Abstract

We report an innovative technique for the visualization of cells through an overlying scattering medium by combining femtosecond laser bone ablation and two-photon excitation fluorescence (TPEF) microscopy. We demonstrate the technique by imaging hair cells in an intact mouse cochlea ex vivo. Intracochlear imaging is important for the assessment of hearing disorders. However, the small size of the cochlea and its encasement in the densest bone in the body present challenging obstacles, preventing the visualization of the intracochlear microanatomy using standard clinical imaging modalities. The controlled laser ablation reduces the optical scattering of the cochlear bone while the TPEF allows visualization of individual cells behind the bone. We implemented optical coherence tomography (OCT) simultaneously with the laser ablation to enhance the precision of the ablation and prevent inadvertent damage to the cells behind the bone.

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

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2019 (4)

Y. Ren, L. D. Landegger, and K. M. Stankovic, “Gene therapy for human sensorineural hearing loss,” Front. Cell. Neurosci. 13, 323 (2019).
[Crossref]

S. Nyberg, N. J. Abbott, X. R. Shi, P. S. Steyger, and A. Dabdoub, “Delivery of therapeutics to the inner ear: The challenge of the blood-labyrinth barrier,” Sci. Transl. Med. 11(482), eaao0935 (2019).
[Crossref]

W. J. Li, J. Q. Zheng, Y. P. Zhang, F. S. Yuan, and P. J. Lyu, “Temperature and depth evaluation of the in vitro effects of femtosecond laser on oral soft tissue, with or without air-cooling,” Lasers Med. Sci. 34(4), 649–658 (2019).
[Crossref]

E. Kakkava, M. Romito, D. B. Conkey, D. Loterie, K. M. Stankovic, C. Moser, and D. Psaltis, “Selective femtosecond laser ablation via two-photon fluorescence imaging through a multimode fiber,” Biomed. Opt. Express 10(2), 423–433 (2019).
[Crossref]

2018 (4)

J. S. Iyer, N. Zhu, S. Gasilov, H. M. Ladak, S. K. Agrawal, and K. M. Stankovic, “Visualizing the 3D cytoarchitecture of the human cochlea in an intact temporal bone using synchrotron radiation phase contrast imaging,” Biomed. Opt. Express 9(8), 3757–3767 (2018).
[Crossref]

Y. J. Zhao, T. T. Yu, C. Zhang, Z. Li, Q. M. Luo, T. H. Xu, and D. Zhu, “Skull optical clearing window for in vivo imaging of the mouse cortex at synaptic resolution,” Light: Sci. Appl. 7(1), 9 (2018).
[Crossref]

T. G. Landry, M. L. Bance, R. B. Adamson, and J. A. Brown, “No effect of prolonged pulsed high frequency ultrasound imaging of the basilar membrane on cochlear function or hair cell survival found in an initial study,” Hear. Res. 363, 28–38 (2018).
[Crossref]

L. A. Avakyan, E. V. Paramonova, J. Coutinho, S. Oberg, V. S. Bystrov, and L. A. Bugaev, “Optoelectronics and defect levels in hydroxyapatite by first-principles,” J. Chem. Phys. 148(15), 154706 (2018).
[Crossref]

2017 (3)

M. Risoud, J. Sircoglou, G. Dedieu, M. Tardivel, C. Vincent, and N. X. Bonne, “Imaging and cell count in cleared intact cochlea in the mongolian gerbil using laser scanning confocal microscopy,” Eur. Ann. Otorhinolaryngol.-Head Neck Dis. 134(4), 221–224 (2017).
[Crossref]

L. Nolte, N. Tinne, J. Schulze, D. Heinemann, G. C. Antonopoulos, H. Meyer, H. G. Nothwang, T. Lenarz, A. Heisterkamp, A. Warnecke, and T. Ripken, “Scanning laser optical tomography for in toto eimaging of the murine cochlea,” PLoS One 12(4), 10 (2017).
[Crossref]

J. E. Sagers, L. D. Landegger, S. Worthington, J. B. Nadol, and K. M. Stankovic, “Human cochlear histopathology reflects clinical signatures of primary neural degeneration,” Sci. Rep. 7(1), 4884 (2017).
[Crossref]

2016 (2)

J. S. Iyer, S. A. Batts, K. K. Chu, M. I. Sahin, H. M. Leung, G. J. Tearney, and K. M. Stankovic, “Micro-optical coherence tomography of the mammalian cochlea,” Sci. Rep. 6(1), 10 (2016).
[Crossref]

D. B. Conkey, N. Stasio, E. E. Morales-Delgado, M. Romito, C. Moser, and D. Psaltis, “Lensless two-photon imaging through a multicore fiber with coherence-gated digital phase conjugation,” J. Biomed. Opt. 21(4), 045002 (2016).
[Crossref]

2015 (4)

L. J. Mortensen, C. Alt, R. Turcotte, M. Masek, T. M. Liu, D. C. Cote, C. Xu, G. Intini, and C. P. Lin, “Femtosecond laser bone ablation with a high repetition rate fiber laser source,” Biomed. Opt. Express 6(1), 32–42 (2015).
[Crossref]

E. E. Morales-Delgado, D. Psaltis, and C. Moser, “Two-photon imaging through a multimode fiber,” Opt. Express 23(25), 32158–32170 (2015).
[Crossref]

H. Y. Lee, P. D. Raphael, J. Park, A. K. Ellerbee, B. E. Applegate, and J. S. Oghalai, “Noninvasive in vivo imaging reveals differences between tectorial membrane and basilar membrane traveling waves in the mouse cochlea,” Proc. Natl. Acad. Sci. U. S. A. 112(10), 3128–3133 (2015).
[Crossref]

J. H. Park, W. Sun, and M. Cui, “High-resolution in vivo imaging of mouse brain through the intact skull,” Proc. Natl. Acad. Sci. U. S. A. 112(30), 9236–9241 (2015).
[Crossref]

2014 (3)

2013 (5)

S. L. Jacques, “Optical properties of biological tissues: A review,” Phys. Med. Biol. 58(11), R37–R61 (2013).
[Crossref]

D. Zhu, K. V. Larin, Q. M. Luo, and V. V. Tuchin, “Recent progress in tissue optical clearing,” Laser Photonics Rev. 7(5), 732–757 (2013).
[Crossref]

D. C. Jeong, P. S. Tsai, and D. Kleinfeld, “All-optical osteotomy to create windows for transcranial imaging in mice,” Opt. Express 21(20), 23160–23168 (2013).
[Crossref]

E. Papagiakoumou, A. Begue, B. Leshem, O. Schwartz, B. M. Stell, J. Bradley, D. Oron, and V. Emiliani, “Functional patterned multiphoton excitation deep inside scattering tissue,” Nat. Photonics 7(4), 274–278 (2013).
[Crossref]

L. T. Cangueiro and R. Vilar, “Influence of the pulse frequency and water cooling on the femtosecond laser ablation of bovine cortical bone,” Appl. Surf. Sci. 283, 1012–1017 (2013).
[Crossref]

2012 (5)

L. T. Cangueiro, R. Vilar, A. M. B. do Rego, and V. S. F. Muralha, “Femtosecond laser ablation of bovine cortical bone,” J. Biomed. Opt. 17(12), 125005 (2012).
[Crossref]

X. Yang, Y. Pu, C. L. Hsieh, C. A. Ong, D. Psaltis, and K. M. Stankovic, “Two-photon microscopy of the mouse cochlea in situ for cellular diagnosis,” J. Biomed. Opt. 18(3), 031104 (2012).
[Crossref]

A. P. Mosk, A. Lagendijk, G. Lerosey, and M. Fink, “Controlling waves in space and time for imaging and focusing in complex media,” Nat. Photonics 6(5), 283–292 (2012).
[Crossref]

T. Okano and M. W. Kelley, “Stem cell therapy for the inner ear: Recent advances and future directions,” Trends Amplif. 16(1), 4–18 (2012).
[Crossref]

X. Yang, C. L. Hsieh, Y. Pu, and D. Psaltis, “Three-dimensional scanning microscopy through thin turbid media,” Opt. Express 20(3), 2500–2506 (2012).
[Crossref]

2010 (5)

C. L. Hsieh, Y. Pu, R. Grange, and D. Psaltis, “Digital phase conjugation of second harmonic radiation emitted by nanoparticles in turbid media,” Opt. Express 18(12), 12283–12290 (2010).
[Crossref]

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]

S. Popoff, G. Lerosey, M. Fink, A. C. Boccara, and S. Gigan, “Image transmission through an opaque material,” Nat. Commun. 1(1), 81 (2010).
[Crossref]

P. J. Drew, A. Y. Shih, J. D. Driscoll, P. M. Knutsen, P. Blinder, D. Davalos, K. Akassoglou, P. S. Tsai, and D. Kleinfeld, “Chronic optical access through a polished and reinforced thinned skull,” Nat. Methods 7(12), 981–984 (2010).
[Crossref]

G. Yang, F. Pan, C. N. Parkhurst, J. Grutzendler, and W. B. Gan, “Thinned-skull cranial window technique for long-term imaging of the cortex in live mice,” Nat. Protoc. 5(2), 201–208 (2010).
[Crossref]

2008 (3)

A. A. Poznyakovskiy, T. Zahnert, Y. Kalaidzidis, R. Schmidt, B. Fischer, J. Baumgart, and Y. M. Yarin, “The creation of geometric three-dimensional models of the inner ear based on micro computer tomography data,” Hear. Res. 243(1–2), 95–104 (2008).
[Crossref]

O. Kermani, W. Fabian, and H. Lubatschowski, “Real-time optical coherence tomography-guided femtosecond laser sub-bowman keratomileusis on human donor eyes,” Am. J. Ophthalmol. 146(1), 42–45 (2008).
[Crossref]

G. H. MacDonald and E. W. Rubel, “Three-dimensional imaging of the intact mouse cochlea by fluorescent laser scanning confocal microscopy,” Hear. Res. 243(1–2), 1–10 (2008).
[Crossref]

2007 (4)

B. Girard, D. Yu, M. R. Armstrong, B. C. Wilson, C. M. L. Clokie, and R. J. D. Miller, “Effects of femtosecond laser irradiation on osseous tissues,” Lasers Surg. Med. 39(3), 273–285 (2007).
[Crossref]

F. Y. Chen, N. Choudhury, J. F. Zheng, S. Matthews, A. L. Nutall, and S. L. Jacques, “In vivo imaging and low-coherence interferometry of organ of corti vibration,” J. Biomed. Opt. 12(2), 021006 (2007).
[Crossref]

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

L. M. Tiede, S. M. Rocha-Sanchez, R. Hallworth, M. G. Nichols, and K. Beisel, “Determination of hair cell metabolic state in isolated cochlear preparations by two-photon microscopy,” J. Biomed. Opt. 12(2), 021004 (2007).
[Crossref]

2005 (2)

V. V. Tuchin, “Optical clearing of tissues and blood using the immersion method,” J. Phys. D: Appl. Phys. 38(15), 2497–2518 (2005).
[Crossref]

A. Vogel, J. Noack, G. Huttman, and G. Paltauf, “Mechanisms of femtosecond laser nanosurgery of cells and tissues,” Appl. Phys. B: Lasers Opt. 81(8), 1015–1047 (2005).
[Crossref]

2004 (2)

K. Kawamoto, S. H. Sha, R. Minoda, M. Izumikawa, H. Kuriyama, J. Schacht, and Y. Raphael, “Antioxidant gene therapy can protect hearing and hair cells from ototoxicity,” Mol. Ther. 9(2), 173–181 (2004).
[Crossref]

N. Ugryumova, S. J. Matcher, and D. P. Attenburrow, “Measurement of bone mineral density via light scattering,” Phys. Med. Biol. 49(3), 469–483 (2004).
[Crossref]

2003 (1)

K. Kawamoto, M. Yagi, T. Stover, S. Kanzaki, and Y. Raphael, “Hearing and hair cells are protected by adenoviral gene therapy with tgf-beta 1 and gdnf,” Mol. Ther. 7(4), 484–492 (2003).
[Crossref]

2002 (1)

Y. Raphael, “Cochlear pathology, sensory cell death and regeneration,” Br. Med. Bull. 63(1), 25–38 (2002).
[Crossref]

2000 (1)

S. K. Yoo, G. Wang, J. T. Rubinstein, and M. W. Vannier, “Three-dimensional geometric modeling of the cochlea using helico-spiral approximation,” IEEE Trans. Biomed. Eng. 47(10), 1392–1402 (2000).
[Crossref]

1999 (2)

S. A. Boppart, J. Herrmann, C. Pitris, D. L. Stamper, M. E. Brezinski, and J. G. Fujimoto, “High-resolution optical coherence tomography-guided laser ablation of surgical tissue,” J. Surg. Res. 82(2), 275–284 (1999).
[Crossref]

J. Noack and A. Vogel, “Laser-induced plasma formation in water at nanosecond to femtosecond time scales: Calculation of thresholds, absorption coefficients, and energy density,” IEEE J. Quantum Electron. 35(8), 1156–1167 (1999).
[Crossref]

1997 (2)

A. O. Ugnell and P. A. Oberg, “The optical properties of the cochlear bone,” Med. Eng. Phys. 19(7), 630–636 (1997).
[Crossref]

X. Liu, D. Du, and G. Mourou, “Laser ablation and micromachining with ultrashort laser pulses,” IEEE J. Quantum Electron. 33(10), 1706–1716 (1997).
[Crossref]

1996 (3)

A. A. Oraevsky, L. B. DaSilva, A. M. Rubenchik, M. D. Feit, M. E. Glinsky, M. D. Perry, B. M. Mammini, W. Small, and B. C. Stuart, “Plasma mediated ablation of biological tissues with nanosecond-to-femtosecond laser pulses: Relative role of linear and nonlinear absorption,” IEEE J. Sel. Top. Quantum Electron. 2(4), 801–809 (1996).
[Crossref]

T. Juhasz, G. A. Kastis, C. Suarez, Z. Bor, and W. E. Bron, “Time-resolved observations of shock waves and cavitation bubbles generated by femtosecond laser pulses in corneal tissue and water,” Lasers Surg. Med. 19(1), 23–31 (1996).
[Crossref]

W. S. Noyes, T. V. McCaffrey, D. A. Fabry, M. S. Robinette, and V. J. Suman, “Effect of temperature elevation on rabbit cochlear function as measured by distortion-product otoacoustic emissions,” Otolaryngol. Head Neck Surg. 115(6), 548–552 (1996).
[Crossref]

1993 (1)

M. Firbank, M. Hiraoka, M. Essenpreis, and D. T. Delpy, “Measurement of the optical-properties of the skull in the wavelength range 650–950 nm,” Phys. Med. Biol. 38(4), 503–510 (1993).
[Crossref]

1990 (2)

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

K. M. Yoo and R. R. Alfano, “Time-resolved coherent and incoherent components of forward light-scattering in random-media,” Opt. Lett. 15(6), 320–322 (1990).
[Crossref]

1988 (1)

S. C. Feng, C. Kane, P. A. Lee, and A. D. Stone, “Correlations and fluctuations of coherent wave transmission through disordered media,” Phys. Rev. Lett. 61(7), 834–837 (1988).
[Crossref]

1976 (1)

F. Williams, S. P. Varma, and S. Hillenius, “Liquid water as a lone-pair amorphous-semiconductor,” J. Chem. Phys. 64(4), 1549–1554 (1976).
[Crossref]

Abbott, N. J.

S. Nyberg, N. J. Abbott, X. R. Shi, P. S. Steyger, and A. Dabdoub, “Delivery of therapeutics to the inner ear: The challenge of the blood-labyrinth barrier,” Sci. Transl. Med. 11(482), eaao0935 (2019).
[Crossref]

Adamson, R. B.

T. G. Landry, M. L. Bance, R. B. Adamson, and J. A. Brown, “No effect of prolonged pulsed high frequency ultrasound imaging of the basilar membrane on cochlear function or hair cell survival found in an initial study,” Hear. Res. 363, 28–38 (2018).
[Crossref]

Agrawal, S. K.

Akassoglou, K.

P. J. Drew, A. Y. Shih, J. D. Driscoll, P. M. Knutsen, P. Blinder, D. Davalos, K. Akassoglou, P. S. Tsai, and D. Kleinfeld, “Chronic optical access through a polished and reinforced thinned skull,” Nat. Methods 7(12), 981–984 (2010).
[Crossref]

Alfano, R. R.

Alt, C.

Antonopoulos, G. C.

L. Nolte, N. Tinne, J. Schulze, D. Heinemann, G. C. Antonopoulos, H. Meyer, H. G. Nothwang, T. Lenarz, A. Heisterkamp, A. Warnecke, and T. Ripken, “Scanning laser optical tomography for in toto eimaging of the murine cochlea,” PLoS One 12(4), 10 (2017).
[Crossref]

Applegate, B. E.

H. Y. Lee, P. D. Raphael, J. Park, A. K. Ellerbee, B. E. Applegate, and J. S. Oghalai, “Noninvasive in vivo imaging reveals differences between tectorial membrane and basilar membrane traveling waves in the mouse cochlea,” Proc. Natl. Acad. Sci. U. S. A. 112(10), 3128–3133 (2015).
[Crossref]

Armstrong, M. R.

B. Girard, D. Yu, M. R. Armstrong, B. C. Wilson, C. M. L. Clokie, and R. J. D. Miller, “Effects of femtosecond laser irradiation on osseous tissues,” Lasers Surg. Med. 39(3), 273–285 (2007).
[Crossref]

Attenburrow, D. P.

N. Ugryumova, S. J. Matcher, and D. P. Attenburrow, “Measurement of bone mineral density via light scattering,” Phys. Med. Biol. 49(3), 469–483 (2004).
[Crossref]

Avakyan, L. A.

L. A. Avakyan, E. V. Paramonova, J. Coutinho, S. Oberg, V. S. Bystrov, and L. A. Bugaev, “Optoelectronics and defect levels in hydroxyapatite by first-principles,” J. Chem. Phys. 148(15), 154706 (2018).
[Crossref]

Bance, M. L.

T. G. Landry, M. L. Bance, R. B. Adamson, and J. A. Brown, “No effect of prolonged pulsed high frequency ultrasound imaging of the basilar membrane on cochlear function or hair cell survival found in an initial study,” Hear. Res. 363, 28–38 (2018).
[Crossref]

Batts, S. A.

J. S. Iyer, S. A. Batts, K. K. Chu, M. I. Sahin, H. M. Leung, G. J. Tearney, and K. M. Stankovic, “Micro-optical coherence tomography of the mammalian cochlea,” Sci. Rep. 6(1), 10 (2016).
[Crossref]

Baumgart, J.

A. A. Poznyakovskiy, T. Zahnert, Y. Kalaidzidis, R. Schmidt, B. Fischer, J. Baumgart, and Y. M. Yarin, “The creation of geometric three-dimensional models of the inner ear based on micro computer tomography data,” Hear. Res. 243(1–2), 95–104 (2008).
[Crossref]

Begue, A.

E. Papagiakoumou, A. Begue, B. Leshem, O. Schwartz, B. M. Stell, J. Bradley, D. Oron, and V. Emiliani, “Functional patterned multiphoton excitation deep inside scattering tissue,” Nat. Photonics 7(4), 274–278 (2013).
[Crossref]

Beisel, K.

L. M. Tiede, S. M. Rocha-Sanchez, R. Hallworth, M. G. Nichols, and K. Beisel, “Determination of hair cell metabolic state in isolated cochlear preparations by two-photon microscopy,” J. Biomed. Opt. 12(2), 021004 (2007).
[Crossref]

Ben-Yakar, A.

O. Ferhanoglu, M. Yildirim, K. Subramanian, and A. Ben-Yakar, “A 5-mm piezo-scanning fiber device for high speed ultrafast laser microsurgery,” Biomed. Opt. Express 5(7), 2023–2036 (2014).
[Crossref]

C. L. Hoy, O. Ferhanoglu, M. Yildirim, K. H. Kim, S. S. Karajanagi, K. M. C. Chan, J. B. Kobler, S. M. Zeitels, and A. Ben-Yakar, “Clinical ultrafast laser surgery: Recent advances and future directions,” IEEE J. Sel. Top. Quantum Electron. 20(2), 14 (2014).
[Crossref]

Blinder, P.

P. J. Drew, A. Y. Shih, J. D. Driscoll, P. M. Knutsen, P. Blinder, D. Davalos, K. Akassoglou, P. S. Tsai, and D. Kleinfeld, “Chronic optical access through a polished and reinforced thinned skull,” Nat. Methods 7(12), 981–984 (2010).
[Crossref]

Boccara, A. C.

S. Popoff, G. Lerosey, M. Fink, A. C. Boccara, and S. Gigan, “Image transmission through an opaque material,” Nat. Commun. 1(1), 81 (2010).
[Crossref]

Bonne, N. X.

M. Risoud, J. Sircoglou, G. Dedieu, M. Tardivel, C. Vincent, and N. X. Bonne, “Imaging and cell count in cleared intact cochlea in the mongolian gerbil using laser scanning confocal microscopy,” Eur. Ann. Otorhinolaryngol.-Head Neck Dis. 134(4), 221–224 (2017).
[Crossref]

Boppart, S. A.

S. A. Boppart, J. Herrmann, C. Pitris, D. L. Stamper, M. E. Brezinski, and J. G. Fujimoto, “High-resolution optical coherence tomography-guided laser ablation of surgical tissue,” J. Surg. Res. 82(2), 275–284 (1999).
[Crossref]

Bor, Z.

T. Juhasz, G. A. Kastis, C. Suarez, Z. Bor, and W. E. Bron, “Time-resolved observations of shock waves and cavitation bubbles generated by femtosecond laser pulses in corneal tissue and water,” Lasers Surg. Med. 19(1), 23–31 (1996).
[Crossref]

Bradley, J.

E. Papagiakoumou, A. Begue, B. Leshem, O. Schwartz, B. M. Stell, J. Bradley, D. Oron, and V. Emiliani, “Functional patterned multiphoton excitation deep inside scattering tissue,” Nat. Photonics 7(4), 274–278 (2013).
[Crossref]

Brezinski, M. E.

S. A. Boppart, J. Herrmann, C. Pitris, D. L. Stamper, M. E. Brezinski, and J. G. Fujimoto, “High-resolution optical coherence tomography-guided laser ablation of surgical tissue,” J. Surg. Res. 82(2), 275–284 (1999).
[Crossref]

Bron, W. E.

T. Juhasz, G. A. Kastis, C. Suarez, Z. Bor, and W. E. Bron, “Time-resolved observations of shock waves and cavitation bubbles generated by femtosecond laser pulses in corneal tissue and water,” Lasers Surg. Med. 19(1), 23–31 (1996).
[Crossref]

Brown, J. A.

T. G. Landry, M. L. Bance, R. B. Adamson, and J. A. Brown, “No effect of prolonged pulsed high frequency ultrasound imaging of the basilar membrane on cochlear function or hair cell survival found in an initial study,” Hear. Res. 363, 28–38 (2018).
[Crossref]

Bugaev, L. A.

L. A. Avakyan, E. V. Paramonova, J. Coutinho, S. Oberg, V. S. Bystrov, and L. A. Bugaev, “Optoelectronics and defect levels in hydroxyapatite by first-principles,” J. Chem. Phys. 148(15), 154706 (2018).
[Crossref]

Bystrov, V. S.

L. A. Avakyan, E. V. Paramonova, J. Coutinho, S. Oberg, V. S. Bystrov, and L. A. Bugaev, “Optoelectronics and defect levels in hydroxyapatite by first-principles,” J. Chem. Phys. 148(15), 154706 (2018).
[Crossref]

Cangueiro, L. T.

L. T. Cangueiro and R. Vilar, “Influence of the pulse frequency and water cooling on the femtosecond laser ablation of bovine cortical bone,” Appl. Surf. Sci. 283, 1012–1017 (2013).
[Crossref]

L. T. Cangueiro, R. Vilar, A. M. B. do Rego, and V. S. F. Muralha, “Femtosecond laser ablation of bovine cortical bone,” J. Biomed. Opt. 17(12), 125005 (2012).
[Crossref]

Chan, K. M. C.

C. L. Hoy, O. Ferhanoglu, M. Yildirim, K. H. Kim, S. S. Karajanagi, K. M. C. Chan, J. B. Kobler, S. M. Zeitels, and A. Ben-Yakar, “Clinical ultrafast laser surgery: Recent advances and future directions,” IEEE J. Sel. Top. Quantum Electron. 20(2), 14 (2014).
[Crossref]

Chen, F. Y.

F. Y. Chen, N. Choudhury, J. F. Zheng, S. Matthews, A. L. Nutall, and S. L. Jacques, “In vivo imaging and low-coherence interferometry of organ of corti vibration,” J. Biomed. Opt. 12(2), 021006 (2007).
[Crossref]

Cho, N. H.

Choudhury, N.

F. Y. Chen, N. Choudhury, J. F. Zheng, S. Matthews, A. L. Nutall, and S. L. Jacques, “In vivo imaging and low-coherence interferometry of organ of corti vibration,” J. Biomed. Opt. 12(2), 021006 (2007).
[Crossref]

Chu, K. K.

J. S. Iyer, S. A. Batts, K. K. Chu, M. I. Sahin, H. M. Leung, G. J. Tearney, and K. M. Stankovic, “Micro-optical coherence tomography of the mammalian cochlea,” Sci. Rep. 6(1), 10 (2016).
[Crossref]

Clokie, C. M. L.

B. Girard, D. Yu, M. R. Armstrong, B. C. Wilson, C. M. L. Clokie, and R. J. D. Miller, “Effects of femtosecond laser irradiation on osseous tissues,” Lasers Surg. Med. 39(3), 273–285 (2007).
[Crossref]

Cobbold, R. S. C.

R. S. C. Cobbold, Foundations of Biomedical Ultrasound (Oxford University Press, 2007).

Conkey, D. B.

E. Kakkava, M. Romito, D. B. Conkey, D. Loterie, K. M. Stankovic, C. Moser, and D. Psaltis, “Selective femtosecond laser ablation via two-photon fluorescence imaging through a multimode fiber,” Biomed. Opt. Express 10(2), 423–433 (2019).
[Crossref]

D. B. Conkey, N. Stasio, E. E. Morales-Delgado, M. Romito, C. Moser, and D. Psaltis, “Lensless two-photon imaging through a multicore fiber with coherence-gated digital phase conjugation,” J. Biomed. Opt. 21(4), 045002 (2016).
[Crossref]

Cote, D. C.

Coutinho, J.

L. A. Avakyan, E. V. Paramonova, J. Coutinho, S. Oberg, V. S. Bystrov, and L. A. Bugaev, “Optoelectronics and defect levels in hydroxyapatite by first-principles,” J. Chem. Phys. 148(15), 154706 (2018).
[Crossref]

Cui, M.

J. H. Park, W. Sun, and M. Cui, “High-resolution in vivo imaging of mouse brain through the intact skull,” Proc. Natl. Acad. Sci. U. S. A. 112(30), 9236–9241 (2015).
[Crossref]

Dabdoub, A.

S. Nyberg, N. J. Abbott, X. R. Shi, P. S. Steyger, and A. Dabdoub, “Delivery of therapeutics to the inner ear: The challenge of the blood-labyrinth barrier,” Sci. Transl. Med. 11(482), eaao0935 (2019).
[Crossref]

DaSilva, L. B.

A. A. Oraevsky, L. B. DaSilva, A. M. Rubenchik, M. D. Feit, M. E. Glinsky, M. D. Perry, B. M. Mammini, W. Small, and B. C. Stuart, “Plasma mediated ablation of biological tissues with nanosecond-to-femtosecond laser pulses: Relative role of linear and nonlinear absorption,” IEEE J. Sel. Top. Quantum Electron. 2(4), 801–809 (1996).
[Crossref]

Davalos, D.

P. J. Drew, A. Y. Shih, J. D. Driscoll, P. M. Knutsen, P. Blinder, D. Davalos, K. Akassoglou, P. S. Tsai, and D. Kleinfeld, “Chronic optical access through a polished and reinforced thinned skull,” Nat. Methods 7(12), 981–984 (2010).
[Crossref]

Dedieu, G.

M. Risoud, J. Sircoglou, G. Dedieu, M. Tardivel, C. Vincent, and N. X. Bonne, “Imaging and cell count in cleared intact cochlea in the mongolian gerbil using laser scanning confocal microscopy,” Eur. Ann. Otorhinolaryngol.-Head Neck Dis. 134(4), 221–224 (2017).
[Crossref]

Delpy, D. T.

M. Firbank, M. Hiraoka, M. Essenpreis, and D. T. Delpy, “Measurement of the optical-properties of the skull in the wavelength range 650–950 nm,” Phys. Med. Biol. 38(4), 503–510 (1993).
[Crossref]

Denk, W.

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

do Rego, A. M. B.

L. T. Cangueiro, R. Vilar, A. M. B. do Rego, and V. S. F. Muralha, “Femtosecond laser ablation of bovine cortical bone,” J. Biomed. Opt. 17(12), 125005 (2012).
[Crossref]

Drew, P. J.

P. J. Drew, A. Y. Shih, J. D. Driscoll, P. M. Knutsen, P. Blinder, D. Davalos, K. Akassoglou, P. S. Tsai, and D. Kleinfeld, “Chronic optical access through a polished and reinforced thinned skull,” Nat. Methods 7(12), 981–984 (2010).
[Crossref]

Driscoll, J. D.

P. J. Drew, A. Y. Shih, J. D. Driscoll, P. M. Knutsen, P. Blinder, D. Davalos, K. Akassoglou, P. S. Tsai, and D. Kleinfeld, “Chronic optical access through a polished and reinforced thinned skull,” Nat. Methods 7(12), 981–984 (2010).
[Crossref]

Du, D.

X. Liu, D. Du, and G. Mourou, “Laser ablation and micromachining with ultrashort laser pulses,” IEEE J. Quantum Electron. 33(10), 1706–1716 (1997).
[Crossref]

Ellerbee, A. K.

H. Y. Lee, P. D. Raphael, J. Park, A. K. Ellerbee, B. E. Applegate, and J. S. Oghalai, “Noninvasive in vivo imaging reveals differences between tectorial membrane and basilar membrane traveling waves in the mouse cochlea,” Proc. Natl. Acad. Sci. U. S. A. 112(10), 3128–3133 (2015).
[Crossref]

Emiliani, V.

E. Papagiakoumou, A. Begue, B. Leshem, O. Schwartz, B. M. Stell, J. Bradley, D. Oron, and V. Emiliani, “Functional patterned multiphoton excitation deep inside scattering tissue,” Nat. Photonics 7(4), 274–278 (2013).
[Crossref]

Essenpreis, M.

M. Firbank, M. Hiraoka, M. Essenpreis, and D. T. Delpy, “Measurement of the optical-properties of the skull in the wavelength range 650–950 nm,” Phys. Med. Biol. 38(4), 503–510 (1993).
[Crossref]

Fabian, W.

O. Kermani, W. Fabian, and H. Lubatschowski, “Real-time optical coherence tomography-guided femtosecond laser sub-bowman keratomileusis on human donor eyes,” Am. J. Ophthalmol. 146(1), 42–45 (2008).
[Crossref]

Fabry, D. A.

W. S. Noyes, T. V. McCaffrey, D. A. Fabry, M. S. Robinette, and V. J. Suman, “Effect of temperature elevation on rabbit cochlear function as measured by distortion-product otoacoustic emissions,” Otolaryngol. Head Neck Surg. 115(6), 548–552 (1996).
[Crossref]

Feit, M. D.

A. A. Oraevsky, L. B. DaSilva, A. M. Rubenchik, M. D. Feit, M. E. Glinsky, M. D. Perry, B. M. Mammini, W. Small, and B. C. Stuart, “Plasma mediated ablation of biological tissues with nanosecond-to-femtosecond laser pulses: Relative role of linear and nonlinear absorption,” IEEE J. Sel. Top. Quantum Electron. 2(4), 801–809 (1996).
[Crossref]

Feng, S. C.

S. C. Feng, C. Kane, P. A. Lee, and A. D. Stone, “Correlations and fluctuations of coherent wave transmission through disordered media,” Phys. Rev. Lett. 61(7), 834–837 (1988).
[Crossref]

Ferhanoglu, O.

C. L. Hoy, O. Ferhanoglu, M. Yildirim, K. H. Kim, S. S. Karajanagi, K. M. C. Chan, J. B. Kobler, S. M. Zeitels, and A. Ben-Yakar, “Clinical ultrafast laser surgery: Recent advances and future directions,” IEEE J. Sel. Top. Quantum Electron. 20(2), 14 (2014).
[Crossref]

O. Ferhanoglu, M. Yildirim, K. Subramanian, and A. Ben-Yakar, “A 5-mm piezo-scanning fiber device for high speed ultrafast laser microsurgery,” Biomed. Opt. Express 5(7), 2023–2036 (2014).
[Crossref]

Fink, M.

A. P. Mosk, A. Lagendijk, G. Lerosey, and M. Fink, “Controlling waves in space and time for imaging and focusing in complex media,” Nat. Photonics 6(5), 283–292 (2012).
[Crossref]

S. Popoff, G. Lerosey, M. Fink, A. C. Boccara, and S. Gigan, “Image transmission through an opaque material,” Nat. Commun. 1(1), 81 (2010).
[Crossref]

Firbank, M.

M. Firbank, M. Hiraoka, M. Essenpreis, and D. T. Delpy, “Measurement of the optical-properties of the skull in the wavelength range 650–950 nm,” Phys. Med. Biol. 38(4), 503–510 (1993).
[Crossref]

Fischer, B.

A. A. Poznyakovskiy, T. Zahnert, Y. Kalaidzidis, R. Schmidt, B. Fischer, J. Baumgart, and Y. M. Yarin, “The creation of geometric three-dimensional models of the inner ear based on micro computer tomography data,” Hear. Res. 243(1–2), 95–104 (2008).
[Crossref]

Fujimoto, J. G.

S. A. Boppart, J. Herrmann, C. Pitris, D. L. Stamper, M. E. Brezinski, and J. G. Fujimoto, “High-resolution optical coherence tomography-guided laser ablation of surgical tissue,” J. Surg. Res. 82(2), 275–284 (1999).
[Crossref]

Gan, W. B.

G. Yang, F. Pan, C. N. Parkhurst, J. Grutzendler, and W. B. Gan, “Thinned-skull cranial window technique for long-term imaging of the cortex in live mice,” Nat. Protoc. 5(2), 201–208 (2010).
[Crossref]

Gasilov, S.

Gigan, S.

S. Popoff, G. Lerosey, M. Fink, A. C. Boccara, and S. Gigan, “Image transmission through an opaque material,” Nat. Commun. 1(1), 81 (2010).
[Crossref]

Girard, B.

B. Girard, D. Yu, M. R. Armstrong, B. C. Wilson, C. M. L. Clokie, and R. J. D. Miller, “Effects of femtosecond laser irradiation on osseous tissues,” Lasers Surg. Med. 39(3), 273–285 (2007).
[Crossref]

Glinsky, M. E.

A. A. Oraevsky, L. B. DaSilva, A. M. Rubenchik, M. D. Feit, M. E. Glinsky, M. D. Perry, B. M. Mammini, W. Small, and B. C. Stuart, “Plasma mediated ablation of biological tissues with nanosecond-to-femtosecond laser pulses: Relative role of linear and nonlinear absorption,” IEEE J. Sel. Top. Quantum Electron. 2(4), 801–809 (1996).
[Crossref]

Grange, R.

Grutzendler, J.

G. Yang, F. Pan, C. N. Parkhurst, J. Grutzendler, and W. B. Gan, “Thinned-skull cranial window technique for long-term imaging of the cortex in live mice,” Nat. Protoc. 5(2), 201–208 (2010).
[Crossref]

Hallworth, R.

L. M. Tiede, S. M. Rocha-Sanchez, R. Hallworth, M. G. Nichols, and K. Beisel, “Determination of hair cell metabolic state in isolated cochlear preparations by two-photon microscopy,” J. Biomed. Opt. 12(2), 021004 (2007).
[Crossref]

Heinemann, D.

L. Nolte, N. Tinne, J. Schulze, D. Heinemann, G. C. Antonopoulos, H. Meyer, H. G. Nothwang, T. Lenarz, A. Heisterkamp, A. Warnecke, and T. Ripken, “Scanning laser optical tomography for in toto eimaging of the murine cochlea,” PLoS One 12(4), 10 (2017).
[Crossref]

Heisterkamp, A.

L. Nolte, N. Tinne, J. Schulze, D. Heinemann, G. C. Antonopoulos, H. Meyer, H. G. Nothwang, T. Lenarz, A. Heisterkamp, A. Warnecke, and T. Ripken, “Scanning laser optical tomography for in toto eimaging of the murine cochlea,” PLoS One 12(4), 10 (2017).
[Crossref]

Herrmann, J.

S. A. Boppart, J. Herrmann, C. Pitris, D. L. Stamper, M. E. Brezinski, and J. G. Fujimoto, “High-resolution optical coherence tomography-guided laser ablation of surgical tissue,” J. Surg. Res. 82(2), 275–284 (1999).
[Crossref]

Hillenius, S.

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Figures (6)

Fig. 1.
Fig. 1. Experimental setup for ultrafast laser ablation of cochlear bone. (a) Laser ablation setup combined with the OCT system. The ablation beam is expanded, collimated and directed into the OCT head. After the beamsplitter (BS), both OCT beam and ablation beam reach a pair of galvanometric mirrors (GM1 and GM2) and are then redirected toward the focusing objective (OBJ) onto the sample (S). L1 and L2, lenses. M1-M4, mirrors. (b) User interface for the control of laser ablation. The interface allows the control of simultaneous real time OCT and BF imaging systems, the choice of the laser parameters for ablation, the selection of the targeted area and the OCT imaging comparison of the sample before and after ablation.
Fig. 2.
Fig. 2. Preparation of a whole mount sample covered with a bony chip for TPEF efficiency studies. (a) Sectional sketch of the sample. The whole mount includes a fixed OC stained with Rhodamine 6G and placed between two microscope slides (in blue). The bony chip varies in thickness (based on precise laser ablation) and is placed on the coverslipped whole mount. (b) Schematic of the light transmission through cochlear bone. Depending on bone thickness, a certain amount of light will excite the OC and a fraction of emitted light will be collected back for imaging. CB, cochlear bone. OC, organ of Corti. OBJ, objective.
Fig. 3.
Fig. 3. Dissection of a murine cochlea. (a) Photograph of an extracted murine inner ear. (b) Image of the cochlea as viewed using the integrated BF microscope in the OCT system. Anatomic details are clearly visible. Arrows point to the natural windows (round and oval windows) in the cochlea. Scale bar: 1 mm.
Fig. 4.
Fig. 4. Ultrafast laser ablation of murine cochlear bone. (a) Bright-field view of the ablated bone area (150×150 µm2). (b) A-scan OCT of the bone sample along the yellow dashed line in (a) before ablation. (c) A-scan OCT of the bone sample along the yellow dashed line in (a) after ablation. Scale bars: 50 µm. (d) Single-round ablation depth (rate of ablation) as a function of pulse energy delivered to the sample at various focal positions. Blue squares, laser focus is on the bone surface. Green circles, laser focus is 5 µm into the bone surface. Red triangles, laser focus is 10 µm into the bone surface. Cyan triangles, laser focus is 20 µm into the bone surface. Black solid diamonds, average rate of ablation. Error bars represent one standard deviation. Black line is a visual aide. (e) Ablation depth as a function of rounds of ablation at constant feeding steps of the laser focus. Colors represent pulse energy used. Blue, 0.82 µJ. Green, 1.3 µJ. Red, 2.0 µJ. Cyan, 2.8 µJ. Symbols represent feeding step size. Squares, 5 µm. Circles, 10 µm. Triangles, 20 µm. Gray shaded region shows range of ablation depth practically achievable. (f) Measurements of the optical properties of bone based on ablation-controlled thickness. The combined scattering and absorption coefficient is 203 cm−1, which are not separated. Gray shaded region suggests the possible range of variations among different samples.
Fig. 5.
Fig. 5. Effects of bone thickness on the imaging through cochlear bone. (a) Distorted laser focus of 0.25 NA through different bone thicknesses. Curves are the intensity line profiles across the center of the focal spots normalized with the undistorted focus intensity. Insets show the corresponding images of the foci. (b) TPEF microscopy images in cochlear whole mounts through three bone thicknesses at three levels of excitation laser power. Mouse intracochlear structures are clearly visible through bone chips of 60 µm and 100 µm thickness. The images show signs of photobleaching at the thickness of 60 µm, and reduced acuity and contrast at 100 µm thickness. Images through a 250 µm thick bone chip requires the highest excitation power used to reveal vaguely identifiable structures with a significantly compromised acuity and contrast. The excitation wavelength used was 785 nm, and the whole mounts were stained with Rhodamine 6G. IHC, inner hair cell. OHC, outer hair cell. TC, tunnel of Corti. Scale bars: 20 µm.
Fig. 6.
Fig. 6. Intracochlear hair cell imaging in intact murine cochlea through laser-ablated bone. (a) The BF image of the 3D intact cochlea before the ablation. Red dashed rectangle indicates the ablation area. (b) Cross-sectional OCT image acquired along the red arrow line in (a). (c) The BF image of the 3D intact cochlea before the ablation. (d) Cross-sectional OCT image acquired along the red arrow line in (c). Scale bars: 100 µm. (e) (f) (g) Three TPEF microscopy images acquired while focusing from the external ablated cochlear surface to the region of the organ of Corti, revealing intracochlear cells and anatomic details. Hair cells were stained with Phalloidin 488. AB, apical bone. OC, organ of Corti. SM, scala media. M, interscalar septum. IHC, inner hair cell. OHC, outer hair cell. TC, tunnel of Corti. Scale bars: 10 µm.

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