본문 바로가기
KERD
논문KCI 등재

Tinnitus and the Triple Network Model: A Perspective

Dirk De Ridder|송재진|Sven Vanneste|Divya Adhia
대한이비인후과학회 (Korean Society of Otorhinolaryngology-Head and Neck Surgery)|2022.08|Clinical and Experimental Otorhinolaryngology|제15권 제3호|pp. 205-212|DOI https://doi.org/10.21053/ceo.2022.00815

1

조회

0

다운로드

3

인용

0

참고문헌

키워드

TinnitusDefault Mode NetworkSalience NetworkExecutive Network

초록

Tinnitus is defined as the conscious awareness of a sound without an identifiable external sound source, and tinnitus disorder as tinnitus with associated suffering. Chronic tinnitus has been anatomically and phenomenologically separated into three pathways: a lateral “sound” pathway, a medial “suffering” pathway, and a descending noise-canceling pathway. Here, the triple network model is proposed as a unifying framework common to neuropsychiatric disorders. It proposes that abnormal interactions among three cardinal networks—the self-representational default mode network, the behavioral relevance-encoding salience network and the goal-oriented central executive network—underlie brain disorders. Tinnitus commonly leads to negative cognitive, emotional, and autonomic responses, phenomenologically expressed as tinnitus-related suffering, processed by the medial pathway. This anatomically overlaps with the salience network, encoding the behavioral relevance of the sound stimulus. Chronic tinnitus can also become associated with the self-representing default mode network and becomes an intrinsic part of the self-percept. This is likely an energy-saving evolutionary adaptation, by detaching tinnitus from sympathetic energy-consuming activity. Eventually, this can lead to functional disability by interfering with the central executive network. In conclusion, these three pathways can be extended to a triple network model explaining all tinnitus-associated comorbidities. This model paves the way for the development of individualized treatment modalities.

Abstract

Tinnitus is defined as the conscious awareness of a sound without an identifiable external sound source, and tinnitus disorder as tinnitus with associated suffering. Chronic tinnitus has been anatomically and phenomenologically separated into three pathways: a lateral “sound” pathway, a medial “suffering” pathway, and a descending noise-canceling pathway. Here, the triple network model is proposed as a unifying framework common to neuropsychiatric disorders. It proposes that abnormal interactions among three cardinal networks—the self-representational default mode network, the behavioral relevance-encoding salience network and the goal-oriented central executive network—underlie brain disorders. Tinnitus commonly leads to negative cognitive, emotional, and autonomic responses, phenomenologically expressed as tinnitus-related suffering, processed by the medial pathway. This anatomically overlaps with the salience network, encoding the behavioral relevance of the sound stimulus. Chronic tinnitus can also become associated with the self-representing default mode network and becomes an intrinsic part of the self-percept. This is likely an energy-saving evolutionary adaptation, by detaching tinnitus from sympathetic energy-consuming activity. Eventually, this can lead to functional disability by interfering with the central executive network. In conclusion, these three pathways can be extended to a triple network model explaining all tinnitus-associated comorbidities. This model paves the way for the development of individualized treatment modalities.

참고문헌 (116)

  1. De Ridder D, "Tinnitus and tinnitus disorder : theoretical and operational definitions(an international multidisciplinary proposal)", Prog Brain Res, 260, pp.1~25 (2021)
  2. Vanneste S, "The neural network of phantom sound changes over time : a comparison between recent-onset and chronic tinnitus patients", Eur J Neurosci, 34(5), pp.718~731 (2011)
  3. Wallhausser-Franke E, "Transition from acute to chronic tinnitus : predictors for the development of chronic distressing tinnitus", Front Neurol, 8, pp.605~ (2017)
  4. McCormack A, "A systematic review of the reporting of tinnitus prevalence and severity", Hear Res, 337, pp.70~79 (2016)
  5. Gibrin PC, "Prevalence of tinnitus complaints and probable association with hearing loss, diabetes mellitus and hypertension in elderly", Codas, 25(2), pp.176~180 (2013)
  6. Baguley DM, "Hyperacusis : major research questions", HNO, 66(5), pp.358~363 (2018)
  7. 박의현, "Psychiatric Distress as a Common Risk Factor for Tinnitus and Joint Pain: A National Population-Based Survey", Clinical and Experimental Otorhinolaryngology, 13(3), pp.234~240 (2020), 대한이비인후과학회[DOI]
  8. Cronlein T, "Insomnia in patients with chronic tinnitus : cognitive and emotional distress as moderator variables", J Psychosom Res, 83, pp.65~68 (2016)
  9. Asnis GM, "Insomnia in tinnitus patients : a prospective study finding a significant relationship", Int Tinnitus J, 24(2), pp.65~69 (2021)
  10. Clarke NA, "Associations between subjective tinnitus and cognitive performance : systematic review and meta-analyses", Trends Hear, 24, pp.2331216520918416~ (2020)
  11. NeffP, "The impact of tinnitus distress on cognition", Sci Rep, 11(1), pp.2243~ (2021)
  12. Dawes P, "Natural history of tinnitus in adults : a cross-sectional and longitudinal analysis", BMJ Open, 10(12), pp.e041290~ (2020)
  13. Fuller T, "Cognitive behavioural therapy for tinnitus", Cochrane Database Syst Rev, 1(1), pp.CD012614~ (2020)
  14. De Ridder D, "Phantom percepts : tinnitus and pain as persisting aversive memory networks", Proc Natl Acad Sci U S A, 108(20), pp.8075~8080 (2011)
  15. De Ridder D, "The Darwinian plasticity hypothesis for tinnitus and pain", Prog Brain Res, 166, pp.55~60 (2007)
  16. De Ridder D, "The Bayesian brain in imbalance : medial, lateral and descending pathways in tinnitus and pain : a perspective", Prog Brain Res, 262, pp.309~334 (2021)
  17. Jeanmonod D, "Low-threshold calcium spike bursts in the human thalamus: common physiopathology for sensory, motor and limbic positive symptoms", Brain, 119(Pt 2), pp.363~375 (1996)
  18. Llinas RR, "Thalamocortical dysrhythmia : a neurological and neuropsychiatric syndrome characterized by magnetoencephalography", Proc Natl Acad Sci U S A, 96(26), pp.15222~15227 (1999)
  19. Moller AR, "Similarities between severe tinnitus and chronic pain", J Am Acad Audiol, 11(3), pp.115~124 (2000)
  20. Moller AR, "Similarities between chronic pain and tinnitus", Am J Otol, 18(5), pp.577~585 (1997)
  21. Moller AR, "Tinnitus and pain", Prog Brain Res, 166, pp.47~53 (2007)
  22. Rauschecker JP, "Frontostriatal gating of tinnitus and chronic pain", Trends Cogn Sci, 19(10), pp.567~578 (2015)
  23. Tonndorf J, "The analogy between tinnitus and pain : a suggestion for a physiological basis of chronic tinnitus", Hear Res, 28(2-3), pp.271~275 (1987)
  24. Vanneste S, "Thalamocortical dysrhythmia detected by machine learning", Nat Commun, 9(1), pp.1103~ (2018)
  25. Vanneste S, "Tinnitus and neuropathic pain share a common neural substrate in the form of specific brain connectivity and microstate profiles", Prog Neuropsychopharmacol Biol Psychiatry, 88, pp.388~400 (2019)
  26. De Ridder D, "Electrical stimulation of auditory and somatosensory cortices for treatment of tinnitus and pain", Prog Brain Res, 166, pp.377~388 (2007)
  27. De Ridder D, "Textbook of tinnitus", pp.753~762 (2011), Springer
  28. "Neuroanatomy, spinothalamic tract" (2022)[URL]
  29. De Ridder D, "The anatomy of pain and suffering in the brain and its clinical implications", Neurosci Biobehav Rev, 130, pp.125~146 (2021)
  30. De Ridder D, "Burst and tonic spinal cord stimulation : different and common brain mechanisms", Neuromodulation, 19(1), pp.47~59 (2016)
  31. Frot M, "Parallel processing of nociceptive A-delta inputs in SII and midcingulate cortex in humans", J Neurosci, 28(4), pp.944~952 (2008)
  32. Vanneste S, "Chronic pain as a brain imbalance between pain input and pain suppression", Brain Commun, 3(1), pp.fcab014~ (2021)
  33. Yearwood T, "Comparison of neural activity in chronic pain patients during tonic and burst spinal cord stimulation using fluorodeoxyglucose positron emission tomography", Neuromodulation, 23(1), pp.56~63 (2020)
  34. Bushnell MC, "Cognitive and emotional control of pain and its disruption in chronic pain", Nat Rev Neurosci, 14(7), pp.502~511 (2013)
  35. Rainville P, "Dissociation of sensory and affective dimensions of pain using hypnotic modulation", Pain, 82(2), pp.159~171 (1999)
  36. Menon V, "Large-scale brain networks and psychopathology : a unifying triple network model", Trends Cogn Sci, 15(10), pp.483~506 (2011)
  37. Greicius MD, "Functional connectivity in the resting brain : a network analysis of the default mode hypothesis", Proc Natl Acad Sci U S A, 100(1), pp.253~258 (2003)
  38. Buckner RL, "The brain’s default network : anatomy, function, and relevance to disease", Ann N Y Acad Sci, 1124, pp.1~38 (2008)
  39. Seeley WW, "Dissociable intrinsic connectivity networks for salience processing and executive control", J Neurosci, 27(9), pp.2349~2356 (2007)
  40. Vincent JL, "Evidence for a frontoparietal control system revealed by intrinsic functional connectivity", J Neurophysiol, 100(6), pp.3328~3342 (2008)
  41. Fox MD, "The human brain is intrinsically organized into dynamic, anticorrelated functional networks", Proc Natl Acad Sci U S A, 102(27), pp.9673~9678 (2005)
  42. Goulden N, "The salience network is responsible for switching between the default mode network and the central executive network : replication from DCM", Neuroimage, 99, pp.180~190 (2014)
  43. Menon V, "Saliency, switching, attention and control: a network model of insula function", Brain Struct Funct, 214(5-6), pp.655~667 (2010)
  44. Sridharan D, "A critical role for the right fronto-insular cortex in switching between central-executive and default-mode networks", Proc Natl Acad Sci U S A, 105(34), pp.12569~12574 (2008)
  45. Sha Z, "Common dysfunction of large-scale neurocognitive networks across psychiatric disorders", Biol Psychiatry, 85(5), pp.379~388 (2019)
  46. Sha Z, "Meta-connectomic analysis reveals commonly disrupted functional architectures in network modules and connectors across brain disorders", Cereb Cortex, 28(12), pp.4179~4194 (2018)
  47. De Ridder D, "Pain and the triple network model", Front Neurol, 13, pp.757241~ (2022)
  48. Boly M, "Cerebral processing of auditory and noxious stimuli in severely brain injured patients: differences between VS and MCS", Neuropsychol Rehabil, 15(3-4), pp.283~289 (2005)
  49. Boly M, "Auditory processing in severely brain injured patients : differences between the minimally conscious state and the persistent vegetative state", Arch Neurol, 61(2), pp.233~238 (2004)
  50. Boly M, "Preserved feedforward but impaired top-down processes in the vegetative state", Science, 332(6031), pp.858~862 (2011)
  51. Laureys S, "Auditory processing in the vegetative state", Brain, 123(Pt 8), pp.1589~1601 (2000)
  52. Laureys S, "Cerebral processing in the minimally conscious state", Neurology, 63(5), pp.916~918 (2004)
  53. De Ridder D, "An integrative model of auditory phantom perception : tinnitus as a unified percept of interacting separable subnetworks", Neurosci Biobehav Rev, 44, pp.16~32 (2014)
  54. De Ridder D, "Anterior cingulate implants for tinnitus : report of 2 cases", J Neurosurg, 124(4), pp.893~901 (2016)
  55. Vanneste S, "The neural correlates of tinnitus-related distress", Neuroimage, 52(2), pp.470~480 (2010)
  56. De Ridder D, "The distressed brain : a group blind source separation analysis on tinnitus", PLoS One, 6(10), pp.e24273~ (2011)
  57. Beard AW, "Results of leucotomy operations for tinnitus", J Psychosom Res, 9(1), pp.29~32 (1965)
  58. Elithorn A, "Prefrontal leucotomy in the treatment of tinnitus", Proc R Soc Med, 46(10), pp.832~833 (1953)
  59. van der Loo E, "Tinnitus intensity dependent gamma oscillations of the contralateral auditory cortex", PLoS One, 4(10), pp.e7396~ (2009)
  60. Smits M, "Lateralization of functional magnetic resonance imaging(fMRI)activation in the auditory pathway of patients with lateralized tinnitus", Neuroradiology, 49(8), pp.669~679 (2007)
  61. Song JJ, "Dysfunctional noise cancelling of the rostral anterior cingulate cortex in tinnitus patients", PLoS One, 10(4), pp.e0123538~ (2015)
  62. Seydell-Greenwald A, "Functional MRI evidence for a role of ventral prefrontal cortex in tinnitus", Brain Res, 1485, pp.22~39 (2012)
  63. Axelsson A, "Tinnitus : a study of its prevalence and characteristics", Br J Audiol, 23(1), pp.53~62 (1989)
  64. Cima RF, "Catastrophizing and fear of tinnitus predict quality of life in patients with chronic tinnitus", Ear Hear, 32(5), pp.634~641 (2011)
  65. Weise C, "The role of catastrophizing in recent onset tinnitus : its nature and association with tinnitus distress and medical utilization", Int J Audiol, 52(3), pp.177~188 (2013)
  66. Hebert S, "The sound of stress : blunted cortisol reactivity to psychosocial stress in tinnitus sufferers", Neurosci Lett, 411(2), pp.138~142 (2007)
  67. Hebert S, "Salivary cortisol levels, subjective stress, and tinnitus intensity in tinnitus sufferers during noise exposure in the laboratory", Int J Hyg Environ Health, 212(1), pp.37~44 (2009)
  68. Hinton DE, "Tinnitus among Cambodian refugees : relationship to PTSD severity", J Trauma Stress, 19(4), pp.541~546 (2006)
  69. Kogler L, "Psychosocial versus physiological stress : meta-analyses on deactivations and activations of the neural correlates of stress reactions", Neuroimage, 119, pp.235~251 (2015)
  70. Koolhaas JM, "Stress revisited : a critical evaluation of the stress concept", Neurosci Biobehav Rev, 35(5), pp.1291~1301 (2011)
  71. Ulrich-Lai YM, "Neural regulation of endocrine and autonomic stress responses", Nat Rev Neurosci, 10(6), pp.397~409 (2009)
  72. Russell G, "The human stress response", Nat Rev Endocrinol, 15(9), pp.525~534 (2019)
  73. Staufenbiel SM, "Hair cortisol, stress exposure, and mental health in humans : a systematic review", Psychoneuroendocrinology, 38(8), pp.1220~1235 (2013)
  74. Gilam G, "Neural indicators of interpersonal anger as cause and consequence of combat training stress symptoms", Psychol Med, 47(9), pp.1561~1572 (2017)
  75. Joos K, "Disentangling depression and distress networks in the tinnitus brain", PLoS One, 7(7), pp.e40544~ (2012)
  76. Vachon-Presseau E, "Acute stress contributes to individual differences in pain and pain-related brain activity in healthy and chronic pain patients", J Neurosci, 33(16), pp.6826~6833 (2013)
  77. Telesford QK, "The brain as a complex system : using network science as a tool for understanding the brain", Brain Connect, 1(4), pp.295~308 (2011)
  78. Bullmore E, "Complex brain networks : graph theoretical analysis of structural and functional systems", Nat Rev Neurosci, 10(3), pp.186~198 (2009)
  79. Sporns O, "Organization, development and function of complex brain networks", Trends Cogn Sci, 8(9), pp.418~425 (2004)
  80. Suarez LE, "Linking structure and function in macroscale brain networks", Trends Cogn Sci, 24(4), pp.302~315 (2020)
  81. Mohan A, "Graph theoretical analysis of brain connectivity in phantom sound perception", Sci Rep, 6, pp.19683~ (2016)
  82. Elgoyhen AB, "Tinnitus : network pathophysiology-network pharmacology", Front Syst Neurosci, 6, pp.1~ (2012)
  83. Schmidt SA, "Default mode, dorsal attention and auditory resting state networks exhibit differential functional connectivity in tinnitus and hearing loss", PLoS One, 8(10), pp.e76488~ (2013)
  84. Song JJ, "The balance between Bayesian inference and default mode determines the generation of tinnitus from decreased auditory input : a volume entropy-based study", Hum Brain Mapp, 42(12), pp.4059~4073 (2021)
  85. Eggermont JJ, "Separate auditory pathways for the induction and maintenance of tinnitus and hyperacusis?", Prog Brain Res, 260, pp.101~127 (2021)
  86. Hu J, "The neural mechanisms of tinnitus : a perspective from functional magnetic resonance imaging", Front Neurosci, 15, pp.621145~ (2021)
  87. Zhou GP, "Disrupted intraregional brain activity and functional connectivity in unilateral acute tinnitus patients with hearing loss", Front Neurosci, 13, pp.1010~ (2019)
  88. Chen YC, "Alterations of the default mode network and cognitive impairment in patients with unilateral chronic tinnitus", Quant Imaging Med Surg, 8(10), pp.1020~1029 (2018)
  89. Schmidt SA, "Connectivity of precuneus to the default mode and dorsal attention networks : a possible invariant marker of long-term tinnitus", Neuroimage Clin, 16, pp.196~204 (2017)
  90. Lanting C, "Tinnitus-and task-related differences in resting-state networks", Adv Exp Med Biol, 894, pp.175~187 (2016)
  91. Chen YC, "Tinnitus distress is associated with enhanced resting-state functional connectivity within the default mode network", Neuropsychiatr Dis Treat, 14, pp.1919~1927 (2018)
  92. Lee SY, "Cortical oscillatory signatures reveal the prerequisites for tinnitus perception : a comparison of subjects with sudden sensorineural hearing loss with and without tinnitus", Front Neurosci, 14, pp.596647~ (2020)
  93. Han JJ, "Pre-treatment ongoing cortical oscillatory activity predicts improvement of tinnitus after partial peripheral reafferentation with hearing aids", Front Neurosci, 14, pp.410~ (2020)
  94. Friston K., "The free-energy principle: a unified brain theory?", Nat Rev Neurosci, 11(2), pp.127~138 (2010)
  95. Friston K, "The free-energy principle: a rough guide to the brain?", Trends Cogn Sci, 3(7), pp.293~301 (2009)
  96. Hitze B, "How the selfish brain organizes its supply and demand", Front Neuroenergetics, 2, pp.7~ (2010)
  97. Peters A, "The selfish brain : competition for energy resources", Neurosci Biobehav Rev, 28(2), pp.143~180 (2004)
  98. Taylor KS, "Association between resting-state brain functional connectivity and muscle sympathetic burst incidence", J Neurophysiol, 115(2), pp.662~673 (2016)
  99. Babo-Rebelo M, "Neural responses to heartbeats in the default network encode the self in spontaneous thoughts", J Neurosci, 36(30), pp.7829~7840 (2016)
  100. Sjostrom L, "Epinephrine sensitivity with respect to metabolic rate and other variables in women", Am J Physiol, 245(5 Pt 1), pp.E431~E442 (1983)
  101. Fellows IW, "The effect of adrenaline upon cardiovascular and metabolic functions in man", Clin Sci(Lond), 69(2), pp.215~222 (1985)
  102. Holland-Fischer P, "Increased energy expenditure and glucose oxidation during acute nontraumatic skin pain in humans", Eur J Anaesthesiol, 26(4), pp.311~317 (2009)
  103. Xu Z, "Effect of postoperative analgesia on energy metabolism and role of cyclooxygenase-2 inhibitors for postoperative pain management after abdominal surgery in adults", Clin J Pain, 29(7), pp.570~576 (2013)
  104. Straub RH, "The brain and immune system prompt energy shortage in chronic inflammation and ageing", Nat Rev Rheumatol, 13(12), pp.743~751 (2017)
  105. Whitehorn JC, "The metabolic rate in emotional moods induced by suggestion in hypnosis", Am J Psychiatry, 86(4), pp.661~666 (1930)
  106. Schmidt WD, "Resting metabolic rate is influenced by anxiety in college men", J Appl Physiol(1985), 80(2), pp.638~642 (1996)
  107. Mohamad N, "The consequences of tinnitus and tinnitus severity on cognition : a review of the behavioural evidence", Hear Res, 332, pp.199~209 (2016)
  108. Tegg-Quinn S, "The impact of tinnitus upon cognition in adults : a systematic review", Int J Audiol, 55(10), pp.533~540 (2016)
  109. Vanneste S, "The neural correlates of cognitive dysfunction in phantom sounds", Brain Res, 1642, pp.170~179 (2016)
  110. Maudoux A, "Connectivity graph analysis of the auditory resting state network in tinnitus", Brain Res, 1485, pp.10~21 (2012)
  111. Maudoux A, "Auditory resting-state network connectivity in tinnitus : a functional MRI study", PLoS One, 7(5), pp.e36222~ (2012)
  112. Shahsavarani S, "Salience, emotion, and attention : the neural networks underlying tinnitus distress revealed using music and rest", Brain Res, 1755, pp.147277~ (2021)
  113. Kandeepan S, "Tinnitus distress: a paradoxical attention to the sound?", J Neurol, 6(9), pp.2197~2207 (2019)
  114. Xu XM, "Altered spatial and temporal brain connectivity in the salience network of sensorineural hearing loss and tinnitus", Front Neurosci, 13, pp.246~ (2019)
  115. Amaral AA, "Tinnitus-related abnormalities in visual and salience networks during a one-back task with distractors", Hear Res, 326, pp.15~29 (2015)
  116. De Ridder D, "The Bayesian brain : phantom percepts resolve sensory uncertainty", Neurosci Biobehav Rev, 44, pp.4~15 (2014)

관련 논문AI추천

Changes in the Laterality of Functional Connectivity Associated with Tinnitus: Resting-State fMRI Study류창우, 박문서, 변재용, 신예지, 장건호대한자기공명의과학회 · Investigative Magnetic Resonance Imaging2019 · 제23권 제1호The Pathophysiology of Tinnitus: Involvement of the Somatosensory, Brain, and Limbic Systems김태화, 이기은, 이유리, 전승익, 조성민, 진인기한국청각언어재활학회 · Audiology and Speech Research2020 · 제16권 제1호Neural Mechanisms and Models of Tinnitus Generation한우재, Fatima T. Husain한국청각언어재활학회 · Audiology and Speech Research2009 · 제5권 제1호Tinnitus: Characteristics, Causes, Mechanisms, and Treatments김태유, 신경식, 이호원, 임준성, 한병인대한신경과학회 · Journal of Clinical Neurology2009 · 제5권 제1호The Role of Cognitive Control in Tinnitus and Its Relation to Speech-in-Noise PerformanceFatima T. Husain, Yihsin Tai대한청각학회 · Journal of Audiology & Otology2019 · 제23권 제1호Non-Invasive Neuromodulation for TinnitusLangguth Berthold대한청각학회 · Journal of Audiology & Otology2020 · 제24권 제3호

이 간행물의 다른 논문 (9건)

Saccular Pathology Is Most Commonly Found in Patients With General Vestibular Disorders김정기, 신승호, 김성헌, 심대보, 나지나, 이전미, 이현진pp. 213-219Hyaluronan Synthase 1: A Novel Candidate Gene Associated With Late-Onset Non-syndromic Hereditary Hearing Loss김태경, 최영미, 이성수, 이창준, 조형호, Alphonse Umugirepp. 220-229Clinical and Laboratory Features of Various Criteria of Eosinophilic Chronic Rhinosinusitis: A Systematic Review and Meta-AnalysisMohammed Abdullah Basurrah, 김도현, 김성원, 황세환pp. 230-246Presentation Patterns and Surgical Management of the Complications of Thread Rhinoplasty진홍률, 김수진pp. 247-253Aeroallergen Sensitization Status in South Korea From 2018 to 2021조재훈, 김진국, 김수현, 김인태, 민도식pp. 254-263
원문 보기