Journal of Advanced Medical Sciences and Applied Technologies

Journal of Advanced Medical Sciences and Applied Technologies

Theoretical Tinnitus Multimodality Framework: A Neurofunctional Model

Document Type : Hypothesis

Authors
Iman Ghodratitoostani 1
Alexandre C.B.Delbem 2
Mohammad Torabi-Nami 3
Bahador Makkiabadi 4
Hamid Jalilvand 5
Tanit Ganz Sanchez 6
1 Interunidades Bioengenharia (EESC/FMRP/IQSC), Universidade De São Paulo, São Carlos, SP, Brazil
2 USP-Institute of Mathematics and Computer Science, Universidade De São Paulo, São Carlos, SP,
3 Department of Neuroscience, School of Advanced Medical Sciences and Technologies, Shiraz University of Medical Sciences, Shiraz
4 Department of Medical Physics and Biomedical Engineering, School of Medicine, Tehran University of Medical Sciences, Tehran
5 Department of Audiology, School of Rehabilitation Sciences, Shahid Beheshti Medical Sciences University, Tehran
6 University of São Paulo, Medical School, São Paulo
10.18869/nrip.jamsat.2.1.181
Abstract
Our knowledge about subjective tinnitus physiopathology has improved in the last decades, while information to understand the main mechanisms that transform a neutral phantom sound to tinnitus distress appear to be inadequate. The current review presents evidence from several studies using neuroimaging, electrophysiology and brain lesion techniques aiming at hypothesizing a new realistic multimodality tinnitus framework which can better explain the structural and functional brain connectivity in different stages of tinnitus development. Further to the present work, a full review of the entire literature should be prompted to discuss evidence to more comprehensively investigate the relationship between structural and functional connectivity of tinnitus. Progresses in such framework will shed lights to the tinnitus neurofunctional model and further evidence-based treatment modalities. 
Keywords
Tinnitus
Neurofunctional model
Neuroimaging
Electrophysiology
Functional connectivity
Structural Connectivity
  1. Seydell-Greenwald A, Leaver AM, Turesky TK, Morgan S, Kim HJ, Rauschecker JP. Functional MRI evidence for a role of ventral prefrontal cortex in tinnitus. Brain research. 2012;1485:22-39.
  2. Seydell-Greenwald A, Raven EP, Leaver AM, Turesky TK, Rauschecker JP. Diffusion imaging of auditory and auditory-limbic connectivity in tinnitus: preliminary evidence and methodological challenges. Neural plasticity. 2014;2014:145943.
  3. Rauschecker JP, Leaver AM, Mühlau M. Tuning out the noise: limbic-auditory interactions in tinnitus. Neuron. 2010;66:819-26.
  4. Pinault D. The thalamic reticular nucleus: structure, function and concept. Brain research Brain research reviews. 2004;46(1):1-31.
  5. Weese GD, Phillips JM, Brown VJ. Attentional orienting is impaired by unilateral lesions of the thalamic reticular nucleus in the rat. The Journal of neuroscience : the official journal of the Society for Neuroscience. 1999;19(22):10135-9.
  6. Baldauf ZB. Dual chemoarchitectonic lamination of the visual sector of the thalamic reticular nucleus. Neuroscience. 2010;165(3):801-18.
  7. Zikopoulos B, Barbas H. Circuits formultisensory integration and attentional modulation through the prefrontal cortex and the thalamic reticular nucleus in primates. Reviews in the neurosciences. 2007;18(6):417-38.
  8. Shosaku A, Sumitomo I. Auditory neurons in the rat thalamic reticular nucleus. Experimental brain research Experimentelle Hirnforschung Experimentation cerebrale. 1983;49(3):432-42.
  9. Yu XJ, Xu XX, Chen X, He SG, He JF. Slow Recovery From Excitation of Thalamic Reticular Nucleus Neurons. Journal of neurophysiology. 2009;101(2):980-7.
  10. Kimura A, Imbe H, Donishi T, Tamai Y. Axonal projections of single auditory neurons in the thalamic reticular nucleus: implications for tonotopy-related gating function and cross-modal modulation. Eur J Neurosci. 2007;26(12):3524-35.
  11. Krause M, Hoffmann WE, Hajos M. Auditory sensory gating in hippocampus and reticular thalamic neurons in anesthetized rats. Biological psychiatry. 2003;53(3):244-53.
  12. Mayo JP. Intrathalamic mechanisms of visual attention. J Neurophysiol. 2009;101(3):1123-5.
  13. Zikopoulos B, Barbas H. Prefrontal projections to the thalamic reticular nucleus form a unique circuit for attentional mechanisms. The Journal of neuroscience : the official journal of the Society for Neuroscience. 2006;26(28):7348-61.
  14. Torres-Garcia ME, Solis O, Patricio A, Rodriguez-Moreno A, Camacho-Abrego I, Limon ID, et al. Dendritic morphology changes in neurons from the prefrontal cortex, hippocampus and nucleus accumbens in rats after lesion of the thalamic reticular nucleus. Neuroscience. 2012;223:429-38.
  15. Churchill L, Zahm DS, Kalivas PW. The mediodorsal nucleus of the thalamus in rats--I. forebrain gabaergic innervation. Neuroscience. 1996;70(1):93-102.
  16. Churchill L, Zahm DS, Duffy P, Kalivas PW. The mediodorsal nucleus of the thalamus in rats--II. Behavioral and neurochemical effects of GABA agonists. Neuroscience. 1996;70(1):103-12.
  17. Zahm DS, Williams E, Wohltmann C. Ventral striatopallidothalamic projection: IV. Relative involvements of neurochemically distinct subterritories in the ventral pallidum and adjacent parts of the rostroventral forebrain. The Journal of comparative neurology. 1996;364(2):340-62.
  18. O'Donnell P, Lavin A, Enquist LW, Grace AA, Card JP. Interconnected parallel circuits between rat nucleus accumbens and thalamus revealed by retrograde transynaptic transport of pseudorabies virus. The Journal of neuroscience : the official journal of the Society for Neuroscience. 1997;17(6):2143-67.
  19. Kimura A, Yokoi I, Imbe H, Donishi T, Kaneoke Y. Auditory thalamic reticular nucleus of the rat: anatomical nodes for modulation of auditory and cross-modal sensory processing in the loop connectivity between the cortex and thalamus. The Journal of comparative neurology. 2012;520(7):1457-80.
  20. Zikopoulos B, Barbas H. Pathways for emotions and attention converge on the thalamic reticular nucleus in primates. The Journal of neuroscience : the official journal of the Society for Neuroscience. 2012;32(15):5338-50.
  21. Barbas H, Zikopoulos B, Timbie C. Sensory pathways and emotional context for action in primate prefrontal cortex. Biological psychiatry. 2011;69(12):1133-9.
  22. Roberts LE, Eggermont JJ, Caspary DM, Shore SE, Melcher JR, Kaltenbach JA. Ringing ears: the neuroscience of tinnitus. The Journal of neuroscience : the official journal of the Society for Neuroscience. 2010;30(45):14972-9.
  23. Gu JW, Halpin CF, Nam EC, Levine RA, Melcher JR. Tinnitus, diminished sound-level tolerance, and elevated auditory activity in humans with clinically normal hearing sensitivity. J Neurophysiol. 2010;104(6):3361-70.
  24. Logothetis NK. What we can do and what we cannot do with fMRI. Nature. 2008;453(7197):869-78.
  25. Gusnard DA, Raichle ME. Searching for a baseline: functional imaging and the resting human brain. Nature reviews Neuroscience. 2001;2(10):685-94.
  26. Seydell-Greenwald A, Leaver AM, Turesky TK, Morgan S, Kim HJ, Rauschecker JP. Functional MRI evidence for a role of ventral prefrontal cortex in tinnitus. Brain research. 2012.
  27. Bar M. A cognitive neuroscience hypothesis of mood and depression. Trends in cognitive sciences. 2009;13(11):456-63.
  28. Blood AJ, Zatorre RJ, Bermudez P, Evans AC. Emotional responses to pleasant and unpleasant music correlate with activity in paralimbic brain regions. Nat Neurosci. 1999;2(4):382-7.
  29. Breiter HC, Aharon I, Kahneman D, Dale A, Shizgal P. Functional imaging of neural responses to expectancy and experience of monetary gains and losses. Neuron. 2001;30(2):619-39.
  30. Kable JW, Glimcher PW. The neurobiology of decision: consensus and controversy. Neuron. 2009;63(6):733-45.
  31. Ressler KJ, Mayberg HS. Targeting abnormal neural circuits in mood and anxiety disorders: from the laboratory to the clinic. Nat Neurosci. 2007;10(9):1116-24.
  32. Sotres-Bayon F, Quirk GJ. Prefrontal control of fear: more than just extinction. Current opinion in neurobiology. 2010;20(2):231-5.
  33. Langguth B. A review of tinnitus symptoms beyond 'ringing in the ears': a call to action. Current medical research and opinion. 2011;27(8):1635-43.
  34. Halford JB, Anderson SD. Tinnitus severity measured by a subjective scale, audiometry and clinical judgement. The Journal of laryngology and otology. 1991;105(2):89-93.
  35. Halford JB, Anderson SD. Anxiety and depression in tinnitus sufferers. Journal of psychosomatic research. 1991;35(4-5):383-90.
  36. Robinson S. Antidepressants for treatment of tinnitus. Prog Brain Res. 2007;166:263-71.
  37. Muhlau M, Rauschecker JP, Oestreicher E, Gaser C, Rottinger M, Wohlschlager AM, et al. Structural brain changes in tinnitus. Cereb Cortex. 2006;16(9):1283-8.
  38. Langguth B, Kleinjung T, Landgrebe M. Tinnitus: the complexity of standardization. Evaluation & the health professions. 2011;34(4):429-33.
  39. Moller AR. Pathophysiology of tinnitus. Otolaryngol Clin North Am. 2003;36(2):249-66, v-vi.
  40. Moller AR. Neural plasticity in tinnitus. Prog Brain Res. 2006;157:365-72.
  41. Mahlke C, Wallhausser-Franke E. Evidence for tinnitus-related plasticity in the auditory and limbic system, demonstrated by arg3.1 and c-fos immunocytochemistry. Hear Res. 2004;195(1-2):17-34.
  42. Landgrebe M, Langguth B, Rosengarth K, Braun S, Koch A, Kleinjung T, et al. Structural brain changes in tinnitus: grey matter decrease in auditory and non-auditory brain areas. NeuroImage. 2009;46(1):213-8.
  43. Lanting CP, de Kleine E, van Dijk P. Neural activity underlying tinnitus generation: results from PET and fMRI. Hear Res. 2009;255(1-2):1-13.
  44. Kaltenbach JA, Godfrey DA. Dorsal cochlear nucleus hyperactivity and tinnitus: are they related? American journal of audiology. 2008;17(2):S148-61.
  45. Shulman A. A Final Common Pathway for Tinnitus - The Medial Temporal Lobe System. Int Tinnitus J. 1995;1(2):115-26.
  46. De Ridder D, Vanneste S, Congedo M. The distressed brain: a group blind source separation analysis on tinnitus. PloS one. 2011;6(10):e24273.
  47. Rauschecker JP, Leaver AM, Muhlau M. Tuning out the noise: limbic-auditory interactions in tinnitus. Neuron. 2010;66(6):819-26.
  48. Divac I, Mogensen J, Marinkovic S, Martensson R. On the projections from the neostriatum to the cerebral cortex: the "displaced" neurons. Neuroscience. 1987;21(1):197-205.
  49. Ferry AT, Ongur D, An X, Price JL. Prefrontal cortical projections to the striatum in macaque monkeys: evidence for an organization related to prefrontal networks. The Journal of comparative neurology. 2000;425(3):447-70.
  50. Jayaraman A. Anatomical evidence for cortical projections from the striatum in the cat. Brain research. 1980;195(1):29-36.
  51. Schlee W, Mueller N, Hartmann T, Keil J, Lorenz I, Weisz N. Mapping cortical hubs in tinnitus. BMC biology. 2009;7:80.
  52. LeDoux J. The amygdala. Current biology : CB. 2007;17(20):R868-74.
  53. Sah P, Lopez De Armentia M. Excitatory synaptic transmission in the lateral and central amygdala. Annals of the New York Academy of Sciences. 2003;985:67-77.
  54. Kraus KS, Canlon B. Neuronal connectivity and interactions between the auditory and limbic systems. Effects of noise and tinnitus. Hear Res. 2012;288(1-2):34-46.
  55. Rasia-Filho AA, Londero RG, Achaval M. Functional activities of the amygdala: an overview. Journal of psychiatry & neuroscience : JPN. 2000;25(1):14-23.
  56. Phelps EA, LeDoux JE. Contributions of the amygdala to emotion processing: from animal models to human behavior. Neuron. 2005;48(2):175-87.
  57. Davis M, Whalen PJ. The amygdala: vigilance and emotion. Molecular psychiatry. 2001;6(1):13-34.
  58. Baxter MG, Murray EA. The amygdala and reward. Nature reviews Neuroscience. 2002;3(7):563-73.
  59. Sander D, Grafman J, Zalla T. The human amygdala: an evolved system for relevance detection. Reviews in the neurosciences. 2003;14(4):303-16.
  60. Zald DH. The human amygdala and the emotional evaluation of sensory stimuli. Brain research Brain research reviews. 2003;41(1):88-123.
  61. Pessoa L. Reprint of: Emotion and cognition and the amygdala: from "what is it?" to "what's to be done?". Neuropsychologia. 2011;49(4):681-94.
  62. Compton RJ. The interface between emotion and attention: a review of evidence from psychology and neuroscience. Behavioral and cognitive neuroscience reviews. 2003;2(2):115-29.
  63. Compton RJ, Banich MT, Mohanty A, Milham MP, Herrington J, Miller GA, et al. Paying attention to emotion: an fMRI investigation of cognitive and emotional stroop tasks. Cognitive, affective & behavioral neuroscience. 2003;3(2):81-96.
  64. Murray EA, Wise SP. What, if anything, can monkeys tell us about human amnesia when they can't say anything at all? Neuropsychologia. 2010;48(8):2385-405.
  65. Murray EA. The amygdala, reward and emotion. Trends in cognitive sciences. 2007;11(11):489-97.
  66. Bechara A, Damasio H, Damasio AR. Role of the amygdala in decision-making. Annals of the New York Academy of Sciences. 2003;985:356-69.
  67. Balleine BW, Killcross S. Parallel incentive processing: an integrated view of amygdala function. Trends Neurosci. 2006;29(5):272-9.
  68. Pessoa L. Emotion and cognition and the amygdala: from "what is it?" to "what's to be done?". Neuropsychologia. 2010;48(12):3416-29.
  69. Salzman CD, Fusi S. Emotion, cognition, and mental state representation in amygdala and prefrontal cortex. Annual review of neuroscience. 2010;33:173-202.
  70. Maren S. What the amygdala does and doesn't do in aversive learning. Learn Mem. 2003;10(5):306-8.
  71. Maren S. Synaptic mechanisms of associative memory in the amygdala. Neuron. 2005;47(6):783-6.
  72. Weinberger NM. The medial geniculate, not the amygdala, as the root of auditory fear conditioning. Hear Res. 2011;274(1-2):61-74.
  73. Armony JL, Quirk GJ, LeDoux JE. Differential effects of amygdala lesions on early and late plastic components of auditory cortex spike trains during fear conditioning. The Journal of neuroscience : the official journal of the Society for Neuroscience. 1998;18(7):2592-601.
  74. Pedemonte M, Pena JL, Velluti RA. Firing of inferior colliculus auditory neurons is phase-locked to the hippocampus theta rhythm during paradoxical sleep and waking. Experimental brain research Experimentelle Hirnforschung Experimentation cerebrale. 1996;112(1):41-6.
  75. Ising H, Kruppa B. Health effects caused by noise: evidence in the literature from the past 25 years. Noise & health. 2004;6(22):5-13.
  76. Czisch M, Wehrle R, Stiegler A, Peters H, Andrade K, Holsboer F, et al. Acoustic oddball during NREM sleep: a combined EEG/fMRI study. PloS one. 2009;4(8):e6749.
  77. Boso M, Politi P, Barale F, Enzo E. Neurophysiology and neurobiology of the musical experience. Functional neurology. 2006;21(4):187-91.
  78. Limb CJ. Structural and functional neural correlates of music perception. The anatomical record Part A, Discoveries in molecular, cellular, and evolutionary biology. 2006;288(4):435-46.
  79. Jentschke S, Koelsch S, Friederici AD. Investigating the relationship of music and language in children: influences of musical training and language impairment. Annals of the New York Academy of Sciences. 2005;1060:231-42.
  80. Morris JS, Friston KJ, Dolan RJ. Experience-dependent modulation of tonotopic neural responses in human auditory cortex. Proceedings Biological sciences / The Royal Society. 1998;265(1397):649-57.
  81. Hariri AR, Mattay VS, Tessitore A, Fera F, Weinberger DR. Neocortical modulation of the amygdala response to fearful stimuli. Biological psychiatry. 2003;53(6):494-501.
  82. Weinberger NM. Associative representational plasticity in the auditory cortex: a synthesis of two disciplines. Learn Mem. 2007;14(1-2):1-16.
  83. Froemke RC, Martins AR. Spectrotemporal dynamics of auditory cortical synaptic receptive field plasticity. Hear Res. 2011;279(1-2):149-61.
  84. He DF, Chen FJ, Zhou SC. GABA mediaties the inhibitory effect of lateral amygdaloid nucleus stimulation on the acoustic response of neurons in A I cortex: An in vivo microiontophoretic study. Sheng li xue bao : [Acta physiologica Sinica]. 2004;56(3):374-8.
  85. Marsh RA, Fuzessery ZM, Grose CD, Wenstrup JJ. Projection to the inferior colliculus from the basal nucleus of the amygdala. The Journal of neuroscience : the official journal of the Society for Neuroscience. 2002;22(23):10449-60.
  86. Mohedano-Moriano A, Pro-Sistiaga P, Arroyo-Jimenez MM, Artacho-Perula E, Insausti AM, Marcos P, et al. Topographical and laminar distribution of cortical input to the monkey entorhinal cortex. Journal of anatomy. 2007;211(2):250-60.
  87. Munoz-Lopez MM, Mohedano-Moriano A, Insausti R. Anatomical pathways for auditory memory in primates. Frontiers in neuroanatomy. 2010;4:129.
  88. O'Mara S. The subiculum: what it does, what it might do, and what neuroanatomy has yet to tell us. Journal of anatomy. 2005;207(3):271-82.
  89. Eichenbaum H. Hippocampus: cognitive processes and neural representations that underlie declarative memory. Neuron. 2004;44(1):109-20.
  90. DeVito LM, Eichenbaum H. Distinct contributions of the hippocampus and medial prefrontal cortex to the "what-where-when" components of episodic-like memory in mice. Behavioural brain research. 2010;215(2):318-25.
  91. Burgess N, Maguire EA, O'Keefe J. The human hippocampus and spatial and episodic memory. Neuron. 2002;35(4):625-41.
  92. Phelps EA. Human emotion and memory: interactions of the amygdala and hippocampal complex. Current opinion in neurobiology. 2004;14(2):198-202.
  93. Richter-Levin G. The amygdala, the hippocampus, and emotional modulation of memory. The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry. 2004;10(1):31-9.
  94. Abe K. Modulation of hippocampal long-term potentiation by the amygdala: a synaptic mechanism linking emotion and memory. Japanese journal of pharmacology. 2001;86(1):18-22.
  95. Richter-Levin G, Akirav I. Amygdala-hippocampus dynamic interaction in relation to memory. Molecular neurobiology. 2000;22(1-3):11-20.
  96. Watanabe T, Yagishita S, Kikyo H. Memory of music: roles of right hippocampus and left inferior frontal gyrus. NeuroImage. 2008;39(1):483-91.
  97. Mitterschiffthaler MT, Fu CH, Dalton JA, Andrew CM, Williams SC. A functional MRI study of happy and sad affective states induced by classical music. Human brain mapping. 2007;28(11):1150-62.
  98. Angelucci F, Fiore M, Ricci E, Padua L, Sabino A, Tonali PA. Investigating the neurobiology of music: brain-derived neurotrophic factor modulation in the hippocampus of young adult mice. Behavioural pharmacology. 2007;18(5-6):491-6.
  99. Warden MR, Selimbeyoglu A, Mirzabekov JJ, Lo M, Thompson KR, Kim SY, et al. A prefrontal cortex-brainstem neuronal projection that controls response to behavioural challenge. Nature. 2012;492(7429):428-32.
  100. Alvarez JA, Emory E. Executive function and the frontal lobes: a meta-analytic review. Neuropsychology review. 2006;16(1):17-42.
  101. Price JL. Prefrontal cortical networks related to visceral function and mood. Annals of the New York Academy of Sciences. 1999;877:383-96.
  102. Sesack SR, Pickel VM. Prefrontal cortical efferents in the rat synapse on unlabeled neuronal targets of catecholamine terminals in the nucleus accumbens septi and on dopamine neurons in the ventral tegmental area. The Journal of comparative neurology. 1992;320(2):145-60.
  103. Vertes RP. Interactions among the medial prefrontal cortex, hippocampus and midline thalamus in emotional and cognitive processing in the rat. Neuroscience. 2006;142(1):1-20.
  104. Jay TM, Witter MP. Distribution of hippocampal CA1 and subicular efferents in the prefrontal cortex of the rat studied by means of anterograde transport of Phaseolus vulgaris-leucoagglutinin. The Journal of comparative neurology. 1991;313(4):574-86.
  105. Lewis DA, Anderson SA. The functional architecture of the prefrontal cortex and schizophrenia. Psychological medicine. 1995;25(5):887-94.
  106. O'Donnell P, Grace AA. Synaptic interactions among excitatory afferents to nucleus accumbens neurons: hippocampal gating of prefrontal cortical input. The Journal of neuroscience : the official journal of the Society for Neuroscience. 1995;15(5 Pt 1):3622-39.
  107. Goto Y, O'Donnell P. Network synchrony in the nucleus accumbens in vivo. The Journal of neuroscience : the official journal of the Society for Neuroscience. 2001;21(12):4498-504.
  108. Silva-Gomez AB, Rojas D, Juarez I, Flores G. Decreased dendritic spine density on prefrontal cortical and hippocampal pyramidal neurons in postweaning social isolation rats. Brain research. 2003;983(1-2):128-36.
  109. Kolb B, Forgie M, Gibb R, Gorny G, Rowntree S. Age, experience and the changing brain. Neurosci Biobehav Rev. 1998;22(2):143-59.
  110. Leaver AM, Renier L, Chevillet MA, Morgan S, Kim HJ, Rauschecker JP. Dysregulation of limbic and auditory networks in tinnitus. Neuron. 2011;69(1):33-43.
  111. Leaver AM, Seydell-Greenwald A, Turesky TK, Morgan S, Kim HJ, Rauschecker JP. Cortico-limbic morphology separates tinnitus from tinnitus distress. Frontiers in systems neuroscience. 2012;6:21.
  112. Tomasi D, Caparelli EC, Chang L, Ernst T. fMRI-acoustic noise alters brain activation during working memory tasks. NeuroImage. 2005;27(2):377-86.
  113. Levesque J, Eugene F, Joanette Y, Paquette V, Mensour B, Beaudoin G, et al. Neural circuitry underlying voluntary suppression of sadness. Biological psychiatry. 2003;53(6):502-10.
  114. Brown P, Molliver ME. Dual serotonin (5-HT) projections to the nucleus accumbens core and shell: relation of the 5-HT transporter to amphetamine-induced neurotoxicity. The Journal of neuroscience : the official journal of the Society for Neuroscience. 2000;20(5):1952-63.
  115. McCormick DA, Wang Z. Serotonin and noradrenaline excite GABAergic neurones of the guinea-pig and cat nucleus reticularis thalami. The Journal of physiology. 1991;442:235-55.
  116. Pape HC, McCormick DA. Noradrenaline and serotonin selectively modulate thalamic burst firing by enhancing a hyperpolarization-activated cation current. Nature. 1989;340(6236):715-8.
  117. Guillery RW, Sherman SM. Thalamic relay functions and their role in corticocortical communication: generalizations from the visual system. Neuron. 2002;33(2):163-75.
  118. Llinas R, Jahnsen H. Electrophysiology of mammalian thalamic neurones in vitro. Nature. 1982;297(5865):406-8.
  119. Sherman SM. A wake-up call from the thalamus. Nat Neurosci. 2001;4(4):344-6.
  120. Ploghaus A, Becerra L, Borras C, Borsook D. Neural circuitry underlying pain modulation: expectation, hypnosis, placebo. Trends in cognitive sciences. 2003;7(5):197-200.
  121. Drevets WC, Price JL, Simpson JR, Jr., Todd RD, Reich T, Vannier M, et al. Subgenual prefrontal cortex abnormalities in mood disorders. Nature. 1997;386(6627):824-7.
  122. Mayberg HS, Lozano AM, Voon V, McNeely HE, Seminowicz D, Hamani C, et al. Deep brain stimulation for treatment-resistant depression. Neuron. 2005;45(5):651-60.
  123. Blood AJ, Zatorre RJ. Intensely pleasurable responses to music correlate with activity in brain regions implicated in reward and emotion. Proc Natl Acad Sci U S A. 2001;98(20):11818-23.
  124. Gruber AJ, Hussain RJ, O'Donnell P. The nucleus accumbens: a switchboard for goal-directed behaviors. PloS one. 2009;4(4):e5062.
  125. Johansen-Berg H, Gutman DA, Behrens TE, Matthews PM, Rushworth MF, Katz E, et al. Anatomical connectivity of the subgenual cingulate region targeted with deep brain stimulation for treatment-resistant depression. Cereb Cortex. 2008;18(6):1374-83.
  126. Ongur D, Price JL. The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cereb Cortex. 2000;10(3):206-19.
  127. McCullough LD, Sokolowski JD, Salamone JD. A neurochemical and behavioral investigation of the involvement of nucleus accumbens dopamine in instrumental avoidance. Neuroscience. 1993;52(4):919-25.
  128. Ambroggi F, Ishikawa A, Fields HL, Nicola SM. Basolateral amygdala neurons facilitate reward-seeking behavior by exciting nucleus accumbens neurons. Neuron. 2008;59(4):648-61.
  129. Hoffman HJ, Reed GW. Epidemiology of tinnitus. Tinnitus: Theory and Management2004. p. 16e41.
  130. Levine RA, Abel M, Cheng H. CNS somatosensory-auditory interactions elicit or modulate tinnitus. Experimental brain research Experimentelle Hirnforschung Experimentation cerebrale. 2003;153(4):643-8.
  131. Alster J, Shemesh Z, Ornan M, Attias J. Sleep disturbance associated with chronic tinnitus. Biological psychiatry. 1993;34(1-2):84-90.
  132. Folmer RL, Griest SE. Tinnitus and insomnia. Am J Otolaryngol. 2000;21(5):287-93.
  133. Hallam RS. Correlates of sleep disturbance in chronic distressing tinnitus. Scandinavian audiology. 1996;25(4):263-6.
  134. Kaltenbach JA. Neurophysiologic mechanisms of tinnitus. J Am Acad Audiol. 2000;11(3):125-37.
  135. Eggermont JJ. Correlated neural activity as the driving force for functional changes in auditory cortex. Hear Res. 2007;229(1-2):69-80.
  136. Eggermont JJ, Roberts LE. The neuroscience of tinnitus. Trends in neurosciences. 2004;27(11):676-82.
  137. Norena AJ, Eggermont JJ. Changes in spontaneous neural activity immediately after an acoustic trauma: implications for neural correlates of tinnitus. Hearing research. 2003;183(1-2):137-53.
  138. Kaltenbach JA, Zacharek MA, Zhang J, Frederick S. Activity in the dorsal cochlear nucleus of hamsters previously tested for tinnitus following intense tone exposure. Neurosci Lett. 2004;355(1-2):121-5.
  139. 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(1-2):28-38.
  140. Muhlnickel W, Elbert T, Taub E, Flor H. Reorganization of auditory cortex in tinnitus. Proc Natl Acad Sci U S A. 1998;95(17):10340-3.
  141. Eggermont JJ. Cortical tonotopic map reorganization and its implications for treatment of tinnitus. Acta oto-laryngologica Supplementum. 2006(556):9-12.
  142. Rajan R, Irvine DR. Neuronal responses across cortical field A1 in plasticity induced by peripheral auditory organ damage. Audiology & neuro-otology. 1998;3(2-3):123-44.
  143. Langguth B, Landgrebe M, Kleinjung T, Sand GP, Hajak G. Tinnitus and depression. The world journal of biological psychiatry : the official journal of the World Federation of Societies of Biological Psychiatry. 2011;12(7):489-500.
  144. Lenhardt ML, Shulman A, Goldstein BA. The role of the insula cortex in the final common pathway for tinnitus: experience using ultra-high-frequency therapy. Int Tinnitus J. 2008;14(1):13-6.
  145. Robinson SK, Viirre ES, Stein MB. Antidepressant therapy in tinnitus. Hear Res. 2007;226(1-2):221-31.
  146. Zenner HP, Pfister M, Birbaumer N. Tinnitus sensitization: Sensory and psychophysiological aspects of a new pathway of acquired centralization of chronic tinnitus. Otology & neurotology : official publication of the American Otological Society, American Neurotology Society [and] European Academy of Otology and Neurotology. 2006;27:1054-63.
Journal of Advanced Medical Sciences and Applied Technologies
Volume 2, Issue 1 - Serial Number 1
6
March 2016
Pages 181-189