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Research Article

Minimal-invasive enhancement of auditory perception by terahertz wave modulation

Xiaoxuan Tan1,§Kaijie Wu1,§Shuang Liu2Yifang Yuan1Chao Chang1,3( )Wei Xiong2( )
Innovation Laboratory of Terahertz Biophysics, National Innovation Institute of Defense Technology, Beijing 100071, China
School of Life Science, Tsinghua University, Beijing 100071, China
School of Physics, Peking University, Beijing 100071, China

§ Xiaoxuan Tan and Kaijie Wu contributed equally to this work.

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Graphical Abstract

Our exciting results demonstrate a minimal-invasive, non-thermal, and reversible means ofmodulating cochlear hair cell signaling by exposure to terahertz light energy without introducing anyexogenous gene.

Abstract

Hearing impairment is a common disease affecting a substantial proportion of the global population. Currently, the most effective clinical treatment for patients with sensorineural deafness is to implant an artificial electronic cochlea. However, the improvements to hearing perception are variable and limited among healthy subjects. Moreover, cochlear implants have disadvantages, such as crosstalk derived from the currents that spread into non-target tissue between the electrodes. Here, in this work, we describe terahertz wave modulation, a new and minimally invasive technology that can enhance hearing perception in animals by reversible modulation of currents in cochlear hair cells. Using single-cell electrophysiology, guinea pig audiometry, and molecular dynamics simulations, we show that THM can reversibly increase mechano-electrical transducer currents (~ 50% higher) and voltage-gated K+ currents in cochlear hair cells through collective resonance of –C=O groups. In addition, measurement of auditory brainstem response (ABR) in guinea pigs treated with THM indicated a ~ 10 dB increase in hearing sensitivity. This study thus reports a new method of highly spatially selective hearing enhancement without introducing any exogeneous gene, which has potential applications for treatment of hearing disorders as well as several other areas of neuroscience.

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References

1

Sun, S. H.; Babola, T.; Pregernig, G.; So, K. S.; Nguyen, M.; Su, S. S. M.; Palermo, A. T.; Bergles, D. E.; Burns, J. C.; Müller, U. Hair cell mechanotransduction regulates spontaneous activity and spiral ganglion subtype specification in the auditory system. Cell 2018, 174, 1247–1263.e15.

2

Qiu, X. F.; Müller, U. Mechanically gated ion channels in mammalian hair cells. Front. Cell. Neurosci. 2018, 12, 100.

3

Clause, A.; Kim, G.; Sonntag, M.; Weisz, C. J. C.; Vetter, D. E.; Rübsamen, R.; Kandler, K. The precise temporal pattern of prehearing spontaneous activity is necessary for tonotopic map refinement. Neuron 2014, 82, 822–835.

4

Corns, L. F.; Johnson, S. L.; Roberts, T.; Ranatunga, K. M.; Hendry, A.; Ceriani, F.; Safieddine, S.; Steel, K. P.; Forge, A.; Petit, C. et al. Mechanotransduction is required for establishing and maintaining mature inner hair cells and regulating efferent innervation. Nat. Commun. 2018, 9, 4015.

5

Wu, Z. Z; Grillet, N.; Zhao, B.; Cunningham, C.; Harkins-Perry, S.; Coste, B.; Ranade, S.; Zebarjadi, N.; Beurg, M.; Fettiplace, R. et al. Mechanosensory hair cells express two molecularly distinct mechanotransduction channels. Nat. Neurosci. 2017, 20, 24–33.

6

Delmas, P.; Coste, B. Mechano-gated ion channels in sensory systems. Cell 2013, 155, 278–284.

7

Wilson, B. S.; Finley, C. C.; Lawson, D. T.; Wolford, R. D.; Eddington, D. K.; Rabinowitz, W. M. Better speech recognition with cochlear implants. Nature 1991, 352, 236–238.

8

Kipping, D.; Krüger, B.; Nogueira, W. The role of electroneural versus electrophonic stimulation on psychoacoustic electric-acoustic masking in cochlear implant users with residual hearing. Hear. Res. 2020, 395, 108036.

9

Zeng, F. G.; Rebscher, S.; Harrison, W.; Sun, X. A.; Feng, H. H. Cochlear implants: System design, integration, and evaluation. IEEE Rev. Biomed. Eng. 2008, 1, 115–142.

10

Huet, A. T.; Rankovic, V. Application of targeting-optimized chronos for stimulation of the auditory pathway. Methods Mol. Biol. 2021, 2191, 261–285.

11

Oshima, K.; Shin, K.; Diensthuber, M.; Peng, A. W.; Ricci, A. J.; Heller, S. Mechanosensitive hair cell-like cells from embryonic and induced pluripotent stem cells. Cell 2010, 141, 704–716.

12

Li, H. W.; Roblin, G.; Liu, H.; Heller, S. Generation of hair cells by stepwise differentiation of embryonic stem cells. Proc. Natl. Acad. Sci. USA 2003, 100, 13495–13500.

13

Chen, W.; Jongkamonwiwat, N.; Abbas, L.; Eshtan, S. J.; Johnson, S. L.; Kuhn, S.; Milo, M.; Thurlow, J. K.; Andrews, P. W.; Marcotti, W. et al. Restoration of auditory evoked responses by human ES-cell-derived otic progenitors. Nature 2012, 490, 278–282.

14

Lee, D. S.; Lee, J. S.; Oh, S. H.; Kim, S. K.; Kim, J. W.; Chung, J. K.; Lee, M. C.; Kim, C. S. Cross-modal plasticity and cochlear implants. Nature 2001, 409, 149–150.

15

Friesen, L. M.; Shannon, R. V.; Baskent, D.; Wang, X. S. Speech recognition in noise as a function of the number of spectral channels: Comparison of acoustic hearing and cochlear implants. J. Acoust. Soc. Am. 2001, 110, 1150–1163.

16

Wang, J. X.; Lu, J. R.; Tian, L. Effect of fiberoptic collimation technique on 808 nm wavelength laser stimulation of cochlear neurons. Photomed. Laser Surg. 2016, 34, 252–257.

17

Wang, J. X.; Lu, J. R.; Li, C.; Xu, L.; Li, X. F.; Tian, L. Pulsed 980 nm short wavelength infrared neural stimulation in cochlea and laser parameter effects on auditory response characteristics. BioMed. Eng. Online 2015, 14, 89.

18

Fork, R. L. Laser stimulation of nerve cells in Aplysia. Science 1971, 171, 907–908.

19

Liu, X.; Qiao, Z.; Chai, Y. M.; Zhu, Z.; Wu, K. J.; Ji, W. L.; Li, D. G.; Xiao, Y. J.; Mao, L. Q.; Chang, C. et al. Nonthermal and reversible control of neuronal signaling and behavior by midinfrared stimulation. Proc. Natl. Acad. Sci. USA 2021, 118, e2015685118.

20

Zhang, J. X.; He, Y.; Liang, S. S.; Liao, X.; Li, T.; Qiao, Z.; Chang, C.; Jia, H. B.; Chen, X. W. Non-invasive, opsin-free mid-infrared modulation activates cortical neurons and accelerates associative learning. Nat. Commun. 2021, 12, 2730.

21

Izzo, A. D.; Walsh, J. T. Jr.; Jansen, E. D.; Bendett, M.; Webb, J.; Ralph, H.; Richter, C. P. Optical parameter variability in laser nerve stimulation: A study of pulse duration, repetition rate, and wavelength. IEEE Trans. Biomed. Eng. 2007, 54, 1108–1114.

22

Izzo, A. D.; Richter, C. P.; Jansen, E. D.; Walsh, J. T. Jr. Laser stimulation of the auditory nerve. Lasers Surg. Med. 2006, 38, 745–753.

23

Zhao, B.; Wu, Z. Z.; Grillet, N.; Yan, L. X.; Xiong, W.; Harkins-Perry, S.; Müller, U. TMIE is an essential component of the mechanotransduction machinery of cochlear hair cells. Neuron 2014, 84, 954–967.

24

Richter, C. P.; Bayon, R.; Izzo, A. D.; Otting, M.; Suh, E.; Goyal, S.; Hotaling, J.; Walsh, J. T. Jr. Optical stimulation of auditory neurons: Effects of acute and chronic deafening. Hear. Res. 2008, 242, 42–51.

25

Azimzadeh, J. B.; Fabella, B. A.; Kastan, N. R.; Hudspeth, A. J. Thermal excitation of the mechanotransduction apparatus of hair cells. Neuron 2018, 97, 586–595.e4.

26

Liu, S.; Wang, S. F.; Zou, L. Z.; Li, J.; Song, C. M.; Chen, J. F.; Hu, Q.; Liu, L.; Huang, P. B.; Xiong, W. TMC1 is an essential component of a leak channel that modulates tonotopy and excitability of auditory hair cells in mice. eLife 2019, 8, e47441.

27

Albert, E. S.; Bec, J. M.; Desmadryl, G.; Chekroud, K.; Travo, C.; Gaboyard, S.; Bardin, F.; Marc, I.; Dumas, M.; Lenaers, G. et al. TRPV4 channels mediate the infrared laser-evoked response in sensory neurons. J. Neurophysiol. 2012, 107, 3227–3234.

28

Stujenske, J. M.; Spellman, T.; Gordon, J. A. Modeling the spatiotemporal dynamics of light and heat propagation for in vivo optogenetics. Cell Rep. 2015, 12, 525–534.

29

Songer, J. E.; Eatock, R. A. Tuning and timing in mammalian type I hair cells and calyceal synapses. J. Neurosci. 2013, 33, 3706–3724.

30

Jovanovic, S.; Milenkovic, I. Purinergic modulation of activity in the developing auditory pathway. Neurosci. Bull. 2020, 36, 1285–1298.

31

Dierich, M.; Altoè, A.; Koppelmann, J.; Evers, S.; Renigunta, V.; Schäfer, M. K.; Naumann, R.; Verhulst, S.; Oliver, D.; Leitner, M. G. Optimized tuning of auditory inner hair cells to encode complex sound through synergistic activity of six independent K+ current entities. Cell Rep. 2020, 32, 107869.

32

Babola, T. A.; Kersbergen, C. J.; Wang, H. C.; Bergles, D. E. Purinergic signaling in cochlear supporting cells reduces hair cell excitability by increasing the extracellular space. eLife 2020, 9, e52160.

33

Wang, H. C.; Lin, C. C.; Cheung, R.; Zhang-Hooks, Y.; Agarwal, A.; Ellis-Davies, G.; Rock, J.; Bergles, D. E. Spontaneous activity of cochlear hair cells triggered by fluid secretion mechanism in adjacent support cells. Cell 2015, 163, 1348–1359.

34

Johnson, S. L.; Eckrich, T.; Kuhn, S.; Zampini, V.; Franz, C.; Ranatunga, K. M.; Roberts, T. P.; Masetto, S.; Knipper, M.; Kros, C. J. et al. Position-dependent patterning of spontaneous action potentials in immature cochlear inner hair cells. Nat. Neurosci. 2011, 14, 711–717.

35

Kang, S. W.; Ahn, J. W.; Ahn, S. C. Inhibition of K+ outward currents by linopirdine in the cochlear outer hair cells of circling mice within the first postnatal week. Korean J. Physiol. Pharmacol. 2017, 21, 251–257.

36

Kopec, W.; Köpfer, D. A.; Vickery, O. N.; Bondarenko, A. S.; Jansen, T. L. C.; de Groot, B. L.; Zachariae, U. Direct knock-on of desolvated ions governs strict ion selectivity in K+ channels. Nat. Chem. 2018, 10, 813–820.

37
Huang, K. Solid State Physics, 2nd ed.; Peking University Press: Beijing, 2014.
38

Furness, D. N.; Katori, Y.; Kumar, B. N.; Hackney, C. M. The dimensions and structural attachments of tip links in mammalian cochlear hair cells and the effects of exposure to different levels of extracellular calcium. Neuroscience 2008, 154, 10–21.

39

Gillespie, P. G.; Müller, U. Mechanotransduction by hair cells: Models, molecules, and mechanisms. Cell 2009, 139, 33–44.

40

Beurg, M.; Xiong, W.; Zhao, B.; Müller, U.; Fettiplace, R. Subunit determination of the conductance of hair-cell mechanotransducer channels. Proc. Natl. Acad. Sci. USA 2015, 112, 1589–1594.

41

Johnson, S. L.; Beurg, M.; Marcotti, W.; Fettiplace, R. Prestin-driven cochlear amplification is not limited by the outer hair cell membrane time constant. Neuron 2011, 70, 1143–1154.

42

Xiong, W.; Grillet, N.; Elledge, H. M.; Wagner, T. F. J.; Zhao, B.; Johnson, K. R.; Kazmierczak, P.; Müller, U. TMHS is an integral component of the mechanotransduction machinery of cochlear hair cells. Cell 2012, 151, 1283–1295.

43

Thrane, L.; Jacobsen, R. H.; Uhd Jepsen, P.; Keiding, S. R. THz reflection spectroscopy of liquid water. Chem. Phys. Lett. 1995, 240, 330–333.

44

Heyden, M.; Sun, J.; Funkner, S.; Mathias, G.; Forbert, H.; Havenith, M.; Marx, D. Dissecting the THz spectrum of liquid water from first principles via correlations in time and space. Proc. Natl. Acad. Sci. USA 2010, 107, 12068–12073.

45

Chen, X. R.; Wang, Q. H.; Ni, F. Y.; Ma, J. P. Structure of the full-length Shaker potassium channel Kv1. 2 by normal-mode-based X-ray crystallographic refinement. Proc. Natl. Acad. Sci. USA 2010, 107, 11352–11357.

46

Noskov, S. Y.; Bernèche, S.; Roux, B. Control of ion selectivity in potassium channels by electrostatic and dynamic properties of carbonyl ligands. Nature 2004, 431, 830–834.

47

Payandeh, J.; Scheuer, T.; Zheng, N.; Catterall, W. A. The crystal structure of a voltage-gated sodium channel. Nature 2011, 475, 353–358.

48

Tirado-Rives, J.; Jorgensen, W. J. Performance of B3LYP density functional methods for a large set of organic molecules. J. Chem. Theory Comput. 2008, 4, 297–306.

49

Huang, Z.; Chen, B.; Gao, G. Q. IR vibrational assignments for TATB from the density functional B3LYP/6-31G(d) method. J. Mol. Struct. 2005, 752, 87–92.

50
Frisch, M. J.; Trucks, G. W.; Schlegel, H. B.; Scuseria, G. E.; Robb, M. A.; Cheeseman, J. R.; Scalmani, G.; Barone, V.; Petersson, G. A.; Nakatsuji, H. et al. Gaussian 09, Revision A. 01; Gaussian, Inc.: Wallingford CT, 2009.
Nano Research
Pages 5235-5244
Cite this article:
Tan X, Wu K, Liu S, et al. Minimal-invasive enhancement of auditory perception by terahertz wave modulation. Nano Research, 2022, 15(6): 5235-5244. https://doi.org/10.1007/s12274-022-4127-7
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Received: 03 December 2021
Revised: 29 December 2021
Accepted: 30 December 2021
Published: 02 April 2022
© Tsinghua University Press 2022
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