Abstract

Iterative multi-photon adaptive compensation technique (IMPACT) has been developed for wavefront measurement and compensation in highly scattering tissues. Our previous report was largely based on the measurements of fixed tissue. Here we demonstrate the advantages of IMPACT for in vivo imaging and report the latest results. In particular, we show that IMPACT can be used for functional imaging of awake mice, and greatly improve the in vivo neuron imaging in mouse cortex at large depth (~660 microns). Moreover, IMPACT enables neuron imaging through the intact skull of adult mice, which promises noninvasive optical measurements in mouse brain.

© 2014 Optical Society of America

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2014 (2)

K. Wang, D. E. Milkie, A. Saxena, P. Engerer, T. Misgeld, M. E. Bronner, J. Mumm, and E. Betzig, “Rapid adaptive optical recovery of optimal resolution over large volumes,” Nat. Methods 11(6), 625–628 (2014).
[Crossref] [PubMed]

Z. V. Guo, S. A. Hires, N. Li, D. H. O’Connor, T. Komiyama, E. Ophir, D. Huber, C. Bonardi, K. Morandell, D. Gutnisky, S. Peron, N. L. Xu, J. Cox, and K. Svoboda, “Procedures for Behavioral Experiments in Head-Fixed Mice,” PLoS ONE 9(2), e88678 (2014).
[Crossref] [PubMed]

2013 (1)

T. Lämmermann, P. V. Afonso, B. R. Angermann, J. M. Wang, W. Kastenmüller, C. A. Parent, and R. N. Germain, “Neutrophil swarms require LTB4 and integrins at sites of cell death in vivo,” Nature 498(7454), 371–375 (2013).
[Crossref] [PubMed]

2012 (5)

R. Fiolka, K. Si, and M. Cui, “Complex wavefront corrections for deep tissue focusing using low coherence backscattered light,” Opt. Express 20(15), 16532–16543 (2012).
[Crossref]

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

K. Si, R. Fiolka, and M. Cui, “Breaking the spatial resolution barrier via iterative sound-light interaction in deep tissue microscopy,” Sci. Rep. 2, 748 (2012).
[Crossref] [PubMed]

K. Si, R. Fiolka, and M. Cui, “Fluorescence imaging beyond the ballistic regime by ultrasound pulse guided digital phase conjugation,” Nat. Photonics 6(10), 657–661 (2012).
[Crossref] [PubMed]

X. Tao, J. Crest, S. Kotadia, O. Azucena, D. C. Chen, W. Sullivan, and J. Kubby, “Live imaging using adaptive optics with fluorescent protein guide-stars,” Opt. Express 20(14), 15969–15982 (2012).
[Crossref] [PubMed]

2011 (2)

X. Tao, B. Fernandez, O. Azucena, M. Fu, D. Garcia, Y. Zuo, D. C. Chen, and J. Kubby, “Adaptive optics confocal microscopy using direct wavefront sensing,” Opt. Lett. 36(7), 1062–1064 (2011).
[Crossref] [PubMed]

Z. Popovic, P. Knutsson, J. Thaung, M. Owner-Petersen, and J. Sjöstrand, “Noninvasive imaging of human foveal capillary network using dual-conjugate adaptive optics,” Invest. Ophthalmol. Vis. Sci. 52(5), 2649–2655 (2011).
[Crossref] [PubMed]

2010 (1)

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

2009 (2)

2008 (3)

D. Débarre, E. J. Botcherby, M. J. Booth, and T. Wilson, “Adaptive optics for structured illumination microscopy,” Opt. Express 16(13), 9290–9305 (2008).
[Crossref] [PubMed]

I. M. Vellekoop and A. P. Mosk, “Universal optimal transmission of light through disordered materials,” Phys. Rev. Lett. 101(12), 120601 (2008).
[Crossref] [PubMed]

D. S. Greenberg, A. R. Houweling, and J. N. Kerr, “Population imaging of ongoing neuronal activity in the visual cortex of awake rats,” Nat. Neurosci. 11(7), 749–751 (2008).
[Crossref] [PubMed]

2007 (2)

I. M. Vellekoop and A. P. Mosk, “Focusing coherent light through opaque strongly scattering media,” Opt. Lett. 32(16), 2309–2311 (2007).
[Crossref] [PubMed]

H.-T. Xu, F. Pan, G. Yang, and W.-B. Gan, “Choice of cranial window type for in vivo imaging affects dendritic spine turnover in the cortex,” Nat. Neurosci. 10(5), 549–551 (2007).
[Crossref] [PubMed]

2006 (1)

M. Rueckel, J. A. Mack-Bucher, and W. Denk, “Adaptive wavefront correction in two-photon microscopy using coherence-gated wavefront sensing,” Proc. Natl. Acad. Sci. U.S.A. 103(46), 17137–17142 (2006).
[Crossref] [PubMed]

2005 (3)

2004 (1)

A. Nimmerjahn, F. Kirchhoff, J. N. Kerr, and F. Helmchen, “Sulforhodamine 101 as a specific marker of astroglia in the neocortex in vivo,” Nat. Methods 1(1), 31–37 (2004).
[Crossref] [PubMed]

2002 (2)

M. J. Booth, M. A. A. Neil, R. Juskaitis, and T. Wilson, “Adaptive aberration correction in a confocal microscope,” Proc. Natl. Acad. Sci. U.S.A. 99(9), 5788–5792 (2002).
[Crossref] [PubMed]

S. Stoll, J. Delon, T. M. Brotz, and R. N. Germain, “Dynamic imaging of T cell-dendritic cell interactions in lymph nodes,” Science 296(5574), 1873–1876 (2002).
[Crossref] [PubMed]

1999 (1)

A. Roorda and D. R. Williams, “The arrangement of the three cone classes in the living human eye,” Nature 397(6719), 520–522 (1999).
[Crossref] [PubMed]

1997 (2)

J. Liang, D. R. Williams, and D. T. Miller, “Supernormal vision and high-resolution retinal imaging through adaptive optics,” J. Opt. Soc. Am. A 14(11), 2884–2892 (1997).
[Crossref] [PubMed]

K. Svoboda, W. Denk, D. Kleinfeld, and D. W. Tank, “In vivo dendritic calcium dynamics in neocortical pyramidal neurons,” Nature 385(6612), 161–165 (1997).
[Crossref] [PubMed]

1990 (1)

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

1974 (1)

Afonso, P. V.

T. Lämmermann, P. V. Afonso, B. R. Angermann, J. M. Wang, W. Kastenmüller, C. A. Parent, and R. N. Germain, “Neutrophil swarms require LTB4 and integrins at sites of cell death in vivo,” Nature 498(7454), 371–375 (2013).
[Crossref] [PubMed]

Angermann, B. R.

T. Lämmermann, P. V. Afonso, B. R. Angermann, J. M. Wang, W. Kastenmüller, C. A. Parent, and R. N. Germain, “Neutrophil swarms require LTB4 and integrins at sites of cell death in vivo,” Nature 498(7454), 371–375 (2013).
[Crossref] [PubMed]

Azucena, O.

Betzig, E.

K. Wang, D. E. Milkie, A. Saxena, P. Engerer, T. Misgeld, M. E. Bronner, J. Mumm, and E. Betzig, “Rapid adaptive optical recovery of optimal resolution over large volumes,” Nat. Methods 11(6), 625–628 (2014).
[Crossref] [PubMed]

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

Bonardi, C.

Z. V. Guo, S. A. Hires, N. Li, D. H. O’Connor, T. Komiyama, E. Ophir, D. Huber, C. Bonardi, K. Morandell, D. Gutnisky, S. Peron, N. L. Xu, J. Cox, and K. Svoboda, “Procedures for Behavioral Experiments in Head-Fixed Mice,” PLoS ONE 9(2), e88678 (2014).
[Crossref] [PubMed]

Booth, M. J.

Botcherby, E. J.

Bridges, W. B.

Bronner, M. E.

K. Wang, D. E. Milkie, A. Saxena, P. Engerer, T. Misgeld, M. E. Bronner, J. Mumm, and E. Betzig, “Rapid adaptive optical recovery of optimal resolution over large volumes,” Nat. Methods 11(6), 625–628 (2014).
[Crossref] [PubMed]

Brotz, T. M.

S. Stoll, J. Delon, T. M. Brotz, and R. N. Germain, “Dynamic imaging of T cell-dendritic cell interactions in lymph nodes,” Science 296(5574), 1873–1876 (2002).
[Crossref] [PubMed]

Brown, W. P.

Brunner, P. T.

Chen, D. C.

Chen, T.-w.

H. Dana, T.-w. Chen, A. Hu, B. C. Shields, C. Guo, L. L. Looger, D. S. Kim, and K. Svoboda, “Thy1-GCaMP6 transgenic mice for neuronla population imaging in vivo,” PLoS ONE. in press.

Cox, J.

Z. V. Guo, S. A. Hires, N. Li, D. H. O’Connor, T. Komiyama, E. Ophir, D. Huber, C. Bonardi, K. Morandell, D. Gutnisky, S. Peron, N. L. Xu, J. Cox, and K. Svoboda, “Procedures for Behavioral Experiments in Head-Fixed Mice,” PLoS ONE 9(2), e88678 (2014).
[Crossref] [PubMed]

Crest, J.

Cui, M.

R. Fiolka, K. Si, and M. Cui, “Complex wavefront corrections for deep tissue focusing using low coherence backscattered light,” Opt. Express 20(15), 16532–16543 (2012).
[Crossref]

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

K. Si, R. Fiolka, and M. Cui, “Breaking the spatial resolution barrier via iterative sound-light interaction in deep tissue microscopy,” Sci. Rep. 2, 748 (2012).
[Crossref] [PubMed]

K. Si, R. Fiolka, and M. Cui, “Fluorescence imaging beyond the ballistic regime by ultrasound pulse guided digital phase conjugation,” Nat. Photonics 6(10), 657–661 (2012).
[Crossref] [PubMed]

Dana, H.

H. Dana, T.-w. Chen, A. Hu, B. C. Shields, C. Guo, L. L. Looger, D. S. Kim, and K. Svoboda, “Thy1-GCaMP6 transgenic mice for neuronla population imaging in vivo,” PLoS ONE. in press.

Débarre, D.

Delon, J.

S. Stoll, J. Delon, T. M. Brotz, and R. N. Germain, “Dynamic imaging of T cell-dendritic cell interactions in lymph nodes,” Science 296(5574), 1873–1876 (2002).
[Crossref] [PubMed]

Denk, W.

M. Rueckel, J. A. Mack-Bucher, and W. Denk, “Adaptive wavefront correction in two-photon microscopy using coherence-gated wavefront sensing,” Proc. Natl. Acad. Sci. U.S.A. 103(46), 17137–17142 (2006).
[Crossref] [PubMed]

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

K. Svoboda, W. Denk, D. Kleinfeld, and D. W. Tank, “In vivo dendritic calcium dynamics in neocortical pyramidal neurons,” Nature 385(6612), 161–165 (1997).
[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]

Durst, M.

Engerer, P.

K. Wang, D. E. Milkie, A. Saxena, P. Engerer, T. Misgeld, M. E. Bronner, J. Mumm, and E. Betzig, “Rapid adaptive optical recovery of optimal resolution over large volumes,” Nat. Methods 11(6), 625–628 (2014).
[Crossref] [PubMed]

Fernandez, B.

Fiolka, R.

R. Fiolka, K. Si, and M. Cui, “Complex wavefront corrections for deep tissue focusing using low coherence backscattered light,” Opt. Express 20(15), 16532–16543 (2012).
[Crossref]

K. Si, R. Fiolka, and M. Cui, “Breaking the spatial resolution barrier via iterative sound-light interaction in deep tissue microscopy,” Sci. Rep. 2, 748 (2012).
[Crossref] [PubMed]

K. Si, R. Fiolka, and M. Cui, “Fluorescence imaging beyond the ballistic regime by ultrasound pulse guided digital phase conjugation,” Nat. Photonics 6(10), 657–661 (2012).
[Crossref] [PubMed]

Fu, M.

Gan, W.-B.

H.-T. Xu, F. Pan, G. Yang, and W.-B. Gan, “Choice of cranial window type for in vivo imaging affects dendritic spine turnover in the cortex,” Nat. Neurosci. 10(5), 549–551 (2007).
[Crossref] [PubMed]

Garcia, D.

Germain, R. N.

T. Lämmermann, P. V. Afonso, B. R. Angermann, J. M. Wang, W. Kastenmüller, C. A. Parent, and R. N. Germain, “Neutrophil swarms require LTB4 and integrins at sites of cell death in vivo,” Nature 498(7454), 371–375 (2013).
[Crossref] [PubMed]

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

S. Stoll, J. Delon, T. M. Brotz, and R. N. Germain, “Dynamic imaging of T cell-dendritic cell interactions in lymph nodes,” Science 296(5574), 1873–1876 (2002).
[Crossref] [PubMed]

Greenberg, D. S.

D. S. Greenberg, A. R. Houweling, and J. N. Kerr, “Population imaging of ongoing neuronal activity in the visual cortex of awake rats,” Nat. Neurosci. 11(7), 749–751 (2008).
[Crossref] [PubMed]

Guo, C.

H. Dana, T.-w. Chen, A. Hu, B. C. Shields, C. Guo, L. L. Looger, D. S. Kim, and K. Svoboda, “Thy1-GCaMP6 transgenic mice for neuronla population imaging in vivo,” PLoS ONE. in press.

Guo, Z. V.

Z. V. Guo, S. A. Hires, N. Li, D. H. O’Connor, T. Komiyama, E. Ophir, D. Huber, C. Bonardi, K. Morandell, D. Gutnisky, S. Peron, N. L. Xu, J. Cox, and K. Svoboda, “Procedures for Behavioral Experiments in Head-Fixed Mice,” PLoS ONE 9(2), e88678 (2014).
[Crossref] [PubMed]

Gutnisky, D.

Z. V. Guo, S. A. Hires, N. Li, D. H. O’Connor, T. Komiyama, E. Ophir, D. Huber, C. Bonardi, K. Morandell, D. Gutnisky, S. Peron, N. L. Xu, J. Cox, and K. Svoboda, “Procedures for Behavioral Experiments in Head-Fixed Mice,” PLoS ONE 9(2), e88678 (2014).
[Crossref] [PubMed]

Helmchen, F.

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

A. Nimmerjahn, F. Kirchhoff, J. N. Kerr, and F. Helmchen, “Sulforhodamine 101 as a specific marker of astroglia in the neocortex in vivo,” Nat. Methods 1(1), 31–37 (2004).
[Crossref] [PubMed]

Hires, S. A.

Z. V. Guo, S. A. Hires, N. Li, D. H. O’Connor, T. Komiyama, E. Ophir, D. Huber, C. Bonardi, K. Morandell, D. Gutnisky, S. Peron, N. L. Xu, J. Cox, and K. Svoboda, “Procedures for Behavioral Experiments in Head-Fixed Mice,” PLoS ONE 9(2), e88678 (2014).
[Crossref] [PubMed]

Houweling, A. R.

D. S. Greenberg, A. R. Houweling, and J. N. Kerr, “Population imaging of ongoing neuronal activity in the visual cortex of awake rats,” Nat. Neurosci. 11(7), 749–751 (2008).
[Crossref] [PubMed]

Hu, A.

H. Dana, T.-w. Chen, A. Hu, B. C. Shields, C. Guo, L. L. Looger, D. S. Kim, and K. Svoboda, “Thy1-GCaMP6 transgenic mice for neuronla population imaging in vivo,” PLoS ONE. in press.

Huber, D.

Z. V. Guo, S. A. Hires, N. Li, D. H. O’Connor, T. Komiyama, E. Ophir, D. Huber, C. Bonardi, K. Morandell, D. Gutnisky, S. Peron, N. L. Xu, J. Cox, and K. Svoboda, “Procedures for Behavioral Experiments in Head-Fixed Mice,” PLoS ONE 9(2), e88678 (2014).
[Crossref] [PubMed]

Ji, N.

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

Juskaitis, R.

M. J. Booth, M. A. A. Neil, R. Juskaitis, and T. Wilson, “Adaptive aberration correction in a confocal microscope,” Proc. Natl. Acad. Sci. U.S.A. 99(9), 5788–5792 (2002).
[Crossref] [PubMed]

Kastenmüller, W.

T. Lämmermann, P. V. Afonso, B. R. Angermann, J. M. Wang, W. Kastenmüller, C. A. Parent, and R. N. Germain, “Neutrophil swarms require LTB4 and integrins at sites of cell death in vivo,” Nature 498(7454), 371–375 (2013).
[Crossref] [PubMed]

Kerr, J. N.

D. S. Greenberg, A. R. Houweling, and J. N. Kerr, “Population imaging of ongoing neuronal activity in the visual cortex of awake rats,” Nat. Neurosci. 11(7), 749–751 (2008).
[Crossref] [PubMed]

A. Nimmerjahn, F. Kirchhoff, J. N. Kerr, and F. Helmchen, “Sulforhodamine 101 as a specific marker of astroglia in the neocortex in vivo,” Nat. Methods 1(1), 31–37 (2004).
[Crossref] [PubMed]

Kim, D. S.

H. Dana, T.-w. Chen, A. Hu, B. C. Shields, C. Guo, L. L. Looger, D. S. Kim, and K. Svoboda, “Thy1-GCaMP6 transgenic mice for neuronla population imaging in vivo,” PLoS ONE. in press.

Kirchhoff, F.

A. Nimmerjahn, F. Kirchhoff, J. N. Kerr, and F. Helmchen, “Sulforhodamine 101 as a specific marker of astroglia in the neocortex in vivo,” Nat. Methods 1(1), 31–37 (2004).
[Crossref] [PubMed]

Kleinfeld, D.

K. Svoboda, W. Denk, D. Kleinfeld, and D. W. Tank, “In vivo dendritic calcium dynamics in neocortical pyramidal neurons,” Nature 385(6612), 161–165 (1997).
[Crossref] [PubMed]

Knutsson, P.

Z. Popovic, P. Knutsson, J. Thaung, M. Owner-Petersen, and J. Sjöstrand, “Noninvasive imaging of human foveal capillary network using dual-conjugate adaptive optics,” Invest. Ophthalmol. Vis. Sci. 52(5), 2649–2655 (2011).
[Crossref] [PubMed]

J. Thaung, P. Knutsson, Z. Popovic, and M. Owner-Petersen, “Dual-conjugate adaptive optics for wide-field high-resolution retinal imaging,” Opt. Express 17(6), 4454–4467 (2009).
[Crossref] [PubMed]

Komiyama, T.

Z. V. Guo, S. A. Hires, N. Li, D. H. O’Connor, T. Komiyama, E. Ophir, D. Huber, C. Bonardi, K. Morandell, D. Gutnisky, S. Peron, N. L. Xu, J. Cox, and K. Svoboda, “Procedures for Behavioral Experiments in Head-Fixed Mice,” PLoS ONE 9(2), e88678 (2014).
[Crossref] [PubMed]

Kotadia, S.

Kubby, J.

Lämmermann, T.

T. Lämmermann, P. V. Afonso, B. R. Angermann, J. M. Wang, W. Kastenmüller, C. A. Parent, and R. N. Germain, “Neutrophil swarms require LTB4 and integrins at sites of cell death in vivo,” Nature 498(7454), 371–375 (2013).
[Crossref] [PubMed]

Lazzara, S. P.

Li, N.

Z. V. Guo, S. A. Hires, N. Li, D. H. O’Connor, T. Komiyama, E. Ophir, D. Huber, C. Bonardi, K. Morandell, D. Gutnisky, S. Peron, N. L. Xu, J. Cox, and K. Svoboda, “Procedures for Behavioral Experiments in Head-Fixed Mice,” PLoS ONE 9(2), e88678 (2014).
[Crossref] [PubMed]

Liang, J.

Looger, L. L.

H. Dana, T.-w. Chen, A. Hu, B. C. Shields, C. Guo, L. L. Looger, D. S. Kim, and K. Svoboda, “Thy1-GCaMP6 transgenic mice for neuronla population imaging in vivo,” PLoS ONE. in press.

Mack-Bucher, J. A.

M. Rueckel, J. A. Mack-Bucher, and W. Denk, “Adaptive wavefront correction in two-photon microscopy using coherence-gated wavefront sensing,” Proc. Natl. Acad. Sci. U.S.A. 103(46), 17137–17142 (2006).
[Crossref] [PubMed]

Milkie, D. E.

K. Wang, D. E. Milkie, A. Saxena, P. Engerer, T. Misgeld, M. E. Bronner, J. Mumm, and E. Betzig, “Rapid adaptive optical recovery of optimal resolution over large volumes,” Nat. Methods 11(6), 625–628 (2014).
[Crossref] [PubMed]

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

Miller, D. T.

Misgeld, T.

K. Wang, D. E. Milkie, A. Saxena, P. Engerer, T. Misgeld, M. E. Bronner, J. Mumm, and E. Betzig, “Rapid adaptive optical recovery of optimal resolution over large volumes,” Nat. Methods 11(6), 625–628 (2014).
[Crossref] [PubMed]

Morandell, K.

Z. V. Guo, S. A. Hires, N. Li, D. H. O’Connor, T. Komiyama, E. Ophir, D. Huber, C. Bonardi, K. Morandell, D. Gutnisky, S. Peron, N. L. Xu, J. Cox, and K. Svoboda, “Procedures for Behavioral Experiments in Head-Fixed Mice,” PLoS ONE 9(2), e88678 (2014).
[Crossref] [PubMed]

Mosk, A. P.

I. M. Vellekoop and A. P. Mosk, “Universal optimal transmission of light through disordered materials,” Phys. Rev. Lett. 101(12), 120601 (2008).
[Crossref] [PubMed]

I. M. Vellekoop and A. P. Mosk, “Focusing coherent light through opaque strongly scattering media,” Opt. Lett. 32(16), 2309–2311 (2007).
[Crossref] [PubMed]

Mumm, J.

K. Wang, D. E. Milkie, A. Saxena, P. Engerer, T. Misgeld, M. E. Bronner, J. Mumm, and E. Betzig, “Rapid adaptive optical recovery of optimal resolution over large volumes,” Nat. Methods 11(6), 625–628 (2014).
[Crossref] [PubMed]

Neil, M. A. A.

M. J. Booth, M. A. A. Neil, R. Juskaitis, and T. Wilson, “Adaptive aberration correction in a confocal microscope,” Proc. Natl. Acad. Sci. U.S.A. 99(9), 5788–5792 (2002).
[Crossref] [PubMed]

Nimmerjahn, A.

A. Nimmerjahn, F. Kirchhoff, J. N. Kerr, and F. Helmchen, “Sulforhodamine 101 as a specific marker of astroglia in the neocortex in vivo,” Nat. Methods 1(1), 31–37 (2004).
[Crossref] [PubMed]

Nussmeier, T. A.

O’Connor, D. H.

Z. V. Guo, S. A. Hires, N. Li, D. H. O’Connor, T. Komiyama, E. Ophir, D. Huber, C. Bonardi, K. Morandell, D. Gutnisky, S. Peron, N. L. Xu, J. Cox, and K. Svoboda, “Procedures for Behavioral Experiments in Head-Fixed Mice,” PLoS ONE 9(2), e88678 (2014).
[Crossref] [PubMed]

O’Meara, T. R.

Ophir, E.

Z. V. Guo, S. A. Hires, N. Li, D. H. O’Connor, T. Komiyama, E. Ophir, D. Huber, C. Bonardi, K. Morandell, D. Gutnisky, S. Peron, N. L. Xu, J. Cox, and K. Svoboda, “Procedures for Behavioral Experiments in Head-Fixed Mice,” PLoS ONE 9(2), e88678 (2014).
[Crossref] [PubMed]

Oron, D.

Owner-Petersen, M.

Z. Popovic, P. Knutsson, J. Thaung, M. Owner-Petersen, and J. Sjöstrand, “Noninvasive imaging of human foveal capillary network using dual-conjugate adaptive optics,” Invest. Ophthalmol. Vis. Sci. 52(5), 2649–2655 (2011).
[Crossref] [PubMed]

J. Thaung, P. Knutsson, Z. Popovic, and M. Owner-Petersen, “Dual-conjugate adaptive optics for wide-field high-resolution retinal imaging,” Opt. Express 17(6), 4454–4467 (2009).
[Crossref] [PubMed]

Pan, F.

H.-T. Xu, F. Pan, G. Yang, and W.-B. Gan, “Choice of cranial window type for in vivo imaging affects dendritic spine turnover in the cortex,” Nat. Neurosci. 10(5), 549–551 (2007).
[Crossref] [PubMed]

Parent, C. A.

T. Lämmermann, P. V. Afonso, B. R. Angermann, J. M. Wang, W. Kastenmüller, C. A. Parent, and R. N. Germain, “Neutrophil swarms require LTB4 and integrins at sites of cell death in vivo,” Nature 498(7454), 371–375 (2013).
[Crossref] [PubMed]

Peron, S.

Z. V. Guo, S. A. Hires, N. Li, D. H. O’Connor, T. Komiyama, E. Ophir, D. Huber, C. Bonardi, K. Morandell, D. Gutnisky, S. Peron, N. L. Xu, J. Cox, and K. Svoboda, “Procedures for Behavioral Experiments in Head-Fixed Mice,” PLoS ONE 9(2), e88678 (2014).
[Crossref] [PubMed]

Popovic, Z.

Z. Popovic, P. Knutsson, J. Thaung, M. Owner-Petersen, and J. Sjöstrand, “Noninvasive imaging of human foveal capillary network using dual-conjugate adaptive optics,” Invest. Ophthalmol. Vis. Sci. 52(5), 2649–2655 (2011).
[Crossref] [PubMed]

J. Thaung, P. Knutsson, Z. Popovic, and M. Owner-Petersen, “Dual-conjugate adaptive optics for wide-field high-resolution retinal imaging,” Opt. Express 17(6), 4454–4467 (2009).
[Crossref] [PubMed]

Roorda, A.

A. Roorda and D. R. Williams, “The arrangement of the three cone classes in the living human eye,” Nature 397(6719), 520–522 (1999).
[Crossref] [PubMed]

Rueckel, M.

M. Rueckel, J. A. Mack-Bucher, and W. Denk, “Adaptive wavefront correction in two-photon microscopy using coherence-gated wavefront sensing,” Proc. Natl. Acad. Sci. U.S.A. 103(46), 17137–17142 (2006).
[Crossref] [PubMed]

Sanguinet, J. A.

Saxena, A.

K. Wang, D. E. Milkie, A. Saxena, P. Engerer, T. Misgeld, M. E. Bronner, J. Mumm, and E. Betzig, “Rapid adaptive optical recovery of optimal resolution over large volumes,” Nat. Methods 11(6), 625–628 (2014).
[Crossref] [PubMed]

Shields, B. C.

H. Dana, T.-w. Chen, A. Hu, B. C. Shields, C. Guo, L. L. Looger, D. S. Kim, and K. Svoboda, “Thy1-GCaMP6 transgenic mice for neuronla population imaging in vivo,” PLoS ONE. in press.

Si, K.

K. Si, R. Fiolka, and M. Cui, “Fluorescence imaging beyond the ballistic regime by ultrasound pulse guided digital phase conjugation,” Nat. Photonics 6(10), 657–661 (2012).
[Crossref] [PubMed]

K. Si, R. Fiolka, and M. Cui, “Breaking the spatial resolution barrier via iterative sound-light interaction in deep tissue microscopy,” Sci. Rep. 2, 748 (2012).
[Crossref] [PubMed]

R. Fiolka, K. Si, and M. Cui, “Complex wavefront corrections for deep tissue focusing using low coherence backscattered light,” Opt. Express 20(15), 16532–16543 (2012).
[Crossref]

Silberberg, Y.

Sjöstrand, J.

Z. Popovic, P. Knutsson, J. Thaung, M. Owner-Petersen, and J. Sjöstrand, “Noninvasive imaging of human foveal capillary network using dual-conjugate adaptive optics,” Invest. Ophthalmol. Vis. Sci. 52(5), 2649–2655 (2011).
[Crossref] [PubMed]

Srinivas, S.

Stoll, S.

S. Stoll, J. Delon, T. M. Brotz, and R. N. Germain, “Dynamic imaging of T cell-dendritic cell interactions in lymph nodes,” Science 296(5574), 1873–1876 (2002).
[Crossref] [PubMed]

Strickler, J. H.

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

Sullivan, W.

Svoboda, K.

Z. V. Guo, S. A. Hires, N. Li, D. H. O’Connor, T. Komiyama, E. Ophir, D. Huber, C. Bonardi, K. Morandell, D. Gutnisky, S. Peron, N. L. Xu, J. Cox, and K. Svoboda, “Procedures for Behavioral Experiments in Head-Fixed Mice,” PLoS ONE 9(2), e88678 (2014).
[Crossref] [PubMed]

K. Svoboda, W. Denk, D. Kleinfeld, and D. W. Tank, “In vivo dendritic calcium dynamics in neocortical pyramidal neurons,” Nature 385(6612), 161–165 (1997).
[Crossref] [PubMed]

H. Dana, T.-w. Chen, A. Hu, B. C. Shields, C. Guo, L. L. Looger, D. S. Kim, and K. Svoboda, “Thy1-GCaMP6 transgenic mice for neuronla population imaging in vivo,” PLoS ONE. in press.

Tal, E.

Tang, J.

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

Tank, D. W.

K. Svoboda, W. Denk, D. Kleinfeld, and D. W. Tank, “In vivo dendritic calcium dynamics in neocortical pyramidal neurons,” Nature 385(6612), 161–165 (1997).
[Crossref] [PubMed]

Tao, X.

Thaung, J.

Z. Popovic, P. Knutsson, J. Thaung, M. Owner-Petersen, and J. Sjöstrand, “Noninvasive imaging of human foveal capillary network using dual-conjugate adaptive optics,” Invest. Ophthalmol. Vis. Sci. 52(5), 2649–2655 (2011).
[Crossref] [PubMed]

J. Thaung, P. Knutsson, Z. Popovic, and M. Owner-Petersen, “Dual-conjugate adaptive optics for wide-field high-resolution retinal imaging,” Opt. Express 17(6), 4454–4467 (2009).
[Crossref] [PubMed]

van Howe, J.

Vellekoop, I. M.

I. M. Vellekoop and A. P. Mosk, “Universal optimal transmission of light through disordered materials,” Phys. Rev. Lett. 101(12), 120601 (2008).
[Crossref] [PubMed]

I. M. Vellekoop and A. P. Mosk, “Focusing coherent light through opaque strongly scattering media,” Opt. Lett. 32(16), 2309–2311 (2007).
[Crossref] [PubMed]

Wang, J. M.

T. Lämmermann, P. V. Afonso, B. R. Angermann, J. M. Wang, W. Kastenmüller, C. A. Parent, and R. N. Germain, “Neutrophil swarms require LTB4 and integrins at sites of cell death in vivo,” Nature 498(7454), 371–375 (2013).
[Crossref] [PubMed]

Wang, K.

K. Wang, D. E. Milkie, A. Saxena, P. Engerer, T. Misgeld, M. E. Bronner, J. Mumm, and E. Betzig, “Rapid adaptive optical recovery of optimal resolution over large volumes,” Nat. Methods 11(6), 625–628 (2014).
[Crossref] [PubMed]

Watanabe, T.

Webb, W. W.

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

Williams, D. R.

Wilson, T.

Xu, C.

Xu, H.-T.

H.-T. Xu, F. Pan, G. Yang, and W.-B. Gan, “Choice of cranial window type for in vivo imaging affects dendritic spine turnover in the cortex,” Nat. Neurosci. 10(5), 549–551 (2007).
[Crossref] [PubMed]

Xu, N. L.

Z. V. Guo, S. A. Hires, N. Li, D. H. O’Connor, T. Komiyama, E. Ophir, D. Huber, C. Bonardi, K. Morandell, D. Gutnisky, S. Peron, N. L. Xu, J. Cox, and K. Svoboda, “Procedures for Behavioral Experiments in Head-Fixed Mice,” PLoS ONE 9(2), e88678 (2014).
[Crossref] [PubMed]

Yang, G.

H.-T. Xu, F. Pan, G. Yang, and W.-B. Gan, “Choice of cranial window type for in vivo imaging affects dendritic spine turnover in the cortex,” Nat. Neurosci. 10(5), 549–551 (2007).
[Crossref] [PubMed]

Zhu, G.

Zipfel, W.

Zuo, Y.

Appl. Opt. (1)

Invest. Ophthalmol. Vis. Sci. (1)

Z. Popovic, P. Knutsson, J. Thaung, M. Owner-Petersen, and J. Sjöstrand, “Noninvasive imaging of human foveal capillary network using dual-conjugate adaptive optics,” Invest. Ophthalmol. Vis. Sci. 52(5), 2649–2655 (2011).
[Crossref] [PubMed]

J. Opt. Soc. Am. A (1)

Nat. Methods (4)

A. Nimmerjahn, F. Kirchhoff, J. N. Kerr, and F. Helmchen, “Sulforhodamine 101 as a specific marker of astroglia in the neocortex in vivo,” Nat. Methods 1(1), 31–37 (2004).
[Crossref] [PubMed]

K. Wang, D. E. Milkie, A. Saxena, P. Engerer, T. Misgeld, M. E. Bronner, J. Mumm, and E. Betzig, “Rapid adaptive optical recovery of optimal resolution over large volumes,” Nat. Methods 11(6), 625–628 (2014).
[Crossref] [PubMed]

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

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

Nat. Neurosci. (2)

H.-T. Xu, F. Pan, G. Yang, and W.-B. Gan, “Choice of cranial window type for in vivo imaging affects dendritic spine turnover in the cortex,” Nat. Neurosci. 10(5), 549–551 (2007).
[Crossref] [PubMed]

D. S. Greenberg, A. R. Houweling, and J. N. Kerr, “Population imaging of ongoing neuronal activity in the visual cortex of awake rats,” Nat. Neurosci. 11(7), 749–751 (2008).
[Crossref] [PubMed]

Nat. Photonics (1)

K. Si, R. Fiolka, and M. Cui, “Fluorescence imaging beyond the ballistic regime by ultrasound pulse guided digital phase conjugation,” Nat. Photonics 6(10), 657–661 (2012).
[Crossref] [PubMed]

Nature (3)

K. Svoboda, W. Denk, D. Kleinfeld, and D. W. Tank, “In vivo dendritic calcium dynamics in neocortical pyramidal neurons,” Nature 385(6612), 161–165 (1997).
[Crossref] [PubMed]

T. Lämmermann, P. V. Afonso, B. R. Angermann, J. M. Wang, W. Kastenmüller, C. A. Parent, and R. N. Germain, “Neutrophil swarms require LTB4 and integrins at sites of cell death in vivo,” Nature 498(7454), 371–375 (2013).
[Crossref] [PubMed]

A. Roorda and D. R. Williams, “The arrangement of the three cone classes in the living human eye,” Nature 397(6719), 520–522 (1999).
[Crossref] [PubMed]

Opt. Express (5)

Opt. Lett. (4)

Phys. Rev. Lett. (1)

I. M. Vellekoop and A. P. Mosk, “Universal optimal transmission of light through disordered materials,” Phys. Rev. Lett. 101(12), 120601 (2008).
[Crossref] [PubMed]

PLoS ONE (1)

Z. V. Guo, S. A. Hires, N. Li, D. H. O’Connor, T. Komiyama, E. Ophir, D. Huber, C. Bonardi, K. Morandell, D. Gutnisky, S. Peron, N. L. Xu, J. Cox, and K. Svoboda, “Procedures for Behavioral Experiments in Head-Fixed Mice,” PLoS ONE 9(2), e88678 (2014).
[Crossref] [PubMed]

Proc. Natl. Acad. Sci. U.S.A. (3)

M. Rueckel, J. A. Mack-Bucher, and W. Denk, “Adaptive wavefront correction in two-photon microscopy using coherence-gated wavefront sensing,” Proc. Natl. Acad. Sci. U.S.A. 103(46), 17137–17142 (2006).
[Crossref] [PubMed]

M. J. Booth, M. A. A. Neil, R. Juskaitis, and T. Wilson, “Adaptive aberration correction in a confocal microscope,” Proc. Natl. Acad. Sci. U.S.A. 99(9), 5788–5792 (2002).
[Crossref] [PubMed]

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

Sci. Rep. (1)

K. Si, R. Fiolka, and M. Cui, “Breaking the spatial resolution barrier via iterative sound-light interaction in deep tissue microscopy,” Sci. Rep. 2, 748 (2012).
[Crossref] [PubMed]

Science (2)

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

S. Stoll, J. Delon, T. M. Brotz, and R. N. Germain, “Dynamic imaging of T cell-dendritic cell interactions in lymph nodes,” Science 296(5574), 1873–1876 (2002).
[Crossref] [PubMed]

Other (2)

P. Kner, J. Sedat, D. Agard, and Z. Kam, “Applying adaptive optics to three-dimensional wide-field microscopy,” in MOEMS-MEMS 2008 Micro and Nanofabrication, (International Society for Optics and Photonics, 2008), 688809–688809–688812.

H. Dana, T.-w. Chen, A. Hu, B. C. Shields, C. Guo, L. L. Looger, D. S. Kim, and K. Svoboda, “Thy1-GCaMP6 transgenic mice for neuronla population imaging in vivo,” PLoS ONE. in press.

Supplementary Material (5)

» Media 1: AVI (828 KB)     
» Media 2: AVI (1183 KB)     
» Media 3: AVI (1217 KB)     
» Media 4: AVI (71 KB)     
» Media 5: AVI (72 KB)     

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Figures (5)

Fig. 1
Fig. 1 The pixel splitting pattern for a 492-pixel segmented MEMS DM (Boston Micromachines Corporation, MA, USA). The red and blue colors represent the two pixel groups.
Fig. 2
Fig. 2 Setup of the multiphoton microscope integrated with IMPACT. RL: relay lens, DM: deformable mirror, M: mirror, DBS: long-pass dichroic beam splitter, L: lens, PMT: photomultiplier tube.
Fig. 3
Fig. 3 Function imaging of S1 cortex with awake, head-restrained GP5.17 mice. (a) Astrocyte imaging with system compensation at 220 µm under the dura. The ‘ + ’ shows the position where the IMPACT measurement was performed. Scale bar: 15 µm. (b) Astrocyte imaging with full (system + sample) compensation. (c) and (d) are the system compensation pattern and full compensation pattern, respectively. (e) shows the signal intensity comparison at the location marked by the arrows in (a). (f) shows the two color imaging of astrocytes and neurons (see Media 1). Red: SR-101 labelled astrocytes, Green: GCaMP6f expressing neurons. Scale bar: 5 µm. (g) ROIs for observing calcium signals. (h) Fluorescence dynamics from spontaneous neuron activity. The numbers correspond to the ROIs labeled in (g).
Fig. 4
Fig. 4 (a) S1 cortex of Thy1-YFP (H line) mice at large depth (~656 µm under the dura). (a) and (b) show the images acquired with system correction (Media 2) and full correction (Media 3), respectively. Scale bar: 5 µm. Laser power applied: ~90 mW. In (b), the yellow arrow marks a spine on the apical dendrite, the white arrow marks the soma of the layer 5 pyramidal cells. (c) shows the full compensation profile. (d) shows the signal intensity comparison at the location marked by the arrows in (a).
Fig. 5
Fig. 5 High resolution neuron imaging at S1 cortex through the intact skull in adult Thy1-YFP (H line) mice. (a) shows the volume view of the dendrite and spines imaged with full correction at 110-126 µm under the bottom of the skull. Volume size: 15x15x16 µm3. Laser power applied: ~80 mW. The volume view is rendered by the segmentation masks of the Simple Neurite Tracer in ImageJ. (b) and (c) show one cross-section of (a) acquired with full correction (Media 4) and system correction (Media 5), respectively. The scale bar is 2 µm. (d) shows the applied full compensation profile.

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