Functional Brain Regions Linked to Tinnitus Pathology and Compensation During Task Performance: A Systematic Review.
fMRI
imaging
neural correlates
neural enhancement
regions of interest
tinnitus
Journal
Otolaryngology--head and neck surgery : official journal of American Academy of Otolaryngology-Head and Neck Surgery
ISSN: 1097-6817
Titre abrégé: Otolaryngol Head Neck Surg
Pays: England
ID NLM: 8508176
Informations de publication
Date de publication:
Dec 2023
Dec 2023
Historique:
revised:
24
06
2023
received:
05
03
2023
accepted:
11
07
2023
medline:
22
11
2023
pubmed:
31
7
2023
entrez:
31
7
2023
Statut:
ppublish
Résumé
To systematically search the literature and organize relevant advancements in the connection between tinnitus and the activity of different functional brain regions using functional magnetic resonance imaging (fMRI). MEDLINE (OVID), EMBASE (OVID), CINAHL (EBSCO), Web of Science, ProQuest Dissertations & Theses Global, Cochrane Database of Systematic Reviews, and PROSPERO from inception to April 2022. Studies with adult human subjects who suffer from tinnitus and underwent fMRI to relate specific regions of interest to tinnitus pathology or compensation were included. In addition, fMRI had to be performed with a paradigm of stimuli that would stimulate auditory brain activity. Exclusion criteria included non-English studies, animal studies, and studies that utilized a resting state magnetic resonance imaging or other imaging modalities. The auditory cortex may work to dampen the effects of central gain. Results from different studies show variable changes in the Heschl's gyrus (HG), with some showing increased activity and others showing inhibition and volume loss. After controlling for hyperacusis and other confounders, tinnitus does not seem to influence the inferior colliculus (IC) activation. However, there is decreased connectivity between the auditory cortex and IC. The cochlear nucleus (CN) generally shows increased activation in tinnitus patients. fMRI evidence indicates significant inhibition of thalamic gating. Activating the thalamus may be of important therapeutic potential. Patients with tinnitus have significantly altered neuronal firing patterns, especially within the auditory network, when compared to individuals without tinnitus. Tinnitus and hyperacusis commonly coexist, making differentiation of the effects of these 2 phenomena frequently difficult.
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
1409-1423Informations de copyright
© 2023 The Authors. Otolaryngology-Head and Neck Surgery published by Wiley Periodicals LLC on behalf of American Academy of Otolaryngology-Head and Neck Surgery Foundation.
Références
Baguley D, McFerran D, Hall D. Tinnitus. Lancet. 2013;382(9904):1600-1607.
McCormack A, Edmondson-Jones M, Somerset S, Hall D. A systematic review of the reporting of tinnitus prevalence and severity. Hear Res. 2016;337:70-79.
Tunkel DE, Bauer CA, Sun GH, et al. Clinical practice guideline. Otolaryngol Head Neck Surg. 2014;151(2_suppl):S1-S40.
Khedr EM, Ahmed MA, Shawky OA, Mohamed ES, El Attar GS, Mohammad KA. Epidemiological study of chronic tinnitus in Assiut, Egypt. Neuroepidemiology. 2010;35(1):45-52.
Michikawa T, Nishiwaki Y, Kikuchi Y, et al. Prevalence and factors associated with tinnitus: a community-based study of Japanese elders. J Epidemiol. 2010;20(4):271-276.
Palmer KT. Occupational exposure to noise and the attributable burden of hearing difficulties in Great Britain. Occup Environ Med. 2002;59(9):634-639.
Zenner HP. A systematic classification of tinnitus generator mechanisms. Int Tinnitus J. 1998;4(2):109-113.
Eggermont JJ, Tyler RS. Physiological mechanisms and neural models. In: Tyler RS, ed. Tinnitus Handbook. Vol 1, 1st ed. Singular Publishing Group; 2000:85-122.
Caspary DM, Llano DA. Auditory thalamic circuits and GABAA receptor function: putative mechanisms in tinnitus pathology. Hear Res. 2017;349:197-207.
Llinás RR, Steriade M. Bursting of thalamic neurons and states of vigilance. J Neurophysiol. 2006;95(6):3297-3308.
Salvi RJ, Wang J, Ding D. Auditory plasticity and hyperactivity following cochlear damage. Hear Res. 2000;147(1-2):261-274.
Li S, Choi V, Tzounopoulos T. Pathogenic plasticity of Kv7.2/3 channel activity is essential for the induction of tinnitus. Proc Natl Acad Sci USA. 2013;110(24):9980-9985.
Llinás R, Urbano FJ, Leznik E, Ramírez RR, van Marle HJF. Rhythmic and dysrhythmic thalamocortical dynamics: GABA systems and the edge effect. Trends Neurosci. 2005;28(6):325-333.
Yang S, Weiner BD, Zhang LS, Cho S-J, Bao S. Homeostatic plasticity drives tinnitus perception in an animal model. Proc Natl Acad Sci USA. 2011;108(36):14974-14979.
Haider HF, Bojić T, Ribeiro SF, Paço J, Hall DA, Szczepek AJ. Pathophysiology of subjective tinnitus: triggers and maintenance. Front Neurosci. 2018;12:866.
Noreña AJ. Revisiting the cochlear and central mechanisms of tinnitus and therapeutic approaches. Audiol Neurotol. 2015;20(suppl 1):53-59.
Schlee W, Lorenz I, Hartmann T, Müller N, Schulz H, Weisz N. A global brain model of tinnitus. In: Moeller AR, Languth B, de Ridder D, Kleinjung T, eds. Textbook of Tinnitus. Springer; 2011:161-169.
De Ridder D, Elgoyhen AB, Romo R, Langguth B. Phantom percepts: tinnitus and pain as persisting aversive memory networks. Proc Natl Acad Sci USA. 2011;108(20):8075-8080.
Joanna Briggs Institute. Checklist for Systematic Reviews and Research Syntheses. Joanna Briggs Institute; 2017.
Page MJ, McKenzie JE, Bossuyt PM, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. PLoS Med. 2021;18(3):e1003583.
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.
Melcher JR, Sigalovsky IS, Guinan JJ, Levine RA. Lateralized tinnitus studied with functional magnetic resonance imaging: abnormal inferior colliculus activation. J Neurophysiol. 2000;83(2):1058-1072.
Gu JW, Halpin CF, Nam E-C, 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):3361-3370.
Melcher JR, Levine RA, Bergevin C, Norris B. The auditory midbrain of people with tinnitus: abnormal sound-evoked activity revisited. Hear Res. 2009;257(1-2):63-74.
Carpenter-Thompson JR, Akrofi K, Schmidt SA, Dolcos F, Husain FT. Alterations of the emotional processing system may underlie preserved rapid reaction time in tinnitus. Brain Res. 2014;1567:28-41.
Carpenter-Thompson JR, Schmidt SA, Husain FT. Neural plasticity of mild tinnitus: an fMRI investigation comparing those recently diagnosed with tinnitus to those that had tinnitus for a long period of time. Neural Plast. 2015;2015:1-11.
Lanting CP, De Kleine E, Bartels H, Van Dijk P. Functional imaging of unilateral tinnitus using fMRI. Acta Otolaryngol. 2008;128(4):415-421.
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.
Lanting CP, de Kleine E, Eppinga RN, van Dijk P. Neural correlates of human somatosensory integration in tinnitus. Hear Res. 2010;267(1-2):78-88.
Lanting CP, de Kleine E, Langers DRM, van Dijk P. Unilateral tinnitus: changes in connectivity and response lateralization measured with fMRI. PLoS One. 2014;9(10):e110704.
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.
Langers DRM, de Kleine E, van Dijk P. Tinnitus does not require macroscopic tonotopic map reorganization. Front Syst Neurosci. 2012;6:2.
Golm D, Schmidt-Samoa C, Dechent P, Kröner-Herwig B. Tinnitus- related distress: evidence from fMRI of an emotional stroop task. BMC Ear Nose Throat Disord. 2016;16(1):10.
Davies JE, Gander PE, Hall DA. Does chronic tinnitus alter the emotional response function of the amygdala?: a sound-evoked fMRI study. Front Aging Neurosci. 2017;9:31.
Smits M, Kovacs S, de Ridder D, Peeters RR, van Hecke P, Sunaert S. Lateralization of functional magnetic resonance imaging (fMRI) activation in the auditory pathway of patients with lateralized tinnitus. Neuroradiology. 2007;49(8):669-679.
Wunderlich AP, Schönfeldt-Lecuona C, Wolf RC, Dorn K, Bachor E, Freund W. Cortical activation during a pitch discrimination task in tinnitus patients and controls-an fMRI study. Audiol Neurotol. 2009;15:137-148.
Zenke JK, Rahman S, Guo Q, Leung AWS, Gomaa NA. Central processing in tinnitus: fMRI study outlining patterns of activation using an auditory discrimination task in normal versus tinnitus patients. Otol Neurotol. 2021;42(8):e1170-e1180.
Koops EA, van Dijk P. Hyperacusis in tinnitus patients relates to enlarged subcortical and cortical responses to sound except at the tinnitus frequency. Hear Res. 2021;401:108158.
Song AW, Wong EC, Tan SG, Hyde JS. Diffusion weighted fMRI at 1.5 T. Magn Reson Med. 1996;35(2):155-158.
Heeger DJ, Ress D. What does fMRI tell us about neuronal activity? Nat Rev Neurosci. 2002;3(2):142-151.
Ogawa S, Lee TM, Kay AR, Tank DW. Brain magnetic resonance imaging with contrast dependent on blood oxygenation. Proc Natl Acad Sci USA. 1990;87(24):9868-9872.
San Juan JD, Zhai T, Ash-Rafzadeh A, et al. Tinnitus and auditory cortex: using adapted functional near-infrared spectroscopy to measure resting-state functional connectivity. Neuroreport. 2021;32(1):66-75.
Wong PCM, Uppunda AK, Parrish TB, Dhar S. Cortical Mechanisms of Speech Perception in Noise. J Speech Lang Hear Res. 2008;51(4):1026-1041.
Khalighinejad B, Patel P, Herrero JL, Bickel S, Mehta AD, Mesgarani N. Functional characterization of human Heschl's gyrus in response to natural speech. Neuroimage. 2021;235:118003.
Bendor D. Does a pitch center exist in auditory cortex? J Neurophysiol. 2012;107(3):743-746.
Schneider P, Sluming V, Roberts N, et al. Structural and functional asymmetry of lateral Heschl's gyrus reflects pitch perception preference. Nat Neurosci. 2005;8(9):1241-1247.
Warrier C, Wong P, Penhune V, et al. Relating structure to function: heschl's gyrus and acoustic processing. J Neurosci. 2009;29(1):61-69.
Zhang L, Wang J, Sun H, Feng G, Gao Z. Interactions between the hippocampus and the auditory pathway. Neurobiol Learn Mem. 2022;189:107589.
Berger JI, Coomber B. Tinnitus-related changes in the inferior colliculus. Front Neurol. 2015;6:61.
Mafi AM, Russ MG, Hofer LN, Pham VQ, Young JW, Mellott JG. Inferior collicular cells that project to the auditory thalamus are increasingly surrounded by perineuronal nets with age. Neurobiol Aging. 2021;105:1-15.
Baizer JS, Manohar S, Paolone NA, Weinstock N, Salvi RJ. Understanding tinnitus: the dorsal cochlear nucleus, organization and plasticity. Brain Res. 2012;1485:40-53.
Winer JA, Saint Marie RL, Larue DT, Oliver DL. GABAergic feedforward projections from the inferior colliculus to the medial geniculate body. Proc Natl Acad Sci USA. 1996;93(15):8005-8010.
Peruzzi D, Bartlett E, Smith PH, Oliver DL. A monosynaptic GABAergic input from the inferior colliculus to the medial geniculate body in rat. J Neurosci. 1997;17(10):3766-3777.
Bartlett EL, Smith PH. Anatomic, intrinsic, and synaptic properties of dorsal and ventral division neurons in rat medial geniculate body. J Neurophysiol. 1999;81(5):1999-2016.
Zhang J. Auditory cortex stimulation to suppress tinnitus: mechanisms and strategies. Hear Res. 2013;295:38-57.
Baumann O, Borra RJ, Bower JM, et al. Consensus paper: the role of the cerebellum in perceptual processes. Cerebellum. 2015;14(2):197-220.
Rauschecker JP, Leaver AM, Mühlau M. Tuning out the noise: limbic-auditory interactions in tinnitus. Neuron. 2010;66(6):819-826.
Lan L, Chen Y-C, Shang S, et al. Topological features of limbic dysfunction in chronicity of tinnitus with intact hearing: new hypothesis for ‘noise-cancellation’ mechanism. Prog Neuropsychopharmacol Biol Psychiatry. 2022;113:110459.
Mennink LM, Van Dijk JMC, Van Der Laan BFAM, Metzemaekers JDM, Van Laar PJ, Van Dijk P. The relation between flocculus volume and tinnitus after cerebellopontine angle tumor surgery. Hear Res. 2018;361:113-120.
Mennink LM, van Dijk JMC, van Dijk P. The cerebellar (para)flocculus: a review on its auditory function and a possible role in tinnitus. Hear Res. 2020;398:108081.
Chai Z, Ma C, Jin X. Cortical stimulation for treatment of neurological disorders of hyperexcitability: a role of homeostatic plasticity. Neural Regen Res. 2019;14(1):34.
Deklerck AN, Marechal C, Pérez Fernández AM, Keppler H, Van Roost D, Dhooge IJM. Invasive neuromodulation as a treatment for tinnitus: a systematic review. Neuromodulation Technol Neural Interface. 2020;23(4):451-462.
Kleinjung T, Eichhammer P, Landgrebe M, et al. Combined temporal and prefrontal transcranial magnetic stimulation for tinnitus treatment: a pilot study. Otolaryngol Head Neck Surg. 2008;138(4):497-501.