Skip to main content
SpringerLink
Log in

Abnormal Functional Connectivity Within Default Mode Network and Salience Network Related to Tinnitus Severity

Journal of the Association for Research in Otolaryngology volume 24, pages 453–462 (2023)Cite this article

Abstract

Background

Previous studies have demonstrated that tinnitus is associated with neural changes in the cerebral cortex. This study is aimed at investigating the central nervous characteristics of tinnitus patients with different severity by using a rs-EEG.

Participants and Methods

rs-EEG was recorded in fifty-seven patients with chronic tinnitus and twenty-seven healthy controls. Tinnitus patients were divided into moderate-to-severe tinnitus group and slight-to-mild tinnitus group based on their Tinnitus Handicap Inventory (THI) scores. Source localization and functional connectivity analyses were used to measure the changes in central levels and examine the altered network patterns. The correlation between functional connectivity and tinnitus severity was analyzed.

Result

Compared to the healthy controls, all tinnitus patients showed significant activation in the auditory cortex (middle temporal lobe, BA 21), while moderate-to-severe tinnitus group showed enhanced connectivity between the parahippocampus and posterior cingulate gyrus. Moreover, the moderate-to-severe tinnitus group had enhanced functional connectivity between auditory cortex and insula compared to the slight-to-mild tinnitus group. The connections between the insula and the parahippocampal and posterior cingulate gyrus were positively correlated with THI scores.

Conclusion

The current study reveals that patients with moderate-to-severe tinnitus demonstrate greater changes in the central brain areas, including the auditory cortex, insula, parahippocampus and posterior cingulate gyrus. In addition, enhanced connections were found between the insula and the auditory cortex, as well as the posterior cingulate gyrus and the parahippocampus, which suggests abnormality in the auditory network, salience network, and default mode network. Specifically, the insula is the core region of the neural pathway that is composed of the auditory cortex, insula, and parahippocampus/posterior cingulate gyrus. This suggests that the severity of tinnitus is affected by multiple brain regions.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Availability of Data and Materials

The original contributions presented in this study are included in the article/material; further inquiries can be directed to the corresponding authors.

References

  1. Tunkel DE et al (2014) Clinical practice guideline: tinnitus. Otolaryngol Head Neck Surg 151(2):1–40

    PubMed  Google Scholar 

  2. Yang H et al (2018) Prevalence and factors associated with tinnitus: data from adult residents in Guangdong province. South of China Int J Audiol 57(12):892–899

    PubMed  Google Scholar 

  3. Kim HJ et al (2015) Analysis of the prevalence and associated risk factors of tinnitus in adults. PLoS ONE 10(5):e0127578

    Article  PubMed  PubMed Central  Google Scholar 

  4. Reavis KM et al (2020) Prevalence of self-reported depression symptoms and perceived anxiety among community-dwelling U.S. adults reporting tinnitus. PerspectASHA SIGs 5(4):959–970

  5. Tegg-Quinn S et al (2016) The impact of tinnitus upon cognition in adults: a systematic review. Int J Audiol 55(10):533–540

    Article  PubMed  Google Scholar 

  6. Schecklmann M et al (2013) Neural correlates of tinnitus duration and distress: a positron emission tomography study. Hum Brain Mapp 34(1):233–240

    Article  PubMed  Google Scholar 

  7. Burton H et al (2012) Altered networks in bothersome tinnitus: a functional connectivity study. BMC Neurosci 13:3

    Article  PubMed  PubMed Central  Google Scholar 

  8. Maudoux A et al (2012) Auditory resting-state network connectivity in tinnitus: a functional MRI study. PLoS ONE 7(5):e36222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. De Ridder D et al (2022) Tinnitus and the triple network model: a perspective. Clin Exp Otorhinolaryngol 15(3):205–212

    Article  PubMed  PubMed Central  Google Scholar 

  10. Vanneste S et al (2010) The neural correlates of tinnitus-related distress. Neuroimage 52(2):470–480

    Article  PubMed  Google Scholar 

  11. Elgoyhen AB et al (2014) Identifying tinnitus-related genes based on a side-effect network analysis. CPT Pharmacometrics Syst Pharmacol 3(1):e97

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Joos K et al (2014) Polarity specific suppression effects of transcranial direct current stimulation for tinnitus. Neural Plast 2014:930860

    Article  PubMed  PubMed Central  Google Scholar 

  13. Uddin LQ (2015) Salience processing and insular cortical function and dysfunction. Nat Rev Neurosci 16(1):55–61

    Article  CAS  PubMed  Google Scholar 

  14. Husain FT, Schmidt SA (2014) Using resting state functional connectivity to unravel networks of tinnitus. Hear Res 307:153–162

    Article  PubMed  Google Scholar 

  15. Schmidt SA, Carpenter-Thompson J, Husain FT (2017) Connectivity of precuneus to the default mode and dorsal attention networks: a possible invariant marker of long-term tinnitus. Neuroimage Clinical 16:196–204

  16. Han JJ, et al (2020) Pre-treatment ongoing cortical oscillatory activity predicts improvement of tinnitus after partial peripheral reafferentation with hearing aids. Front Neurosci 14:410

  17. Shahsavarani S et al (2021) Salience, emotion, and attention: the neural networks underlying tinnitus distress revealed using music and rest. Brain Res 1755:147277

    Article  CAS  PubMed  Google Scholar 

  18. Cai Y et al (2019) Inhibition of brain area and functional connectivity in idiopathic sudden sensorineural hearing loss with tinnitus, based on resting-state EEG. Front Neurosci 13:851

    Article  PubMed  PubMed Central  Google Scholar 

  19. De Ridder D, Congedo M, Vanneste S (2015) The neural correlates of subjectively perceived and passively matched loudness perception in auditory phantom perception. Brain Behav 5(5):e00331

    Article  PubMed  PubMed Central  Google Scholar 

  20. Newman CW, Sandridge SA, Jacobson GP (1998) Psychometric adequacy of the Tinnitus Handicap Inventory (THI) for evaluating treatment outcome. J Am Acad Audiol 9(2):153–160

    CAS  PubMed  Google Scholar 

  21. Lan L et al (2021) Alterations of brain activity and functional connectivity in transition from acute to chronic tinnitus. Hum Brain Mapp 42(2):485–494

    Article  PubMed  Google Scholar 

  22. Pascual-Marqui RD (2002) Standardized low-resolution brain electromagnetic tomography (sLORETA): technical details. Methods Find Exp Clin Pharmacol  24:5–12

  23. Pascual-Marqui RD et al (1952) Assessing interactions in the brain with exact low-resolution electromagnetic tomography. Philos Trans A Math Phys Eng Sci 2011 369(1952):3768–3784

    Google Scholar 

  24. Pascual-Marqui RD (2007) Discrete, 3D distributed, linear imaging methods of electric neuronal activity. Part 1: exact, zero error localization

  25. Vanneste S, Song JJ, De Ridder D (2018) Thalamocortical dysrhythmia detected by machine learning. Nat Commun 9(1):1103

    Article  PubMed  PubMed Central  Google Scholar 

  26. Friston KJ (2011) Functional and effective connectivity: a review. Brain Connect 1(1):13–36

    Article  PubMed  Google Scholar 

  27. Milz P et al (2014) sLORETA intracortical lagged coherence during breath counting in meditation-naive participants. Front Hum Neurosci 8:303

    Article  PubMed  PubMed Central  Google Scholar 

  28. Song JJ et al (2015) Onset-related differences in neural substrates of tinnitus-related distress: the anterior cingulate cortex in late-onset tinnitus, and the frontal cortex in early-onset tinnitus. Brain Struct Funct 220(1):571–584

    Article  PubMed  Google Scholar 

  29. Nichols TE, Holmes AP (2002) Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum Brain Mapp 15(1):1–25

    Article  PubMed  Google Scholar 

  30. Uddin LQ et al (2017) Structure and function of the human insula. J Clin Neurophysiol 34(4):300–306

    Article  PubMed  PubMed Central  Google Scholar 

  31. Bamiou DE, Musiek FE, Luxon LM (2003) The insula (Island of Reil) and its role in auditory processing. Literature review. Brain Res Rev 42(2):143–154

  32. Roberts KL, Hall DA (2008) Examining a supramodal network for conflict processing: a sytematic review and novel functional magnetic resonance imaging data for related visual and auditory stroop tasks. J Cogn Neurosci 20(6):1063–1078

  33. Leaver AM et al (2012) Cortico-limbic morphology separates tinnitus from tinnitus distress. Front Syst Neurosci 6:21

    Article  PubMed  PubMed Central  Google Scholar 

  34. Vanneste S, De Ridder D (2013) Brain areas controlling heart rate variability in tinnitus and tinnitus-related distress. PLoS ONE 8(3):e59728

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Chen YC et al (2015) Altered intra- and interregional synchronization in resting-state cerebral networks associated with chronic tinnitus. Neural Plast 2015:475382

    Article  PubMed  PubMed Central  Google Scholar 

  36. Demertzi A, Soddu A, Laureys S (2013) Consciousness supporting networks. Curr Opin Neurobiol 23(2):239–244

    Article  CAS  PubMed  Google Scholar 

  37. Gasquoine PG (2014) Contributions of the insula to cognition and emotion. Neuropsychol Rev 24(2):77–87

    Article  PubMed  Google Scholar 

  38. Chiong W et al (2013) The salience network causally influences default mode network activity during moral reasoning. Brain 136(Pt 6):1929–1941

    Article  PubMed  PubMed Central  Google Scholar 

  39. Catani M et al (2012) Beyond cortical localization in clinico-anatomical correlation. Cortex 48(10):1262–1287

    Article  PubMed  Google Scholar 

  40. Elgoyhen AB et al (2015) Tinnitus: perspectives from human neuroimaging. Nat Rev Neurosci 16(10):632–642

    Article  CAS  PubMed  Google Scholar 

  41. Greicius MD et al (2003) Functional connectivity in the resting brain: a network analysis of the default mode hypothesis. Proc Natl Acad Sci USA 100(1):253–258

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This research was supported by the Project Fund of Zhuhai Science and Technology Innovation Bureau in 2022 (project number: 222000400085); National Natural Science Foundation of China (82271165 and 82071062); Key R&D Program of Guangdong Province, China (grant no. 2018B030339001); and Guangdong Basic and Applied Basic Research Foundation (grant no. 2021A1515012038).

Author information

Author notes

  1. Binbin Xiong and Zhao Liu contributed equally to this work.

Authors and Affiliations

  1. Zhuhai Hospital Affiliated with Jinan University, Zhuhai, Guangdong, 519000, China

    Binbin Xiong

  2. Center for Hearing and Balance, Zhuhai Hospital of Integrated of Traditional Chinese Medicine and Western Medicine, Zhuhai, Guangdong, 519000, China

    Binbin Xiong, Zhao Liu, Jing Yang & Wenqiang Xu

  3. The First Clinical Medical College of Jinan University, Guangzhou, 510630, China

    Jiahong Li, Xiayin Huang & Yiqing Zheng

  4. Sun Yat-sen Memorial Hospital, Sun Yat-sen University, 107 Yan Jiang West Road, 510120, Guangzhou, China

    Jiahong Li, Xiayin Huang, Yuexin Cai & Yiqing Zheng

  5. Department of Otolaryngology, Sun Yat-sen Memorial Hospital, Sun Yat-sen University, Guangzhou City, Guangdong Province, China

    Yuexin Cai & Yiqing Zheng

  6. Department of Radiology, Nanjing First Hospital, Nanjing Medical University, Nanjing, China

    Yu-Chen Chen

Authors
  1. Binbin Xiong
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhao Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jiahong Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xiayin Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jing Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Wenqiang Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yu-Chen Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Yuexin Cai
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Yiqing Zheng
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

YXC and YQZ contributed to designing the research studies; YXC, BBX contributed to conducting the experiments; JHL and XYH contributed to acquiring the data; JHL, YJ, WQX, and CYC contributed to the analysis of the data; BBX, ZL, YXC, and CYC contributed to the interpretation of the data and the result. BBX and ZL contributed to the drafting of the article. All authors have revised the manuscript critically for important intellectual content, read, and approved the final manuscript.

Corresponding authors

Correspondence to Yuexin Cai or Yiqing Zheng.

Ethics declarations

Competing Interests

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xiong, B., Liu, Z., Li, J. et al. Abnormal Functional Connectivity Within Default Mode Network and Salience Network Related to Tinnitus Severity. JARO 24, 453–462 (2023). https://doi.org/10.1007/s10162-023-00905-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10162-023-00905-2

Keywords

search

Navigation