Abstract

We developed a spectral domain optical coherence tomography (SDOCT) fiber optic probe for imaging and sub-nanometer displacement measurements inside the mammalian cochlea. The probe, 140 μm in diameter, can scan laterally up to 400 μm by means of a piezoelectric bender. Two different sampling rates are used, 10 kHz for high-resolution B-scan imaging, and 100 kHz for displacement measurements in order to span the auditory frequency range of gerbil (~50 kHz). Once the cochlear structures are recognized, the scanning range is gradually decreased and ultimately stopped with the probe pointing at the selected angle to measure the simultaneous displacements of multiple structures inside the organ of Corti (OC). The displacement measurement is based on spectral domain phase microscopy. The displacement noise level depends on the A-scan signal of the structure within the OC and we have attained levels as low as ~0.02 nm in in vivo measurements. The system’s broadband infrared light source allows for an imaging depth of ~2.7 mm, and axial resolution of ~3 μm. In future development, the probe can be coupled with an electrode for time-locked voltage and displacement measurements in order to explore the electro-mechanical feedback loop that is key to cochlear processing. Here, we describe the fabrication of the laterally-scanning optical probe, and demonstrate its functionality with in vivo experiments.

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

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2018 (2)

N. P. Cooper, A. Vavakou, and M. van der Heijden, “Vibration hotspots reveal longitudinal funneling of sound-evoked motion in the mammalian cochlea,” Nat. Commun. 9(1), 3054 (2018).
[Crossref] [PubMed]

W. He, D. Kemp, and T. Ren, “Timing of the reticular lamina and basilar membrane vibration in living gerbil cochleae,” eLife 7, 1–17 (2018).
[Crossref] [PubMed]

2017 (1)

N. C. Lin, C. P. Hendon, and E. S. Olson, “Signal Competition in optical coherence tomography and its relevance for cochlear vibrometry,” J. Acoust. Soc. Am. 141(1), 395–405 (2017).
[Crossref] [PubMed]

2016 (2)

2015 (2)

M. E. Pawlowski, S. Shrestha, J. Park, B. E. Applegate, J. S. Oghalai, and T. S. Tkaczyk, “Miniature, minimally invasive, tunable endoscope for investigation of the middle ear,” Biomed. Opt. Express 6(6), 2246–2257 (2015).
[Crossref] [PubMed]

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] [PubMed]

2014 (3)

2013 (1)

W. Dong and E. S. Olson, “Detection of cochlear amplification and its activation,” Biophys. J. 105(4), 1067–1078 (2013).
[Crossref] [PubMed]

2012 (1)

2010 (1)

R. K. Wang and A. L. Nuttall, “Phase-sensitive optical coherence tomography imaging of the tissue motion within the organ of Corti at a subnanometer scale: a preliminary study,” J. Biomed. Opt. 15(5), 056005 (2010).
[Crossref] [PubMed]

2008 (1)

J. Lin, H. Staecker, and M. S. Jafri, “Optical Coherence Tomography Imaging of the Inner Ear: A Feasibility study with Implications for Cochlear Implantation,” Ann. Otol. Rhinol. Laryngol. 117(5), 341–346 (2008).
[Crossref] [PubMed]

2007 (2)

W. S. Rhode, “Basilar membrane mechanics in the 6-9 kHz region of sensitive chinchilla cochleae,” J. Acoust. Soc. Am. 121(5 Pt1), 2792–2804 (2007).
[Crossref] [PubMed]

Y. Mao, S. Chang, S. Sherif, and C. Flueraru, “Graded-index fiber lens proposed for ultrasmall probes used in biomedical imaging,” Appl. Opt. 46(23), 5887–5894 (2007).
[Crossref] [PubMed]

2006 (1)

S. S. Hong and D. M. Freeman, “Doppler optical coherence microscopy for studies of cochlear mechanics,” J. Biomed. Opt. 11(5), 054014 (2006).
[Crossref] [PubMed]

2005 (3)

2003 (1)

M. van der Heijden and P. X. Joris, “Cochlear phase and amplitude retrieved from the auditory nerve at arbitrary frequencies,” J. Neurosci. 23(27), 9194–9198 (2003).
[Crossref] [PubMed]

2002 (2)

E. H. Overstreet, A. N. Temchin, and M. A. Ruggero, “Basilar membrane vibrations near the round window of the gerbil cochlea,” J. Assoc. Res. Otolaryngol. 3(3), 351–361 (2002).
[Crossref] [PubMed]

W. A. Reed, M. F. Yan, and M. J. Schnitzer, “Gradient-index fiber-optic microprobes for minimally invasive in vivo low-coherence interferometry,” Opt. Lett. 27(20), 1794–1796 (2002).
[Crossref] [PubMed]

2001 (2)

E. S. Olson, “Intracochlear pressure measurements related to cochlear tuning,” J. Acoust. Soc. Am. 110(1), 349–367 (2001).
[Crossref] [PubMed]

T. Ren and A. L. Nuttall, “Basilar membrane vibration in the basal turn of the sensitive gerbil cochlea,” Hear. Res. 151(1-2), 48–60 (2001).
[Crossref] [PubMed]

1996 (1)

S. M. Khanna, C. J. Koester, J.-F. Willemin, R. Daendliker, and H. Rosskothen, “Noninvasive optical system for the study of the function of inner ear in living animals,” SPIE 2732, 64–81 (1996).
[Crossref]

1987 (1)

W. L. Emkey and C. Jack, “Analysis and Evaluation of Graded-Index Fiber-Lenses,” J. Lightwave Technol. 5(9), 1156–1164 (1987).
[Crossref]

1980 (1)

D. P. Corey and A. J. Hudspeth, “Mechanical stimulation and micromanipulation with piezoelectric bimorph elements,” J. Neurosci. Methods 3(2), 183–202 (1980).
[Crossref] [PubMed]

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] [PubMed]

M. E. Pawlowski, S. Shrestha, J. Park, B. E. Applegate, J. S. Oghalai, and T. S. Tkaczyk, “Miniature, minimally invasive, tunable endoscope for investigation of the middle ear,” Biomed. Opt. Express 6(6), 2246–2257 (2015).
[Crossref] [PubMed]

Bouma, B.

Cense, B.

Chandra, N.

Chang, S.

Cheon, G. W.

S. S. Gurbani, P. Wilkening, M. Zhao, B. Gonenc, G. W. Cheon, I. I. Iordachita, W. Chien, R. H. Taylor, J. K. Niparko, and J. U. Kang, “Robot-assisted three-dimensional registration for cochlear implant surgery using a common-path swept-source optical coherence tomography probe,” J. Biomed. Opt. 19(5), 057004 (2014).
[Crossref] [PubMed]

Chien, W.

S. S. Gurbani, P. Wilkening, M. Zhao, B. Gonenc, G. W. Cheon, I. I. Iordachita, W. Chien, R. H. Taylor, J. K. Niparko, and J. U. Kang, “Robot-assisted three-dimensional registration for cochlear implant surgery using a common-path swept-source optical coherence tomography probe,” J. Biomed. Opt. 19(5), 057004 (2014).
[Crossref] [PubMed]

Chin, L.

Choma, M. A.

Cooper, N. P.

N. P. Cooper, A. Vavakou, and M. van der Heijden, “Vibration hotspots reveal longitudinal funneling of sound-evoked motion in the mammalian cochlea,” Nat. Commun. 9(1), 3054 (2018).
[Crossref] [PubMed]

Corey, D. P.

D. P. Corey and A. J. Hudspeth, “Mechanical stimulation and micromanipulation with piezoelectric bimorph elements,” J. Neurosci. Methods 3(2), 183–202 (1980).
[Crossref] [PubMed]

Creazzo, T. L.

Curatolo, A.

Daendliker, R.

S. M. Khanna, C. J. Koester, J.-F. Willemin, R. Daendliker, and H. Rosskothen, “Noninvasive optical system for the study of the function of inner ear in living animals,” SPIE 2732, 64–81 (1996).
[Crossref]

de Boer, J.

Dong, W.

W. Dong and E. S. Olson, “Detection of cochlear amplification and its activation,” Biophys. J. 105(4), 1067–1078 (2013).
[Crossref] [PubMed]

Doyle, B. J.

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] [PubMed]

M. A. Choma, A. K. Ellerbee, C. Yang, T. L. Creazzo, and J. A. Izatt, “Spectral-domain phase microscopy,” Opt. Lett. 30(10), 1162–1164 (2005).
[Crossref] [PubMed]

Emkey, W. L.

W. L. Emkey and C. Jack, “Analysis and Evaluation of Graded-Index Fiber-Lenses,” J. Lightwave Technol. 5(9), 1156–1164 (1987).
[Crossref]

Flueraru, C.

Freeman, D. M.

S. S. Hong and D. M. Freeman, “Doppler optical coherence microscopy for studies of cochlear mechanics,” J. Biomed. Opt. 11(5), 054014 (2006).
[Crossref] [PubMed]

Gonenc, B.

S. S. Gurbani, P. Wilkening, M. Zhao, B. Gonenc, G. W. Cheon, I. I. Iordachita, W. Chien, R. H. Taylor, J. K. Niparko, and J. U. Kang, “Robot-assisted three-dimensional registration for cochlear implant surgery using a common-path swept-source optical coherence tomography probe,” J. Biomed. Opt. 19(5), 057004 (2014).
[Crossref] [PubMed]

Gurbani, S. S.

S. S. Gurbani, P. Wilkening, M. Zhao, B. Gonenc, G. W. Cheon, I. I. Iordachita, W. Chien, R. H. Taylor, J. K. Niparko, and J. U. Kang, “Robot-assisted three-dimensional registration for cochlear implant surgery using a common-path swept-source optical coherence tomography probe,” J. Biomed. Opt. 19(5), 057004 (2014).
[Crossref] [PubMed]

Haorah, J.

He, W.

W. He, D. Kemp, and T. Ren, “Timing of the reticular lamina and basilar membrane vibration in living gerbil cochleae,” eLife 7, 1–17 (2018).
[Crossref] [PubMed]

Hendon, C. P.

N. C. Lin, C. P. Hendon, and E. S. Olson, “Signal Competition in optical coherence tomography and its relevance for cochlear vibrometry,” J. Acoust. Soc. Am. 141(1), 395–405 (2017).
[Crossref] [PubMed]

Hong, S. S.

S. S. Hong and D. M. Freeman, “Doppler optical coherence microscopy for studies of cochlear mechanics,” J. Biomed. Opt. 11(5), 054014 (2006).
[Crossref] [PubMed]

Hubbi, B.

Hudspeth, A. J.

D. P. Corey and A. J. Hudspeth, “Mechanical stimulation and micromanipulation with piezoelectric bimorph elements,” J. Neurosci. Methods 3(2), 183–202 (1980).
[Crossref] [PubMed]

Iordachita, I. I.

S. S. Gurbani, P. Wilkening, M. Zhao, B. Gonenc, G. W. Cheon, I. I. Iordachita, W. Chien, R. H. Taylor, J. K. Niparko, and J. U. Kang, “Robot-assisted three-dimensional registration for cochlear implant surgery using a common-path swept-source optical coherence tomography probe,” J. Biomed. Opt. 19(5), 057004 (2014).
[Crossref] [PubMed]

Izatt, J.

Izatt, J. A.

Jack, C.

W. L. Emkey and C. Jack, “Analysis and Evaluation of Graded-Index Fiber-Lenses,” J. Lightwave Technol. 5(9), 1156–1164 (1987).
[Crossref]

Jafri, M. S.

J. Lin, H. Staecker, and M. S. Jafri, “Optical Coherence Tomography Imaging of the Inner Ear: A Feasibility study with Implications for Cochlear Implantation,” Ann. Otol. Rhinol. Laryngol. 117(5), 341–346 (2008).
[Crossref] [PubMed]

Joris, P. X.

M. van der Heijden and P. X. Joris, “Cochlear phase and amplitude retrieved from the auditory nerve at arbitrary frequencies,” J. Neurosci. 23(27), 9194–9198 (2003).
[Crossref] [PubMed]

Kang, J. U.

S. S. Gurbani, P. Wilkening, M. Zhao, B. Gonenc, G. W. Cheon, I. I. Iordachita, W. Chien, R. H. Taylor, J. K. Niparko, and J. U. Kang, “Robot-assisted three-dimensional registration for cochlear implant surgery using a common-path swept-source optical coherence tomography probe,” J. Biomed. Opt. 19(5), 057004 (2014).
[Crossref] [PubMed]

Kemp, D.

W. He, D. Kemp, and T. Ren, “Timing of the reticular lamina and basilar membrane vibration in living gerbil cochleae,” eLife 7, 1–17 (2018).
[Crossref] [PubMed]

Kennedy, B. F.

Kennedy, K. M.

Khanna, S. M.

S. M. Khanna, C. J. Koester, J.-F. Willemin, R. Daendliker, and H. Rosskothen, “Noninvasive optical system for the study of the function of inner ear in living animals,” SPIE 2732, 64–81 (1996).
[Crossref]

Koester, C. J.

S. M. Khanna, C. J. Koester, J.-F. Willemin, R. Daendliker, and H. Rosskothen, “Noninvasive optical system for the study of the function of inner ear in living animals,” SPIE 2732, 64–81 (1996).
[Crossref]

Latham, B.

Lee, H. Y.

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] [PubMed]

Lin, J.

J. Lin, H. Staecker, and M. S. Jafri, “Optical Coherence Tomography Imaging of the Inner Ear: A Feasibility study with Implications for Cochlear Implantation,” Ann. Otol. Rhinol. Laryngol. 117(5), 341–346 (2008).
[Crossref] [PubMed]

Lin, N. C.

N. C. Lin, C. P. Hendon, and E. S. Olson, “Signal Competition in optical coherence tomography and its relevance for cochlear vibrometry,” J. Acoust. Soc. Am. 141(1), 395–405 (2017).
[Crossref] [PubMed]

Liu, X.

Mao, Y.

McLaughlin, R. A.

Mujat, M.

Munro, P. R. T.

Niparko, J. K.

S. S. Gurbani, P. Wilkening, M. Zhao, B. Gonenc, G. W. Cheon, I. I. Iordachita, W. Chien, R. H. Taylor, J. K. Niparko, and J. U. Kang, “Robot-assisted three-dimensional registration for cochlear implant surgery using a common-path swept-source optical coherence tomography probe,” J. Biomed. Opt. 19(5), 057004 (2014).
[Crossref] [PubMed]

Nuttall, A. L.

R. K. Wang and A. L. Nuttall, “Phase-sensitive optical coherence tomography imaging of the tissue motion within the organ of Corti at a subnanometer scale: a preliminary study,” J. Biomed. Opt. 15(5), 056005 (2010).
[Crossref] [PubMed]

T. Ren and A. L. Nuttall, “Basilar membrane vibration in the basal turn of the sensitive gerbil cochlea,” Hear. Res. 151(1-2), 48–60 (2001).
[Crossref] [PubMed]

Oghalai, J. S.

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] [PubMed]

M. E. Pawlowski, S. Shrestha, J. Park, B. E. Applegate, J. S. Oghalai, and T. S. Tkaczyk, “Miniature, minimally invasive, tunable endoscope for investigation of the middle ear,” Biomed. Opt. Express 6(6), 2246–2257 (2015).
[Crossref] [PubMed]

Olson, E. S.

N. C. Lin, C. P. Hendon, and E. S. Olson, “Signal Competition in optical coherence tomography and its relevance for cochlear vibrometry,” J. Acoust. Soc. Am. 141(1), 395–405 (2017).
[Crossref] [PubMed]

Y. Wang and E. S. Olson, “Cochlear perfusion with a viscous fluid,” Hear. Res. 337, 1–11 (2016).
[Crossref] [PubMed]

W. Dong and E. S. Olson, “Detection of cochlear amplification and its activation,” Biophys. J. 105(4), 1067–1078 (2013).
[Crossref] [PubMed]

E. S. Olson, “Intracochlear pressure measurements related to cochlear tuning,” J. Acoust. Soc. Am. 110(1), 349–367 (2001).
[Crossref] [PubMed]

Overstreet, E. H.

E. H. Overstreet, A. N. Temchin, and M. A. Ruggero, “Basilar membrane vibrations near the round window of the gerbil cochlea,” J. Assoc. Res. Otolaryngol. 3(3), 351–361 (2002).
[Crossref] [PubMed]

Park, B.

Park, J.

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] [PubMed]

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N. C. Lin, C. P. Hendon, and E. S. Olson, “Signal Competition in optical coherence tomography and its relevance for cochlear vibrometry,” J. Acoust. Soc. Am. 141(1), 395–405 (2017).
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R. K. Wang and A. L. Nuttall, “Phase-sensitive optical coherence tomography imaging of the tissue motion within the organ of Corti at a subnanometer scale: a preliminary study,” J. Biomed. Opt. 15(5), 056005 (2010).
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[Crossref]

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N. Cooper and M. van der Heijden, “Spatial profiles of sound-evoked vibration in the gerbil cochlea,” AIP Conference Proceedings 1965, C. Bergevin, S. Puria, eds. (2018), p. 080001.

Supplementary Material (1)

NameDescription
» Visualization 1       Probe scanning demonstration.

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Figures (6)

Fig. 1
Fig. 1 A. Microscope image of the probe. B. The A-scan of a water-immersed mirror measured by the probe. The full width at half maximum is 12 μm. C, D. Measured beam profile in the x and y-axes. E. Photograph of the probe on the piezoelectric bender. F. Probe insertion schematic for the in vivo experiments.
Fig. 2
Fig. 2 Probe setup is nonCP for imaging, which uses an external reference arm containing a polarization controller, collimator, iris diaphragm, and a retro-reflector. Once the cochlear structures are recognized, the probe is centered at the desired angle (with the DC voltage controlling the piezoelectric bender that is holding the probe) while scanning (with the sawtooth voltage waveform controlling the bender). The scanning range is gradually decreased and ultimately stopped to position (with only the DC voltage) the probe at the cochlear sensory tissue. We then switched to the CP setup (shown in the blue line).
Fig. 3
Fig. 3 Flow diagram for the modification steps for the signal that drives the bender. A. The original driving signal tapped from the Telesto x-axis scanner has a spike at the end of each period. B. By adding a DC voltage, the spikes are shifted out of the power supply range. Next, the de-spiked signal is low-pass filtered and AC coupled. Then a potentiometer-controlled voltage divider controls the amplitude of the driving signal to vary the scanning FOV. (See Visualization 1 for demonstration.) A DC voltage added to the AC signal with a summing amplifier is used to control the bender “set” angle. The piezo driver multiplies the drive signal by x20.
Fig. 4
Fig. 4 A. Top shows a sketch of the cochlear cross-section. The probe accessed the cochlea’s sensory tissue through the transparent round window. The boxed area is magnified in the lower sketch with the major cochlear structures labeled. B. The B-scan image with the scanning probe, showing the primary structures as in the magnified sketch. The lateral FOV of scanning was gradually decreased (one reduction step shown) and finally stopped for displacement measurements (A-scan location shown with the red dotted line).
Fig. 5
Fig. 5 A. The Fourier-transformed time domain stimulus at 60 dB SPL. B. The displacement frequency spectrum of the BM in the organ of Corti, with a noise floor ~0.02 nm.
Fig. 6
Fig. 6 A. The B-scan of the gerbil cochlea taken with the bulk optics SDOCT system. The RWM is at 540 μm, and the OC is at 600-800 μm. The bench-top and probe SDOCT were measured at the same location for displacement comparison. The bulk-optics’ and probe’s relative beam positions are plotted in the dotted lines, based on their measured A-scans shown on the sides of the B-scan image. The A-scans on the left and right are positioned vertically to coincide with the structures in the B-scan. B. The OC structures’ tuning curves (magnitude referenced to the stapes) and the phases (referenced to the ear canal) are similar for both of the systems.

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