Evidence for differential modulation of primary and nonprimary auditory cortex by forward masking in tinnitus

Hearing Research

Volumn 327, Issue , 2015, Pages 9-27

  Roberts, Larry E ^a,b   Bosnyak, Daniel J ^a,b   Bruce, Ian C ^a,b   Gander, Phillip E ^a   Paul, Brandon T ^a  

^a MCMASTER UNIVERSITY   (Canada)

^b MCMASTER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; AGE; AGED; ARTICLE; AUDIOMETRY; AUDITORY CORTEX; CLINICAL ARTICLE; CONTROLLED STUDY; EVOKED AUDITORY RESPONSE; FEMALE; FORWARD MASKING; HEARING IMPAIRMENT; HUMAN; MALE; NEUROMODULATION; PRIORITY JOURNAL; SOUND INTENSITY; TINNITUS; ADOLESCENT; ADVERSE EFFECTS; AUDITORY EVOKED POTENTIAL; AUDITORY STIMULATION; AUDITORY THRESHOLD; BIOLOGICAL MODEL; CASE CONTROL STUDY; CHRONIC DISEASE; ELECTROENCEPHALOGRAPHY; HEARING; MIDDLE AGED; NOISE; PATHOPHYSIOLOGY; PERCEPTION; PSYCHOLOGY; PSYCHOPHYSICS; SOUND DETECTION; YOUNG ADULT;

ACOUSTIC STIMULATION; ADOLESCENT; ADULT; AGED; AUDIOMETRY; AUDITORY CORTEX; AUDITORY PERCEPTION; AUDITORY THRESHOLD; CASE-CONTROL STUDIES; CHRONIC DISEASE; ELECTROENCEPHALOGRAPHY; EVOKED POTENTIALS, AUDITORY; FEMALE; HUMANS; MALE; MIDDLE AGED; MODELS, NEUROLOGICAL; NOISE; PERCEPTUAL MASKING; PSYCHOACOUSTICS; SOUND SPECTROGRAPHY; TINNITUS; YOUNG ADULT;

EID: 84929168476     PISSN: 03785955     EISSN: 18785891     Source Type: Journal    
DOI: 10.1016/j.heares.2015.04.011     Document Type: Article

References (96)

1. Adjamian P., Sereda M., Zobay O., Hall D.A., Palmer A.R. Neuromagnetic indicators of tinnitus and tinnitus masking in patients with and without hearing loss. J.Assoc. Res. Otolaryngol. 2012, 13:715-731.
2. Bauer C.A., Turner J.G., Caspary D.M., Myers K.S., Brozoski T.J. Tinnitus and inferior colliculus activity in chinchillas related to three distinct patterns of cochlear trauma. J.Neurosci. Res. 2008, 86:2564-2578.
3. Bidet-Caulet A., Fischer C., Besle J., Aguera P.E., Giard M.H., Bertrand O. Effects of selective attention on the electrophysiological representation of concurrent sounds in the human auditory cortex. J.Neurosci. 2007, 27:9252-9261.
4. Boyen K., de Kleine E., van Dijk P., Langers D.R.M. Tinnitus-related dissociation between cortical and subcortical neural activity in humans with mild to moderate sensorineural hearing loss. Hear Res. 2014, 312:48-59. 10.1016/j.heares.2014.03.001.
5. Brattico E., Tervaniemi M., Picton T.W. Effects of brief discrimination-training on the auditory N1 wave. NeuroReport 2003, 14:2489-2492.
6. Brozoski T.J., Bauer C.A., Caspary D.M. Elevated fusiform cell activity in the dorsal cochlear nucleus of chinchillas with psychophysical evidence of tinnitus. J.Neurosci. 2002, 22:2383-2390.
7. Butler R.A. Effects of changes in stimulus frequency and intensity on habituation of the human vertex potential. J.Acoust. Soc. Am. 1968, 44:945-950.
8. Cuny C., Noreña A., El Massioui F., Chéry-Croze S. Reduced attention shift in response to auditory changes in subjects with tinnitus. Audiol. Neurootol. 2004, 9:294-302.
9. De Jongh A., Baayen J.C., de Munck J.C., Heethaar R.M., Vandertop W.P., Stam C.J. The influence of brain tumor treatment on pathological delta activity in MEG. Neuroimage 2003, 20:2291-2301.
10. De Ridder D., Elgoyhen A.B., Romo R., Langguth B. Phantom percepts: tinnitus and pain as persisting aversive memory networks. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:8075-8080.
11. Delorme A., Makeig S. EEGLab: an open source toolbox for analysis of single-trial EEG dynamics. J.Neurosci. Methods 2004, 134:9-21.
12. Diesch E., Andermann M., Rupp A. Is the effect of tinnitus on auditory steady-state response amplitude mediated by attention?. Front. Syst. Neurosci. 2012, 6:38. 10.3389/fnsys.2012.00038.
13. Diesch E., Andermann M., Flor H., Rupp A. Functional and structural aspects of tinnitus- related enhancement and suppression of auditory cortex activity. Neuroimage 2010, 50:1545-1559.
14. Diesch E., Andermann M., Flor H., Rupp A. Interaction among the components of multiple auditory steady-state responses: enhancement in tinnitus patients, inhibition in controls. Neuroscience 2010, 167:540-553.
15. Dietrich V., Nieschalk M., Stoll W., Rajan R., Pantev C. Cortical reorganization in patients with high frequency cochlear hearing loss. Hear Res. 2001, 158:95-101.
16. Eggermont J.J. On the pathophysiology of tinnitus: a review and a peripheral model. Hear Res. 1990, 48:111-124.
17. Eggermont J.J., Roberts L.E. The neuroscience of tinnitus. Trends Neurosci. 2004, 27:676-682. (On-line ahead of print).
18. Eggermont J.J., Roberts L.E. Tinnitus: animal models and findings in humans. Cell. Tissue. Res. 2014, 10.1007/s00441-014-1992-8.
19. Engineer N.D., Riley J.R., Seale J.D., Vrana W.A., Shetake J.A., Sudanagunta S.P., Borland M.S., Kilgard M.P. Reversing pathological neural activity using targeted plasticity. Nature 2011, 470:101-104.
20. Furman A.C., Kujawa S.G., Liberman C. Noise-induced cochlear neuropathy is selective for fibers with low spontaneous rates. J.Neurophysiol. 2013, 110:577-586.
21. Galazyuk A., Grimsley C., Longenecker R. Sound-triggered Suppression of Neuronal Firing in the Auditory Cortex: Implication to the Residual Inhibition of Tinnitus 2014, Annual Meeting of the Association for Research in Otolaryngoloy, PS-825.
22. Gander P.E., Bosnyak D.J., Roberts L.E. Evidence for modality-specific but not frequency-specific modulation of human primary auditory cortex by attention. Hear. Res. 2010, 268:213-226.
23. Gander P.E., Bosnyak D.J., Roberts L.E. Acoustic experience but not attention modifies neural population phase expressed in human primary auditory cortex. Hear. Res. 2010, 269:81-94.
24. Godey B., Schwartz D., de Graaf J.B., Chauvel P., Liegeois-Chauvel C. Neuromagnetic source localization of auditory evoked fields and intracerebral evoked potentials: a comparison of data in the same patients. Clin. Neurophysiol. 2001, 112:1850-1859.
25. Gu J.W., Herrmann B.S., Levine R.A., Melcher J.R. Brainstem auditory evoked potentials suggest a role for the ventral cochlear nucleus in tinnitus. J.Assoc. Res. Otolaryngol. 2012 Dec, 13(6):819-833. (Epub 2012 Aug 7). 10.1007/s10162-012-0344-1.
26. Gu J.W., Halpin C.F., Nam E.C., Levine R.A., Melcher J.R. Tinnitus, diminished sound-Level tolerance, and elevated auditory activity in humans with clinically normal hearing sensitivity. J.Neurophysiol. 2010, 104:3361-3370.
27. Hébert S., Fournier P., Noreña A.J. The auditory sensitivity is increased in tinnitus ears. J.Neurosci. 2013, 33:2356-2364.
28. Hoke M., Feldmann H., Lütkenhöner B., Lehnertz K. Objective evidence of tinnitus in auditory evoked magnetic fields. Hear. Res. 1989, 37:281-286.
29. Husain F.T., Schmidt S.A. Using resting state functional connectivity to unravel networks of tinnitus. Hear. Res. 2014, 307:153-162.
30. Jacobson G.P., McCaslin D.L. Areexamination of the long latency N1 response in patients with tinnitus. J.Amer. Acad. Audiol. 2003, 14:393-400.
31. Jacobson G.P., Ahmad B.K., Moran J., Newman C.W., Tepley N., Wharton J. Auditory evoked cortical magnetic field (M100-M200) measurements in tinnitus and normal groups. Hear. Res. 1991, 56:44-52.
32. Kaas J.H., Hackett T.A. Subdivisions of auditory cortex and processing streams in primates. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:11793-11799.
33. Kadner A., Viirre E., Wester D.C., Walsh S.F., Hestenes J., Vankov A., Pineda J.A. Lateral inhibition in the auditory cortex: an EEG index of tinnitus?. Neuroreport 2002, 13:443-446.
34. Kahlbrock N., Weisz N. Transient reduction of tinnitus intensity is marked by concomitant reductions of delta band power. BMC Biol. 2008, 6. 10.1186/1741-7007-6-4.
35. Kalappa B.I., Brozoski T.J., Turner J.G., Caspary D.M. Single unit hyperactivity and bursting in the auditory thalamus of awake rats directly correlates with behavioural evidence of tinnitus. J.Physiol. 2014 Nov 15, 592(Pt. 22):5065-5078. (Epub 2014 Sep12). 10.1113/jphysiol.2014.278572.
36. Kaltenbach J.A., Zacharek M.A., Zhang J., Frederick S. Activity in the dorsal cochlear nucleus of hamsters previously tested for tinnitus following intense tone exposure. Neurosci. Lett. 2004, 355:121-125.
37. Koehler S., Shore S. Stimulus timing-dependent plasticity in dorsal cochlear nucleus is altered in tinnitus. J.Neurosci. 2013, 50:19647-19656.
38. Koehler S.D., Shore S.E. Stimulus-timing dependent multisensory plasticity in the guinea pig dorsal cochlear nucleus. PloS One 2013, 8:e59828. 10.1371/journal.pone.0059828.
39. Kujawa S.G., Liberman M.C. Adding insult to injury: cochlear nerve degeneration after "temporary" noise-induced hearing loss. J.Neurosci. 2009, 29:14077-14085.
40. Langers D.R., de Kleine E., van Dijk P. Tinnitus does not require macroscopic tonotopic map reorganization. Front. Syst. Neurosci. 2012, 6(2). 10.3389/fnsys.2012.00002.
41. Langers D.R.M., Backes W.H., van Dijk P. Representation of lateralization and tonotopy in primary versus secondary human auditory cortex. NeuroImage 2007, 34:264-273.
42. Lanting C.P., de Kleine E., van Dijk P. Neural activity underlying tinnitus generation: results from PET and fMRI. Hear. Res. 2009, 255:1-13.
43. Lanting C.P., de Kleine E., Langers D.R.M., van Dijk P. Unilateral tinnitus: changes in connectivity and response lateralization measured with fMRI. PLoS One 2014, 9:e110704. 10.1371/journal.pone.0110704.
44. Lee C.Y., Jaw F.S., Pan S.L., Lin M.Y., Young Y.H. Auditory cortical evoked potentials in tinnitus patients with normal audiological presentation. J.Formos. Med. Assoc. 2007, 106:979-985.
45. Liu X.P., Chen L. Forward acoustic masking enhances the auditory brainstem response in a diotic, but not dichotic, paradigm in salicylate-induced tinnitus. Hear Res. 2015, 323:51-60.
46. Llinás R., Urbano F.J., Leznik E., Ramírez R.R., van Marle H.J. Rhythmic and dysrhythmic thalamocortical dynamics: GABA systems and the edge effect. Trends Neurosci. 2005, 28:325-333.
47. Lütkenhöner B., Steinsträter O. High-precision neuromagnetic study of the functional organization of the human auditory cortex. Audiol. Neurootol. 1998, 3:191-213.
48. Lütkenhöner B., Krumbholz K., Seither-Preisler A. Studies of tonotopy based on waveN100 of the auditory evoked field are problematic. NeuroImage 2003, 19:935-949.
49. Meinzer M., Elbert T., Wienbruch C., Djundja D., Barthel G., Rockstroh B. Intensive language training enhances brain plasticity in chronic aphasia. BMC Biol. 2004, 2:20,. 10.1186/1741-7007-2-20.
50. Mulders W.H., Robertson D. Progressive centralization of midbrain hyperactivity after acoustic trauma. Neuroscience 2011, 192:753-760.
51. Noreña A.J., Eggermont J.J. Changes in spontaneous neural activity immediately after an acoustic trauma: implications for neural correlates of tinnitus. Hear. Res. 2003, 183:137-153.
52. Noreña A., Eggermont J.J. Enriched acoustic environment after noise trauma abolishes neural signs of tinnitus. Neuroreport 2006, 17:559-563.
53. Noreña A.J., Gourévitch B., Aizawa N., Eggermont J.J. Spectrally enhanced acoustic environment disrupts frequency representation in cat auditory cortex. Nat. Neurosci. 2006, 9:932-939.
54. Noreña A., Micheyl C., Chéry-Croze S., Collet L. Psychoacoustic characterization of the tinnitus spectrum: implications for the underlying mechanisms of tinnitus. Audiol. Neurootol 2002, 7:358-369.
55. Noreña A.J., Cransac H., Chery-Croze S. Towards an objectification by classification of tinnitus. Clin. Neurophysiol. 1999, 110:666-675.
56. Osaki Y., Nishimura H., Takasawa M., Imaizumi M., Kawashima T., Iwaki T., Oku N., Hashikawa K., Doi K., Nishimura T., Hatazawa J., Kubo T. Neural mechanism of residual inhibition of tinnitus in cochlear implant users. NeuroReport 2005, 16:1625-1628.
57. Paltoglou A.E., Sumner C.J., Hall D.A. Examining the role of frequency specificity in the enhancement and suppression of human cortical activity by auditory selective attention. Hear Res. 2009, 257:106-118.
58. Pantev C., Roberts L.E., Elbert T., Ross B., Wienbruch C. Tonotopic organization of the sources of human auditory steady-state responses. Hear. Res. 1996, 101:62-74.
59. Paul B., Bruce I., Bosnyak D., Roberts L.E. Modulation of electrocortical brain activity by attention in normal hearing and in tinnitus. Neural Plast. 2014, Article ID 127824, (Epub 2014 Jun 12). 10.1155/2014/127824.
60. Pienkowski M., Eggermont J.J. Long-term, partially-reversible reorganization of frequency tuning in mature cat primary auditory cortex can be induced by passive exposure to moderate-level sounds. Hear. Res. 2009, 257:24-40.
61. Pienkowski M., Munguia R., Eggermont J.J. Passive exposure of adult cats to band limited tone pip ensembles or noise leads to long-term response suppression in auditory cortex. Hear. Res. 2011, 277:117-126.
62. Pienkowski M., Eggermont J.J. 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 2012, 33:305-314.
63. Plack C.J., Barker D., Prendergast G. Perceptual consequences of "hidden" hearing loss. Trends Hear. 2014, 18:1-11.
64. Pozo K., Goda Y. Unraveling mechanisms of homeostatic synaptic plasticity. Neuron 2010, 66:337-351.
65. Rajan R., Irvine D.R.F., Wise L.Z., Heil P. Effect of unilateral partial cochlear lesions in adults cats on representation of lesioned and unlesioned cochleas in primary auditory cortex. J.Comp. Neurol. 1993, 338:17-49.
66. Roberts L.E. Neural plasticity and neural synchrony in tinnitus. Textbook of Tinnitus 2010, 103-112. Humana-Springer. A. Møller, T. Kleinjung, B. Langguth, D. De Ridder (Eds.).
67. Roberts L.E., Husain F.T., Eggermont J.J. Role of attention in the generation and modulation of tinnitus. Neurosci. Biobehav. Rev. 2013, 37:1754-1773. 10.1016/j.neubiorev.2013.07.007.
68. Roberts L.E., Bosnyak D.J., Thompson D.C. Neural plasticity expressed in central auditory structures with and without tinnitus. Front. Syst. Neurosci. 2012, 6:40. 10.3389/fnsys.2012.00040.
69. Roberts L.E., Moffat G., Bosnyak D.J. Residual inhibition functions in relation to tinnitus spectra and auditory threshold shift. Acta Otolaryngol. 2006, (Suppl.556):27-33.
70. Roberts L.E., Eggermont J.J., Caspary D.C., Shore S.E., Melcher J.R., Kaltenbach J.A. Ringing ears: the neuroscience of tinnitus. J.Neurosci. 2010, 30:14980-14986.
71. Roberts L.E., Moffat G., Baumann M., Ward L.M., Bosnyak D.J. Residual inhibition functions overlap tinnitus spectra and the region of auditory threshold shift. J.Assoc. Res. Otolaryngol. 2008, 9:417-435.
72. Robertson D., Irvine D.R.F. Plasticity of frequency organization in auditory cortex of guinea pigs with partial unilateral deafness. J.Comp. Neurol. 1989, 282:456-461.
73. Ross B., Borgmann C., Draganova R., Roberts L.E., Pantev C. Ahigh-precision magnetoencephalographic study of human auditory steady-state responses to amplitude-modulated tones. J.Acoust. Soc. Am. 2000, 108:679-691.
74. Sarter M., Hasselmo M.E., Bruno J.P., Givens B. Unraveling the attentional functions of cortical cholinergic inputs: interactions between signal-driven and cognitive modulation of signal detection. Brain Res. Rev. 2005, 48:98-111.
75. Schatte R., McApline D. Tinnitus with a normal audiogram: physiological evidence for hidden hearing loss and computational model. J.Neurosci. 2011, 31:13452-13457.
76. Scholl B., Wehr M. Disruption of balanced cortical excitation and inhibition by acoustic trauma. J.Neurophysiol. 2008, 100:646-656.
77. Schreiner C.E., Cynader M.S. Basic functional organization of second auditory cortical field (AII) of the cat. J.Neurophysiol. 1984, 51:1284-1305.
78. Schreiner C.E., Winer J.A. Auditory cortex mapmaking: principles, projections, and plasticity. Neuron 2007, 56:356-365.
79. Sedley W., Teki S., Kumar S., Barnes G.R., Bamiou D.E., Griffiths T.D. Single-subject oscillatory gamma responses in tinnitus. Brain 2012, 135:3089-3100. 10.1093/brain/aws220.
80. Seki S., Eggermont J.J. Changes in cat primary auditory cortex after minor-to-moderate pure-tone induced hearing loss. Hear. Res. 2002, 173:172-186.
81. Seki S., Eggermont J.J. Changes in spontaneous firing rate and neural synchrony in cat primary auditory cortex after localized tone-induced hearing loss. Hear. Res. 2003, 180:28-38.
82. Sereda M., Hall D.A., Bosnyak D.J., Edmondson-Jones M., Roberts L.E., Adjamian P., Palmer A.R. Re-examining the relationship between audiometric profile and tinnitus pitch. Int. J. Audiol. 2011, 50:303-312.
83. Sereda M., Adjamian P., Edmondson-Jones M., Palmer A.R., Hall D.A. Auditory evoked magnetic fields in individuals with tinnitus. Hear. Res. 2013, 302:50-59.
84. Sergeyenko Y., Lall L., Liberman M.C., Kujawa S.G. Age-related cochlear synaptopathy: an early-onset contributor to auditory functional decline. J.Neurosci. 2013, 33:13686-13694.
85. Stefanescu R.A., Koehler S.D., Shore S.E. Stimulus-timing dependent modifications of rate-level functions in animals with and without tinnitus. J.Neurophysiol. 2015, (in press).
86. Tan C.M., Lecluyse W., McFerran D., Meddis R. Tinnitus and patterns of hearing loss. J.Assoc. Res. Otolaryngol. 2013, 14:275-282. 10.1007/s10162-013-0371-6.
87. Tardif E., Clarke S. Intrinsic connectivity of human auditory areas: a tracing study with Dil. Euro. J. Neurosci. 2001, 13:1045-1050.
88. Turrigiano G.G., Nelson S.B. Homeostatic plasticity in the developing nervous system. Nat. Rev. Neurosci. 2004, 5:97-107.
89. Vanneste S., De Ridder D. The auditory and nonauditory brain areas involved in tinnitus: an emergent property of multiple parallel overlapping subnetworks. Front. Syst. Neurosci. 2012, 6. 10.3389/fnsys.2012.00031.
90. Vieth J.B., Kober H., Grummich P. Sources of spontaneous slow waves associated with brain lesions, localized by using the MEG. Brain Topogr. 1996, 8:215-221.
91. Vogler D.P., Robertson D., Mulders W.H. Hyperactivity following unilateral hearing loss in characterized cells in the inferior colliculus. Neurosci 2014, 265:28-36.
92. Wehr M., Zador A.M. Synaptic mechanisms of forward suppression in rat auditory cortex. Neuron 2005, 47:437-445.
93. Wienbruch C., Paul I., Weisz N., Elbert T., Roberts L.E. Frequency organization of the 40-Hz auditory steady-state response in normal hearing and in tinnitus. Neuroimage 2006, 33:180-194.
94. Weisz N., Moratti S., Meinzer M., Dohrmann K., Elbert T. Tinnitus perception and distress is related to abnormal spontaneous brain activity as measured by magnetoencephalography. PLoS Med. 2005, (2):e153.
95. Weisz N., Muller S., Schlee W., Dohrmann K., Hartmann T., Elbert T. The neural code of auditory phantom perception. J.Neurosci. 2007, 27:1479-1484.
96. Yang S., Weiner B.D., Zhang L.S., Cho S.J., Bao S. Homeostatic plasticity drives tinnitus perception in an animal model. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:14974-14979.