Infrared neural stimulation fails to evoke neural activity in the deaf guinea pig cochlea

Hearing Research

Volumn 324, Issue , 2015, Pages 46-53

  Thompson, Alexander C ^a   Fallon, James B ^b,c   Wise, Andrew K ^b,c   Wade, Scott A ^a   Shepherd, Robert K ^b,c   Stoddart, Paul R ^a  

^a SWINBURNE UNIVERSITY OF TECHNOLOGY   (Australia)

^b Bionics Institute   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUDITORY STIMULATION; CELL ACTIVITY; CELL SURVIVAL; CLICK; CLINICAL EFFECTIVENESS; CONTROLLED STUDY; ELECTROSTIMULATION; EVOKED AUDITORY RESPONSE; EVOKED BRAIN STEM AUDITORY RESPONSE; FEMALE; HAIR CELL; HEARING IMPAIRMENT; INFRARED NEURAL STIMULATION; MALE; NERVE CELL STIMULATION; NERVE POTENTIAL; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; SPIRAL LAMINA; STIMULUS RESPONSE; ACOUSTICS; ANIMAL; COCHLEA; COCHLEA PROSTHESIS; COCHLEAR HAIR CELL; COCHLEAR IMPLANTATION; GUINEA PIG; INFRARED RADIATION; NERVE CELL; PATHOPHYSIOLOGY; PHYSIOLOGY; SPIRAL GANGLION;

ACOUSTIC STIMULATION; ACOUSTICS; ANIMALS; COCHLEA; COCHLEAR IMPLANTATION; COCHLEAR IMPLANTS; DEAFNESS; ELECTRIC STIMULATION; FEMALE; GUINEA PIGS; HAIR CELLS, AUDITORY; INFRARED RAYS; MALE; NEURONS; SPIRAL GANGLION;

EID: 84928322281     PISSN: 03785955     EISSN: 18785891     Source Type: Journal    
DOI: 10.1016/j.heares.2015.03.005     Document Type: Article

References (44)

1. Albert E.S., Bec J.-M., Desmadryl G., Chekroud K., Travo C., Gaboyard S., Bardin F., Marc I., Dumas M., Lenaers G., Hamel C., Muller A., Chabbert C. TRPV4 channels mediate the infrared laser evoked response in sensory neurons. J.Neurophysiol. 2012, 107(12):3227-3234. 10.1152/jn.00424.2011.
2. Brown W.G.A., Needham K., Nayagam B.A., Stoddart P.R. Whole cell patch clamp for investigating the mechanisms of infrared neural stimulation. J.Vis. Exp. 2013, 77:e50444. 10.3791/50444.
3. Cayce J.M., Friedman R.M., Chen G., Jansen E.D., Mahadevan-Jansen A., Roe A.W. Infrared neural stimulation of primary visual cortex in non-human primates. NeuroImage 2014, 84:181-190. 10.1016/j.neuroimage.2013.08.040.
4. Chernov M., Roe A.W. Infrared neural stimulation: a new stimulation tool for central nervous system applications. Neurophotonics 2014, 1(1). 011011-011011. 10.1117/1.NPh.1.1.011011.
5. Coco A., Epp S.B., Fallon J.B., Xu J., Millard R.E., Shepherd R.K. Does cochlear implantation and electrical stimulation affect residual hair cells and spiral ganglion neurons?. Hear. Res. 2007, 225(1-2):60-70. 10.1016/j.heares.2006.12.004.
6. Dittami G.M., Rajguru S.M., Lasher R.A., Hitchcock R.W., Rabbitt R.D. Intracellular calcium transients evoked by pulsed infrared radiation in neonatal cardiomyocytes. J.Physiol. 2011, 589(6):1295-1306. 10.1113/jphysiol.2010.198804.
7. Friesen L.M., Shannon R.V., Baskent D., Wang X. 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.
8. George S.S., Wise A.K., Shivdasani M.N., Shepherd R.K., Fallon J.B. Evaluation of focused multipolar stimulation for cochlear implants in acutely deafened cats. J.Neural Eng. 2014, 11(6):065003. 10.1088/1741-2560/11/6/065003.
9. Hardie N.A., Shepherd R.K. Sensorineural hearing loss during development: morphological and physiological response of the cochlea and auditory brainstem. Hear. Res. 1999, 128(1-2):147-165. 10.1016/S0378-5955(98)00209-3.
10. Hernandez V.H., Gehrt A., Reuter K., Jing Z., Jeschke M., Mendoza Schulz A., Hoch G., Bartels M., Vogt G., Garnham C.W., Yawo H., Fukazawa Y., Augustine G.J., Bamberg E., Kügler S., Salditt T., de Hoz L., Strenzke N., Moser T. Optogenetic stimulation of the auditory pathway. J.Clin. Investigation 2014, 124(3):1114-1129. 10.1172/JCI69050.
11. Izzo A.D., Richter C.-P., Jansen E.D., Walsh J.T. Laser stimulation of the auditory nerve. Lasers Surg. Med. 2006, 38(8):745-753.
12. Izzo A.D., Walsh J.T., 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(6):1108-1114.
13. Jenkins M.W., Duke A.R., Gu S., Doughman Y., Chiel H.J., Fujioka H., Watanabe M., Jansen E.D., Rollins A.M. Optical pacing of the embryonic heart. Nat. Photonics 2010, 4(9):623-626. 10.1038/nphoton.2010.166.
14. Kral A., Hartmann R., Tillein J., Heid S., Klinke R. Hearing after congenital deafness: central auditory plasticity and sensory deprivation. Cereb. Cortex 2002, 12(8):797-807. 10.1093/cercor/12.8.797.
15. Kramer R.H., Fortin D.L., Trauner D. New photochemical tools for controlling neuronal activity. Curr. Opin. Neurobiol. 2009, 19(5):544-552. 10.1016/j.conb.2009.09.004.
16. Landry T.G., Wise A.K., Fallon J.B., Shepherd R.K. Spiral ganglion neuron survival and function in the deafened cochlea following chronic neurotrophic treatment. Hear. Res. 2011, 282(1-2):303-313. 10.1016/j.heares.2011.06.007.
17. Liu Q., Frerck M.J., Holman H.A., Jorgensen E.M., Rabbitt R.D. Exciting cell membranes with a blustering heat shock. Biophys. J. 2014, 106(8):1570-1577. 10.1016/j.bpj.2014.03.008.
18. Lumbreras V., Bas E., Gupta C., Rajguru S.M. Pulsed infrared radiation excites cultured neonatal spiral and vestibular ganglion neurons by modulating mitochondrial calcium cycling. J.Neurophysiol. 2014, 10.1152/jn.00253.2014.
19. Matic A.I., Robinson A.M., Young H.K., Badofsky B., Rajguru S.M., Stock S., Richter C.-P. Behavioral and electrophysiological responses evoked by chronic infrared neural stimulation of the cochlea. PLoS One 2013, 8(3):e58189. 10.1371/journal.pone.0058189.
20. Moreno L.E., Rajguru S.M., Matic A.I., Yerram N., Robinson A.M., Hwang M., Stock S., Richter C.-P. Infrared neural stimulation: beam path in the guinea pig cochlea. Hear. Res. 2011, 282(1-2):289-302. 10.1016/j.heares.2011.06.006.
21. National Institute on Deafness and Other Communication Disorders. (accessed 27.02.15.). http://www.nidcd.nih.gov/health/hearing/pages/coch.aspx.
22. Okunade O., Santos-Sacchi J. IR laser-induced perturbations of the voltage-dependent solute carrier protein SLC26a5. Biophys. J. 2013, 105(8):1822-1828. 10.1016/j.bpj.2013.09.008.
23. Paviolo C., Haycock J.W., Cadusch P.J., McArthur S.L., Stoddart P.R. Laser exposure of gold nanorods can induce intracellular calcium transients. J.Biophot. 2013, 7(10):761-765. 10.1002/jbio.201300043.
24. Rajguru S.M., Richter C.-P., Matic A.I., Holstein G.R., Highstein S.M., Dittami G.M., Rabbitt R.D. Infrared photostimulation of the crista ampullaris. J.Physiol. 2011, 589(6):1283-1294. 10.1113/jphysiol.2010.198333.
25. Rettenmaier A., Lenarz T., Reuter G. Nanosecond laser pulse stimulation of spiral ganglion neurons and model cells. Biomed. Opt. Express 2014, 5(4):1014. 10.1364/BOE.5.001014.
26. Richter C.-P., Bayon R., Izzo A.D., Otting M., Suh E., Goyal S., Hotaling J., Walsh J.T. Optical stimulation of auditory neurons: effects of acute and chronic deafening. Hear. Res. 2008, 242(1-2):42-51.
27. Richter C.-P., Matic A.I., Wells J.D., Jansen E.D., Walsh J.T. Neural stimulation with optical radiation. Laser & Photonics Rev. 2011, 5(1):68-80. 10.1002/lpor.200900044.
28. Schultz M., Baumhoff P., Kallweit N., Sato M., Krüger A., Ripken T., Lenarz T., Kral A. Optical Stimulation of the Hearing and Deaf Cochlea under Thermal and Stress Confinement Condition 2014, vol. 8928. 892816-892816-7.
29. Schultz M., Baumhoff P., Maier H., Teudt I.U., Krüger A., Lenarz T., Kral A. Nanosecond laser pulse stimulation of the inner ear a wavelength study. Biomed. Opt. Express 2012, 3(12):3332-3345. 10.1364/BOE.3.003332.
30. Shapiro M.G., Homma K., Villarreal S., Richter C.-P., Bezanilla F. Infrared light excites cells by changing their electrical capacitance. Nat. Commun. 2012, 3:736. 10.1038/ncomms1742.
31. Shepherd R.K., Hardie N.A. Deafness-induced changes in the auditory pathway: implications for cochlear implants. Audiol. Neurotol. 2001, 6(6):305-318.
32. Teudt I.U., Maier H., Richter C.-P., Kral A. Acoustic events and "optophonic" cochlear responses induced by pulsed near-infrared LASER. IEEE Trans. Biomed. Eng. 2011, 58(6):1648-1655. 10.1109/TBME.2011.2108297.
33. Teudt I.U., Nevel A.E., Izzo A.D., Walsh J.T., Richter C.-P. Optical stimulation of the facial nerve: a new monitoring technique?. Laryngoscope 2007, 117(9):1641-1647. 10.1097/MLG.0b013e318074ec00.
34. Thompson A.C., Wade S.A., Brown W.G.A., Stoddart P.R. Modeling of light absorption in tissue during infrared neural stimulation. J.Biomed. Opt. 2012, 17(7). 075002-075002-6. 10.1117/1.JBO.17.7.075002.
35. Thompson A.C., Wade S.A., Cadusch P.J., Brown W.G.A., Stoddart P.R. Modeling of the temporal effects of heating during infrared neural stimulation. J.Biomed. Opt. 2013, 18(3). 035004-035004. 10.1117/1.JBO.18.3.035004.
36. Thompson A.C., Wade S.A., Pawsey N.C., Stoddart P.R. Infrared neural stimulation: influence of stimulation site spacing and repetition rates on heating. IEEE Trans. Biomed. Eng. 2013, 60(12):3534-3541. 10.1109/TBME.2013.2272796.
37. Verma R.U., Guex A.A., Hancock K.E., Durakovic N., McKay C.M., Slama M.C.C., Brown M.C., Lee D.J. Auditory responses to electric and infrared neural stimulation of the rat cochlear nucleus. Hear. Res. 2014, 310:69-75. 10.1016/j.heares.2014.01.008.
38. Wells J., Kao C., Jansen E.D., Konrad P., Mahadevan-Jansen A. Application of infrared light for invivo neural stimulation. J.Biomed. Opt. 2005, 10(6). 064003-064003-12. 10.1117/1.2121772.
39. Wells J., Kao C., Konrad P., Milner T., Kim J., Mahadevan-Jansen A., Jansen E.D. Biophysical mechanisms of transient optical stimulation of peripheral nerve. Biophys. J. 2007, 93(7):2567-2580. 10.1529/biophysj.107.104786.
40. Wells J., Kao C., Mariappan K., Albea J., Jansen E.D., Konrad P., Mahadevan-Jansen A. Optical stimulation of neural tissue invivo. Opt. Lett. 2005, 30(5):504-506. 10.1364/OL.30.000504.
41. Wenzel G.I., Balster S., Zhang K., Lim H.H., Reich U., Massow O., Lubatschowski H., Ertmer W., Lenarz T., Reuter G. Green laser light activates the inner ear. J.Biomed. Opt. 2009, 14(4). 044007-044007. 10.1117/1.3174389.
42. Wise A.K., Fallon J.B., Neil A.J., Pettingill L.N., Geaney M.S., Skinner S.J., Shepherd R.K. Combining cell-based therapies and neural prostheses to promote neural survival. Neurotherapeutics 2011, 8(4):774-787. 10.1007/s13311-011-0070-0.
43. Xu S.-A., Shepherd R.K., Chen Y., Clark G.M. Profound hearing loss in the cat following the single co-administration of kanamycin and ethacrynic acid. Hear. Res. 1993, 70(2):205-215. 10.1016/0378-5955(93)90159-X.
44. Zhou Y., Gopalakrishnan V., Richardson J.S. Actions of neurotoxic β-amyloid on calcium homeostasis and viability of PC12 cells are blocked by antioxidants but not by calcium channel antagonists. J.Neurochem. 1996, 67(4):1419-1425. 10.1046/j.1471-4159.1996.67041419.x.