Abstract

For in vivo deep tissue imaging, high order wavefront measurement and correction is needed for handling the severe wavefront distortion. Towards such a goal, we have developed the iterative multi-photon adaptive compensation technique (IMPACT). In this work, we explore using IMPACT to perform calcium imaging of neocortex through the intact skull of adult mice, and to image through the highly scattering white matter on the hippocampus surface.

© 2015 Optical Society of America

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References

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  1. F. Helmchen and W. Denk, “Deep tissue two-photon microscopy,” Nat. Methods 2(12), 932–940 (2005).
    [Crossref] [PubMed]
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    [Crossref] [PubMed]
  3. 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 neuronal population imaging in vivo,” PLoS ONE 9(9), e108697 (2014).
    [Crossref] [PubMed]
  4. K. Chung and K. Deisseroth, “CLARITY for mapping the nervous system,” Nat. Methods 10(6), 508–513 (2013).
    [Crossref] [PubMed]
  5. N. G. Horton, K. Wang, D. Kobat, C. G. Clark, F. W. Wise, C. B. Schaffer, and C. Xu, “In vivo three-photon microscopy of subcortical structures within an intact mouse brain,” Nat. Photonics 7(3), 205–209 (2013).
    [Crossref] [PubMed]
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    [Crossref] [PubMed]
  7. 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]
  8. O. Katz, P. Heidmann, M. Fink, and S. Gigan, “Non-invasive single-shot imaging through scattering layers and around corners via speckle correlations,” Nat. Photonics 8(10), 784–790 (2014).
    [Crossref]
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    [Crossref] [PubMed]
  10. O. Katz, E. Small, and Y. Silberberg, “Looking around corners and through thin turbid layers in real time with scattered incoherent light,” Nat. Photonics 6(8), 549–553 (2012).
    [Crossref]
  11. C. L. Hsieh, Y. Pu, R. Grange, G. Laporte, and D. Psaltis, “Imaging through turbid layers by scanning the phase conjugated second harmonic radiation from a nanoparticle,” Opt. Express 18(20), 20723–20731 (2010).
    [Crossref] [PubMed]
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  13. X. Xu, H. Liu, and L. V. Wang, “Time-reversed ultrasonically encoded optical focusing into scattering media,” Nat. Photonics 5(3), 154–157 (2011).
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  14. Y. M. Wang, B. Judkewitz, C. A. Dimarzio, and C. Yang, “Deep-tissue focal fluorescence imaging with digitally time-reversed ultrasound-encoded light,” Nat. Commun. 3, 928 (2012).
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  15. 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]
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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
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    [Crossref] [PubMed]
  24. L. Kong and M. Cui, “In vivo fluorescence microscopy via iterative multi-photon adaptive compensation technique,” Opt. Express 22(20), 23786–23794 (2014).
    [Crossref] [PubMed]
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    [Crossref] [PubMed]
  26. G. Katona, G. Szalay, P. Maák, A. Kaszás, M. Veress, D. Hillier, B. Chiovini, E. S. Vizi, B. Roska, and B. Rózsa, “Fast two-photon in vivo imaging with three-dimensional random-access scanning in large tissue volumes,” Nat. Methods 9(2), 201–208 (2012).
    [Crossref] [PubMed]
  27. M. Cui, “A numerical study of multi-conjugate large area wavefront correction for deep tissue microscopy ” submitted (2015).

2014 (4)

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 neuronal population imaging in vivo,” PLoS ONE 9(9), e108697 (2014).
[Crossref] [PubMed]

O. Katz, P. Heidmann, M. Fink, and S. Gigan, “Non-invasive single-shot imaging through scattering layers and around corners via speckle correlations,” Nat. Photonics 8(10), 784–790 (2014).
[Crossref]

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]

L. Kong and M. Cui, “In vivo fluorescence microscopy via iterative multi-photon adaptive compensation technique,” Opt. Express 22(20), 23786–23794 (2014).
[Crossref] [PubMed]

2013 (5)

H. P. Paudel, C. Stockbridge, J. Mertz, and T. Bifano, “Focusing polychromatic light through strongly scattering media,” Opt. Express 21(14), 17299–17308 (2013).
[Crossref] [PubMed]

P. Kner, “Phase diversity for three-dimensional imaging,” J. Opt. Soc. Am. A 30(10), 1980–1987 (2013).
[Crossref] [PubMed]

K. Chung and K. Deisseroth, “CLARITY for mapping the nervous system,” Nat. Methods 10(6), 508–513 (2013).
[Crossref] [PubMed]

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

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 (9)

Y. M. Wang, B. Judkewitz, C. A. Dimarzio, and C. Yang, “Deep-tissue focal fluorescence imaging with digitally time-reversed ultrasound-encoded light,” Nat. Commun. 3, 928 (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]

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]

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]

G. Katona, G. Szalay, P. Maák, A. Kaszás, M. Veress, D. Hillier, B. Chiovini, E. S. Vizi, B. Roska, and B. Rózsa, “Fast two-photon in vivo imaging with three-dimensional random-access scanning in large tissue volumes,” Nat. Methods 9(2), 201–208 (2012).
[Crossref] [PubMed]

O. Katz, E. Small, and Y. Silberberg, “Looking around corners and through thin turbid layers in real time with scattered incoherent light,” Nat. Photonics 6(8), 549–553 (2012).
[Crossref]

S. G. Adie, B. W. Graf, A. Ahmad, P. S. Carney, and S. A. Boppart, “Computational adaptive optics for broadband optical interferometric tomography of biological tissue,” Proc. Natl. Acad. Sci. U.S.A. 109(19), 7175–7180 (2012).
[Crossref] [PubMed]

D. B. Conkey, A. M. Caravaca-Aguirre, and R. Piestun, “High-speed scattering medium characterization with application to focusing light through turbid media,” Opt. Express 20(2), 1733–1740 (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 (1)

X. Xu, H. Liu, and L. V. Wang, “Time-reversed ultrasonically encoded optical focusing into scattering media,” Nat. Photonics 5(3), 154–157 (2011).
[Crossref] [PubMed]

2010 (2)

D. A. Dombeck, C. D. Harvey, L. Tian, L. L. Looger, and D. W. Tank, “Functional imaging of hippocampal place cells at cellular resolution during virtual navigation,” Nat. Neurosci. 13(11), 1433–1440 (2010).
[Crossref] [PubMed]

C. L. Hsieh, Y. Pu, R. Grange, G. Laporte, and D. Psaltis, “Imaging through turbid layers by scanning the phase conjugated second harmonic radiation from a nanoparticle,” Opt. Express 18(20), 20723–20731 (2010).
[Crossref] [PubMed]

2009 (1)

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]

G. Lerosey, J. de Rosny, A. Tourin, and M. Fink, “Focusing beyond the diffraction limit with far-field time reversal,” Science 315(5815), 1120–1122 (2007).
[Crossref] [PubMed]

2005 (1)

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

2002 (1)

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]

Adie, S. G.

S. G. Adie, B. W. Graf, A. Ahmad, P. S. Carney, and S. A. Boppart, “Computational adaptive optics for broadband optical interferometric tomography of biological tissue,” Proc. Natl. Acad. Sci. U.S.A. 109(19), 7175–7180 (2012).
[Crossref] [PubMed]

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]

Ahmad, A.

S. G. Adie, B. W. Graf, A. Ahmad, P. S. Carney, and S. A. Boppart, “Computational adaptive optics for broadband optical interferometric tomography of biological tissue,” Proc. Natl. Acad. Sci. U.S.A. 109(19), 7175–7180 (2012).
[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]

Bifano, T.

Booth, M. J.

D. Débarre, E. J. Botcherby, T. Watanabe, S. Srinivas, M. J. Booth, and T. Wilson, “Image-based adaptive optics for two-photon microscopy,” Opt. Lett. 34(16), 2495–2497 (2009).
[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]

Boppart, S. A.

S. G. Adie, B. W. Graf, A. Ahmad, P. S. Carney, and S. A. Boppart, “Computational adaptive optics for broadband optical interferometric tomography of biological tissue,” Proc. Natl. Acad. Sci. U.S.A. 109(19), 7175–7180 (2012).
[Crossref] [PubMed]

Botcherby, E. J.

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]

Caravaca-Aguirre, A. M.

Carney, P. S.

S. G. Adie, B. W. Graf, A. Ahmad, P. S. Carney, and S. A. Boppart, “Computational adaptive optics for broadband optical interferometric tomography of biological tissue,” Proc. Natl. Acad. Sci. U.S.A. 109(19), 7175–7180 (2012).
[Crossref] [PubMed]

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 neuronal population imaging in vivo,” PLoS ONE 9(9), e108697 (2014).
[Crossref] [PubMed]

Chiovini, B.

G. Katona, G. Szalay, P. Maák, A. Kaszás, M. Veress, D. Hillier, B. Chiovini, E. S. Vizi, B. Roska, and B. Rózsa, “Fast two-photon in vivo imaging with three-dimensional random-access scanning in large tissue volumes,” Nat. Methods 9(2), 201–208 (2012).
[Crossref] [PubMed]

Chung, K.

K. Chung and K. Deisseroth, “CLARITY for mapping the nervous system,” Nat. Methods 10(6), 508–513 (2013).
[Crossref] [PubMed]

Clark, C. G.

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

Conkey, D. B.

Crest, J.

Cui, M.

L. Kong and M. Cui, “In vivo fluorescence microscopy via iterative multi-photon adaptive compensation technique,” Opt. Express 22(20), 23786–23794 (2014).
[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]

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]

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 neuronal population imaging in vivo,” PLoS ONE 9(9), e108697 (2014).
[Crossref] [PubMed]

de Rosny, J.

G. Lerosey, J. de Rosny, A. Tourin, and M. Fink, “Focusing beyond the diffraction limit with far-field time reversal,” Science 315(5815), 1120–1122 (2007).
[Crossref] [PubMed]

Débarre, D.

Deisseroth, K.

K. Chung and K. Deisseroth, “CLARITY for mapping the nervous system,” Nat. Methods 10(6), 508–513 (2013).
[Crossref] [PubMed]

Denk, W.

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

Dimarzio, C. A.

Y. M. Wang, B. Judkewitz, C. A. Dimarzio, and C. Yang, “Deep-tissue focal fluorescence imaging with digitally time-reversed ultrasound-encoded light,” Nat. Commun. 3, 928 (2012).
[Crossref] [PubMed]

Dombeck, D. A.

D. A. Dombeck, C. D. Harvey, L. Tian, L. L. Looger, and D. W. Tank, “Functional imaging of hippocampal place cells at cellular resolution during virtual navigation,” Nat. Neurosci. 13(11), 1433–1440 (2010).
[Crossref] [PubMed]

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]

Fink, M.

O. Katz, P. Heidmann, M. Fink, and S. Gigan, “Non-invasive single-shot imaging through scattering layers and around corners via speckle correlations,” Nat. Photonics 8(10), 784–790 (2014).
[Crossref]

G. Lerosey, J. de Rosny, A. Tourin, and M. Fink, “Focusing beyond the diffraction limit with far-field time reversal,” Science 315(5815), 1120–1122 (2007).
[Crossref] [PubMed]

Fiolka, R.

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]

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]

Gigan, S.

O. Katz, P. Heidmann, M. Fink, and S. Gigan, “Non-invasive single-shot imaging through scattering layers and around corners via speckle correlations,” Nat. Photonics 8(10), 784–790 (2014).
[Crossref]

Graf, B. W.

S. G. Adie, B. W. Graf, A. Ahmad, P. S. Carney, and S. A. Boppart, “Computational adaptive optics for broadband optical interferometric tomography of biological tissue,” Proc. Natl. Acad. Sci. U.S.A. 109(19), 7175–7180 (2012).
[Crossref] [PubMed]

Grange, R.

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 neuronal population imaging in vivo,” PLoS ONE 9(9), e108697 (2014).
[Crossref] [PubMed]

Harvey, C. D.

D. A. Dombeck, C. D. Harvey, L. Tian, L. L. Looger, and D. W. Tank, “Functional imaging of hippocampal place cells at cellular resolution during virtual navigation,” Nat. Neurosci. 13(11), 1433–1440 (2010).
[Crossref] [PubMed]

Heidmann, P.

O. Katz, P. Heidmann, M. Fink, and S. Gigan, “Non-invasive single-shot imaging through scattering layers and around corners via speckle correlations,” Nat. Photonics 8(10), 784–790 (2014).
[Crossref]

Helmchen, F.

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

Hillier, D.

G. Katona, G. Szalay, P. Maák, A. Kaszás, M. Veress, D. Hillier, B. Chiovini, E. S. Vizi, B. Roska, and B. Rózsa, “Fast two-photon in vivo imaging with three-dimensional random-access scanning in large tissue volumes,” Nat. Methods 9(2), 201–208 (2012).
[Crossref] [PubMed]

Horton, N. G.

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

Hsieh, C. L.

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 neuronal population imaging in vivo,” PLoS ONE 9(9), e108697 (2014).
[Crossref] [PubMed]

Judkewitz, B.

Y. M. Wang, B. Judkewitz, C. A. Dimarzio, and C. Yang, “Deep-tissue focal fluorescence imaging with digitally time-reversed ultrasound-encoded light,” Nat. Commun. 3, 928 (2012).
[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]

Kaszás, A.

G. Katona, G. Szalay, P. Maák, A. Kaszás, M. Veress, D. Hillier, B. Chiovini, E. S. Vizi, B. Roska, and B. Rózsa, “Fast two-photon in vivo imaging with three-dimensional random-access scanning in large tissue volumes,” Nat. Methods 9(2), 201–208 (2012).
[Crossref] [PubMed]

Katona, G.

G. Katona, G. Szalay, P. Maák, A. Kaszás, M. Veress, D. Hillier, B. Chiovini, E. S. Vizi, B. Roska, and B. Rózsa, “Fast two-photon in vivo imaging with three-dimensional random-access scanning in large tissue volumes,” Nat. Methods 9(2), 201–208 (2012).
[Crossref] [PubMed]

Katz, O.

O. Katz, P. Heidmann, M. Fink, and S. Gigan, “Non-invasive single-shot imaging through scattering layers and around corners via speckle correlations,” Nat. Photonics 8(10), 784–790 (2014).
[Crossref]

O. Katz, E. Small, and Y. Silberberg, “Looking around corners and through thin turbid layers in real time with scattered incoherent light,” Nat. Photonics 6(8), 549–553 (2012).
[Crossref]

Kim, D. S.

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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 neuronal population imaging in vivo,” PLoS ONE 9(9), e108697 (2014).
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G. Katona, G. Szalay, P. Maák, A. Kaszás, M. Veress, D. Hillier, B. Chiovini, E. S. Vizi, B. Roska, and B. Rózsa, “Fast two-photon in vivo imaging with three-dimensional random-access scanning in large tissue volumes,” Nat. Methods 9(2), 201–208 (2012).
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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).
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N. G. Horton, K. Wang, D. Kobat, C. G. Clark, F. W. Wise, C. B. Schaffer, and C. Xu, “In vivo three-photon microscopy of subcortical structures within an intact mouse brain,” Nat. Photonics 7(3), 205–209 (2013).
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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 neuronal population imaging in vivo,” PLoS ONE 9(9), e108697 (2014).
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D. A. Dombeck, C. D. Harvey, L. Tian, L. L. Looger, and D. W. Tank, “Functional imaging of hippocampal place cells at cellular resolution during virtual navigation,” Nat. Neurosci. 13(11), 1433–1440 (2010).
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G. Katona, G. Szalay, P. Maák, A. Kaszás, M. Veress, D. Hillier, B. Chiovini, E. S. Vizi, B. Roska, and B. Rózsa, “Fast two-photon in vivo imaging with three-dimensional random-access scanning in large tissue volumes,” Nat. Methods 9(2), 201–208 (2012).
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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).
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N. G. Horton, K. Wang, D. Kobat, C. G. Clark, F. W. Wise, C. B. Schaffer, and C. Xu, “In vivo three-photon microscopy of subcortical structures within an intact mouse brain,” Nat. Photonics 7(3), 205–209 (2013).
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N. G. Horton, K. Wang, D. Kobat, C. G. Clark, F. W. Wise, C. B. Schaffer, and C. Xu, “In vivo three-photon microscopy of subcortical structures within an intact mouse brain,” Nat. Photonics 7(3), 205–209 (2013).
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J. Opt. Soc. Am. A (1)

Nat. Commun. (1)

Y. M. Wang, B. Judkewitz, C. A. Dimarzio, and C. Yang, “Deep-tissue focal fluorescence imaging with digitally time-reversed ultrasound-encoded light,” Nat. Commun. 3, 928 (2012).
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G. Katona, G. Szalay, P. Maák, A. Kaszás, M. Veress, D. Hillier, B. Chiovini, E. S. Vizi, B. Roska, and B. Rózsa, “Fast two-photon in vivo imaging with three-dimensional random-access scanning in large tissue volumes,” Nat. Methods 9(2), 201–208 (2012).
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Nat. Neurosci. (1)

D. A. Dombeck, C. D. Harvey, L. Tian, L. L. Looger, and D. W. Tank, “Functional imaging of hippocampal place cells at cellular resolution during virtual navigation,” Nat. Neurosci. 13(11), 1433–1440 (2010).
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Nat. Photonics (5)

N. G. Horton, K. Wang, D. Kobat, C. G. Clark, F. W. Wise, C. B. Schaffer, and C. Xu, “In vivo three-photon microscopy of subcortical structures within an intact mouse brain,” Nat. Photonics 7(3), 205–209 (2013).
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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 (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).
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Opt. Express (5)

Opt. Lett. (2)

PLoS ONE (1)

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 neuronal population imaging in vivo,” PLoS ONE 9(9), e108697 (2014).
[Crossref] [PubMed]

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

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]

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).
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S. G. Adie, B. W. Graf, A. Ahmad, P. S. Carney, and S. A. Boppart, “Computational adaptive optics for broadband optical interferometric tomography of biological tissue,” Proc. Natl. Acad. Sci. U.S.A. 109(19), 7175–7180 (2012).
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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 (1)

G. Lerosey, J. de Rosny, A. Tourin, and M. Fink, “Focusing beyond the diffraction limit with far-field time reversal,” Science 315(5815), 1120–1122 (2007).
[Crossref] [PubMed]

Other (1)

M. Cui, “A numerical study of multi-conjugate large area wavefront correction for deep tissue microscopy ” submitted (2015).

Supplementary Material (4)

» Media 1: AVI (2251 KB)     
» Media 2: AVI (2251 KB)     
» Media 3: AVI (714 KB)     
» Media 4: AVI (1385 KB)     

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Figures (3)

Fig. 1
Fig. 1 Setup of the IMPACT based multi-photon imaging system. RL: relay lens, DM: deformable mirror, M: mirror, DBS: long-pass dichroic beam splitter, L: lens, PMT: photomultiplier tube. The inset: photo of the head-restrained mouse under anesthesia. HP: head post; GM: gas mask.
Fig. 2
Fig. 2 Calcium imaging through the intact skull of adult mice. (a) The scheme of through skull imaging. (b) and (c) The dendrites and spines labeled by dsRed and GCaMP6 at 176 µm below the surface of the skull, acquired with the full compensation (e). Scale bar: 5 µm. The image stack at 168-197 µm is shown in Media 1. (d) The regions of interest (ROIs) used for signal extraction. (f) Calcium dynamics at these ROIs due to spontaneous neural activities. The raw data is shown in Media 2.
Fig. 3
Fig. 3 Imaging through the white matter on the hippocampal surface (cortex aspirated). (a) The volume view of the hippocampus (100 × 100 × 650 µm3) from the CA1 region to the dentate gyrus. A: alveus, PC: pyramidal cells of CA1, DGC: dentate granule cells. Laser power used: 26 mW (P1) for the top 400 µm, 78 mW (P2) for the bottom 250 µm. (b) The myelinated axons at 18 µm depth. The red dash circle highlights the cell body of a microglia. (c) and (d) are the system and full compensation pattern at 398 µm depth. (e) and (f) are the corresponding images acquired with the system and full correction, respectively. Scale bar: 6 µm. Laser power: 75 mW. The image stack at 391-400 µm is shown in Media 3. (g) The signal intensity comparison along the dash line in (e). (h) and (i) are the images of the dentate granule cells at 579 µm depth acquired with the system compensation pattern (c) and the full compensation pattern (j), respectively. Scale bar: 10 µm. Laser power: 75 mW. The image stack at 570-588 µm is shown in Media 4. (k) The signal intensity comparison along the dash line in (h).

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