The auditory and non-auditory brain areas involved in tinnitus. An emergent property of multiple parallel overlapping subnetworks

Frontiers in Systems Neuroscience

Volumn , Issue MAY 2012, 2012, Pages

  Vanneste, Sven ^a   De Ridder, Dirk ^a  

^a ANTWERP UNIVERSITY HOSPITAL   (Belgium)

Author keywords

EEG; Emergent property; Multiple parallel overlapping subnetworks; Non auditory brain areas

Indexed keywords

ANTERIOR CINGULATE; ARTICLE; AUDITORY CORTEX; AUDITORY LATERALIZATION; AUDITORY NERVOUS SYSTEM; DISEASE CLASSIFICATION; DORSAL ANTERIOR CINGULATE CORTEX; ELECTROENCEPHALOGRAM; HEARING; HUMAN; INFERIOR FRONTAL GYRUS; INSULA; LOUDNESS; NERVE CELL NETWORK; ORBITAL CORTEX; PARAHIPPOCAMPAL GYRUS; PATHOPHYSIOLOGY; POSTERIOR CINGULATE; PRECUNEUS; PREFRONTAL CORTEX; SUBGENUAL ANTERIOR CINGULATE CORTEX; SUPPLEMENTARY MOTOR AREA; TINNITUS;

EID: 84864989349     PISSN: 16625137     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnsys.2012.00031     Document Type: Article

References (110)

1. Alain, C., Woods, D. L., and Knight, R. T. (1998). A distributed cortical network for auditory sensory memory in humans. Brain Res. 812, 23-37.
2. Alpini, D., and Cesarani, A. (2006). Tinnitus as an alarm bell: stress reaction tinnitus model. ORL J. Otorhinolaryngol. Relat. Spec. 68, 31-36. discussion 36-37.
3. Andersson, G., and Westin, V. (2008). Understanding tinnitus distress: introducing the concepts of moderators and mediators. Int. J. Audiol. (Suppl. 2), S106-S111.
4. Angrilli, A., Bianchin, M., Radaelli, S., Bertagnoni, G., and Pertile, M. (2008). Reduced startle reflex and aversive noise perception in patients with orbitofrontal cortex lesions. Neuropsychologia 46, 1179-1184.
5. Asada, H., Fukuda, Y., Tsunoda, S., Yamaguchi, M., and Tonoike, M. (1999). Frontal midline theta rhythms reflect alternative activation of prefrontal cortex and anterior cingulate cortex in humans. Neurosci. Lett. 274, 29-32.
6. Axelsson, A., and Ringdahl, A. (1989). Tinnitus-a study of its prevalence and characteristics. Br. J. Audiol. 23, 53-62.
7. Beauregard, M. (2007). Mind does really matter: evidence from neuroimaging studies of emotional self-regulation, psychotherapy, and placebo effect. Prog. Neurobiol. 81, 218-236.
8. Behrens, T. E., Woolrich, M. W., Walton, M. E., and Rushworth, M. F. (2007). Learning the value of information in an uncertain world. Nat. Neurosci. 10, 1214-1221.
9. Bickford, P. C., Luntz-Leybman, V., and Freedman, R. (1993). Auditory sensory gating in the rat hippocampus: modulation by brainstem activity. Brain Res. 607, 33-38.
10. Blood, A. J., Zatorre, R. J., Bermudez, P., and Evans, A. C. (1999). Emotional responses to pleasant and unpleasant music correlate with activity in paralimbic brain regions. Nat. Neurosci. 2, 382-387.
11. Bodner, M., Kroger, J., and Fuster, J. M. (1996). Auditory memory cells in dorsolateral prefrontal cortex. Neuroreport 7, 1905-1908.
12. Boly, M., Faymonville, M. E., Peigneux, P., Lambermont, B., Damas, P., Del Fiore, G., Degueldre, C., Franck, G., Luxen, A., Lamy, M., Moonen, G., Maquet, P., and Laureys, S. (2004). Auditory processing in severely brain injured patients: differences between the minimally conscious state and the persistent vegetative state. Arch. Neurol. 61, 233-238.
13. Boly, M., Faymonville, M. E., Peigneux, P., Lambermont, B., Damas, F., Luxen, A., Lamy, M., Moonen, G., Maquet, P., and Laureys, S. (2005). Cerebral processing of auditory and noxious stimuli in severely brain injured patients: differences between VS and MCS. Neuropsychol. Rehabil. 15, 283-289.
14. Boutros, N. N., Mears, R., Pflieger, M. E., Moxon, K. A., Ludowig, E., and Rosburg, T. (2008). Sensory gating in the human hippocampal and rhinal regions: regional differences. Hippocampus 18, 310-316.
15. Bradley, M. M., Codispoti, M., Sabatinelli, D., and Lang, P. J. (2001). Emotion and motivation II: sex differences in picture processing. Emotion 1, 300-319.
16. Brozoski, T. J., Bauer, C. A., and Caspary, D. M. (2002). Elevated fusiform cell activity in the dorsal cochlear nucleus of chinchillas with psychophysical evidence of tinnitus. J. Neurosci. 22, 2383-2390.
17. Buckner, R. L., Raichle, M. E., Miezin, F. M., and Petersen, S. E. (1996). Functional anatomic studies of memory retrieval for auditory words and visual pictures. J. Neurosci. 16, 6219-6235.
18. Craig, A. D. (2002). How do you feel? Interoception: the sense of the physiological condition of the body. Nat. Rev. Neurosci. 3, 655-666.
19. Craig, A. D. (2003). Interoception: the sense of the physiological condition of the body. Curr. Opin. Neurobiol. 13, 500-505.
20. Critchley, H. D. (2005). Neural mechanisms of autonomic, affective, and cognitive integration. J. Comp. Neurol. 493, 154-166.
21. Critchley, H. D., Corfield, D. R., Chandler, M. P., Mathias, C. J., and Dolan, R. J. (2000). Cerebral correlates of autonomic cardiovascular arousal: a functional neuroimaging investigation in humans. J. Physiol. 523(Pt 1), 259-270.
22. Critchley, H. D., Mathias, C. J., and Dolan, R. J. (2001). Neural activity in the human brain relating to uncertainty and arousal during anticipation. Neuron 29, 537-545.
23. Critchley, H. D., Wiens, S., Rotshtein, P., Ohman, A., and Dolan, R. J. (2004). Neural systems supporting interoceptive awareness. Nat. Neurosci. 7, 189-195.
24. Crone, N. E., Boatman, D., Gordon, B., and Hao, L. (2001). Induced electrocorticographic gamma activity during auditory perception. Brazier Award-winning article, 2001. Clin. Neurophysiol. 112, 565-582.
25. Damasio, A. R. (1996). The somatic marker hypothesis and the possible functions of the prefrontal cortex. Philos. Trans. R. Soc. Lond. B Biol. Sci. 351, 1413-1420.
26. Dehaene, S., Changeux, J. P., Naccache, L., Sackur, J., and Sergent, C. (2006). Conscious, preconscious, and subliminal processing: a testable taxonomy. Trends Cogn. Sci. 10, 204-211.
27. de Lafuente, V., and Romo, R. (2005). Neuronal correlates of subjective sensory experience. Nat. Neurosci. 8, 1698-1703.
28. De Ridder, D., de Mulder, G., Verstraeten, E., Seidman, M., Elisevich, K., Sunaert, S., Kovacs, S., K. van der Kelen, van de Heyning, P., and Moller, A. (2007a). Auditory cortex stimulation for tinnitus. Acta Neurochir. Suppl. 97, 451-462.
29. De Ridder, D., de Mulder, G., Menovsky, T., Sunaert, S., and Kovacs, S. (2007b). Electrical stimulation of auditory and somatosensory cortices for treatment of tinnitus and pain. Prog. Brain Res. 166, 377-388.
30. De Ridder, D., de Mulder, G., Verstraeten, E., van der Kelen, K., Sunaert, S., Smits, M., Kovacs, S., Verlooy, J., van de Heyning, P., and Moller, A. R. (2006a). Primary and secondary auditory cortex stimulation for intractable tinnitus. ORL J. Otorhinolaryngol. Relat. Spec. 68, 48-54. discussion 54-55.
31. De Ridder, D., Fransen, H., Francois, O., Sunaert, S., Kovacs, S., and van de Heyning, P. (2006b). Amygdalohippocampal involvement in tinnitus and auditory memory. Acta Otolaryngol. Suppl. 556, 50-53.
32. De Ridder, D., Elgoyhen, A. B., Romo, R., and Langguth, B. (2011a). Phantom percepts: tinnitus and pain as persisting aversive memory networks. Proc. Natl. Acad. Sci. U.S.A. 108, 8075-8080.
33. De Ridder, D., Vanneste, S., and Congedo, M. (2011b). The distressed brain: a group blind source separation analysis on tinnitus. PLoS One 6:e24273. doi: 10.1371/journal.pone.0024273
34. Dias, R., Robbins, T. W., and Roberts, A. C. (1996). Dissociation in prefrontal cortex of affective and attentional shifts. Nature 380, 69-72.
35. Dineen, R., Doyle, J., and Bench, J. (1997). Audiological and psychological characteristics of a group of tinnitus sufferers, prior to tinnitus management training. Br. J. Audiol. 31, 27-38.
36. Eggermont, J. J. (2005). Tinnitus: neurobiological substrates. Drug Discov. Today 10, 1283-1290.
37. Eggermont, J. J., and Roberts, L. E. (2004). The neuroscience of tinnitus. Trends Neurosci. 27, 676-682.
38. Engineer, N. D., Riley, J. R., Seale, J. D., Vrana, W. A., Shetake, J. A., Sudanagunta, S. P., Borland, M. S., and Kilgard, M. P. (2011). Reversing pathological neural activity using targeted plasticity. Nature 470, 101-104.
39. Frysztak, R. J., and Neafsey, E. J. (1994). The effect of medial frontal cortex lesions on cardio- vascular conditioned emotional responses in the rat. Brain Res. 643, 181-193.
40. Gard, M. G., and Kring, A. M. (2007). Sex differences in the time course of emotion. Emotion 7, 429-437.
41. Gray, J. R., Braver, T. S., and Raichle, M. E. (2002). Integration of emotion and cognition in the lateral prefrontal cortex. Proc. Natl. Acad. Sci. U.S.A. 99, 4115-4120.
42. Guitton, M. J., Caston, J., Ruel, J., Johnson, R. M., Pujol, R., and Puel, J. L. (2003). Salicylate induces tinnitus through activation of cochlear NMDA receptors. J. Neurosci. 23, 3944-3952.
43. Gusnard, D. A., Akbudak, E., Shulman, G. L., and Raichle, M. E. (2001). Medial prefrontal cortex and selfreferential mental activity: relation to a default mode of brain function. Proc. Natl. Acad. Sci. U.S.A. 98, 4259-4264
44. Hallam, R. S. (1996). Correlates of sleep disturbance in chronic distressing tinnitus. Scand. Audiol. 25, 263-266.
45. Heller, A. J. (2003). Classification and epidemiology of tinnitus. Otolaryngol. Clin. North Am. 36, 239-248.
46. Inanaga, K. (1998). Frontal midline theta rhythm and mental activity. Psychiatry Clin. Neurosci. 52, 555-566.
47. Jancke, L., Shah, N. J., Posse, S., Grosse-Ryuken, M., and Muller-Gartner, H. W. (1998). Intensity coding of auditory stimuli: an fMRI study. Neuropsychologia 36, 875-883.
48. Jastreboff, P. J. (1990). Phantom auditory perception (tinnitus): mechanisms of generation and perception. Neurosci. Res. 8, 221-254.
49. Jastreboff, P. J., and Sasaki, C. T. (1986). Salicylate-induced changes in spontaneous activity of single units in the inferior colliculus of the guinea pig. J. Acoust. Soc. Am. 80, 1384-1391.
50. Joliot, M., Ribary, U., and Llinas, R. (1994). Human oscillatory brain activity near 40 Hz coexists with cognitive temporal binding. Proc. Natl. Acad. Sci. U.S.A. 91, 11748-11751.
51. Kennerley, S. W., Walton, M. E., Behrens, T. E., Buckley, M. J., and Rushworth, M. F. (2006). Optimal decision making and the anterior cingulate cortex. Nat. Neurosci. 9, 940-947.
52. Knight, R. T., Scabini, D., and Woods, D. L. (1989). Prefrontal cortex gating of auditory transmission in humans. Brain Res. 504, 338-342.
53. Koch, K., Pauly, K., Kellermann, T., Seiferth, N. Y., Reske, M., Backes, V., Stocker, T., Shah, N. J., Amunts, K., Kircher, T., Schneider, F., and Habel, U. (2007). Gender differences in the cognitive control of emotion: an fMRI study. Neuropsychologia 45, 2744-2754.
54. Kreyberg, S., Torvik, A., Bjorneboe, A., Wiik-Larsen, W., and Jacobsen, D. (1992). Trimethyltin poisoning: report of a case with postmortem examination. Clin. Neuropathol. 11, 256-259.
55. Kubota, Y., Sato, W., Toichi, M., Murai, T., Okada, T., Hayashi, A., and Sengoku, A. (2001). Frontal midline theta rhythm is correlated with cardiac autonomic activities during the performance of an attention demanding meditation procedure. Brain Res. Cogn. Brain Res. 11, 281-287.
56. Laureys, S. (2005). The neural correlate of (un)awareness: lessons from the vegetative state. Trends Cogn. Sci. 9, 556-559.
57. Laureys, S., Faymonville, M. E., Degueldre, C., Fiore, G. D., Damas, P., Lambermont, B., Janssens, N., Aerts, J., Franck, G., Luxen, A., Moonen, G., Lamy, M., and Maquet, P. (2000). Auditory processing in the vegetative state. Brain 123(Pt 8), 1589-1601.
58. Laureys, S., Faymonville, M. E., Peigneux, P., Damas, P., Lambermont, B., Del Fiore, G., Degueldre, C., Aerts, J., Luxen, A., Franck, G., Lamy, M., Moonen, G., and Maquet, P. (2002). Cortical processing of noxious somatosensory stimuli in the persistent vegetative state. Neuroimage 17, 732-741.
59. Le, T. H., Pardo, J. V., and Hu, X. (1998). 4 T-fMRI study of nonspatial shifting of selective attention: cerebellar and parietal contributions. J. Neurophysiol. 79, 1535-1548.
60. Lewis, J. W., Beauchamp, M. S., and deYoe, E. A. (2000). A comparison of visual and auditory motion processing in human cerebral cortex. Cereb. Cortex 10, 873-888.
61. Llinás, R., Urbano, F. J., Leznik, E., Ramirez, R. R., and van Marle, H. J. (2005). Rhythmic and dysrhythmic thalamocortical dynamics: GABA systems and the edge effect. Trends Neurosci. 28, 325-333.
62. Llinas, R., Ribary, U., Contreras, D., and Pedroarena, C. (1998). The neuronal basis for consciousness. Philos. Trans. R. Soc. Lond. B Biol. Sci. 353, 1841-1849.
63. Llinas, R., Ribary, U., Joliot, M., and Wang, X. (1994). "Content and context in temporal thalamocortical binding," in Temporal Coding in the Brain, eds G. Buzsaki, R. Llinasand, and W. Singer (Berlin: Springer-Verlag), 251-272.
64. Llinás, R. R., Ribary, U., Jeanmonod, D., Kronberg, E., and Mitra, P. P. (1999). Thalamocortical dysrhythmia: a neurological and neuropsychiatric syndrome characterized by magnetoencephalography. Proc. Natl. Acad. Sci. U.S.A. 96, 15222-15227.
65. Lockwood, A. H., Salvi, R. J., and Burkard, R. F. (2002). Tinnitus. N. Engl. J. Med. 347, 904-910.
66. Lorenz, I., Muller, N., Schlee, W., Hartmann, T., and Weisz, N. (2009). Loss of alpha power is related to increased gamma synchronization-A marker of reduced inhibition in tinnitus? Neurosci. Lett. 453, 225-228.
67. Masten, C. L., Eisenberger, N. I., Borofsky, L. A., Pfeifer, J. H., McNealy, K., Mazziotta, J. C., and Dapretto, M. (2009). Neural correlates of social exclusion during adolescence: understanding the distress of peer rejection. Soc. Cogn. Affect. Neurosci. 4, 143-157.
68. McKiernan, K. A., D'Angelo, B. R., Kaufman, J. N., and Binder, J. R. (2006). Interrupting the "stream of consciousness": an fMRI investigation. Neuroimage 29, 1185-1191.
69. Medford, N., and Critchley, H. D. (2010). Conjoint activity of anterior insular and anterior cingulate cortex: awareness and response. Brain Struct. Funct. 214, 535-549.
70. Menon, V., and Uddin, L. Q. (2010). Saliency, switching, attention and control: a network model of insula function. Brain Struct. Funct. 214, 655-667.
71. Melloni, L., Molina, C., Pena, M., Torres, D., Singer, W., and Rodriguez, E. (2007). Synchronization of neural activity across cortical areas correlates with conscious perception. J. Neurosci. 27, 2858-2865.
72. Mitchell, T. V., Morey, R. A., Inan, S., and Belger, A. (2005). Functional magnetic resonance imaging measure of automatic and controlled auditory processing. Neuroreport 16, 457-461.
73. Muhlau, M., Rauschecker, J. P., Oestreicher, E., Gaser, C., Rottinger, M., Wohlschlager, A. M., Simon, F., Etgen, T., Conrad, B., and Sander, D. (2006). Structural brain changes in tinnitus. Cereb. Cortex 16, 1283-1288.
74. 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.
75. Nicolas-Puel, C., Faulconbridge, R. L., Guitton, M., Puel, J. L., Mondain, M., and Uziel, A. (2002). Characteristics of tinnitus and etiology of associated hearing loss: a study of 123 patients. Int. Tinnitus J. 8, 37-44.
76. Norena, A., Cransac, H., and Chery-Croze, S. (1999). Towards an objectification by classification of tinnitus. Clin. Neurophysiol. 110, 666-675.
77. Norena, A., Micheyl, C., Chery-Croze, S., and Collet, L. (2002). Psychoacoustic characterization of the tinnitus spectrum: implications for the underlying mechanisms of tinnitus. Audiol. Neurootol. 7, 358-369.
78. Norena, A. J. (2011). An integrative model of tinnitus based on a central gain controlling neural sensitivity. Neurosci. Biobehav. Rev. 35, 1089-1109.
79. Norena, A. J., and Eggermont, J. J. (2003). Changes in spontaneous neural activity immediately after an acoustic trauma: implications for neural correlates of tinnitus. Hear. Res. 183, 137-153.
80. Norena, A. J., and Eggermont, J. J. (2006). Enriched acoustic environment after noise trauma abolishes neural signs of tinnitus. Neuroreport 17, 559-563.
81. Ohira, H., Nomura, M., Ichikawa, N., Isowa, T., Iidaka, T., Sato, A., Fukuyama, S., Nakajima, T., and Yamada, J. (2006). Association of neural and physiological responses during voluntary emotion suppression. Neuroimage 29, 721-733.
82. Ongur, D., and Price, J. L. (2000). The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cereb. Cortex 10, 206-219.
83. Oppenheimer, S. (1993). The anatomy and physiology of cortical mechanisms of cardiac control. Stroke 24 (Suppl. 12), I3-I5.
84. Oppenheimer, S. M., Gelb, A., Girvin, J. P., and Hachinski, V. C. (1992). Cardiovascular effects of human insular cortex stimulation. Neurology 42, 1727-1732.
85. Phillips, M. L., Drevets, W. C., Rauch, S. L., and Lane, R. (2003). Neurobiology of emotion perception I: the neural basis of normal emotion perception. Biol. Psychiatry 54, 504-514.
86. Raichle, M. E., MacLeod, A. M., Snyder, A. Z., Powers, W. J., Gusnard, D. A., and Shulman, G. L. (2001). A default mode of brain function. Proc. Natl. Acad. Sci. U.S.A. 98, 676-682.
87. Rey, C., Reinecke, H. J., and Besser, R. (1984). Methyltin intoxication in six men; toxicologic and clinical aspects. Vet. Hum. Toxicol. 26, 121-122.
88. Ribary, U., Ioannides, A. A., Singh, K. D., Hasson, R., Bolton, J. P., Lado, F., Mogilner, A., and Llinas, R. (1991). Magnetic field tomography of coherent thalamocortical 40-Hz oscillations in humans. Proc. Natl. Acad. Sci. U.S.A. 88, 11037-11041.
89. Rutkowski, R. G., and Weinberger, N. M. (2005). Encoding of learned importance of sound by magnitude of representational area in primary auditory cortex. Proc. Natl. Acad. Sci. U.S.A. 102, 13664-13669.
90. Sadaghiani, S., Hesselmann, G., and Kleinschmidt, A. (2009). Distributed and antagonistic contributions of ongoing activity fluctuations to auditory stimulus detection. J. Neurosci. 29, 13410-13417.
91. Schlee, W., Weisz, N., Bertrand, O., Hartmann, T., and Elbert, T. (2008). Using auditory steady state responses to outline the functional connectivity in the tinnitus brain. PLoS One 3:e3720. doi: 10.1371/journal.pone.0003720
92. Schmitt, C., Patak, M., and KronerHerwig, B. (2000). Stress and the onset of sudden hearing loss and tinnitus. Int. Tinnitus J. 6, 41-49.
93. Seeley, W. W., Menon, V., Schatzberg, A. F., Keller, J., Glover, G. H., Kenna, H., Reiss, A. L., and Greicius, M. D. (2007). Dissociable intrinsic connectivity networks for salience processing and executive control. J. Neurosci. 27, 2349-2356.
94. Shargorodsky, J., Curhan, S. G., Curhan, G. C., and Eavey, R. (2010). Change in prevalence of hearing loss in US adolescents. JAMA 304, 772-778.
95. Shulman, A. (1995). A final common pathway for tinnitus - the medial temporal lobe system. Int. Tinnitus J. 1, 115-126.
96. Steriade, M. (2006). Grouping of brain rhythms in corticothalamic systems. Neuroscience 137, 1087-1106.
97. Tiitinen, H., Sinkkonen, J., Reinikainen, K., Alho, K., Lavikainen, J., and Naatanen, R. (1993). Selective attention enhances the auditory 40-Hz transient response in humans. Nature 364, 59-60.
98. van der Loo, E., Congedo, M., Vanneste, S., Van de Heyning, P., and De Ridder, D. (2011). Insular lateralization in tinnitus distress. Auton. Neurosci. 165, 191-194.
99. van der Loo, E., Gais, S., Congedo, M., Vanneste, S., Plazier, M., Menovsky, T., Van de Heyning, P., and De Ridder, D. (2009). Tinnitus intensity dependent gamma oscillations of the contralateral auditory cortex. PLoS One 4:e7396. doi: 10.1371/journal.pone.0007396
100. Vanneste, S., Plazier, M., van der Loo, E., Van de Heyning, P., and De Ridder, D. (2010a). The differences in brain activity between narrow band noise and pure tone tinnitus. PLoS One 5:e13618. doi: 10.1371/journal.pone.0013618
101. Vanneste, S., Plazier, M., der Loo, E., de Heyning, P. V., Congedo, M., and De Ridder, D. (2010b). The neural correlates of tinnitus- related distress. Neuroimage 52, 470-480.
102. Vanneste, S., Van de Heyning, P., and De Ridder, D. (2011a). Contralateral parahippocampal gamma-band activity determines noise-like tinnitus laterality: a region of interest analysis. Neuroscience 199, 481-490.
103. Vanneste, S., Van de Heyning, P., and De Ridder, D. (2011b). The neural network of phantom sound changes over time: a comparison between recent-onset and chronic tinnitus patients. Eur. J. Neurosci. 34, 718-731.
104. Vanneste, S., Plazier, M., van der Loo, E., Van de Heyning, P., and De Ridder, D. (2011c). The difference between uni-and bilateral auditory phantom percept. Clin. Neurophysiol. 122, 578-587.
105. Voisin, J., Bidet-Caulet, A., Bertrand, O., and Fonlupt, P. (2006). Listening in silence activates auditory areas: a functional magnetic resonance imaging study. J. Neurosci. 26, 273-278.
106. Wang, J., Rao, H., Wetmore, G. S., Furlan, P. M., Korczykowski, M., Dinges, D. F., and Detre, J. A. (2005). Perfusion functional MRI reveals cerebral blood flow pattern under psychological stress. Proc. Natl. Acad. Sci. U.S.A. 102, 17804-17809.
107. Weisz, N., Moratti, S., Meinzer, M., Dohrmann, K., and Elbert, T. (2005). Tinnitus perception and distress is related to abnormal spontaneous brain activity as measured by magnetoencephalography. PLoS Med. 2:e153. doi: 10.1371/journal.pmed.0020153
108. Wheeler, R. E., Davidson, R. J., and Tomarken, A. J. (1993). Frontal brain asymmetry and emotional reactivity: a biological substrate of affective style. Psychophysiology 30, 82-89.
109. Yoo, S. S., Lee, C. U., and Choi, B. G. (2001). Human brain mapping of auditory imagery: event-related functional MRI study. Neuroreport 12, 3045-3049.
110. Zald, D. H., and Pardo, J. V. (2002). The neural correlates of aversive auditory stimulation. Neuroimage 16(3 Pt 1), 746-753.