Share：
Share this content in WeChat
X
[Chinese][PDF]2921
• Review •
Research progress of magnetic resonance imaging in tinnitus
YU Chen  XIE Jiapei  LIU Xue  BAI Yan  WANG Meiyun 

Cite this article as: YU C, XIE J P, LIU X, et al. Research progress of magnetic resonance imaging in tinnitus[J]. Chin J Magn Reson Imaging, 2024, 15(6): 196-201. DOI:10.12015/issn.1674-8034.2024.06.031.


[Abstract] As one of the most common symptoms in otolaryngology, tinnitus seriously affects the quality of life of millions of people. The mechanism of tinnitus is very complex, and there is currently a lack of standardized and individualized treatment. Magnetic resonance imaging can further explore the pathogenesis of tinnitus from different perspectives such as microstructure and function, which is of great value for studying the pathogenesis and providing new treatment options. This article reviews the application value and latest research progress of magnetic resonance imaging in tinnitus, aiming to provide help for further research on the related mechanisms of tinnitus.
[Keywords] tinnitus；magnetic resonance imaging；neural mechanisms；medical imaging；functional magnetic resonance imaging；limbic system

YU Chen1, 2   XIE Jiapei1, 2   LIU Xue1, 2   BAI Yan2, 3   WANG Meiyun2, 3*  

1 Department of Medical Imaging, Zhengzhou University People's Hospital, Zhengzhou 450003, China

2 Department of Medical Imaging, Henan Provincial People's Hospital, Zhengzhou 450003, China

3 Biomedical Research Institute, Henan Academy of Sciences, Zhengzhou 450046, China

Corresponding author: WANG M Y, E-mail: mywang@zzu.edu.cn

Conflicts of interest   None.

Received  2024-02-23
Accepted  2024-05-31
DOI: 10.12015/issn.1674-8034.2024.06.031
Cite this article as: YU C, XIE J P, LIU X, et al. Research progress of magnetic resonance imaging in tinnitus[J]. Chin J Magn Reson Imaging, 2024, 15(6): 196-201. DOI:10.12015/issn.1674-8034.2024.06.031.

[1]
BAGULEY D, MCFERRAN D, HALL D. Tinnitus[J]. Lancet, 2013, 382(9904): 1600-1607. DOI: 10.1016/s0140-6736(13)60142-7.
[2]
JARACH C M, LUGO A, SCALA M, et al. Global prevalence and incidence of tinnitus: a systematic review and meta-analysis[J]. JAMA Neurol, 2022, 79(9): 888-900. DOI: 10.1001/jamaneurol.2022.2189.
[3]
PARK K W, KULLAR P, MALHOTRA C, et al. Current and emerging therapies for chronic subjective tinnitus[J/OL]. J Clin Med, 2023, 12(20): 6555 [2024-02-22]. https://pubmed.ncbi.nlm.nih.gov/37892692/. DOI: 10.3390/jcm12206555.
[4]
YOUSEF A, HINKLEY L B, NAGARAJAN S S, et al. Neuroanatomic volume differences in tinnitus and hearing loss[J]. Laryngoscope, 2021, 131(8): 1863-1868. DOI: 10.1002/lary.29549.
[5]
MAKANI P, THIOUX M, PYOTT S J, et al. A combined image- and coordinate-based meta-analysis of whole-brain voxel-based morphometry studies investigating subjective tinnitus[J/OL]. Brain Sci, 2022, 12(9): 1192 [2024-02-22]. https://pubmed.ncbi.nlm.nih.gov/36138928/. DOI: 10.3390/brainsci12091192.
[6]
SCHECKLMANN M, LEHNER A, POEPPL T B, et al. Auditory cortex is implicated in tinnitus distress: a voxel-based morphometry study[J]. Brain Struct Funct, 2013, 218(4): 1061-1070. DOI: 10.1007/s00429-013-0520-z.
[7]
BOYEN K, LANGERS D R M, DE KLEINE E, et al. Gray matter in the brain: differences associated with tinnitus and hearing loss[J/OL]. Hear Res, 2013, 295: 67-78 [2024-02-22]. https://pubmed.ncbi.nlm.nih.gov/22446179/. DOI: 10.1016/j.heares.2012.02.010.
[8]
SHAHSAVARANI S, KHAN R ALI, HUSAIN F T. Tinnitus and the brain: a review of functional and anatomical magnetic resonance imaging studies[J]. Perspect ASHA SIGs, 2019, 4(5): 896-909. DOI: 10.1044/2019_pers-sig6-2019-0001.
[9]
ROSEMANN S, RAUSCHECKER J P. Neuroanatomical alterations in middle frontal gyrus and the precuneus related to tinnitus and tinnitus distress[J/OL]. Hear Res, 2022, 424: 108595 [2024-02-22]. https://pubmed.ncbi.nlm.nih.gov/35963187/. DOI: 10.1016/j.heares.2022.108595.
[10]
BESTEHER B, GASER C, IVANŠIĆ D, et al. Chronic tinnitus and the limbic system: Reappraising brain structural effects of distress and affective symptoms[J/OL]. Neuroimage Clin, 2019, 24: 101976 [2024-02-22]. https://pubmed.ncbi.nlm.nih.gov/31494400/. DOI: 10.1016/j.nicl.2019.101976.
[11]
KOOPS E A, DE KLEINE E, VAN DIJK P. Gray matter declines with age and hearing loss, but is partially maintained in tinnitus[J/OL]. Sci Rep, 2020, 10(1): 21801 [2024-02-22]. https://pubmed.ncbi.nlm.nih.gov/33311548/. DOI: 10.1038/s41598-020-78571-0.
[12]
HUSAIN F T, ZIMMERMAN B, TAI Y, et al. Assessing mindfulness-based cognitive therapy intervention for tinnitus using behavioural measures and structural MRI: a pilot study[J]. Int J Audiol, 2019, 58(12): 889-901. DOI: 10.1080/14992027.2019.1629655.
[13]
WEI X, LV H, CHEN Q, et al. Neuroanatomical alterations in patients with tinnitus before and after sound therapy: a combined VBM and SCN study[J/OL]. Front Hum Neurosci, 2021, 14: 607452 [2024-02-22]. https://pubmed.ncbi.nlm.nih.gov/33536889/. DOI: 10.3389/fnhum.2020.607452.
[14]
CHEN Q, LV H, WANG Z D, et al. Multimodal quantitative magnetic resonance imaging of the thalamus in tinnitus patients with different outcomes after sound therapy[J]. CNS Neurosci Ther, 2023, 29(12): 4070-4081. DOI: 10.1111/cns.14330.
[15]
LIN C T, GHOSH S, HINKLEY L B, et al. Multi-tasking deep network for tinnitus classification and severity prediction from multimodal structural MR images[J/OL]. J Neural Eng, 2023, 20(1) [2024-02-22]. https://pubmed.ncbi.nlm.nih.gov/36595270/. DOI: 10.1088/1741-2552/acab33.
[16]
BEAULIEU C. The basis of anisotropic water diffusion in the nervous system - a technical review[J]. NMR Biomed, 2002, 15(7/8): 435-455. DOI: 10.1002/nbm.782.
[17]
AHMED S, MOHAN A, YOO H B, et al. Structural correlates of the audiological and emotional components of chronic tinnitus[J/OL]. Prog Brain Res, 2021, 262: 487-509 [2024-02-22]. https://pubmed.ncbi.nlm.nih.gov/33931193/. DOI: 10.1016/bs.pbr.2021.01.030.
[18]
CHEN Q, WANG Z D, LV H, et al. Reorganization of brain white matter in persistent idiopathic tinnitus patients without hearing loss: evidence from baseline data[J/OL]. Front Neurosci, 2020, 14: 591 [2024-02-22]. https://pubmed.ncbi.nlm.nih.gov/32612504/. DOI: 10.3389/fnins.2020.00591.
[19]
CHEN Q, LV H, WANG Z D, et al. Outcomes at 6 months are related to brain structural and white matter microstructural reorganization in idiopathic tinnitus patients treated with sound therapy[J]. Hum Brain Mapp, 2021, 42(3): 753-765. DOI: 10.1002/hbm.25260.
[20]
LIU L, JIANG H, WANG D, et al. A study of regional homogeneity of resting-state Functional Magnetic Resonance Imaging in mild cognitive impairment[J/OL]. Behav Brain Res, 2021, 402: 113103 [2024-02-22]. https://pubmed.ncbi.nlm.nih.gov/33417993/. DOI: 10.1016/j.bbr.2020.113103.
[21]
THEODOROFF S M, KALTENBACH J A. The role of the brainstem in generating and modulating tinnitus[J]. Am J Audiol, 2019, 28(1S): 225-238. DOI: 10.1044/2018_AJA-TTR17-18-0035.
[22]
KHAN R A, SUTTON B P, TAI Y, et al. A large-scale diffusion imaging study of tinnitus and hearing loss[J/OL]. Sci Rep, 2021, 11(1): 23395 [2024-02-22]. https://pubmed.ncbi.nlm.nih.gov/34862447/. DOI: 10.1038/s41598-021-02908-6.
[23]
ZIMMERMAN B, FINNEGAN M, PAUL S, et al. Functional brain changes during mindfulness-based cognitive therapy associated with tinnitus severity[J/OL]. Front Neurosci, 2019, 13: 747 [2024-02-22]. https://pubmed.ncbi.nlm.nih.gov/31396035/. DOI: 10.3389/fnins.2019.00747.
[24]
ZHOU G P, SHI X Y, WEI H L, et al. Disrupted intraregional brain activity and functional connectivity in unilateral acute tinnitus patients with hearing loss[J/OL]. Front Neurosci, 2019, 13: 1010 [2024-02-22]. https://pubmed.ncbi.nlm.nih.gov/31607851/. DOI: 10.3389/fnins.2019.01010.
[25]
LV H, LIU J D, CHEN Q, et al. Brain effective connectivity analysis facilitates the treatment outcome expectation of sound therapy in patients with tinnitus[J/OL]. IEEE Trans Neural Syst Rehabil Eng, 2023 [2024-02-22]. https://pubmed.ncbi.nlm.nih.gov/37022456/. DOI: 10.1109/TNSRE.2023.3241941.
[26]
DU H L, CHEN J, QIAN X Y, et al. Reduced intra- and inter-network functional connectivity identified in patients with tinnitus with and without hearing loss[J]. Audiol Neurootol, 2024, 29(2): 146-166. DOI: 10.1159/000534659.
[27]
KOK T E, DOMINGO D, HASSAN J, et al. Resting-state networks in tinnitus: a scoping review[J]. Clin Neuroradiol, 2022, 32(4): 903-922. DOI: 10.1007/s00062-022-01170-1.
[28]
DU H L, FENG X, QIAN X Y, et al. Recent-onset and persistent tinnitus: Uncovering the differences in brain activities using resting-state functional magnetic resonance imaging technologies[J/OL]. Front Neurosci, 2022, 16: 976095 [2024-02-22]. https://pubmed.ncbi.nlm.nih.gov/36340775/. DOI: 10.3389/fnins.2022.976095.
[29]
CAI W W, LI Z C, YANG Q T, et al. Abnormal spontaneous neural activity of the central auditory system changes the functional connectivity in the tinnitus brain: a resting-state functional MRI study[J/OL]. Front Neurosci, 2019, 13: 1314 [2024-02-22]. https://pubmed.ncbi.nlm.nih.gov/31920484/. DOI: 10.3389/fnins.2019.01314.
[30]
CHEN Y C, CHEN H Y, BO F, et al. Tinnitus distress is associated with enhanced resting-state functional connectivity within the default mode network[J/OL]. Neuropsychiatr Dis Treat, 2018, 14: 1919-1927 [2024-02-22]. https://pubmed.ncbi.nlm.nih.gov/30122924/. DOI: 10.2147/NDT.S164619.
[31]
BURTON H, WINELAND A, BHATTACHARYA M, et al. Altered networks in bothersome tinnitus: a functional connectivity study[J/OL]. BMC Neurosci, 2012, 13: 3 [2024-02-22]. https://pubmed.ncbi.nlm.nih.gov/22217183/. DOI: 10.1186/1471-2202-13-3.
[32]
KOK T E, DOMINGO D, HASSAN J, et al. Resting-state networks in tinnitus: a scoping review[J]. Clin Neuroradiol, 2022, 32(4): 903-922. DOI: 10.1007/s00062-022-01170-1.
[33]
SCHMIDT S A, CARPENTER-THOMPSON J, HUSAIN F T. Connectivity of precuneus to the default mode and dorsal attention networks: a possible invariant marker of long-term tinnitus[J/OL]. Neuroimage Clin, 2017, 16: 196-204 [2024-02-22]. https://pubmed.ncbi.nlm.nih.gov/28794980/. DOI: 10.1016/j.nicl.2017.07.015.
[34]
LI W, MA X B, WANG Q, et al. Intrinsic network changes in bilateral tinnitus patients with cognitive impairment: a resting-state functional MRI study[J/OL]. Brain Sci, 2022, 12(8): 1049 [2024-02-22]. https://pubmed.ncbi.nlm.nih.gov/36009112/. DOI: 10.3390/brainsci12081049.
[35]
FAN T, GUAN P F, ZHONG X F, et al. Functional connectivity alterations and molecular characterization of the anterior cingulate cortex in tinnitus pathology without hearing loss[J/OL]. Adv Sci, 2024, 11(3): e2304709 [2024-02-22]. https://pubmed.ncbi.nlm.nih.gov/38009798/. DOI: 10.1002/advs.202304709.
[36]
SINGH A, SMITH P F, ZHENG Y W. Targeting the limbic system: insights into its involvement in tinnitus[J/OL]. Int J Mol Sci, 2023, 24(12): 9889 [2024-02-22]. https://pubmed.ncbi.nlm.nih.gov/37373034/. DOI: 10.3390/ijms24129889.
[37]
KAPOLOWICZ M R, THOMPSON L T. Plasticity in limbic regions at early time points in experimental models of tinnitus[J/OL]. Front Syst Neurosci, 2020, 13: 88 [2024-02-22]. https://pubmed.ncbi.nlm.nih.gov/32038184/. DOI: 10.3389/fnsys.2019.00088.
[38]
KIM J Y, KIM Y H, LEE S, et al. Alteration of functional connectivity in tinnitus brain revealed by resting-state fMRI? A pilot study[J]. Int J Audiol, 2012, 51(5): 413-417. DOI: 10.3109/14992027.2011.652677.
[39]
WEI X, LV H, CHEN Q, et al. Surface-based amplitude of low-frequency fluctuation alterations in patients with tinnitus before and after sound therapy: a resting-state functional magnetic resonance imaging study[J/OL]. Front Neurosci, 2021, 15: 709482 [2024-02-22]. https://pubmed.ncbi.nlm.nih.gov/34867147/. DOI: 10.3389/fnins.2021.709482.
[40]
LV H, CHEN Q, WEI X, et al. Sound therapy can modulate the functional connectivity of the auditory network[J/OL]. Prog Neuropsychopharmacol Biol Psychiatry, 2021, 110: 110323 [2024-02-22]. https://pubmed.ncbi.nlm.nih.gov/33838149/. DOI: 10.1016/j.pnpbp.2021.110323.
[41]
MA X Y, CHEN N X, WANG F Y, et al. Surface-based functional metrics and auditory cortex characteristics in chronic tinnitus[J/OL]. Heliyon, 2022, 8(10): e10989 [2024-02-22]. https://pubmed.ncbi.nlm.nih.gov/36276740/. DOI: 10.1016/j.heliyon.2022.e10989.
[42]
KIM J H, CHOI D S, PARK S E, et al. Preoperative localization of the sensorimotor cortex and measurement of tumor perfusion in a single acquisition using ASL technique[J/OL]. J Clin Neurosci, 2019, 59: 367-371 [2024-02-22]. https://pubmed.ncbi.nlm.nih.gov/30391311/. DOI: 10.1016/j.jocn.2018.10.098.
[43]
BARZGARI A, SOJKOVA J, MARITZA DOWLING N, et al. Arterial spin labeling reveals relationships between resting cerebral perfusion and motor learning in Parkinson's disease[J]. Brain Imaging Behav, 2019, 13(3): 577-587. DOI: 10.1007/s11682-018-9877-1.
[44]
ZHENG W M, CUI B, HAN Y, et al. Disrupted regional cerebral blood flow, functional activity and connectivity in Alzheimer's disease: a combined ASL perfusion and resting state fMRI study[J/OL]. Front Neurosci, 2019, 13: 738 [2024-02-22]. https://pubmed.ncbi.nlm.nih.gov/31396033/. DOI: 10.3389/fnins.2019.00738.
[45]
XU Z G, XU J J, CHEN Y C, et al. Aberrant cerebral blood flow in tinnitus patients with migraine: a perfusion functional MRI study[J/OL]. J Headache Pain, 2021, 22(1): 61 [2024-02-22]. https://pubmed.ncbi.nlm.nih.gov/34187358/. DOI: 10.1186/s10194-021-01280-0.
[46]
XU Z G, XU J J, HU J H, et al. Arterial spin labeling cerebral perfusion changes in chronic tinnitus with tension-type headache[J/OL]. Front Neurol, 2021, 12: 698539 [2024-02-22]. https://pubmed.ncbi.nlm.nih.gov/34512515/. DOI: 10.3389/fneur.2021.698539.
[47]
DUMKRIEGER G, CHONG C D, ROSS K, et al. Static and dynamic functional connectivity differences between migraine and persistent post-traumatic headache: a resting-state magnetic resonance imaging study[J]. Cephalalgia, 2019, 39(11): 1366-1381. DOI: 10.1177/0333102419847728.
[48]
CHEN C, YAN M Y, YU Y, et al. Alterations in regional homogeneity assessed by fMRI in patients with migraine without aura[J/OL]. J Med Syst, 2019, 43(9): 298 [2024-02-22]. https://pubmed.ncbi.nlm.nih.gov/31352647/. DOI: 10.1007/s10916-019-1425-z.
[49]
CHENG S R, XU G X, ZHOU J, et al. A multimodal meta-analysis of structural and functional changes in the brain of tinnitus[J/OL]. Front Hum Neurosci, 2020, 14: 28 [2024-02-22]. https://pubmed.ncbi.nlm.nih.gov/32161526/. DOI: 10.3389/fnhum.2020.00028.
[50]
ETKIN A, EGNER T, KALISCH R. Emotional processing in anterior cingulate and medial prefrontal cortex[J]. Trends Cogn Sci, 2011, 15(2): 85-93. DOI: 10.1016/j.tics.2010.11.004.
[51]
UEYAMA T, DONISHI T, UKAI S, et al. Brain regions responsible for tinnitus distress and loudness: a resting-state FMRI study[J/OL]. PLoS One, 2013, 8(6): e67778 [2024-02-22]. https://pubmed.ncbi.nlm.nih.gov/23825684/. DOI: 10.1371/journal.pone.0067778.
[52]
ZIMMERMAN B J, SCHMIDT S A, KHAN R A, et al. Decreased resting perfusion in precuneus and posterior cingulate cortex predicts tinnitus severity[J/OL]. Curr Res Neurobiol, 2021, 2: 100010 [2024-02-22]. https://pubmed.ncbi.nlm.nih.gov/36246506/. DOI: 10.1016/j.crneur.2021.100010.
[53]
HU J H, XU J J, SHANG S A, et al. Cerebral blood flow difference between acute and chronic tinnitus perception: a perfusion functional magnetic resonance imaging study[J/OL]. Front Neurosci, 2021, 15: 752419 [2024-02-22]. https://pubmed.ncbi.nlm.nih.gov/34675772/. DOI: 10.3389/fnins.2021.752419.
[54]
SCHMIDT S A, ZIMMERMAN B, BIDO MEDINA R O, et al. Changes in gray and white matter in subgroups within the tinnitus population[J/OL]. Brain Res, 2018, 1679: 64-74 [2024-02-22]. https://pubmed.ncbi.nlm.nih.gov/29158175/. DOI: 10.1016/j.brainres.2017.11.012.
[55]
RAUSCHECKER J P, LEAVER A M, MÜHLAU M. Tuning out the noise: limbic-auditory interactions in tinnitus[J]. Neuron, 2010, 66(6): 819-826. DOI: 10.1016/j.neuron.2010.04.032.
[56]
LAN L P, LI J H, CHEN Y H, et al. Alterations of brain activity and functional connectivity in transition from acute to chronic tinnitus[J]. Hum Brain Mapp, 2021, 42(2): 485-494. DOI: 10.1002/hbm.25238.
[57]
BROZOSKI T J, BAUER C A. Vigabatrin, a GABA transaminase inhibitor, reversibly eliminates tinnitus in an animal model[J]. J Assoc Res Otolaryngol, 2007, 8(1): 105-118. DOI: 10.1007/s10162-006-0067-2.
[58]
HAN S S, NAM E C, WON J Y, et al. Clonazepam quiets tinnitus: a randomised crossover study with Ginkgo biloba[J]. J Neurol Neurosurg Psychiatry, 2012, 83(8): 821-827. DOI: 10.1136/jnnp-2012-302273.
[59]
BUSTO U, SELLERS E M, NARANJO C A, et al. Withdrawal reaction after long-term therapeutic use of benzodiazepines[J]. N Engl J Med, 1986, 315(14): 854-859. DOI: 10.1056/NEJM198610023151403.
[60]
SEDLEY W, PARIKH J, EDDEN R A E, et al. Human auditory cortex neurochemistry reflects the presence and severity of tinnitus[J]. J Neurosci, 2015, 35(44): 14822-14828. DOI: 10.1523/JNEUROSCI.2695-15.2015.
[61]
CASPARY D M, MILBRANDT J C, HELFERT R H. Central auditory aging: GABA changes in the inferior colliculus[J]. Exp Gerontol, 1995, 30(3/4): 349-360. DOI: 10.1016/0531-5565(94)00052-5.
[62]
LEE A C, GODFREY D A. Current view of neurotransmitter changes underlying tinnitus[J]. Neural Regen Res, 2015, 10(3): 368-370. DOI: 10.4103/1673-5374.153680.
[63]
ISLER B, VON BURG N, KLEINJUNG T, et al. Lower glutamate and GABA levels in auditory cortex of tinnitus patients: a 2D-JPRESS MR spectroscopy study[J/OL]. Sci Rep, 2022, 12(1): 4068 [2024-02-22]. https://pubmed.ncbi.nlm.nih.gov/35260698/. DOI: 10.1038/s41598-022-07835-8.
[64]
WÓJCIK J, KOCHAŃSKI B, CIEŚLA K, et al. An MR spectroscopy study of temporal areas excluding primary auditory cortex and frontal regions in subjective bilateral and unilateral tinnitus[J/OL]. Sci Rep, 2023, 13(1): 18417 [2024-02-22]. https://pubmed.ncbi.nlm.nih.gov/37891242/. DOI: 10.1038/s41598-023-45024-3.
[65]
ZHANG L Q, WU C, MARTEL D T, et al. Noise exposure alters glutamatergic and GABAergic synaptic connectivity in the hippocampus and its relevance to tinnitus[J/OL]. Neural Plast, 2021, 2021: 8833087 [2024-02-22]. https://pubmed.ncbi.nlm.nih.gov/33510780/. DOI: 10.1155/2021/8833087.
[66]
CACACE A T, HU J N, ROMERO S, et al. Glutamate is down-regulated and tinnitus loudness-levels decreased following rTMS over auditory cortex of the left hemisphere: a prospective randomized single-blinded sham-controlled cross-over study[J/OL]. Hear Res, 2018, 358: 59-73 [2024-02-22]. https://pubmed.ncbi.nlm.nih.gov/29150051/. DOI: 10.1016/j.heares.2017.10.017.
[67]
ZÖLLNER H J, POVAŽAN M, HUI S C N, et al. Comparison of different linear-combination modeling algorithms for short-TE proton spectra[J]. NMR Biomed, 2021, 34(4): e4482. DOI: 10.1002/nbm.4482.
[68]
MEYER M, NEFF P, LIEM F, et al. Differential tinnitus-related neuroplastic alterations of cortical thickness and surface area[J/OL]. Hear Res, 2016, 342: 1-12 [2024-02-22]. https://pubmed.ncbi.nlm.nih.gov/27671157/. DOI: 10.1016/j.heares.2016.08.016.

PREV Research progress of magnetic resonance diffusion tensor imaging in glioma grading and genotype prediction
NEXT Research progress of functional magnetic resonance imaging and artificial intelligence in evaluating the staging of nasopharyngeal carcinoma
  


LINK


Tel & Fax: +8610-67113815    E-mail: editor@cjmri.cn