Skip to main content
SpringerLink
Log in

Lateralization effects in brain white matter reorganization in patients with unilateral idiopathic tinnitus: a preliminary study

  • Original Research
  • Published:
Brain Imaging and Behavior Aims and scope Submit manuscript

Abstract

Idiopathic tinnitus can cause significant auditory-related brain structural and functional changes in patients. However, changes in patterns of the lateralization effects in idiopathic tinnitus have yet to be established, especially on white matter (WM) reorganization. In this study, we studied 19 left-sided and 19 right-sided idiopathic tinnitus (LSIT, RSIT) patients and 19 healthy controls (HCs). We combined applied voxel-based morphometry (VBM) and tract-based spatial statistics (TBSS) analyses to investigate altered features of the auditory-related brain WM. We also conducted correlation analyses between the clinical variables and WM changes in the patients. Compared with the HCs, both sided tinnitus patients showed significant auditory-related brain WM alterations. More interestingly, the LSIT patients demonstrated a greater decrease in white matter volume (WMV) in the right medial superior frontal gyrus (SFG) than the RSIT; meanwhile, we also found that compared with the RSIT group, the LSIT group showed significantly increased fractional anisotropy (FA) in the body of the corpus callosum (CC), left cingulum, and right superior longitudinal fasciculus (SLF) and decreased mean diffusivity (MD) in the body of CC. Moreover, relative to the RSIT group, the LSIT group also exhibited increases in WM axial diffusivity (AD) in the left SLF, left cingulum, right middle cerebellar peduncle (MCP), left thalamus, and bilateral forceps major (FM) and decreases in radial diffusivity (RD) in the genu of CC. Additionally, the FA value of the right SLF was closely associated with tinnitus severity in the LSIT. Our study suggests that lateralization has a significant effect on WM reorganization in patients with idiopathic tinnitus; in particular, LSIT patients may experience more severe and widespread alterations in WMV and WM microstructure than the RSIT group, and all these changes are indirectly auditory related. These findings provide new useful information that can lead to a better understanding of the tinnitus mechanisms.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

Data availability

The datasets generated for this study are available on request to the corresponding author.

Abbreviations

LSIT:

left-sided idiopathic tinnitus

RSIT:

right-sided idiopathic tinnitus

HCs:

healthy controls

VBM:

voxel-based morphometry

DTI:

diffusion tensor imaging

TBSS:

tract-based spatial statistics

WMV:

white matter volume

CSF:

cerebrospinal fluid

THI:

tinnitus handicap inventory

MNI:

Montreal Neurological Institute

WMV:

white matter volume

WM:

white matter

FA:

fractional anisotropy

MD:

mean diffusivity

AD:

axial diffusivity

RD:

radial diffusivity

SFG:

superior frontal gyrus

CC:

corpus callosum

MCP:

middle cerebellar peduncle

SLF:

superior longitudinal fasciculus

References

  • Ashburner, J. (2007). A fast diffeomorphic image registration algorithm. Neuroimage, 38, 95–113.

    Article  PubMed  Google Scholar 

  • Baguley, D., McFerran, D., & Hall, D. (2013). Tinnitus. Lancet, 382, 1600–1607.

    Article  Google Scholar 

  • Benson, R. R., Gattu, R., & Cacace, A. T. (2014). Left hemisphere fractional anisotropy increase in noise-induced tinnitus: A diffusion tensor imaging (DTI) study of white matter tracts in the brain. Hearing Research, 309, 8–16.

    Article  PubMed  Google Scholar 

  • Bledsoe, I. O., Stebbins, G. T., Merkitch, D., & Goldman, J. G. (2018). White matter abnormalities in the corpus callosum with cognitive impairment in Parkinson disease. Neurology, 91, e2244–e2255.

    Article  PubMed  PubMed Central  Google Scholar 

  • Boyen, K., Langers, D. R. M., de Kleine, E., & van Dijk, P. (2013). Gray matter in the brain: Differences associated with tinnitus and hearing loss. Hearing Research, 295, 67–78.

    Article  PubMed  Google Scholar 

  • Catani, M., Howard, R. J., Pajevic, S., & Jones, D. K. (2002). Virtual in vivo interactive dissection of white matter fasciculi in the human brain. Neuroimage, 17, 77–94.

    Article  PubMed  Google Scholar 

  • Çavdar, S., Özgür, M., Kuvvet, Y., Bay, H., & Aydogmus, E. (2018). Cortical, subcortical and brain stem connections of the cerebellum via the superior and middle cerebellar peduncle in the rat. The Journal of Integrative Neuroscience, 17, 609–618.

    Article  PubMed  Google Scholar 

  • Chen, Q., Wang, Z., Lv, H., Zhao, P., Yang, Z., Gong, S., & Wang, Z. (2020). Reorganization of brain white matter in persistent idiopathic tinnitus patients without hearing loss: evidence from baseline data. Frontiers in Neuroscience-Switz, 4, 591.

    Article  Google Scholar 

  • Chen, Y., Xia, W., Luo, B., Muthaiah, V. P. K., Xiong, Z., Zhang, J., Wang, J., Salvi, R., & Teng, G. (2015). Frequency-specific alternations in the amplitude of low-frequency fluctuations in chronic tinnitus. Frontiers in Neural Circuits, 9, 67.

    Article  PubMed  PubMed Central  Google Scholar 

  • Crippa, A., Lanting, C., Dijk, P. V., & Roerdink, J. B. T. M. (2010). A diffusion tensor imaging study on the auditory system and tinnitus. The Open Neuroimaging Journal, 4, 16–25.

    Article  PubMed  PubMed Central  Google Scholar 

  • Diesch, E. (2012). Structural changes of the corpus callosum in tinnitus. Frontiers in Systems Neuroscience, 6, 17.

    PubMed  PubMed Central  Google Scholar 

  • Dong, C., Zhao, P., Yang, J., Liu, Z., & Wang, Z. (2015). Incidence of vascular anomalies and variants associated with unilateral venous pulsatile tinnitus in 242 patients based on dual-phase contrast-enhanced computed tomography. Chinese Medical Journal-Peking, 128, 581–585.

    Article  Google Scholar 

  • Eggermont, J. J., & Roberts, L. E. (2004). The neuroscience of tinnitus. Trends in Neurosciences, 27, 676–682.

    Article  CAS  PubMed  Google Scholar 

  • Elgoyhen, A. B., Langguth, B., De Ridder, D., & Vanneste, S. (2015). Tinnitus: perspectives from human neuroimaging. Nature Reviews Neuroscience, 16, 632–642.

    Article  CAS  PubMed  Google Scholar 

  • Fabri, M., Pierpaoli, C., Barbaresi, P., & Polonara, G. (2014). Functional topography of the corpus callosum investigated by DTI and fMRI. World Journal of Radiology, 6, 895–906.

    Article  PubMed  PubMed Central  Google Scholar 

  • Han, L., Na, Z., Chunli, L., Yuchen, C., Pengfei, Z., Hao, W., Xu, C., Peng, Z., Zheng, W., Zhenghan, Y., Shusheng, G., & Zhenchang, W. (2019). Baseline functional connectivity features of neural network nodes can predict improvement after sound therapy through adjusted narrow band noise in tinnitus patients. Frontiers in Neuroscience, 13, 614.

    Article  PubMed  PubMed Central  Google Scholar 

  • Han, L., Yawen, L., Hao, W., Chunli, L., Pengfei, Z., Zhengyu, Z., Zhaodi, W., Zhenghan, Y., Shusheng, G., & Zhenchang, W. (2019). Effects of sound therapy on resting-state functional brain networks in patients with tinnitus: A graph-theoretical-based study. Journal of Magnetic Resonance Imaging, 50, 1731–1741.

    Article  PubMed  Google Scholar 

  • Husain, F. T., Medina, R. E., Davis, C. W., Szymko-Bennett, Y., Simonyan, K., Pajor, N. M., & Horwitz, B. (2011). Neuroanatomical changes due to hearing loss and chronic tinnitus: A combined VBM and DTI study. Brain Research, 1369, 74–88.

    Article  CAS  PubMed  Google Scholar 

  • Husain, F. T., Zimmerman, B., Tai, Y., Finnegan, M. K., Kay, E., Khan, F., Menard, C., & Gobin, R. L. (2019). Assessing mindfulness-based cognitive therapy intervention for tinnitus using behavioural measures and structural MRI: a pilot study. INT J AUDIOL, 58, 889–901.

    Article  PubMed  Google Scholar 

  • Kan, Y., Wang, W., Zhang, S., Ma, H., Wang, Z., & Yang, J. (2019). Neural metabolic activity in idiopathic tinnitus patients after repetitive transcranial magnetic stimulation. The World Journal of Clinical Cases, 7, 1582–1590.

    Article  PubMed  Google Scholar 

  • Krick, C. M., Grapp, M., Daneshvar-Talebi, J., Reith, W., Plinkert, P. K., & Bolay, H. V. (2015). Cortical reorganization in recent-onset tinnitus patients by the Heidelberg Model of Music Therapy. Frontiers in Neuroscience-Switz, 9, 49.

    Google Scholar 

  • Lansley, J. A., Tucker, W., Eriksen, M. R., Riordan-Eva, P., & Connor, S. E. J. (2017). Sigmoid sinus diverticulum, dehiscence, and venous sinus stenosis: potential causes of pulsatile tinnitus in patients with idiopathic intracranial hypertension? American Journal of Neuroradiology, 38, 1783–1788.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lanting, C. P., De Kleine, E., Bartels, H., & Van Dijk, P. (2008). Functional imaging of unilateral tinnitus using fMRI. Acta Oto-Laryngologica, 128, 415–421.

    Article  CAS  PubMed  Google Scholar 

  • Lanting, C. P., de Kleine, E., Langers, D. R. M., & van Dijk, P. (2014). Unilateral tinnitus: changes in connectivity and response lateralization measured with fMRI. PloS One, 9, e110704.

  • Leaver, A. M., Renier, L., Chevillet, M. A., Morgan, S., Kim, H. J., & Rauschecker, J. P. (2011). Dysregulation of limbic and auditory networks in tinnitus. Neuron, 69, 33–43.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee, S., Song, S., Park, S. J., Park, H. G., Choi, B. Y., Koo, J., & Song, J. (2019a). Jugular bulb resurfacing with bone cement for patients with high dehiscent jugular bulb and ipsilateral pulsatile tinnitus. Otology & Neurotology, 40, 192–199.

    Article  Google Scholar 

  • Lee, S., Rhee, J., Shim, Y. J., Kim, Y., Koo, J., De Ridder, D., Vanneste, S., & Song, J. (2019b). Changes in the resting-state cortical oscillatory activity 6 months after modified tinnitus retraining therapy. Frontiers in Neuroscienc-Switz, 13, 1123.

    Article  Google Scholar 

  • Liu, Y., Lv, H., Zhao, P., Liu, Z., Chen, W., Gong, S., Wang, Z., & Zhu, J. (2018). Neuroanatomical alterations in patients with early stage of unilateral pulsatile tinnitus: a voxel-based morphometry study. Neural Plasticity, 2018, 1–7.

    Google Scholar 

  • Lv, H., Liu, C., Wang, Z., Zhao, P., Cheng, X., Yang, Z., Gong, S., & Wang, Z. (2020). Altered functional connectivity of the thalamus in tinnitus patients is correlated with symptom alleviation after sound therapy. Brain Imaging and Behavior, 14(6), 2668-2678

  • Lv, H., Zhao, P., Liu, Z., Liu, X., Ding, H., Liu, L., Wang, G., Xie, J., Zeng, R., Chen, Y., Yang, Z., Gong, S., & Wang, Z. (2018). Lateralization effects on functional connectivity of the auditory network in patients with unilateral pulsatile tinnitus as detected by functional MRI. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 81, 228–235.

    Article  PubMed  Google Scholar 

  • Makris, N., Kennedy, D. N., McInerney, S., Sorensen, A. G., Wang, R., Caviness, V. S., & Pandya, D. N. (2005). Segmentation of subcomponents within the superior longitudinal fascicle in humans: a quantitative, in vivo, DT-MRI study. Cerebral Cortex, 15, 854–869.

    Article  PubMed  Google Scholar 

  • Matsuda, Y., Inagawa, T., & Amano, T. (1993). A case of tinnitus and hearing loss after cerebellar hemorrhage. Stroke, 24, 906–908.

    Article  CAS  PubMed  Google Scholar 

  • Melcher, J. R., Levine, R. A., Bergevin, C., & Norris, B. (2009). The auditory midbrain of people with tinnitus: Abnormal sound-evoked activity revisited. Hearing Research, 257, 63–74.

    Article  PubMed  PubMed Central  Google Scholar 

  • Mirz, F., Gjedde, A., Sdkilde-Jrgensen, H., & Pedersen, C. B. (2000). Functional brain imaging of tinnitus-like perception induced by aversive auditory stimuli. Neuroreport, 11, 633–637.

    Article  CAS  PubMed  Google Scholar 

  • Mtui, E., Gruener, G., & Dockery, P. (2016). Fitzgerald’s clinical neuroanatomy and neuroscience. [Electronic Resource] (7th ed.). Elsevier.

  • Mundada, P., Singh, A., & Lingam, R. K. (2015). CT arteriography and venography in the evaluation of Pulsatile tinnitus with normal otoscopic examination. The Laryngoscope, 125, 979–984.

    Article  PubMed  Google Scholar 

  • Newman, C. W., Jacobson, G. P., & Spitzer, J. B. (1996). Development of the tinnitus handicap inventory. Archives of Otolaryngology–Head & Neck Surgery, 122, 143.

  • Raya, J. G., Horng, A., Dietrich, O., Krasnokutsky, S., Beltran, L. S., Storey, P., Reiser, M. F., Recht, M. P., Sodickson, D. K., & Glaser, C. (2012). Articular cartilage: in vivo diffusion-tensor imaging. Radiology, 262, 550–559.

    Article  PubMed  Google Scholar 

  • Ryu, C., Park, M. S., Byun, J. Y., Jahng, G., & Park, S. (2016). White matter integrity associated with clinical symptoms in tinnitus patients: A tract-based spatial statistics study. European Radiology, 26, 2223–2232.

    Article  PubMed  Google Scholar 

  • Schmidt, S. A., Carpenter-Thompson, J., & Husain, F. T. (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.

    Article  Google Scholar 

  • Schmidt, S. A., Zimmerman, B., Bido Medina, R. O., Carpenter-Thompson, J. R., & Husain, F.T. (2018). Changes in gray and white matter in subgroups within the tinnitus population. BRAIN RES, 1679, 64–74.

    Article  CAS  PubMed  Google Scholar 

  • Schoeff, S., Nicholas, B., Mukherjee, S., & Kesser, B. W. (2014). Imaging prevalence of sigmoid sinus dehiscence among patients with and without pulsatile tinnitus. Otolaryngology–Head and Neck Surgery, 150, 841–846.

    Article  PubMed  Google Scholar 

  • Shelton, A. L., Cornish, K. M., Godler, D., Bui, Q. M., Kolbe, S., & Fielding, J. (2017). White matter microstructure, cognition, and molecular markers in fragile X premutation females. Neurology, 88, 2080–2088.

    Article  CAS  PubMed  Google Scholar 

  • Shim, Y. J., Bae, Y. J., An, G. S., Lee, K., Kim, Y., Lee, S., Choi, B. Y., Choi, B. S., Kim, J. H., Koo, J., & Song, J. (2019). Involvement of the internal auditory canal in subjects with cochlear otosclerosis. Otology & Neurotology, 40, e186–e190.

    Article  Google Scholar 

  • Smith, S. M., Jenkinson, M., Johansen-Berg, H., Rueckert, D., Nichols, T. E., Mackay, C. E., Watkins, K. E., Ciccarelli, O., Cader, M. Z., Matthews, P. M., & Behrens, T. E. J. (2006). Tract-based spatial statistics: Voxelwise analysis of multi-subject diffusion data. Neuroimage, 31, 1487–1505.

    Article  PubMed  Google Scholar 

  • Vanneste, S., Joos, K., & De Ridder, D. (2012). Prefrontal cortex based sex differences in tinnitus perception: same tinnitus intensity, same tinnitus distress, different mood. PLoS One, 7, e31182.

  • Xie, X., Liu, Y., Han, X., Liu, P., Qiu, H., Li, J., & Yu, H. (2019). Differences in intrinsic brain abnormalities between patients with left- and right-sided long-term hearing impairment. Frontiers in Neuroscience-Switz, 13, 206

  • Xue, C., Shi, L., Hui, S. C. N., Wang, D., Lam, T. P., Ip, C. B., Ng, B. K. W., Cheng, J. C. Y., & Chu, W. C. W. (2018). Altered white matter microstructure in the corpus callosum and its cerebral interhemispheric tracts in adolescent idiopathic scoliosis: diffusion tensor imaging analysis. American Journal of Neuroradiology, 39, 1177–1184.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors thank the patients and healthy volunteers who participated in this study and gave generously of their time.

Funding

This work was supported by Grant No.61801311, 61931013 from the National Natural Science Foundation of China, No. [2015] 160 from Beijing Scholars Program, Grant No. 7182044 from Beijing Natural Science Foundation, No. PX2018001 from Beijing Hospitals Authority, QML20180103 from Beijing Hospitals Authority Youth Programme, No. YYZZ2017B01 from Beijing Friendship Hospital, Capital Medical University, No. 2019M660717 from China Postdoctoral Science Foundation and No. 2020-Z2-023 from Beijing Postdoctoral Research Foundation.

Author information

Authors and Affiliations

  1. Department of Radiology, Beijing Friendship Hospital, Capital Medical University, 95 Yongan Road, Xicheng District, Beijing, People’s Republic of China

    Qian Chen, Han Lv, Xuan Wei, Pengfei Zhao, Zhenghan Yang & Zhenchang Wang

  2. Department of Otolaryngology Head and Neck Surgery, Beijing Friendship Hospital, Capital Medical University, 95 Yongan Road, Xicheng District, Beijing, People’s Republic of China

    Zhaodi Wang & Shusheng Gong

Authors
  1. Qian Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Han Lv
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zhaodi Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xuan Wei
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Pengfei Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Zhenghan Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Shusheng Gong
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Zhenchang Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

QC and HL* conducted the research project and conceived the study. QC wrote the manuscript. ZDW/XW/PFZ/ZHY/SSG provided technical and clinical support. HL* and ZCW* reviewed the manuscript and agree to be accountable for all aspects of the work.

Corresponding authors

Correspondence to Han Lv or Zhenchang Wang.

Ethics declarations

Ethical approval

This study was approved by the Institutional Review Board (IRB) of Beijing Friendship Hospital, Capital Medical University (Beijing, China) (IRB number: 2016-P2-012), and written informed consent was obtained from each subject before the study in accordance with the Declaration of Helsinki. 

Consent to participate

All the authors consent to the participation in this study.

Consent to publish

All the authors agreed with the publication of this article.

Conflict of interest

The authors declare no conflicts of interest.

Additional information

Publisher’s note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chen, Q., Lv, H., Wang, Z. et al. Lateralization effects in brain white matter reorganization in patients with unilateral idiopathic tinnitus: a preliminary study. Brain Imaging and Behavior 16, 11–21 (2022). https://doi.org/10.1007/s11682-021-00472-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11682-021-00472-1

Keywords

Search

Navigation