Abstract
Among neural prostheses, cochlear implants (CIs) are considered the most successful devices. To date, they have benefited more than 324,000 patients with severe-to-profound hearing loss. CIs directly stimulate the auditory nerve and restore some hearing. Despite the great success of the devices, the outcomes in performance are variable. CI users often have difficulties in speech recognition in challenging listening environments and their perception of music is limited. It has been argued that performance correlates with the number of independent channels, which can be used to transmit information to the brain. While physical properties of the tissue result in a wide spread of the electrical current in contemporary devices and limit the number of independent channels, other modes of stimulation may provide an opportunity to increase spatial selectivity of neural stimulation and thus increase the number of independent channels for information transfer. An improvement in performance of the implant users is expected. This chapter provides an overview of the opportunities and the contemporary challenges of neural stimulation with light regarding auditory prostheses.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Acker, L., Huang, B., Hancock, K. E., Hauswirth, W., Boyden, E. S., et al. (2011). Channelrhodopsin-2 gene transfection of central auditory neurons: Toward an optical prosthesis. Abstracts of the Association for Research in Otolaryngology, 34, 484.
Albert, E. S., Bec, J. M., Desmadryl, G., Chekroud, K., Travo, C., et al. (2012). TRPV4 channels mediate the infrared laser-evoked response in sensory neurons. Journal of Neurophysiology, 107, 3227–3234.
Amoodi, H. A., Mick, P. T., Shipp, D. B., Friesen, L. M., Nedzelski, J. M., et al. (2012). Results with cochlear implantation in adults with speech recognition scores exceeding current criteria. Otology & Neurotology, 33, 6–12.
Baker, C. A., Montey, K. L., Pongstaporn, T., & Ryugo, D. K. (2010). Postnatal development of the endbulb of held in congenitally deaf cats. Frontiers in Neuroanatomy, 4, 19.
Balaban, C. D., Zhou, J., & Li, H. (2003). Type 1 vanilloid receptor expression by mammalian inner ear ganglion cells. Hearing Research, 175, 165–170.
Balster, S., Wenzel, G. I., Warnecke, A., Steffens, M., Rettenmaier, A., et al. (2014). Optical cochlear implant: Evaluation of insertion forces of optical fibres in a cochlear model and of traumata in human temporal bones. Biomedizinische Technik/Biomedical Engineering, 59, 19–28.
Baskent, D., & Shannon, R. V. (2005). Interactions between cochlear implant electrode insertion depth and frequency-place mapping. The Journal of the Acoustical Society of America, 117, 1405–1416.
Baumhoff, P., Schultz, M., Kallweit, N., Krueger, A., Ripken, T., et al. (2013). Midbrain activity evoked by pulsed laser light. Poster 135, 2013 Conference on Implantable Auditory Prostheses, Lake Tahoe.
Berndt, A., Yizhar, O., Gunaydin, L. A., Hegemann, P., & Deisseroth, K. (2009). Bi-stable neural state switches. Nature Neuroscience, 12, 229–234.
Bernstein, J. G., Garrity, P. A., & Boyden, E. S. (2012). Optogenetics and thermogenetics: Technologies for controlling the activity of targeted cells within intact neural circuits. Current Opinion in Neurobiology, 22, 61–71.
Boutros, P. J., Ahn, J., Fridman, G. Y., Dai, C., Lasker, D., & Della Santina, C. C. (2013). Vestibulo-ocular reflex eye movement responses to infra-red laser stimulation of the mammalian labyrinth. Abstracts of the Association for Research in Otolaryngology, 36, 255.
Boyden, E. S., Zhang, F., Bamberg, E., Nagel, G., & Deisseroth, K. (2005). Millisecond-timescale, genetically targeted optical control of neural activity. Nature Neuroscience, 8, 1263–1268.
Caterina, M. J., Schumacher, M. A., Tominaga, M., Rosen, T. A., Levine, J. D., & Julius, D. (1997). The capsaicin receptor: A heat-activated ion channel in the pain pathway. Nature, 389, 816–824.
Cox, D. B., Platt, R. J., & Zhang, F. (2015). Therapeutic genome editing: Prospects and challenges. Nature Medicine, 21, 121–131.
Darrow, K., Slama, M., Kempfle, J., Boyden, E. S., Polley, D., et al. (2013a). Optogenetic control of central auditory neurons. Abstracts of the Association for Research in Otolaryngology, 36, 695.
Darrow, K., Slama, M., Kempfle, J., Boyden, E. S., Polley, D., et al. (2013b). A comparison of electrical and optical activation of midbrain and cortical pathways in mice expressing channelrhodopsin-2 in the cochlear nucleus. Abstracts of the Association for Research in Otolaryngology, 36, 265.
Della Santina, C. C., Migliaccio, A. A., Hayden, R., Melvin, T. A., Fridman, G. Y., et al. (2010). Current and future management of bilateral loss of vestibular sensation: An update on the Johns Hopkins Multichannel Vestibular Prosthesis Project. Cochlear Implants International, 11(Suppl. 2), 2–11.
Dittami, G. M., Rajguru, S. M., Lasher, R. A., Hitchcock, R. W., & Rabbitt, R. D. (2011). Intracellular calcium transients evoked by pulsed infrared radiation in neonatal cardiomyocytes. Journal of Physiology, 589, 1295–1306.
Feng, H. J., Kao, C., Gallagher, M. J., Jansen, E. D., Mahadevan-Jansen, A., et al. (2010). Alteration of GABAergic neurotransmission by pulsed infrared laser stimulation. Journal of Neuroscience Methods, 192, 110–114.
Firszt, J. B., Koch, D. B., Downing, M., & Litvak, L. (2007). Current steering creates additional pitch percepts in adult cochlear implant recipients. Otology & Neurotology, 28, 629–636.
Fishman, K. E., Shannon, R. V., & Slattery, W. H. (1997). Speech recognition as a function of the number of electrodes used in the SPEAK cochlear implant speech processor. Journal of Speech, Language, and Hearing Research, 40, 1201–1215.
Fridberger, A., & Ren, T. (2006). Local mechanical stimulation of the hearing organ by laser irradiation. NeuroReport, 17, 33–37.
Friedmann, D. R., Green, J., Fang, Y., Ensor, K., Roland, J. T., & Waltzman, S. B. (2015). Sequential bilateral cochlear implantation in the adolescent population. The Laryngoscope, 125(8), 1952–1958.
Golub, J. S., Ling, L., Nie, K., Nowack, A., Shepherd, S. J., et al. (2014). Prosthetic implantation of the human vestibular system. Otology & Neurotology, 35, 136–147.
Green, K. M., Ramsden, R. T., Julyan, P. J., & Hastings, D. E. (2008). Cortical plasticity in the first year after cochlear implantation. Cochlear Implants International, 9, 103–117.
Grill, W. M., Norman, S. E., & Bellamkonda, R. V. (2009). Implanted neural interfaces: Biochallenges and engineered solutions. Annual Review of Biomedical Engineering, 11, 1–24.
Güler, A. D., Lee, H., Iida, T., Shimizu, I., Tominaga, M., & Caterina, M. (2002). Heat-evoked activation of the ion channel, TRPV4. Journal of Neuroscience, 22, 6408–6414.
Harris, D. M., Bierer, S. M., Wells, J. D., & Phillips, J. O. (2009). Optical nerve stimulation for a vestibular prosthesis. In Proceedings of SPIE 7180, Photons and neurons, 71800R.
Hartmann, R., Topp, G., & Klinke, R. (1984). Discharge patterns of cat primary auditory fibers with electrical stimulation of the cochlea. Hearing Research, 13, 47–62.
Hernandez, V. H., Gehrt, A., Reuter, K., Jing, Z., Jeschke, M., et al. (2014). Optogenetic stimulation of the auditory pathway. Journal of Clinical Investigation, 124, 1114–1129.
Holstein, G. R., Martinelli, G. P., Boyle, R., Rabbitt, R. D., & Highstein, S. M. (2004a). Ultrastructural observations of efferent terminals in the crista ampullaris of the toadfish, Opsanus tau. Experimental Brain Research, 155, 265–273.
Holstein, G. R., Rabbitt, R. D., Martinelli, G. P., Friedrich, V. L., Jr., Boyle, R. D., & Highstein, S. M. (2004b). Convergence of excitatory and inhibitory hair cell transmitters shapes vestibular afferent responses. Proceedings of the National Academy of Sciences of the USA, 101, 15766–15771.
Izzo, A. D., Richter, C.-P., Jansen, E. D., & Walsh, J. T. (2006). Laser stimulation of the auditory nerve. Lasers in Surgery and Medicine, 38, 745–753.
Izzo, A. D., Suh, E., Pathria, J., Walsh, J. T., Whitlon, D. S., & Richter, C. P. (2007a). Selectivity of neural stimulation in the auditory system: A comparison of optic and electric stimuli. Journal of Biomedical Optics, 12, 021008.
Izzo, A. D., Walsh, J. T., Jansen, E. D., Bendett, M., et al. (2007b). Optical parameter variability in laser nerve stimulation: A study of pulse duration, repetition rate, and wavelength. IEEE Transactions on Biomedical Engineering, 54, 1108–1114.
Izzo, A. D., Walsh, J. T., Ralph, H., Webb, J., Bendett, M., et al. (2008). Laser stimulation of auditory neurons at shorter pulse durations and penetration depths. Biophysical Journal, 94(8), 3159–3166.
Jeschke, M., & Moser, T. (2015). Considering optogenetic stimulation for cochlear implants. Hearing Research, 322, 224–234.
Katz, E. J., Ilev, I. K., Krauthamer, V., Kim do, H., & Weinreich, D. (2010). Excitation of primary afferent neurons by near-infrared light in vitro. NeuroReport, 21, 662–666.
Limb, C. J. (2006). Cochlear implant-mediated perception of music. Current Opinion in Otolaryngology & Head and Neck Surgery, 14, 337–340.
Limb, C. J., & Roy, A. T. (2014). Technological, biological, and acoustical constraints to music perception in cochlear implant users. Hearing Research, 308, 13–26.
Limb, C. J., Molloy, A. T., Jiradejvong, P., & Braun, A. R. (2010). Auditory cortical activity during cochlear implant-mediated perception of spoken language, melody, and rhythm. Journal of the Association for Research in Otolaryngology, 11, 133–143.
Littlefield, P., Izzo, A. D., Mundi, J., Walsh, J. T., Jansen, E.D., et al. (2008). Characterization of single auditory nerve fibers in response to laser stimulation. In Proceedings of SPIE 6854, Optical interactions with tissue and cells XIX, 68540F.
Liu, L., Parekh-Olmedo, H., & Kmiec, E. B. (2003). The development and regulation of gene repair. Nature Reviews Genetics, 4, 679–689.
Liu, Q., Jorgensen, E., Holman, H., Frerck, M., & Rabbitt, R. D. (2013). Miniature post synaptic currents are entrained by infrared pulses. Abstracts of the Association for Research in Otolaryngology, 36, 464.
Liu, Q., Frerck, M. J., Holman, H. A., Jorgensen, E. M., & Rabbitt, R. D. (2014). Exciting cell membranes with a blustering heat shock. Biophysical Journal, 106, 1570–1577.
Lumbreras, V., Finale, M., Bas, E., Gupta, C., & Rajguru, S. (2013). Pulsed infrared-evoked intracellular calcium transients in cultured neonatal spiral ganglion neurons. Abstracts of the Association for Research in Otolaryngology, 36, 341.
Matic, A. I., Walsh, J. T., Jr., & Richter, C. P. (2011). Spatial extent of cochlear infrared neural stimulation determined by tone-on-light masking. Journal of Biomedical Optics, 16, 118002.
Matic, A. I., Robinson, A. M., Young, H. K., Badofsky, B., Rajguru, S. M., et al. (2013). Behavioral and electrophysiological responses evoked by chronic infrared neural stimulation of the cochlea. PLoS ONE, 8, e58189.
Moser, T. (2015). Optogenetic stimulation of the auditory pathway for research and future prosthetics. Current Opinion in Neurobiology, 34C, 29–36.
Moser, T., Hernandez, V. H., Hoch, G., Reuter, K., Jing, Z., et al. (2013). Optogenetic stimulation of the auditory nerve. Abstracts of the Association for Research in Otolaryngology, 36, 268.
Mukherjea, D., Ghosh, S., Bhatta, P., Sheth, S., Tupal, S., et al. (2015). Early investigational drugs for hearing loss. Expert Opinion on Investigational Drugs, 24, 201–217.
Naito, Y., Tateya, I., Fujiki, N., Hirano, S., Ishizu, K., et al. (2000). Increased cortical activation during hearing of speech in cochlear implant users. Hearing Research, 143, 139–146.
NIDCD Information Clearinghouse. (2015). Cochlear implants. NIH Publication 11-4798. https://www.nidcd.nih.gov/health/cochlear-implants.
Niemz, M. H. (2004). Laser–tissue interactions: Fundamentals and application, 2nd ed. New York: Springer Science + Business Media.
Pezzoli, D., Chiesa, R., De Nardo, L., & Candiani, G. (2012). We still have a long way to go to effectively deliver genes! Journal of Applied Biomaterials & Functional Materials, 10, 82–91.
Phillips, J. O., Ling, L., Nie, K., Jameyson, E., Phillips, C. M., et al. (2015). Vestibular implantation and longitudinal electrical stimulation of the semicircular canal afferents in human subjects. Journal of Neurophysiology, 113, 3866–3892.
Rajguru, S. M., Rabbitt, R. D., Matic, A. I., Highstein, S. M., & Richter, C. P. (2010a). Selective activation of vestibular hair cells by infrared light. Biophysical Journal, 98, 507a.
Rajguru, S. M., Rabbitt, R. R., Matic, A. I., Highstein, S. M., & Richter, C. P. (2010b). Inhibitory and excitatory vestibular afferent responses induced by infrared light stimulation of hair cells. Abstracts of the Association for Research in Otolaryngology, 33, 328.
Redd, E. E., Pongstaporn, T., & Ryugo, D. K. (2000). The effects of congenital deafness on auditory nerve synapses and globular bushy cells in cats. Hearing Research, 147, 160–174.
Redd, E. E., Cahill, H. B., Pongstaporn, T., & Ryugo, D. K. (2002). The effects of congenital deafness on auditory nerve synapses: Type I and type II multipolar cells in the anteroventral cochlear nucleus of cats. Journal of the Association for Research in Otolaryngology, 3, 403–417.
Reiss, L. A., Turner, C. W., Karsten, S. A., Erenberg, S. R., Taylor, J., & Gantz, B. J. (2012). Consonant recognition as a function of the number of stimulation channels in the hybrid short-electrode cochlear implant. The Journal of the Acoustical Society of America, 132, 3406–3417.
Rhee, A. Y., Li, G., Wells, J., & Kao, Y. P. Y. (2008). Photostimulation of sensory neurons of the rat vagus nerve. In S. L. Jacques, W. P. Roach, & R. J. Thomas (Eds.), Optical interactions with tissue and cells: Proceedings of SPIE 6854, Optical interactions with tissue and cells XIX, 68540E. San Francisco.
Richter, C. P., & Tan, X. (2014). Photons and neurons. Hearing Research, 311, 72–88.
Richter, C.-P., Bayon, R., Izzo, A. D., Otting, M., Suh, E., et al. (2008). Optical stimulation of auditory neurons: Effects of acute and chronic deafening. Hearing Research, 242, 42–51.
Richter, C. P., Rajguru, S. M., Matic, A. I., Moreno, E. L., Fishman, A. J., et al. (2011). Spread of cochlear excitation during stimulation with pulsed infrared radiation: Inferior colliculus measurements. Journal of Neural Engineering, 8, 056006.
Rubinstein, J. T. (2004). How cochlear implants encode speech. Current Opinion in Otolaryngology & Head and Neck Surgery, 12, 444–448.
Ryugo, D. K., Pongstaporn, T., Huchton, D. M., & Niparko, J. K. (1997). Ultrastructural analysis of primary endings in deaf white cats: Morphologic alterations in endbulbs of Held. Journal of Comparative Neurology, 385, 230–244.
Saada, A. A., Niparko, J. K., & Ryugo, D. K. (1996). Morphological changes in the cochlear nucleus of congenitally deaf white cats. Brain Research, 736, 315–328.
Schultz, M., Baumhoff, P., Teudt, I. U., Maier, H., Kruger, A., et al. (2012a). Pulsed wavelength-dependent laser stimulation of the inner ear. Biomedizinische Technik/Biomedical Engineering, 57(Suppl 1), doi:10.1515/bmt-2012-4339.
Schultz, M., Baumhoff, P., Maier, H., Teudt, I. U., Kruger, A., et al. (2012b). Nanosecond laser pulse stimulation of the inner ear-a wavelength study. Biomedical Optics Express, 3, 3332–3345.
Shannon, R. V. (2005). Speech and music have different requirements for spectral resolution. International Review of Neurobiology, 70, 121–134.
Shannon, R. V., Galvin, J. J., 3rd, & Baskent, D. (2002). Holes in hearing. Journal of the Association for Research in Otolaryngology, 3, 185–199.
Shannon, R. V., Fu, Q. J., & Galvin, J., 3rd. (2004). The number of spectral channels required for speech recognition depends on the difficulty of the listening situation. Acta Oto-Laryngologica Supplementum, 552, 50–54.
Shapiro, M. G., Homma, K., Villarreal, S., Richter, C. P., & Bezanilla, F. (2012). Infrared light excites cells by changing their electrical capacitance. Nature Communications, 3, 736.
Shepherd, R. K., & Hardie, N. A. (2001). Deafness-induced changes in the auditory pathway: Implications for cochlear implants. Audiology and Neurotology, 6, 305–318.
Snel-Bongers, J., Briaire, J. J., Vanpoucke, F. J., & Frijns, J. H. (2012). Spread of excitation and channel interaction in single- and dual-electrode cochlear implant stimulation. Ear and Hearing, 33, 367–376.
Takumida, M., Kubo, N., Ohtani, M., Suzuka, Y., & Anniko, M. (2005). Transient receptor potential channels in the inner ear: Presence of transient receptor potential channel subfamily 1 and 4 in the guinea pig inner ear. Acta Oto-Laryngologica, 125, 929–934.
Teudt, I. U., Maier, H., Richter, C. P., & Kral, A. (2011). Acoustic events and “optophonic” cochlear responses induced by pulsed near-infrared laser. IEEE Transactions on Biomedical Engineering, 58, 1648–1655.
Thompson, A. C., Fallon, J. B., Wise, A. K., Wade, S. A., Shepherd, R. K., & Stoddart, P. R. (2015). Infrared neural stimulation fails to evoke neural activity in the deaf guinea pig cochlea. Hearing Research, 324, 46–53.
Tirko, N. N., & Ryugo, D. K. (2012). Synaptic plasticity in the medial superior olive of hearing, deaf, and cochlear-implanted cats. Journal of Comparative Neurology, 520, 2202–2217.
Truy, E., Deiber, M. P., Cinotti, L., Mauguiere, F., Froment, J. C., & Morgon, A. (1995). Auditory cortex activity changes in long-term sensorineural deprivation during crude cochlear electrical stimulation: Evaluation by positron emission tomography. Hearing Research, 86, 34–42.
Tuchin, V. (2000). Tissue optics: Light scattering methods and instruments for medical diagnosis. Bellingham, WA: SPIE Press.
van den Honert, C., & Stypulkowski, P. H. (1984). Physiological properties of the electrically stimulated auditory nerve. II. Single fiber recordings. Hearing Research, 14, 225–243.
Welch, A. J., & van Gemert, M. J. C. (2012). Optical-thermal response of laser-irradiated tissue, 2nd ed. New York: Plenum Press,
Wells, J., Kao, C., Konrad, P., Milner, T., Kim, J., et al. (2007). Biophysical mechanisms of transient optical stimulation of peripheral nerve. Biophysical Journal, 93, 2567–2580.
Wenzel, G. I., Balster, S., Zhang, K., Lim, H. H., Reich, U., et al. (2009). Green laser light activates the inner ear. Journal of Biomedical Optics, 14, 044007.
Wilson, B. S., & Dorman, M. F. (2008). Cochlear implants: Current designs and future possibilities. Journal of Rehabilitation Research and Development, 45, 695–730.
Wong, D., Miyamoto, R. T., Pisoni, D. B., Sehgal, M., & Hutchins, G. D. (1999). PET imaging of cochlear-implant and normal-hearing subjects listening to speech and nonspeech. Hearing Research, 132, 34–42.
Xia, N., Tan, X., Young, H., Dummer, M., Hibbs-Brenner, M., & Richter, C.-P. (2015). Multichannel optrode for optical stimulation. Abstracts of the Association for Research in Otolaryngology, 38, 108.
Yizhar, O., Fenno, L. E., Davidson, T. J., Mogri, M., & Deisseroth, K. (2011). Optogenetics in neural systems. Neuron, 71, 9–34.
Young, H. K., Tan, X., Xia, N., & Richter, C. P. (2015). Target structures for cochlear infrared neural stimulation. Neurophotonics, 2, 025002.
Zeng, F.-G., Tang, Q., & Lu, T. (2014). Abnormal pitch perception produced by cochlear implant stimulation. PLoS ONE, 9, e88662.
Zhang, F., Wang, L. P., Boyden, E. S., & Deisseroth, K. (2006). Channelrhodopsin-2 and optical control of excitable cells. Nature Methods, 3, 785–792.
Zhang, K. Y., Wenzel, G. I., Balster, S., Lim, H. H., Lubatschowski, H., et al. (2009). Optoacoustic induced vibrations within the inner ear. Optics Express, 17, 23037–23043.
Zheng, J., Dai, C., Steyger, P. S., Kim, Y., Vass, Z., et al. (2003). Vanilloid receptors in hearing: Altered cochlear sensitivity by vanilloids and expression of TRPV1 in the organ of Corti. Journal of Neurophysiology, 90, 444–455.
Acknowledgments
This work has been funded by the NIDCD, R01-DC011855.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Additional information
Compliance with Ethics Requirements
Xiaodong Tan declares that he has no conflict of interest.
Nan Xia declares that she has no conflict of interest. Nan Xia was supported bu the China scholarship council.
Claus-Peter Richter is the founding Chief technology Officer (CTO) of Resonance Medical, LLC, and is inventor on several patents pertaining to optical stimulation and the design of optical implant electrodes.
Rights and permissions
Copyright information
© 2016 Springer International Publishing Switzerland
About this chapter
Cite this chapter
Tan, X., Xia, N., Richter, CP. (2016). Photons in the Ear. In: Le Prell, C., Lobarinas, E., Popper, A., Fay, R. (eds) Translational Research in Audiology, Neurotology, and the Hearing Sciences. Springer Handbook of Auditory Research, vol 58. Springer, Cham. https://doi.org/10.1007/978-3-319-40848-4_9
Download citation
DOI: https://doi.org/10.1007/978-3-319-40848-4_9
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-40846-0
Online ISBN: 978-3-319-40848-4
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)