Music-induced cortical plasticity and lateral inhibition in the human auditory cortex as foundations for tonal tinnitus treatment

Frontiers in Systems Neuroscience

Volumn , Issue JUNE 2012, 2012, Pages

  Pantev, Christo ^a   Okamoto, Hidehiko ^a,b   Teismann, Henning ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b NATIONAL INSTITUTE FOR PHYSIOLOGICAL SCIENCES   (Japan)

Author keywords

Human auditory cortex; Lateral inhibition; Music induced cortical plasticity; Tailor made notched music training; Tonal tinnitus treatment

Indexed keywords

ACOUSTIC NERVE FIBER; ARTICLE; ATTENTION; AUDIOVISUAL EQUIPMENT; AUDITORY CORTEX; AUDITORY DISCRIMINATION; BRAIN FUNCTION; CELL ACTIVITY; DISEASE SEVERITY; ELECTROENCEPHALOGRAM; EVOKED AUDITORY RESPONSE; HABITUATION; HEARING LOSS; HUMAN; LATERAL INHIBITION; LOUDNESS; MAGNETOENCEPHALOGRAPHY; MISMATCH NEGATIVITY; MUSIC THERAPY; NERVE CELL INHIBITION; NERVE CELL PLASTICITY; NOISE REDUCTION; NONHUMAN; RECEPTIVE FIELD; TAILOR MADE NOTCHED MUSIC TRAINING; THERAPY EFFECT; TINNITUS; TREATMENT DURATION; TREATMENT OUTCOME; WHITE NOISE;

EID: 84865006382     PISSN: 16625137     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnsys.2012.00050     Document Type: Article

References (111)

1. Bangert, M., and Schlaug, G. (2006). Specialization of the specialized in features of external human brain morphology. Eur. J. Neurosci. 24, 1832-1834.
2. Bauer, C. A., Turner, J. G., Caspary, D. M., Myers, K. S., and Brozoski, T. J. (2008). Tinnitus and inferior colliculus activity in chinchillas related to three distinct patterns of cochlear trauma. J. Neurosci. Res. 86, 2564-2578.
3. Bermudez, P., Lerch, J. P., Evans, A. C., and Zatorre, R. J. (2009). Neuroanatomical correlates of musicianship as revealed by cortical thickness and voxel-based morphometry. Cereb. Cortex 19, 1583-1596.
4. Besson, M., Schon, D., Moreno, S., Santos, A., and Magne, C. (2007). Influence of musical expertise and musical training on pitch processing in music and language. Restor. Neurol. Neurosci. 25, 399-410.
5. Burrows, D. L., and Barry, S. J. (1990). Electrophysiological evidence for the critical band in humans: middle-latency responses. J. Acoust. Soc. Am. 88, 180-184.
6. Butler, R. A. (1968). Effect of changes in stimulus frequency and intensity on habituation of the human vertex potential. J. Acoust. Soc. Am. 44, 945-950.
7. Candia, V., Elbert, T., Altenmuller, E., Rau, H., Schafer, T., and Taub, E. (1999). Constraint-induced movement therapy for focal hand dystonia in musicians. Lancet 353, 42-42.
8. Cazals, K., Horner, C., and Huang, Z. W. (1998). Alterations in average spectrum of cochleoneural activity by long-term salicylate treatment in the guinea pig, a plausible index of tinnitus. J. Neurophysiol. 80, 2113-2120.
9. Coles, R. (1984). Epidemiology of tinnitus: (1) prevalence. J. Laryngol. Otol. Suppl. 9, 7-15.
10. Davis, P. B., Paki, B., and Hanley, P. J. (2007). Neuromonics tinnitus treatment: third clinical trial. Ear Hear. 28, 242-259.
11. Diesch, E., Struve, M., Rupp, A., Ritter, S., Hulse, M., and Flor, H. (2004). Enhancement of steady-state auditory evoked magnetic fields in tinnitus. Eur. J. Neurosci. 19, 1093-1104.
12. Eggermont, J. J. (2006). Cortical tonotopic map reorganization and its implications for treatment of tinnitus. Acta Otolaryngol. Suppl. 556, 9-12.
13. Eggermont, J. J., and Roberts, L. E. (2004). The neuroscience of tinnitus. Trends Neurosci. 27, 676-682.
14. Ehret, G., and Merzenich, M. M. (1988). Complex sound analysis (frequency resolution, filtering and spectral integration) by single units of the inferior colliculus of the cat. Brain Res. 472, 139-163.
15. Elbert, T., Pantev, C., Wienbruch, C., Rockstroh, B., and Taub, E. (1995). Increased cortical representation of the fingers of the left hand in string players. Science 270, 305-307.
16. Elbert, T., and Heim, S. (2001). A light and a dark side. Nature 411, 139.
17. Fletcher, H. (1940). Auditory patterns. Rev. Mod. Phys. 12, 47-65.
18. Flor, H., Elbert, T., Knecht, S., Wienbruch, C., Pantev, C., Birbaumer, N., Larbig, W., and Taub, E. (1995). Phantom-limb pain as a perceptual correlate of cortical reorganization following arm amputation. Nature 375, 482-484.
19. Formby, C., Sherlock, L. P., and Gold, S. L. (2003). Adaptive plasticity of loudness induced by chronic attenuation and enhancement of the acoustic background. J. Acoust. Soc. Am. 114, 55-58.
20. Fujioka, T., Trainor, L. J., Ross, B., Kakigi, R., and Pantev, C. (2004). Musical training enhances automatic encoding of melodic contour and interval structure. J. Cogn. Neurosci. 16, 1010-1021.
21. Fujioka, T., Trainor, L. J., Ross, B., Kakigi, R., and Pantev, C. (2005). Automatic encoding of polyphonic melodies in musicians and nonmusicians. J. Cogn. Neurosci. 17, 1578-1592.
22. Gaser, C., and Schlaug, G. (2003). Brain structures differ between musicians and non-musicians. J. Neurosci. 23, 9240-9245.
23. Gilbert, C. D., and Wiesel, T. N. (1992). Receptive field dynamics in adult primary visual cortex. Nature 356, 150-152.
24. Giraux, P., Sirigu, A., Schneider, F., and Dubernard, J. M. (2001). Cortical reorganization in motor cortex after graft of both hands. Nat. Neurosci. 4, 691-692.
25. Hafter, E. R., Schlauch, R. S., and Tang, J. (1993). Attending to auditory filters that were not stimulated directly. J. Acoust. Soc. Am. 94, 743-747.
26. Hari, R. (1990). Magnetic evoked fields of the human brain: basic principles and applications. Electroencephalogr. Clin. Neurophysiol. Suppl. 41, 3-12.
27. Heller, A. (2003). Classification and epidemiology of tinnitus. Otolaryngol. Clin. North Am. 36, 239.
28. Hillyard, S. A., Hink, R. F., Schwent, V. L., and Picton, T. W. (1973). Electrical signs of selective attention in the human brain. Science 182, 177-180.
29. Hoare, D. J., Kowalkowski, V. L., Kang, S., and Hall, D. A. (2011). Systematic review and metaanalyses of randomized controlled trials examining tinnitus management. Laryngoscope 121, 1555-1564.
30. Hubner, R., and Hafter, E. R. (1995). Cuing mechanisms in auditory signal detection. Percept. psychophys. 57, 197-202.
31. Hutchinson, S., Lee, L. H., Gaab, N., and Schlaug, G. (2003). Cerebellar volume of musicians. Cereb. Cortex 13, 943-949.
32. Irvine, D. R. F., and Rajan, R. (1995). "Plasticity in the mature auditory system," in Advances in Hearing Research, eds G. A. Manley, G. M. Klump, C. Köppl, H. Fastl, and H. Oeckinhaus (Singapore: World Scientific Publishing Co.), 3-23.
33. Jancke, L., Gaab, N., Wustenberg, T., Scheich, H., and Heinze, H. J. (2001). Short-term functional plasticity in the human auditory cortex: an fMRI study. Cogn. Brain Res. 12, 479-485.
34. Jastreboff, P. J., and Hazell, J. W. (1993). A neurophysiological approach to tinnitus: clinical implications. Br. J. Audiol. 27, 7-17.
35. Jenkins, W. M., Merzenich, M. M., Ochs, M. T., Allard, T., and Guic-Robles, E. (1990). Functional reorganization of primary somatosensory cortex in adult owl monkeys after behaviorally controlled tactile stimulation. J. Neurophysiol. 63, 82-104.
36. Jääskeläinen, I. P., Ahveninen, J., Bonmassar, G., Dale, A. M., Ilmoniemi, R. J., Levanen, S., Lin, F. H., May, P., Melcher, J., Stufflebeam, S., Tiitinen, H., and Belliveau, J. W. (2004). Human posterior auditory cortex gates novel sounds to consciousness. Proc. Natl. Acad. Sci. U.S.A. 101, 6809-6814.
37. Kaas, J. H., Krubitzer, L. A., Chino, Y. M., Langston, A. L., Polley, E. H., and Blair, N. (1990). Reorganization of retinotopic cortical maps in adult mammals after lesions of the retina. Science 248, 229-231.
38. Kadner, A., Viirre, E., Wester, D. C., Walsh, S. F., Hestenes, J., Vankov, A., and Pineda, J. A. (2002). Lateral inhibition in the auditory cortex: an EEG index of tinnitus? Neuroreport 13, 443-446.
39. Katsuki, Y., Sumi, T., Uchiyama, H., and Watanabe, T. (1958). Electric responses of auditory neurons in cat to sound stimulation. J. Neurophysiol. 21, 569-588.
40. Kiang, N. Y., and Moxon, E. C. (1974). Tails of tuning curves of auditorynerve fibers. J. Acoust. Soc. Am. 55, 620-630.
41. Koelsch, S., Schmidt, B. H., and Kansok, J. (2002). Effects of musical expertise on the early right anterior negativity: an event-related brain potential study. Psychophysiology 39, 657-663.
42. Langguth, B., Kleinjung, T., Landgrebe, M., De Ridder, D., and Hajak, G. (2010). rTMS for the treatment of tinnitus: the role of neuronavigation for coil positioning. Neurophysiol. Clin. 40, 45-58.
43. Lappe, C., Herholz, S. C., Trainor, L. J., and Pantev, C. (2008). Cortical plasticity induced by shortterm unimodal and multimodal musical training. J. Neurosci. 28, 9632-9639.
44. Lotze, M., Scheler, G., Tan, H. R., Braun, C., and Birbaumer, N. (2003). The musician's brain: functional imaging of amateurs and professionals during performance and imagery. Neuroimage 20, 1817-1829.
45. Mach, E. (1865). Über die Wirkung der räumlichen Vertheilung des Lichtreizes auf die Netzhaut. Akademie der Wissenschaften in Wien, Sitzungberichte, math.-nat. Cl. 52, 303-322.
46. Martin, W. H., Schwegler, J. W., Scheibelhoffer, J., and Ronis, M. L. (1993). Salicylate-induced changes in cat auditory nerve activity. Laryngoscope 103, 600-604.
47. Menning, H., Roberts, L. E., and Pantev, C. (2000). Plastic changes in the auditory cortex induced by intensive frequency discrimination training. Neuroreport 11, 817-822.
48. Meredith, M. A., and Stein, B. E. (1983). Interactions among converging sensory inputs in the superior colliculus. Science 221, 389-391.
49. Merzenich, M. M., Kaas, J. H., Wall, J., Nelson, R. J., Sur, M., and Felleman, D. (1983a). Topographic reorganization of somatosensory cortical areas 3b and 1 in adult monkeys following restricted deafferentation. Neuroscience 8, 33-55.
50. Merzenich, M. M., Kaas, J. H., Wall, J. T., Sur, M., Nelson, R. J., and Felleman, D. J. (1983b). Progression of change following median nerve section in the cortical representation of the hand in areas 3b and 1 in adult owl and squirrel monkeys. Neuroscience 10, 639-665.
51. Moore, B. C., Vinay, and Sandhya. (2010). The relationship between tinnitus pitch and the edge frequency of the audiogram in individuals with hearing impairment and tonal tinnitus. Hear. Res. 261, 51-56.
52. Muhlnickel, W., Elbert, T., Taub, E., and Flor, H. (1998). Reorganization of auditory cortex in tinnitus. Proc. Natl. Acad. Sci. U.S.A. 95, 10340-10343.
53. Norena, A. J., and Chery-Croze, S. (2007). Enriched acoustic environment rescales auditory sensitivity. Neuroreport 18, 1251-1255.
54. Norena, A., Micheyl, C., and Chery Croze, S. (2000). An auditory negative after-image as a human model of tinnitus. Hear. Res. 149, 24-32.
55. Norena, A. J., and Eggermont, J. J. (2003). Neural correlates of an auditory afterimage in prmary auditory cortex. J. Assoc. Res. Otolaryngol. 4, 312-328.
56. Norena, A. J., and Eggermont, J. J. (2005). Enriched acoustic environment after noise trauma reduces hearing loss and prevents cortical map reorganization. J. Neurosci. 25, 699-705.
57. Näätänen, R., and Picton, T. (1987). The N1 wave of the human electric and magnetic response to sound: a review and an analysis of the component structure. Psychophysiology 24, 375-425.
58. Näätänen, R., Sams, M., Alho, K., Paavilainen, P., Reinikainen, K., and Sokolov, E. N. (1988). Frequency and location specificity of the human vertex n1-wave. Electroencephalogr. Clin. Neurophysiol. 69, 523-531.
59. O'Connor, K. N., Petkov, C. I., and Sutter, M. L. (2005). Adaptive stimulus optimization for auditory cortical neurons. J. Neurophysiol. 94, 4051-4067.
60. Ochi, K., and Eggermont, J. J. (1997). Effects of quinine on neural activity in cat primary auditory cortex. Hear. Res. 105, 105-118.
61. Oechslin, M. S., Imfeld, A., Loenneker, T., Meyer, M., and Jancke, L. (2010). The plasticity of the superior longitudinal fasciculus as a function of musical expertise: a diffusion tensor imaging study. Front. Hum. Neurosci. 3:76. doi: 10.3389/neuro. 09.076.2009
62. Okamoto, H., Kakigi, R., Gunji, A., Kubo, T., and Pantev, C. (2005). The dependence of the auditory evoked N1m decrement on the bandwidth of preceding notch-filtered noise. Eur. J. Neurosci. 21, 1957-1961.
63. Okamoto, H., Kakigi, R., Gunji, A., and Pantev, C. (2007a). Asymmetric lateral inhibitory neural activity in the auditory system: a magnetoencephalographic study. BMC Neurosci. 8, 33.
64. Okamoto, H., Stracke, H., Wolters, C. H., Schmael, F., and Pantev, C. (2007b). Attention improves population-level frequency tuning in human auditory cortex. J. Neurosci. 27, 10383-10390.
65. Okamoto, H., Ross, B., Kakigi, R., Kubo, T., and Pantev, C. (2004). N1m recovery from decline after exposure to noise with strong spectral contrasts. Hear. Res. 196, 77-86.
66. Okamoto, H., Stracke, H., Lagemann, L., and Pantev, C. (2010a). Bottomup driven involuntary auditory evoked field change: constant sound sequencing amplifies but does not sharpen neural activity. J. Neurophysiol. 103, 244-249.
67. Okamoto, H., Stracke, H., Stoll, W., and Pantev, C. (2010b). Listening to tailor-made notched music reduces tinnitus loudness and tinnitusrelated auditory cortex activity. Proc. Natl. Acad. Sci. U.S.A. 107, 1207-1210.
68. Okamoto, H., Stracke, H., Zwitserlood, P., Roberts, L. E., and Pantev, C. (2009). Frequency-specific modulation of population-level frequency tuning in human auditory cortex. BMC Neurosci. 10, 1.
69. Okamoto, H., Teismann, H., Kakigi, R., and Pantev, C. (2011). Broadened population-level frequency tuning in human auditory cortex of portable music player users. PLoS ONE 6:e17022. doi: 10.1371/ journal.pone.0017022
70. Pantev, C., Bertrand, O., Eulitz, C., Verkindt, C., Hampson, S., Schuierer, G., and Elbert, T. (1995). Specific tonotopic organizations of different areas of the human auditory cortex revealed by simultaneous magnetic and electric recordings. Electroencephalogr. Clin. Neurophysiol. 94, 26-40.
71. Pantev, C., Kevanishvili, Z. S., Galle, E., and Khachidze, O. (1975). ERA- stimulation with free-programable frequency and intensity sequence - a method to reduce the examination time. Arch. Otorhinolaryngol. 211, 43-49.
72. Pantev, C., Okamoto, H., Ross, B., Stoll, W., Ciurlia-Guy, E., Kakigi, R., and Kubo, T. (2004). Lateral inhibition and habituation of the human auditory cortex. Eur. J. Neurosci. 19, 2337-2344.
73. Pantev, C., Oostenveld, R., Engelien, A., Ross, B., Roberts, L. E., and Hoke, M. (1998). Increased auditory cortical representation in musicians. Nature 392, 811-814.
74. Pantev, C., Wollbrink, A., Roberts, L. E., Engelien, A., and Lutkenhoner, B. (1999). Short-term plasticity of the human auditory cortex. Brain Res. 842, 192-199.
75. Pantev, C., and Herholz, S. C. (2011). Plasticity of the human auditory cortex related to musical training. Neurosci. Biobehav. Rev. 35, 2140-2154.
76. Picton, T. W., Hillyard, S. A., Krausz, H. I., and Galambos, R. (1974). Human auditory evoked potentials. I. Evaluation of components. Electroencephalogr. Clin. Neurophysiol. 36, 179-190.
77. Pienkowski, M., and Eggermont, J. J. (2011). Cortical tonotopic map plasticity and behavior. Neurosci. Biobehav. Rev. 35, 2117-2128.
78. Pienkowski, M., and Eggermont, J. J. (2012). Reversible long-term changes in auditory processing in mature auditory cortex in the absence of hearing loss induced by passive, moderate-level sound exposure. Ear Hear. 33, 305-314.
79. Polley, D. B., Steinberg, E. E., and Merzenich, M. M. (2006). Perceptual learning directs auditory cortical map reorganization through top-down influences. J. Neurosci. 26, 4970-4982.
80. Rauschecker, J. P., Leaver, A. M., and Muhlau, M. (2010). Tuning out the noise: limbic-auditory interactions in tinnitus. Neuron 66, 819-826.
81. Rauschecker, J. P., Tian, B., Pons, T., and Mishkin, M. (1997). Serial and parallel processing in rhesus monkey auditory cortex. J. Comp. Neurol. 382, 89-103.
82. Rauschecker, J. P., Tian, B., and Hauser, M. (1995). Processing of complex sounds in the macaque nonprimary auditory cortex. Science 268, 111-114.
83. Recanzone, G., Schreiner, C., and Merzenich, M. (1993). Plasticity in the frequency representation of primary auditory cortex following discrimination training in adult owl monkeys. J. Neurosci. 13, 87-103.
84. Rhode, W. S., and Greenberg, S. (1994). Lateral suppression and inhibition in the cochlear nucleus of the cat. J. Neurophysiol. 71, 493-514.
85. Roberts, L. E., and Bosnyak, D. J. (2011). "Auditory training in tinnitus," in Textbook of Tinnitus, eds A. Møller, T. Kleinjung, B. Langguth, and D. De Ridder (New York, NY: Springer), 563-573.
86. Roberts, L. E., Eggermont, J. J., Caspary, D. M., Shore, S. E., Melcher, J. R., and Kaltenbach, J. A. (2010). Ringing ears: the neuroscience of tinnitus. J. Neurosci. 30, 14972-14979.
87. Robertson, D., and Irvine, D. R. (1989). Plasticity of frequency organization in auditory cortex of guinea pigs with partial unilateral deafness. J. Comp. Neurol. 282, 456-471.
88. Salimpoor, V. N., Benovoy, M., Larcher, K., Dagher, A., and Zatorre, R. J. (2011). Anatomically distinct dopamine release during anticipation and experience of peak emotion to music. Nat. Neurosci. 14, 257-262.
89. Schlaug, G., Jäncke, L., Huang, Y., Staiger, J. F., and Steinmetz, H.(1995a). Increased corpus callosum size in musicians. Neuropsychologia 33, 1047-1055.
90. Schlaug, G., Jancke, L., Huang, Y., and Steinmetz, H. (1995b). In vivo evidence of structural brain asymmetry in musicians. Science 267, 699-701.
91. Schneider, P., Scherg, M., Dosch, H. G., Specht, H. J., Gutschalk, A., and Rupp, A. (2002). Morphology of Heschl's gyrus reflects enhanced activation in the auditory cortex of musicians. Nat. Neurosci. 5, 688-694.
92. Schulte, M., Knief, A., Seither-Preisler, A., and Pantev, C. (2002). Different modes of pitch perception and learning-induced neuronal plasticity of the human auditory cortex. Neural Plast. 9, 161-175.
93. Schulz, M., Ross, B., and Pantev, C. (2003). Evidence for traininginduced crossmodal reorganization of cortical functions in trumpet players. Neuroreport 14, 157-161.
94. Shahin, A. J., Bosnyak, D. J., Trainor, L. J., and Roberts, L. E. (2003). Enhancement of neuroplastic P2 and N1c auditory evoked potentials in musicians. J. Neurosci. 23, 5545-5552.
95. Stouffer, J. L., and Tyler, R. S. (1990). Characterization of tinnitus by tinnitus patients. J. Speech Hear. Disord. 55, 439-453.
96. Stracke, H., Okamoto, H., and Pantev, C. (2010). Customized notched music training reduces tinnitus loudness. Commun. Integr. Biol. 3, 274-277.
97. Suga, N. (1995). Sharpening of frequency tuning by inhibition in the central auditory system: tribute to Yasuji Katsuki. Neurosci. Res. 21, 287-299.
98. Sutter, M. L., Schreiner, C. E., Mclean, M., O'connor, K. N., and Loftus, W. C. (1999). Organization of inhibitory frequency receptive fields in cat primary auditory cortex. J. Neurophysiol. 82, 2358-2371.
99. Sutter, M. L., and Loftus, W. C. (2003). Excitatory and inhibitory intensity tuning in auditory cortex: evidence for multiple inhibitory mechanisms. J. Neurophysiol. 90, 2629-2647.
100. Tass, P. A., Adamchic, I., Freund, H.-J., von Stackelberg, T., and Hauptmann, C. (2012). Counteracting tinnitus by acoustic coordinated reset neuromodulation. Restor. Neurol. Neurosci. 30, 135-159.
101. Teismann, H., Okamoto, H., and Pantev, C. (2011). Short and intense tailor-made notched music training against tinnitus: the tinnitus frequency matters. PLoS ONE 6:e24685. doi: 10.1371/journal.pone.0024685
102. Tervaniemi, M., Rytkonen, M., Schroger, E., Ilmoniemi, R. J., and Naatanen, R. (2001). Superior formation of cortical memory traces for melodic patterns in musicians. Learn. Mem. 8, 295-300.
103. Tyler, R. S., and Conrad-Armes, D. (1983). Tinnitus pitch: a comparison of three measurement methods. Br. J. Audiol. 17, 101-107.
104. Van Zuijen, T. L., Sussman, E., Winkler, I., Näätänen, R., and Tervaniemi, M. (2004). Grouping of sequential sounds-an event-related potential study comparing musicians and nonmusicians. J. Cogn. Neurosci. 16, 331-338.
105. Van Zuijen, T. L., Sussman, E., Winkler, I., Näätänen, R., and Tervaniemi, M. (2005). Auditory organization of sound sequences by a temporal or numerical regularity-a mismatch negativity study comparing musicians and non-musicians. Brain Res. Cogn. Brain Res. 23, 270-276.
106. Von Békésy, G. (1967). Sensory Inhibition. Princeton, NJ: Princeton University Press.
107. Wan, C. Y., and Schlaug, G. (2010). Music making as a tool for promoting brain plasticity across the life span. Neuroscientist 16, 566-577.
108. Wiegrebe, L., Kossl, M., and Schmidt, S. (1996). Auditory enhancement at the absolute threshold of hearing and its relationship to the Zwicker tone. Hear. Res. 100, 171-180.
109. Woldorff, M. G., Gallen, C. C., Hampson, S. A., Hillyard, S. A., Pantev, C., Sobel, D., and Bloom, F. E. (1993). Modulation of early sensory processing in human auditory cortex during auditory selective attention. Proc. Natl. Acad. Sci. U.S.A. 90, 8722-8726.
110. Zatorre, R. J., Chen, J. L., and Penhune, V. B. (2007). When the brain plays music: auditory-motor interactions in music perception and production. Nat. Rev. Neurosci. 8, 547-558.
111. Zhou, X., and Merzenich, M. M. (2012). Environmental noise exposure degrades normal listening processes. Nat. Commun. 3, 843.