Berclaz, M. Villiger, B. M. Wegenast-Braun, T. Lasser, and P. C. Fraering, “Label-free imaging of cerebral β-amyloidosis with extended-focus optical coherence microscopy,” J. Neurosci. 32, 14548–14556 (2012).
[Crossref] [PubMed]

Wiegert, J. S.

D. Huber, D. A. Gutnisky, S. Peron, D. H. O’Connor, J. S. Wiegert, L. Tian, T. G. Oertner, L. L. Looger, and K. Svoboda, “Multiple dynamic representations in the motor cortex during sensorimotor learning,” Nature 484, 473–478 (2012).
[Crossref] [PubMed]

Wilbrecht, L.

A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W. A. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, and L. Wilbrecht, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4, 19–22 (2009).
[Crossref]

Witte, S.

S. Witte, A. Negrean, J. C. Lodder, C. P. J. de Kock, G. Testa Silva, H. D. Mansvelder, and M. L. Groota, “Label-free live brain imaging and targeted patching with third-harmonic generation microscopy,” Proc. Natl. Acad. Sci. U.S.A 108, 5970–5975 (2011).
[Crossref] [PubMed]

Wyss, M. T.

Yamamori, T.

T. Ebina, Y. Masamizu, Y. R. Tanaka, A. Watakabe, R. Hirakawa, Y. Hirayama, R. Hira, S.-I. Terada, D. Koketsu, K. Hikosaka, H. Mizukami, A. Nambu, E. Sasaki, T. Yamamori, and M. Matsuzaki, “Two-photon imaging of neuronal activity in motor cortex of marmosets during upper-limb movement tasks,” Nat. Commun. 9, 1879 (2018).
[Crossref] [PubMed]

O. Sadakane, Y. Masamizu, A. Watakabe, S. I. Terada, M. Ohtsuka, M. Takaji, H. Mizukami, K. Ozawa, H. Kawasaki, M. Matsuzaki, and T. Yamamori, “Long-Term Two-Photon Calcium Imaging of Neuronal Populations with Subcellular Resolution in Adult Non-human Primates,” Cell Reports 13, 1989–1999 (2015).
[Crossref] [PubMed]

Yasuda, R.

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

Yokoyama, H.

Zeilhofer, H. U.

Ziegler, U.

Zuend, M.

Biomed. Opt. Express (3)

Cell Reports (2)

G. L. Galiñanes, C. Bonardi, and D. Huber, “Directional Reaching for Water as a Cortex-Dependent Behavioral Framework for Mice,” Cell Reports 22, 2601–2614 (2018).
[Crossref]

O. Sadakane, Y. Masamizu, A. Watakabe, S. I. Terada, M. Ohtsuka, M. Takaji, H. Mizukami, K. Ozawa, H. Kawasaki, M. Matsuzaki, and T. Yamamori, “Long-Term Two-Photon Calcium Imaging of Neuronal Populations with Subcellular Resolution in Adult Non-human Primates,” Cell Reports 13, 1989–1999 (2015).
[Crossref] [PubMed]

Cell Transplantation (1)

R. Imamura, Y. Isaka, R. M. Sandoval, A. Ori, S. Adamsky, E. Feinstein, B. A. Molitoris, and S. Takahara, “Intravital two-photon microscopy assessment of renal protection efficacy of siRNA for p53 in experimental rat kidney transplantation models,” Cell Transplantation 19, 1659–1670 (2010).
[Crossref] [PubMed]

Current Protocols in Cell Biology (1)

R. K. P. Benninger and D. W. Piston, “Two-Photon Excitation Microscopy for the Study of Living Cells and Tissues,” Current Protocols in Cell Biology 59, 1–24 (2013).
[Crossref]

eLife (1)

N. J. Sofroniew, D. Flickinger, J. King, and K. Svoboda, “A large field of view two-photon mesoscope with subcellular resolution for in vivo imaging,” eLife 5, 1–20 (2016).
[Crossref]

J. Biomed. Opt. (1)

D. A. Boas and A. K. Dunn, “Laser speckle contrast imaging in biomedical optics,” J. Biomed. Opt. 15, 011109 (2014).
[Crossref]

J. Exp. Med. (1)

R. S. Friedman, P. Beemiller, C. M. Sorensen, J. Jacobelli, and M. F. Krummel, “Real-time analysis of T cell receptors in naive cells in vitro and in vivo reveals flexibility in synapse and signaling dynamics,” J. Exp. Med. 207, 2733–2749 (2010).
[Crossref] [PubMed]

J. Microsc. (2)

S. Hell, G. Reiner, C. Cremer, and E. H. K. Stelzer, “Aberrations in confocal fluorescence microscopy induced by mismatches in refractive index,” J. Microsc. 169, 391–405 (1993).
[Crossref]

H. Jacobsen, P. Hanninen, E. Soini, and S. W. Hell, “Refractive-index-induced aberrations in two-photon confocal fluorescence microscopy,” J. Microsc. 176, 226–230 (1994).
[Crossref]

J. Neurosci. (1)

T. Bolmont, A. Bouwens, C. Pache, M. Dimitrov, C. Berclaz, M. Villiger, B. M. Wegenast-Braun, T. Lasser, and P. C. Fraering, “Label-free imaging of cerebral β-amyloidosis with extended-focus optical coherence microscopy,” J. Neurosci. 32, 14548–14556 (2012).
[Crossref] [PubMed]

Nat. Commun. (1)

T. Ebina, Y. Masamizu, Y. R. Tanaka, A. Watakabe, R. Hirakawa, Y. Hirayama, R. Hira, S.-I. Terada, D. Koketsu, K. Hikosaka, H. Mizukami, A. Nambu, E. Sasaki, T. Yamamori, and M. Matsuzaki, “Two-photon imaging of neuronal activity in motor cortex of marmosets during upper-limb movement tasks,” Nat. Commun. 9, 1879 (2018).
[Crossref] [PubMed]

Nat. Methods (2)

N. Ji, “Adaptive optical fluorescence microscopy,” Nat. Methods 14, 374–380 (2017).
[Crossref] [PubMed]

M. R. Looney, E. E. Thornton, D. Sen, W. J. Lamm, R. W. Glenny, and M. F. Krummel, “Stabilized imaging of immune surveillance in the mouse lung,” Nat. Methods 8, 91–96 (2011).
[Crossref]

Nat. Protoc. (1)

A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W. A. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, and L. Wilbrecht, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4, 19–22 (2009).
[Crossref]

Nature (1)

D. Huber, D. A. Gutnisky, S. Peron, D. H. O’Connor, J. S. Wiegert, L. Tian, T. G. Oertner, L. L. Looger, and K. Svoboda, “Multiple dynamic representations in the motor cortex during sensorimotor learning,” Nature 484, 473–478 (2012).
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Neuron (2)

M. L. Andermann, A. M. Kerlin, D. K. Roumis, L. L. Glickfeld, and R. C. Reid, “Functional specialization of mouse higher visual cortical areas,” Neuron 72, 1025–1039 (2011).
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K. Svoboda and R. Yasuda, “Principles of two-photon excitation microscopy and its applications to neuroscience,” Neuron 50, 823–839 (2006).
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Opt. Commun. (1)

P. A. Muriello and K. W. Dunn, “Improving signal levels in intravital multiphoton microscopy using an objective correction collar,” Opt. Commun. 281, 1806–1812 (2008).
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Opt. Express (2)

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

S. Witte, A. Negrean, J. C. Lodder, C. P. J. de Kock, G. Testa Silva, H. D. Mansvelder, and M. L. Groota, “Label-free live brain imaging and targeted patching with third-harmonic generation microscopy,” Proc. Natl. Acad. Sci. U.S.A 108, 5970–5975 (2011).
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D. Kleinfeld, P. P. Mitra, F. Helmchen, and W. Denk, “Fluctuations and stimulus-induced changes in blood flow observed in individual capillaries in layers 2 through 4 of rat neocortex,” Proc. Natl. Acad. Sci. U.S.A 95, 15741–15746 (1998).
[Crossref] [PubMed]

Science (2)

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

N. Olivier, M. A. Luengo-Oroz, L. Duloquin, E. Faure, T. Savy, I. Veilleux, X. Solinas, D. Débarre, P. Bourgine, A. Santos, N. Peyriéras, and E. Beaurepaire, “Cell Lineage Reconstruction of Early zebrafish embryos using label-free nonlinear microscopy,” Science 329, 967–971 (2010).
[Crossref] [PubMed]

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Figures (3)

Fig. 1
Fig. 1 Two-photon fluorescence intensity and FWHM profiles of fluorescent microbeads under different orientation angles, cover glass layers and collar-corrections. (A) Increasing the tilt angle between the optical axis of the two-photon microscope and the axis perpendicular to the imaging window significantly decreases light intensity measured from individual microbeads with a collar corrected objective. Even at small tilt angles of θ = 1° a significant loss of intensity is detected. This effect is amplified when the thickness of the cover glass is doubled. (B) The lack of collar correction drastically decreases the measured bead intensity. (C) With a collar correction, the axial FWHM is fully corrected at θ = 0° tilt angle close to the theoretical limit (green solid line) for single and double cover glass preparations. Increasing the tilt angle significantly degrades the axial resolution. (D) Without collar correction the axial resolution is deceased. The double glass configuration further degrades the axial resolution. The resolution of the uncorrected condition is comparable to a θ = 5° tilt in the corrected condition. (E) Z projection (maximal intensity) of 7 slices (14 µm) at the soma level of a layer 2/3 neuron imaged in the frontal cortex at a 5x magnification factor. The same neuron was imaged at different tilt angles (θ = 0°, 5°, and 10°). (F) Top: zoom in of a neuronal process with boutons acquired at 15× magnification factor. The maximal intensity Z projection (15 slices, 15 µm) was used to obtain the intensity profile of the region of interest on 3 different acquisitions at each tilt angle. Bottom: intensity profiles were aligned to the peaks (thin traces) and averaged (thick traces) for comparison across conditions. Scalebar: 10µm
Fig. 2
Fig. 2 Tilt angle measurement principle. (A) In our configuration, the microscope frontend can be rotated along the microscope plane (in orange) by an angle β and the mouse around the table plane (in blue) by an angle α. (B) The tilt angle can be estimated by mounting the device on an objective. The device comprises a laser source and a target screen placed on opposite sides of the rotating ring. (C) If a tilt θ is present, the reflection angle of the laser beam (red line) will vary depending on the orientation of the device around the optical axis (dotted line), as shown in this panel. (D) This variation in reflective angle ϕ′ will entail a change in position on the target d, depending on the tilt angle θ and the distance L between the cover glass window (blue) and the target.
Fig. 3
Fig. 3 Device characterization. (A) If the glass window is tilted, rotating the device will cause the beam to wander on the target creating an ellipsoid (rotation angle of the device γ is color encoded). (B) The amplitude of the ellipsoid in the longitudinal axis is related to the tilt angle θ as predicted by the geometrical model. (C) The measured amplitudes at specific tilt angles are shown by red circles and are in good agreement with our model, shown by the black curve. (D) A coverslide was put under the microscope and the angle between the coverslide and the rotational plane of the device (θrc) was assessed using the alignment device. (E) Next, the alignment device was replaced by a 25× objective and fluorescein was added to the immersion medium to estimate the angle between the coverslide and the imaging plane (θic). (F) A 3D stack of the fluorescein immersion-coverslide structure was acquired and maximum intensity projections along both lateral axes were used to estimate the position of the interface (red line) and finally calculate the imaging plane to coverslide tilt θic. (G) The difference between the angle measurements for both dimensions are shown for different trials and the mean is reported as a black cross. Overall the average mismatch between the device plane and the imaging plane is below 0.25° in both axes. (H) The tilt adjustment protocol can be summarized into two main steps; firstly, the specimen has to be rotated (α) such that the rotation angle of the alignment device (γ comprising the maximum and minimum amplitude are aligned parallel to the microscope axis (Rotation correction arrow). In a second step, the microscope head is rotated by an angle β (Partial tilt correction arrow), obtained by measuring the longitudinal amplitude of the ellipsoid and converting it into a tilt angle through Eq. (1). Ultimately, once the microscope head is set such that the tilt angle is fully compensated, the beam remains at the same position throughout an entire rotation of the device. (I) The full tilt alignment procedure was performed on 3 animals, and the amplitude of the beam on the target for a full rotation of the device was smaller than 0.5 mm on the target. The dots in panel I represent the centroids of the beam at different rotational angles and for different animals (color indicates the animal).

Equations (1)

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d = 2 L tan ( 2 θ )

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