Maladaptive neural synchrony in tinnitus: Origin and restoration

Frontiers in Neurology

Volumn 6, Issue FEB, 2015, Pages

  Eggermont, Jos J ^a,b   Tass, Peter A ^c,d,e  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

^c FORSCHUNGSZENTRUM JÜLICH   (Germany)

^d STANFORD UNIVERSITY   (United States)

^e UNIVERSITY OF COLOGNE   (Germany)

Author keywords

Brain rhythms; Coordinated reset; Neural plasticity; Neural synchrony; Tinnitus

Indexed keywords

ANTICONVULSIVE AGENT;

AMPLITUDE MODULATION; AUDITORY CORTEX; AUDITORY STIMULATION; BOLD SIGNAL; BRAIN DEPTH STIMULATION; CORTICAL SYNCHRONIZATION; DELTA RHYTHM; ELECTRIC POTENTIAL; ELECTROENCEPHALOGRAM; ELECTROENCEPHALOGRAPHY PHASE SYNCHRONIZATION; EVOKED RESPONSE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GAMMA RHYTHM; HEARING IMPAIRMENT; HUMAN; KINDLING; LOUDNESS; LOW RESOLUTION BRAIN ELECTROMAGNETIC TOMOGRAPHY; MACROSCOPIC SYNCHRONY; MESOSCOPIC SYNCHRONY; MICROSCOPIC SYNCHRONY; NERVE CELL MEMBRANE POTENTIAL; NERVE CELL PLASTICITY; NEUROMODULATION; NONHUMAN; OSCILLATION; PITCH; POSTSYNAPTIC POTENTIAL; RESTING STATE NETWORK; REVIEW; SLOW BRAIN WAVE; SPIKE WAVE; TINNITUS; VISUAL ANALOG SCALE;

EID: 84926480705     PISSN: None     EISSN: 16642295     Source Type: Journal    
DOI: 10.3389/fneur.2015.00029     Document Type: Review

References (183)

1. Eggermont JJ. Tinnitus: processing of phantom sound. In: Koob GF, Le Moal M, Thompson RF, editors. Encyclopedia of Behavioural Neuroscience. (Vol. 3), Oxford: Academic Press (2010). p. 405-11.
2. MacNaughton-Jones H. The etiology of tinnitus aurium. Br Med J (1890) 20:667-72.
3. Eggermont JJ, Roberts LE. The Neuroscience of tinnitus. Trends Neurosci (2004) 27:676-82. doi:10.1016/j.tins.2004.08.010
4. Schaette R, Kempter R. Development of tinnitus-related neuronal hyperactivity through homeostatic plasticity after hearing loss: a computational model. Eur J Neurosci (2006) 23:3124-38. doi:10.1111/j.1460-9568.2006.04774.x
5. Nondahl DM, Cruickshanks KJ, Huang G-H, Klein BEK, Klein R, Nieto FJ, et al. Tinnitus and its risk factors in the Beaver Dam offspring study. Int J Audiol (2011) 50:313-20. doi:10.3109/14992027.2010.551220
6. Varela F, Lachaux JP, Rodriguez E, Martinerie J. The brainweb: phase synchronization and large-scale integration. Nat Rev Neurosci (2001) 2:229-39. doi:10.1038/35067550
7. Braitenberg V, Schüz A. Anatomy of the Cortex. Statistics and Geometry. Berlin: Springer Verlag (1991).
8. Abeles M. Local Cortical Circuits. Berlin: Springer Verlag (1982).
9. Gil Z, Connors BW, Amitai Y. Efficacy of thalamocortical and intracortical synaptic connections: quanta, innervation, and reliability. Neuron (1999) 23:385-97. doi:10.1016/S0896-6273(00)80788-6
10. Miller LM, Escabí MA, Read HL, Schreiner CE. Functional convergence of response properties in the auditory thalamocortical system. Neuron (2001) 32:151-60. doi:10.1016/S0896-6273(01)00445-7
11. Eggermont JJ, Smith GM. Synchrony between single-unit activity and local field potentials in relation to periodicity coding in primary auditory cortex. J Neurophysiol (1995) 73:227-45.
12. Eggermont JJ, Munguia R, Pienkowski M, Shaw G. Comparison of LFP-based and spike-based spectro-temporal receptive fields and neural synchrony in cat primary auditory cortex. PLoS One (2011) 6(5):e20046. doi:10.1371/journal.pone.0020046
13. Britvina T, Eggermont JJ. Multi-frequency stimulation disrupts spindling activity in anesthetized animals. Neuroscience (2008) 151:888-900. doi:10.1016/j.neuroscience.2007.11.028
14. Mitzdorf U. Current source-density method and application in cat cerebral cortex: investigation of evoked potentials and EEG phenomena. Physiol Rev (1985) 65:37-100.
15. Berens P, Keliris GA, Ecker AS, Logothetis NK, Tolias AS. Feature selectivity of the gamma-band of the local field potential in primate primary visual cortex. Front Neurosci (2008) 2:199-207. doi:10.3389/neuro.01.037.2008
16. Steriade M. Grouping of brain rhythms in corticothalamic systems. Neuroscience (2006) 137:1087-106. doi:10.1016/j.neuroscience.2005.10.029
17. Bartos M, Vida I, Jonas P. Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks. Nat Rev Neurosci (2007) 8:45-56. doi:10.1038/nrn2044
18. Fries P, Nikoli D, Singer W. The gamma cycle. Trends Neurosci (2007) 30:309-16. doi:10.1016/j.tins.2007.05.005
19. Wang X-J, Buzsáki G. Gamma oscillation by synaptic inhibition in a hippocampal interneuronal network model. J Neurosci (1996) 16:6402-13.
20. Young CK, Eggermont JJ. Coupling of mesoscopic brain oscillations: recent advances in analytical and theoretical perspectives. Prog Neurobiol (2009) 89:61-78. doi:10.1016/j.pneurobio.2009.06.002
21. Steriade M, Amzica F. Intracortical and corticothalamic coherency of fast spontaneous oscillations. Proc Natl Acad Sci U S A (1996) 93:2533-8. doi:10.1073/pnas.93.6.2533
22. Llinás RR. The intrinsic electrophysiological properties of mammalian neurons: insights into central nervous system function. Science (1988) 242:1654-64. doi:10.1126/science.3059497
23. Buzsáki G, Draguhn A. Neuronal oscillations in cortical networks. Science (2004) 304:1926-9. doi:10.1126/science.1099745
24. Singer W, Gray CM. Visual feature integration and the temporal correlation hypothesis. Annu Rev Neurosci (1995) 18:555-86. doi:10.1146/annurev.ne.18.030195.003011
25. Eggermont JJ. Electric and magnetic fields of synchronous neural activity propagated to the surface of the head: peripheral and central origins of AEPs. In: Burkard RR, Don M, Eggermont JJ, editors. Auditory Evoked Potentials. Baltimore: Lippincott Williams & Wilkins (2007). p. 2-21.
26. Uhlhaas PJ, Singer W. Neural synchrony in brain disorders: relevance for cognitive dysfunctions and pathophysiology. Neuron (2006) 52:155-68. doi:10.1016/j.neuron.2006.09.020
27. Hari R, Salmelin R. Human cortical oscillations: a neuromagnetic view through the skull. Trends Neurosci (1997) 20:44-9. doi:10.1016/S0166-2236(96)10065-5
28. Niedermeyer E. Alpha rhythms as physiological and abnormal phenomena. Int J Psychophysiol (1997) 26:31-49. doi:10.1016/S0167-8760(97)00754-X
29. Nystrom C, Matousek M, Hallstrom T. Relationships between EEG and clinical characteristics in major depressive disorder. Acta Psychiatr Scand (1986) 73:390-4. doi:10.1111/j.1600-0447.1986.tb02700.x
30. Llinás RR, Ribary U, Jeanmonod D, Kronberg E, Mitra PP. Thalamocortical dysrhythmia: a neurological and neuropsychiatric syndrome characterized by magnetoencephalography. Proc Natl Acad Sci U S A (1999) 96:15222-7. doi:10.1073/pnas.96.26.15222
31. Noreña AJ, Eggermont JJ. Enriched acoustic environment after noise trauma abolishes neural signs of tinnitus. Neuroreport (2006) 17:559-63. doi:10.1097/00001756-200604240-00001
32. Noreña AJ, Eggermont JJ. Changes in spontaneous neural activity immediately after an acoustic trauma: implications for neural correlates of tinnitus. Hear Res (2003) 183:137-53. doi:10.1016/S0378-5955(03)00225-9
33. Eggermont JJ, Komiya H. Moderate noise trauma in juvenile cats results in profound cortical topographic map changes in adulthood. Hear Res (2000) 142:89-101. doi:10.1016/S0378-5955(00)00024-1
34. Seki S, Eggermont JJ. 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. doi:10.1016/S0378-5955(03)00074-1
35. Noreña AJ, Tomita M, Eggermont JJ. Neural changes in cat auditory cortex after a transient pure-tone trauma. J Neurophysiol (2003) 90:2387-401. doi:10.1152/jn.00139.2003
36. Noreña AJ, Eggermont JJ. Enriched acoustic environment after noise trauma reduces hearing loss and prevents cortical map reorganization. J Neurosci (2005) 25:699-705. doi:10.1523/JNEUROSCI.2226-04.2005
37. Noreña AJ, Gourévitch B, Aizawa N, Eggermont JJ. Spectrally enhanced acoustic environment disrupts frequency representation in cat auditory cortex. Nat Neurosci (2006) 9:932-9. doi:10.1038/nn1720
38. Engineer ND, Riley JR, Seale JD, Vrana WA, Shetake JA, Sudanagunta SP, et al. Reversing pathological neural activity using targeted plasticity. Nature (2011) 470:101-4. doi:10.1038/nature09656
39. Rajan R. Receptor organ damage causes loss of cortical surround inhibition without topographic map plasticity. Nat Neurosci (1998) 1:138-43. doi:10.1038/388
40. Seki S, Eggermont JJ. Changes in cat primary auditory cortex after minor-to-moderate pure-tone induced hearing loss. Hear Res (2002) 173:172-86. doi:10.1016/S0378-5955(02)00518-X
41. Eggermont JJ. Hearing loss, hyperacusis, and tinnitus: what is modeled in animal research? Hear Res (2013) 295:140-9. doi:10.1016/j.heares.2012.01.005
42. Song J-J, De Ridder D, Schlee W, Van de Heyning P, Vanneste S. "Distressed aging": the differences in brain activity between early- and late-onset tinnitus. Neurobiol Aging (2013) 34:1853-63. doi:10.1016/j.neurobiolaging.2013.01.014
43. 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. doi:10.1371/journal.pmed.0020153
44. Lehtelä L, Salmelin R, Hari R. Evidence for reactive magnetic 10-Hz rhythm in the human auditory cortex. Neurosci Lett (1997) 222:111-4. doi:10.1016/S0304-3940(97)13361-4
45. Kahlbrock N, Weisz N. Transient reduction of tinnitus intensity is marked by concomitant reductions of delta band power. BMC Biol (2008) 6:4. doi:10.1186/1741-7007-6-4
46. Llinás R, Urbano FJ, Leznik E, Ramírez RR, van Marle HJ. Rhythmic and dysrhythmic thalamocortical dynamics: GABA systems and the edge effect. Trends Neurosci (2005) 28:325-33. doi:10.1016/j.tins.2005.04.006
47. Weisz N, Müller S, Schlee W, Dohrmann K, Hartmann T, Elbert T. The neural code of auditory phantom perception. J Neurosci (2007) 27:1479-84. doi:10.1523/JNEUROSCI.3711-06.2007
48. Ashton H, Reid K, Marsh R, Johnson I, Alter K, Griffiths T. High frequency localised "hot spots" in temporal lobes of patients with intractable tinnitus: a quantitative electroencephalographic (QEEG) study. Neurosci Lett (2007) 426:23-8. doi:10.1016/j.neulet.2007.08.034
49. Van der Loo E, Gais S, Congedo M, Vanneste S, Plazier M, Menovsky T, et al. Tinnitus intensity dependent gamma oscillations of the contralateral auditory cortex. PLoS One (2009) 4(10):e7396. doi:10.1371/journal.pone.0007396
50. Lorenz I, Müller N, Schlee W, Hartmann T, Weisz N. Loss of alpha power is related to increased gamma synchronization-A marker of reduced inhibition in tinnitus? Neurosci Lett (2009) 453(3):225-8. doi:10.1016/j.neulet.2009.02.028
51. Schlee W, Hartmann T, Langguth B, Weisz N. Abnormal resting-state cortical coupling in chronic tinnitus. BMC Neurosci (2009) 10:11. doi:10.1186/1471-2202-10-11
52. Schlee W, Mueller N, Hartmann T, Keil J, Lorenz I, Weisz N. Mapping cortical hubs in tinnitus. BMC Biol (2009) 23(7):80. doi:10.1186/1741-7007-7-80
53. Adjamian P, Sereda M, Zobay O, Hall DA, Palmer A. Neuromagnetic indicators of tinnitus and tinnitus masking in patients with and without hearing loss. J Assoc Res Otolaryngol (2012) 13(5):715-31. doi:10.1007/s10162-012-0340-5
54. Ortmann M, Müller N, Schlee W, Weisz N. Rapid increase of gamma power in the auditory cortex following noise trauma in humans. Eur J Neurosci (2011) 33:568-75. doi:10.1111/j.1460-9568.2010.07542.x
55. Eggermont JJ. Neural interaction in cat primary auditory cortex. Dependence on recording depth, electrode separation and age. J Neurophysiol (1992) 68:1216-28.
56. Voss LJ, Baas CH, Hansson L, Li D, Sleigh JW. Investigation into the effect of the general anaesthetic etomidate on local neuronal synchrony in the mouse neocortical slice. Brain Res (2013) 1526:65-70. doi:10.1016/j.brainres.2013.06.013
57. Eggermont JJ. The Correlative Brain; Theory and Experiment in Neural Interaction. Berlin: Springer Verlag (1990).
58. Cohen MR, Maunsell JHR. Attention improves performance primarily by reducing interneuronal correlation. Nat Neurosci (2009) 12(12):1594-600. doi:10.1038/nn.2439
59. Schmidt SA, Akrofi K, Carpenter-Thompson JR, Husain FT. Default mode, dorsal attention and auditory resting state networks exhibit differential functional connectivity in tinnitus and hearing loss. PLoS One (2013) 8(10):e76488. doi:10.1371/journal.pone.0076488
60. Melcher JR, Knudson IM, Levine RA. Subcallosal brain structure: correlation with hearing threshold at supra-clinical frequencies (>8 kHz), but not with tinnitus. Hear Res (2013) 295:79-86. doi:10.1016/j.heares.2012.03.013
61. Boyen K, Langers DRM, de Kleine E, van Dijk P. Gray matter in the brain: differences associated with tinnitus and hearing loss. Hear Res (2013) 295:67-78. doi:10.1016/j.heares.2012.02.010
62. Eggermont JJ. Properties of correlated neural activity clusters in cat auditory cortex resemble those of neural assemblies. J Neurophysiol (2006) 68:746-64.
63. Kajikawa Y, Schroeder CE. How local is the local field potential? Neuron (2011) 72:847-58. doi:10.1016/j.neuron.2011.09.029
64. Cardin JA, Carlén M, Meleti SK, Knoblich U, Ahang F, Deisseroth K, et al. Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature (2009) 459:663-7. doi:10.1038/nature08002
65. Denker M, Roux S, Lindén H, Diesmann M, Riehle A, Grün S. The local field potential reflects surplus spike synchrony. Cereb Cortex (2011) 21:2681-95. doi:10.1093/cercor/bhr040
66. Eggermont JJ. Sound induced correlation of neural activity between and within three auditory cortical areas. J Neurophysiol (2000) 83:2708-22.
67. deCharms RC, Merzenich MM. Primary cortical representation of sounds by the coordination of action-potential timing. Nature (1996) 381:610-3. doi:10.1038/381610a0
68. Eggermont JJ. Firing rate and firing synchrony distinguish dynamic from steady state sound. Neuroreport (1997) 8:2709-13. doi:10.1097/00001756-199708180-00014
69. Mulert C, Jäger L, Propp S, Karch S, Störmann S, Pogarell O, et al. Sound level dependence of the primary auditory cortex: simultaneous measurement with 61-channel EEG and fMRI. Neuroimage (2005) 28:49-58. doi:10.1016/j.neuroimage.2005.05.041
70. Gross J, Schnitzler A, Timmermann L, Ploner M. Gamma oscillations in human primary somatosensory cortex reflect pain perception. PLoS Biol (2007) 5:e133. doi:10.1371/journal.pbio.0050133
71. de Lafuente V, Romo R. Neuronal correlates of subjective sensory experience. Nat Neurosci (2005) 8:1698-703. doi:10.1038/nn1587
72. Dehaene S, Changeux JP, Naccache L, Sackur J, Sergent C. Conscious, preconscious, and subliminal processing: a testable taxonomy. Trends Cogn Sci (2006) 10:204-11. doi:10.1016/j.tics.2006.03.007
73. Luczak A, Barthó P, Harris KD. Spontaneous events outline the realm of possible sensory responses in neocortical populations. Neuron (2009) 62:413-25. doi:10.1016/j.neuron.2009.03.014
74. Dehaene S, Changeux JP. Ongoing spontaneous activity controls access to consciousness: a neuronal model for inattentional blindness. PLoS Biol (2005) 3(5):e141. doi:10.1371/journal.pbio.0030141
75. Fox MD, Raichle ME. Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev Neurosci (2007) 8:700-11. doi:10.1038/nrn2201
76. Fox MD, Snyder AZ, Vincent JL, Corbetta M, Van Essen DC, Raichle ME. The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc Natl Acad Sci U S A (2005) 102:9673-8. doi:10.1073/pnas.0504136102
77. Steriade M, Contreras D, Curro Dossi R, Nunez A. The slow (<1 Hz) oscillation in reticular thalamic and thalamocortical neurons: scenario of sleep rhythm generation in interacting thalamic and neocortical networks. J Neurosci (1993) 13:3284-99.
78. Luczak A, Barthó P, Marguet SL, Buzsáki G, Harris KD. Sequential structure of neocortical spontaneous activity in vivo. Proc Natl Acad Sci U S A (2007) 104:347-52. doi:10.1073/pnas.0605643104
79. Eggermont JJ. Neural interaction in cat primary auditory cortex II. Effects of sound stimulation. J Neurophysiol (1994) 71:246-70.
80. Tsodyks M, Kenet T, Grinvald A, Arieli A. Linking spontaneous activity of single cortical neurons and the underlying functional architecture. Science (1999) 286:1943-6. doi:10.1126/science.286.5446.1943
81. Destexhe A, Contreras D, Steriade M. Spatiotemporal analysis of local field potentials and unit discharges in cat cerebral cortex during natural wake and sleep states. J Neurosci (1999) 19:4595-608.
82. Maudoux A, Lefebvre P, Cabay JE, Demertzi A, Vanhaudenhuyse A, Laureys S, et al. Connectivity graph analysis of the auditory resting state network in tinnitus. Brain Res (2012) 1485:10-21. doi:10.1016/j.brainres.2012.05.006
83. Maudoux A, Lefebvre P, Cabay JE, Demertzi A, Vanhaudenhuyse A, Laureys S, et al. Auditory resting-state network connectivity in tinnitus: a functional MRI study. PLoS One (2012) 7:e36222. doi:10.1371/journal.pone.0036222
84. Vanneste S, van de Heyning P, De Ridder D. The neural network of phantom sound changes over time: a comparison between recent-onset and chronic tinnitus patients. Eur J Neurosci (2011) 34:718-31. doi:10.1111/j.1460-9568.2011.07793.x
85. Golm D, Schmidt-Somoa C, Dechent P, Kröner-Herwich B. Neural correlates of tinnitus related distress: an fMRI-study. Hear Res (2012) 295:67-99. doi:10.1016/j.heares.2012.03.003
86. De Ridder D, Elgoyhen AB, Romo R, Langguth B. Phantom percepts: tinnitus and pain as persisting aversive memory networks. Proc Natl Acad Sci U S A (2011) 108:8075-80. doi:10.1073/pnas.1018466108
87. Jastreboff PJ. Phantom auditory perception (tinnitus): mechanisms of generation and perception. Neurosci Res (1990) 8:221-54. doi:10.1016/0168-0102(90)90031-9
88. Burton H, Wineland A, Bhattacharya M, Nicklaus J, Garcia KS, Piccirillo JF. Altered networks in bothersome tinnitus: a functional connectivity study. BMC Neurosci (2012) 2012(13):3. doi:10.1186/1471-2202-13-3
89. Wineland AM, Burton H, Piccirillo J. Functional connectivity networks in nonbothersome tinnitus. Otolaryngol Head Neck Surg (2012) 147(5):900-6. doi:10.1177/0194599812451414
90. Davies J, Gander PE, Andrews M, Hall DA. Auditory network connectivity in tinnitus patients: a resting-state fMRI study. Int J Audiol (2013) 53(3):192-8. doi:10.3109/14992027.2013.846482
91. Goddard GV, McIntyre DC, Leech CK. A permanent change in brain function resulting from daily electrical stimulation. Exp Neurol (1969) 25:295-330. doi:10.1016/0014-4886(69)90128-9
92. Valentine PA, Teskey GC, Eggermont JJ. Kindling changes burst firing, neural synchrony and tonotopic organization of cat primary auditory cortex. Cereb Cortex (2004) 14:827-39. doi:10.1093/cercor/bhh041
93. Eggermont JJ. Correlated neural activity as the driving force for functional changes in auditory cortex. Hear Res (2007) 229:69-80. doi:10.1016/j.heares.2007.01.008
94. Lopes da Silva FH, Kamphuis W, Titulaer M, Vreugdenhil M, Wadman WJ. An experimental model of progressive epilepsy: the development of kindling of the hippocampus of the rat. Ital J Neurol Sci (1995) 16:45-57. doi:10.1007/BF02229074
95. Racine RJ, Chapman CA, Teskey GC, Milgram NW. Postactivation potentiation in the neocortex. III. Kindling-induced potentiation in the chronic preparation. Brain Res (1995) 702:77-86. doi:10.1016/0006-8993(95)01025-0
96. Chapman AG. Glutamate receptors in epilepsy. Prog Brain Res (1998) 116:371-83. doi:10.1016/S0079-6123(08)60449-5
97. Read HL, Winer JA, Schreiner CE. Modular organization of intrinsic connections associated with spectral tuning in cat auditory cortex. Proc Natl Acad Sci U S A (2001) 98:8042-7. doi:10.1073/pnas.131591898
98. Wallace MN, Kitzes LM, Jones EG. Intrinsic inter- and intralaminar connections and their relationship to the tonotopic map in cat primary auditory cortex. Exp Brain Res (1991) 86:527-44. doi:10.1007/BF00230526
99. Lee CC, Winer JA. Principles governing auditory cortex connections. Cereb Cortex (2005) 15:1804-14. doi:10.1093/cercor/bhi057
100. Tomita M, Eggermont JJ. Cross-correlation and joint spectro-temporal receptive field properties in auditory cortex. J Neurophysiol (2005) 93:378-92. doi:10.1152/jn.00643.2004
101. Yuste R, Bonhoeffer T. Genesis of dendritic spines: insights from ultrastructural and imaging studies. Nat Rev Neurosci (2004) 5:24-34. doi:10.1038/nrn1300
102. Gerstner W, Kempter R, van Hemmen J, Wagner H. A neuronal learning rule for sub-millisecond temporal coding. Nature (1996) 383:76-81. doi:10.1038/383076a0
103. Markram H, Lübke J, Frotscher M, Sakmann B. Regulation of synaptic efficacy by coincidence of postsynaptic aps and epsps. Science (1997) 275:213-5. doi:10.1126/science.275.5297.213
104. Tass PA, Majtanik M. Long-term anti-kindling effects of desynchronizing brain stimulation: a theoretical study. Biol Cybern (2006) 94(1):58-66. doi:10.1007/s00422-005-0028-6
105. Tass PA, Hauptmann C. Therapeutic modulation of synaptic connectivity with desynchronizing brain stimulation. Int J Psychophysiol (2007) 64:53-61. doi:10.1016/j.ijpsycho.2006.07.013
106. Tass PA, Hauptmann C. Anti-kindling achieved by stimulation targeting slow synaptic dynamics. Restor Neurol Neurosci (2009) 27(6):589-609. doi:10.3233/RNN-2009-0484
107. Hauptmann C, Tass PA. Therapeutic rewiring by means of desynchronizing brain stimulation. Biosystems (2007) 89:173-81. doi:10.1016/j.biosystems.2006.04.015
108. Tass PA. Phase Resetting in Medicine and Biology: Stochastic Modelling and Data Analysis. Berlin: Springer Verlag (1999).
109. Tass PA. A model of desynchronizing deep brain stimulation with a demand-controlled coordinated reset of neural subpopulations. Biol Cybern (2003) 89:81-8. doi:10.1007/s00422-003-0425-7
110. Tass PA. Desynchronization by means of a coordinated reset of neural sub-populations - a novel technique for demand-controlled deep brain stimulation. Prog Theor Phys Suppl (2003) 150:281-96. doi:10.1143/PTPS.150.281
111. Tass PA, Qin L, Hauptmann C, Doveros S, Bezard E, Boraud T, et al. Coordinated reset neuromodulation has sustained after-effects in parkinsonian monkeys. Ann Neurol (2012) 72:816-20. doi:10.1002/ana.23663
112. Adamchic I, Hauptmann C, Barnikol UB, Pawelcyk N, Popovych OV, Barnikol T, et al. Coordinated reset has lasting aftereffects in patients with Parkinson's disease. Mov Disord (2014) 29(13):1679-84. doi:10.1002/mds.25923
113. Tass PA, Silchenko A, Hauptmann C, Barnikol U, Speckmann EJ. Long-lasting desynchronization in rat hippocampal slice induced by coordinated reset stimulation. Phys Rev E Stat Nonlin Soft Matter Phys (2009) 80:011902. doi:10.1103/PhysRevE.80.011902
114. Hauptmann C, Tass PA. Cumulative and after-effects of short and weak coordinated reset stimulation - a modeling study. J Neural Eng (2009) 6:016004. doi:10.1088/1741-2560/6/1/016004
115. Lysyansky B, Popovych OP, Tass PA. Multi-frequency activation of neuronal networks by coordinated reset stimulation. Interface Focus (2011) 1:75-85. doi:10.1098/rsfs.2010.0010
116. Best EN. Null space in the Hodgkin-Huxley equations: a critical test. Biophys J (1979) 27:87-104. doi:10.1016/S0006-3495(79)85204-2
117. Demir SS, Butera RJ, DeFranceschi AA, Clark JW, Byrne JH. Phase sensitivity end entrainment in a modeled bursting neuron. Biophys J (1997) 72:579-94. doi:10.1016/S0006-3495(97)78697-1
118. Tateno T, Robinson HPC. Phase resetting curves and oscillatory stability in interneurons of rat somatosensory cortex. Biophys J (2007) 92:683-95. doi:10.1529/biophysj.106.088021
119. Neiman A, Russell D, Yakusheva T, DiLullo A, Tass PA. Response clustering in transient stochastic synchronization and desynchronization of coupled neuronal bursters. Phys Rev E Stat Nonlin Soft Matter Phys (2007) 76:021908. doi:10.1103/PhysRevE.76.021908
120. Perkel DH, Schulman JH, Segundo JP, Bullock TH, Moore GP. Pacemaker neurons - effects of regularly spaced synaptic input. Science (1964) 145:61-3. doi:10.1126/science.145.3627.61
121. Pinsker HM. Aplysia bursting neurons as endogenous oscillators.1. phase-response curves for pulsed inhibitory synaptic input. J Neurophysiol (1977) 40:527-43.
122. Lerma J, Garcia-Austt E. Hippocampal theta rhythm during paradoxical sleep - effects of afferent stimuli and phase-relationships with phasic events. Electroencephalogr Clin Neurophysiol (1985) 60:46-54. doi:10.1016/0013-4694(85)90950-2
123. Jackson A, Spinks RL, Freeman TCB, Wolpert DM, Lemon RN. Rhythm generation in monkey motor cortex explored using pyramidal tract stimulation. J Physiol (2002) 541:685-99. doi:10.1113/jphysiol.2001.015099
124. Prinz AA, Thirumalai V, Marder E. The functional consequences of changes in the strength and duration of synaptic inputs to oscillatory neurons. J Neurosci (2003) 23:943-54.
125. Givens B. Stimulus-evoked resetting of the dentate 1 theta rhythm: relation to working memory. Neuroreport (1996) 8:159-63. doi:10.1097/00001756-199612200-00032
126. Makeig S, Westerfield M, Jung TP, Enghoff S, Townsend J, Courchesne E, et al. Dynamic brain sources of visual evoked responses. Science (2002) 295:690-4. doi:10.1126/science.1066168
127. Jansen BH, Agarwal G, Hegde A, Boutros NN. Phase synchronization of the ongoing EEG and auditory EP generation. Clin Neurophysiol (2003) 114:79-85. doi:10.1016/S1388-2457(02)00327-9
128. Ross B, Herdman AT, Pantev C. Stimulus induced desynchronization of human auditory 40-hz steady-state responses. J Neurophysiol (2005) 94:4082-93. doi:10.1152/jn.00469.2005
129. Van der Werf YD, Paus T. The neural response to transcranial magnetic stimulation of the human motor cortex. I. Intracortical and cortico-cortical contributions. Exp Brain Res (2006) 175:231-45. doi:10.1007/s00221-006-0548-x
130. Popovych OV, Tass PA. Desynchronizing electrical and sensory coordinated reset neuromodulation. Front Hum Neurosci (2012) 6:58. doi:10.3389/fnhum.2012.00058
131. Tass PA, Popovych OV. Unlearning tinnitus-related cerebral synchrony with acoustic coordinated reset stimulation - theoretical concept and modelling. Biol Cybern (2012) 106:27-36. doi:10.1007/s00422-012-0479-5
132. Tass PA, Adamchic I, Freund H-J, von Stackelberg T, Hauptmann C. Counteracting tinnitus by acoustic coordinated reset neuromodulation. Restor Neurol Neurosci (2012) 30:137-59. doi:10.3233/RNN-2012-110218
133. Popovych OV, Yanchuk S, Tass PA. Self-organized noise resistance of oscillatory neural networks with spike timing-dependent plasticity. Sci Rep (2013) 3:2926. doi:10.1038/srep02926
134. Tass PA. Desynchronization of brain rhythms with soft phase-resetting techniques. Biol Cybern (2002) 87:102-15. doi:10.1007/s00422-002-0322-5
135. Chittka L, Brockmann A. Perception space - the final frontier. PLoS Biol (2005) 3(4):e137. doi:10.1371/journal.pbio.0030137
136. Pantev C, Wollbrink A, Roberts LE, Engelien A, Lütkenhöner B. Short-term plasticity of the human auditory cortex. Brain Res (1999) 842:192-9. doi:10.1016/S0006-8993(99)01835-1
137. Okamoto H, Stracke H, Stoll W, Pantev C. Listening to tailor-made music reverses maladaptive auditory cortex reorganization and alleviates tinnitus. Proc Natl Acad Sci U S A (2010) 107(3):1207-10. doi:10.1073/pnas.0911268107
138. Adamchic I, Langguth B, Hauptmann C, Tass PA. Abnormal brain activity and cross-frequency coupling in the tinnitus network. Front Neurosci (2014) 8:284. doi:10.3389/fnins.2014.00284
139. Goebel G, Hiller W. Tinnitus Fragebogen (TF): Ein Instrument zur Erfassung von Belastung und Schweregrad bei Tinnitus. Goettingen: Hogrefe (1993). 90 p.
140. Hallam R, Rachmann S, Hinchcliffe R. Psychological aspects of tinnitus. In: Rachmann S, editor. Contributions to Medical Psychology. (Vol. 3), Oxford: Pergamon Press (1984). p. 31-54.
141. Surr RK, Montgomery AA, Mueller HG. Effect of amplification on tinnitus among new hearing aid users. Ear Hear (1985) 6(2):71-5. doi:10.1097/00003446-198503000-00002
142. Roberts LE, Eggermont JJ, Caspary DM, Shore SE, Melcher JR, Kaltenbach JA. Ringing ears: the neuroscience of tinnitus. J Neurosci (2010) 30(45):14972-9. doi:10.1523/JNEUROSCI.4028-10.2010
143. Terry AM, Jones DM, Davis BR, Slater R. Parametric studies of tinnitus masking and residual inhibition. Br J Audiol (1983) 17:245-56. doi:10.3109/03005368309081485
144. Goebel G, Kahl M, Arnold W, Fichter M. 15-year prospective follow-up study of behavioral therapy in a large sample of inpatients with chronic tinnitus. Acta Otolaryngol Suppl (2006) 556:70-9. doi:10.1080/03655230600895267
145. Adamchic I, Langguth B, Hauptmann C, Tass PA. Psychometric evaluation of Visual Analog Scale for the assessment of chronic tinnitus. Am J Audiol (2012) 21:215-25. doi:10.1044/1059-0889(2012/12-0010)
146. Adamchic I, Tass PA, Langguth B, Hauptmann C, Koller M, Schecklmann M, et al. Linking the tinnitus questionnaire and the clinical global impression: which differences are clinically important? Health Qual Life Outcomes (2012) 10:79. doi:10.1186/1477-7525-10-79
147. Jacobson NS, Truax P. Clinical significance: a statistical approach to defining meaningful change in psychotherapy research. J Consult Clin Psychol (1991) 59:12-9. doi:10.1037/0022-006X.59.1.12
148. Silchenko AN, Adamchic I, Hauptmann C, Tass PA. Impact of acoustic coordinated reset neuromodulation on effective connectivity in a neural network of phantom sound. Neuroimage (2013) 77:133-47. doi:10.1016/j.neuroimage.2013.03.013
149. Adamchic I, Toth T, Hauptmann C, Tass PA. Reversing pathologically increased EEG power by acoustic CR neuromodulation. Hum Brain Mapp (2014) 35:2099-118. doi:10.1002/hbm.22314
150. Adamchic I, Hauptmann C, Tass PA. Changes of oscillatory activity in pitch processing network and related tinnitus relief induced by acoustic CR neuromodulation. Front Syst Neurosci (2012) 6:18. doi:10.3389/fnsys.2012.00018
151. Nichols TE, Holmes AP. Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum Brain Mapp (2002) 15:1-25. doi:10.1002/hbm.1058
152. Pascual-Marqui RD. Standardized low resolution brain electromagnetic tomography (sLORETA): technical details. Methods Find Exp Clin Pharmacol (2002) 24(Suppl D):5-12.
153. Silchenko AN, Adamchic I, Pawelczyk N, Hauptmann C, Maarouf M, Sturm V, et al. Data-driven approach to the estimation of connectivity and time delays in the coupling of interacting neuronal subsystems. J Neurosci Methods (2010) 191:32-44. doi:10.1016/j.jneumeth.2010.06.004
154. Moran RJ, Stephan KE, Seidenbecher T, Pape H-C, Dolan RJ, Friston KJ. Dynamic causal models of steady-state responses. Neuroimage (2009) 44:796-811. doi:10.1016/j.neuroimage.2008.09.048
155. Popovych OV, Tass PA. Macroscopic entrainment of periodically forced oscillatory ensembles. Prog Biophys Mol Biol (2011) 105:98-108. doi:10.1016/j.pbiomolbio.2010.09.018
156. Franosch J-MP, Kempter R, Fastl H, van Hemmen JL. Zwicker tone illusion and noise reduction in the auditory system. Phys Rev Lett (2003) 90:17810. doi:10.1103/PhysRevLett.90.178103
157. Benoit O, Daurat A, Prado J. Slow (0.7-2 Hz) and fast (2-4 Hz) delta components are differently correlated to theta, alpha and beta frequency bands during NREM sleep. Clin Neurophysiol (2000) 111:2103-6. doi:10.1016/S1388-2457(00)00470-3
158. Boyen K, de Kleine E, van Dijk P, Langers DRM. Tinnitus-related dissociation between cortical and subcortical neural activity in humans with mild to moderate sensorineural hearing loss. Hear Res (2014) 312:48-59. doi:10.1016/j.heares.2014.03.001
159. Gu JW, Herrmann BS, Levine RA, Melcher JR. Brainstem auditory evoked potentials suggest a role for the ventral cochlear nucleus in tinnitus. J Assoc Res Otolaryngol (2012) 13:819-33. doi:10.1007/s10162-012-0344-1
160. Dohrmann K, Elbert T, Schlee W, Weisz N. Tuning the tinnitus percept by modification of synchronous brain activity. Restor Neurol Neurosci (2007) 25:371-8.
161. Popovych OV, Tass PA. Control of abnormal synchronization in neurological disorders. Front Neurol (2014) 5:268. doi:10.3389/fneur.2014.00268
162. Rubin JE, Terman D. High frequency stimulation of the subthalamic nucleus eliminates pathological thalamic rhythmicity in a computational model. J Comput Neurosci (2004) 16:211-35. doi:10.1023/B:JCNS.0000025686.47117.67
163. Terman D, Rubin J, Yew A, Wilson C. Activity patterns in a model for the subthalamopallidal network of the basal ganglia. J Neurosci (2002) 22:2963-76.
164. Ebert MC, Hauptmann PA, Tass P. Coordinated reset stimulation in a large-scale model of the STN-GPe circuit. Front Comput Neurosci (2014) 8:154. doi:10.3389/fncom.2014.00154
165. Schaette R, Kempter R. Development of hyperactivity after hearing loss in a computational model of the dorsal cochlear nucleus depends on neuron response type. Hear Res (2008) 240:57-72. doi:10.1016/j.heares.2008.02.006
166. Dominguez M, Becker S, Bruce I, Read H. A spiking neuron model of cortical correlates of sensorineural hearing loss: spontaneous firing, synchrony, and tinnitus. Neural Comput (2006) 18:2942-58. doi:10.1162/neco.2006.18.12.2942
167. Chrostowski M, Yang L, Wilson HR, Bruce IC, Becker S. Can homeostatic plasticity in deafferented primary auditory cortex lead to travelling waves of excitation? J Comput Neurosci (2011) 30:279-99. doi:10.1007/s10827-010-0256-1
168. Kaltenbach JA, Godfrey DA, Neumann JB, McCaslin DL, Afman CE, Zhang J. Changes in spontaneous neural activity in the dorsal cochlear nucleus following exposure to intense sound: relation to threshold shift. Hear Res (1998) 124:78-84. doi:10.1016/S0378-5955(98)00119-1
169. Milner PM. Note on a possible correspondence between the scotomas of migraine and spreading depression of leao. Electroencephalogr Clin Neurophysiol (1958) 10:705. doi:10.1016/0013-4694(58)90073-7
170. Houweling A, Bazhenov M, Timofeev I, Steriade M, Sejnowski T. Homeostatic synaptic plasticity can explain post-traumatic epileptogenesis in chronically isolated neocortex. Cereb Cortex (2005) 15:834-45. doi:10.1093/cercor/bhh184
171. Charles A, Brennan K. Cortical spreading depression - new insights and persistent questions. Cephalalgia (2009) 29(10):1115-24. doi:10.1111/j.1468-2982.2009.01983.x
172. Dahlem MA, Hadjikhani N. Migraine aura: retracting particle-like waves in weakly susceptible cortex. PLoS One (2009) 4:e5007. doi:10.1371/journal.pone.0005007
173. Dahlem MA, Isele TM. Transient localized wave patterns and their application to migraine. J Math Neurosci (2013) 3:7. doi:10.1186/2190-8567-3-7
174. Ermentrout GB, Cowan J. A mathematical theory of visual hallucination patterns. Biol Cybern (1979) 34:137-50. doi:10.1007/BF00336965
175. Tass P. Cortical pattern formation during visual hallucinations. J Biol Phys (1995) 21:177-210. doi:10.1007/BF00712345
176. Tass P. Oscillatory cortical activity during visual hallucinations. J Biol Phys (1997) 23:21-66. doi:10.1023/A:1004990707739
177. Hauptmann C, Ströbel A, Mark Williams W, Patel N, Wurzer H, von Stackelberg T, et al. Acoustic coordinated reset neuromodulation in a real life patient population with chronic tonal tinnitus. Biomed Res Int (2015).
178. Tyler RS, Conrad-Armes D. Tinnitus pitch: a comparison of three measurement methods. Br J Audiol (1983) 17:101-7. doi:10.3109/03005368309078916
179. Burns EM. A comparison of variability among measurements of subjective tinnitus and objective stimuli. Audiology (1984) 23:426-40. doi:10.3109/00206098409081535
180. Henry JA, Flick CL, Gilbert A, Ellingson RM, Fausti SA. Comparison of manual and computer-automated procedures for tinnitus pitch-matching. J Rehabil Res Dev (2004) 41:121-38. doi:10.1682/JRRD.2004.02.0121
181. McMillan GP, Thielman EJ, Wypych K, Henry JA. A Bayesian perspective on tinnitus pitch matching. Ear Hear (2014) 35(6):687-94. doi:10.1097/AUD.0000000000000081
182. Ebbinghaus H. Memory: A Contribution to Experimental Psychology. Educational Reprints. (Vol. 3). New York, NY: Teachers College, Columbia University (1913).
183. Popovych OV, Yanchuk S, Tass PA. The spacing principle for unlearning abnormal neuronal synchrony. PLoS One (2015).