Neuroanatomical Alterations in Patients With Tinnitus Before and After Sound Therapy: A Voxel-Based Morphometry Study
Xuan Wei, Han Lv, Zhaodi Wang, Chunli Liu, Pengling Ren, Peng Zhang, Qian Chen, Yawen Liu, Pengfei Zhao, Shusheng Gong, Zhenghan Yang, Zhenchang Wang, Xuan Wei, Han Lv, Zhaodi Wang, Chunli Liu, Pengling Ren, Peng Zhang, Qian Chen, Yawen Liu, Pengfei Zhao, Shusheng Gong, Zhenghan Yang, Zhenchang Wang
Abstract
According to previous studies, many neuroanatomical alterations have been detected in patients with tinnitus. However, few studies have reported on the morphological changes observed following sound therapy. To explore the brain anatomical alterations in patients with idiopathic tinnitus using voxel-based morphometry (VBM) analysis before and after effective 12 weeks sound therapy. The protocol was registered on ClinicalTrials.gov, ID: NCT02774122. In this study, we collected data from 27 matched healthy control (HC) individuals and 27 idiopathic tinnitus patients before and after 12 weeks of sound therapy by using adjusted narrow band sound. 3.0T MRI system and high-resolution 3D structural images were acquired with a 3D-BRAVO pulse sequence. Structural image data preprocessing was performed using the VBM8 toolbox. The Tinnitus Handicap Inventory (THI) score was acquired in the tinnitus group to assess the severity of tinnitus and tinnitus-related distress. Mann-Whitney U Test, Wilcoxon Signed-Ranks test, and Pearson's correlation analysis were used in the statistical analysis. We found significantly decreased gray matter (GM) volume in the left thalami, right thalami, and cochlear nucleus among the tinnitus patients before sound therapy (baseline) compared to the HC group. However, we did not find significant differences in brain regions between the 12-week treatment and HC groups. According to the results of Wilcoxon Signed-Ranks test, the 12-week sound therapy group demonstrated significant greater brain volume compared with the baseline group among these brain regions. Decreased THI score and changed GM volume were not correlated. This is a useful study for observing the characteristics of neuroanatomical changes in patients with idiopathic tinnitus before and after sound treatment. The study characterized the effect of sound therapy on brain volume. It found that sound therapy had a normalizing effect on the bilateral thalami and cochlear nucleus. Clinical Trial Registration: www.ClinicalTrials.gov, NCT02774122.
Keywords: functional magnetic resonance imaging; sound therapy; thalamus; tinnitus; voxel-based morphometry.
Copyright © 2020 Wei, Lv, Wang, Liu, Ren, Zhang, Chen, Liu, Zhao, Gong, Yang and Wang.
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References
- Adjamian P., Hall D. A., Palmer A. R., Allan T. W., Langers D. R. (2014). Neuroanatomical abnormalities in chronic tinnitus in the human brain. Neurosci. Biobehav. Rev. 45 119–133. 10.1016/j.neubiorev.2014.05.013
- Ashburner J., Friston K. J. (2000). Voxel-based morphometry–the methods. Neuroimage 11(6 Pt 1), 805–821. 10.1006/nimg.2000.0582
- Axelsson A., Prasher D. (2000). Tinnitus induced by occupational and leisure noise. Noise Health 2 47–54.
- Baguley D., McFerran D., Hall D. (2013). Tinnitus. Lancet 382 1600–1607. 10.1016/S0140-6736(13)60142-7
- Berlot E., Arts R., Smit J., George E., Gulban O. F., Moerel M., et al. (2020). A 7 Tesla fMRI investigation of human tinnitus percept in cortical and subcortical auditory areas. Neuroimage Clin. 25 102166. 10.1016/j.nicl.2020.102166
- Boyen K., Langers D. R., de Kleine E., van Dijk P. (2013). Gray matter in the brain: differences associated with tinnitus and hearing loss. Hear. Res. 295 67–78. 10.1016/j.heares.2012.02.010
- Cheng S., Xu G., Zhou J., Qu Y., Li Z., He Z., et al. (2020). A multimodal meta-analysis of structural and functional changes in the brain of tinnitus. Front. Hum. Neurosci. 14:28. 10.3389/fnhum.2020.00028
- De Ridder D., Vanneste S., Congedo M. (2011). The distressed brain: a group blind source separation analysis on tinnitus. PLoS One 6:e24273. 10.1371/journal.pone.0024273
- Dille M. F., Konrad-Martin D., Gallun F., Helt W. J., Gordon J. S., Reavis K. M., et al. (2010). Tinnitus onset rates from chemotherapeutic agents and ototoxic antibiotics: results of a large prospective study. J. Am. Acad. Audiol. 21 409–417. 10.3766/jaaa.21.6.6
- Dobie R. A. (2003). Depression and tinnitus. Otolaryngol. Clin. North Am. 36 383–388. 10.1016/s0030-6665(02)00168-8
- Han L., Na Z., Chunli L., Yuchen C., Pengfei Z., Hao W., et al. (2019a). Baseline functional connectivity features of neural network nodes can predict improvement after sound therapy through adjusted narrow band noise in tinnitus patients. Front. Neurosci. 13:614. 10.3389/fnins.2019.00614
- Han L., Yawen L., Hao W., Chunli L., Pengfei Z., Zhengyu Z., et al. (2019b). Effects of sound therapy on resting-state functional brain networks in patients with tinnitus: a graph-theoretical-based study. J. Magn. Reson. Imaging 50 1731–1741. 10.1002/jmri.26796
- Han L., Zhaohui L., Fei Y., Pengfei Z., Ting L., Cheng D., et al. (2015). Disrupted neural activity in unilateral vascular pulsatile tinnitus patients in the early stage of disease: evidence from resting-state fMRI. Prog. Neuropsychopharmacol. Biol. Psychiatry 59 91–99. 10.1016/j.pnpbp.2015.01.013
- Heller A. J. (2003). Classification and epidemiology of tinnitus. Otolaryngol. Clin. North Am. 36 239–248. 10.1016/s0030-6665(02)00160-3
- Henry J. A., Schechter M. A., Nagler S. M., Fausti S. A. (2002). Comparison of tinnitus masking and tinnitus retraining therapy. J. Am. Acad. Audiol. 13 559–581.
- Husain F. T., Medina R. E., Davis C. W., Szymko-Bennett Y., Simonyan K., Pajor N. M., et al. (2011). Neuroanatomical changes due to hearing loss and chronic tinnitus: a combined VBM and DTI study. Brain Res. 1369 74–88. 10.1016/j.brainres.2010.10.095
- Husain F. T., Zimmerman B., Tai Y., Finnegan M. K., Kay E., Khan F., et al. (2019). Assessing mindfulness-based cognitive therapy intervention for tinnitus using behavioural measures and structural MRI: a pilot study. Int. J. Audiol. 58 889–901. 10.1080/14992027.2019.1629655
- Krick C. M., Argstatter H., Grapp M., Plinkert P. K., Reith W. (2017). Heidelberg neuro-music therapy enhances task-negative activity in tinnitus patients. Front. Neurosci. 11:384. 10.3389/fnins.2017.00384
- 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. Front. Neurosci. 9:49. 10.3389/fnins.2015.00049
- 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. 10.1016/j.neuron.2010.12.002
- Leaver A. M., Turesky T. K., Seydell-Greenwald A., Morgan S., Kim H. J., Rauschecker J. P. (2016). Intrinsic network activity in tinnitus investigated using functional MRI. Hum. Brain Mapp. 37 2717–2735. 10.1002/hbm.23204
- Levine R. A., Oron Y. (2015). Tinnitus. Handb. Clin. Neurol. 129 409–431. 10.1016/B978-0-444-62630-1.00023-8
- Liu Y., Lv H., Zhao P., Liu Z., Chen W., Gong S., et al. (2018). Neuroanatomical alterations in patients with early stage of unilateral pulsatile tinnitus: a voxel-based morphometry study. Neural Plast 2018:4756471. 10.1155/2018/4756471
- Lv H., Zhao P., Liu Z., Li R., Zhang L., Wang P., et al. (2016a). Abnormal resting-state functional connectivity study in unilateral pulsatile tinnitus patients with single etiology: a seed-based functional connectivity study. Eur. J. Radiol. 85 2023–2029. 10.1016/j.ejrad.2016.09.011
- Lv H., Zhao P., Liu Z., Wang G., Zeng R., Yan F., et al. (2016b). Frequency-dependent neural activity in patients with unilateral vascular pulsatile tinnitus. Neural Plast 2016:4918186. 10.1155/2016/4918186
- Lv H., Zhao P., Liu Z., Liu X., Ding H., Liu L., et al. (2018). Lateralization effects on functional connectivity of the auditory network in patients with unilateral pulsatile tinnitus as detected by functional MRI. Prog. Neuropsychopharmacol. Biol. Psychiatry 81 228–235. 10.1016/j.pnpbp.2017.09.020
- Lv H., Liu C., Wang Z., Zhao P., Cheng X., Yang Z., et al. (2020). Altered functional connectivity of the thalamus in tinnitus patients is correlated with symptom alleviation after sound therapy. Brain Imaging Behav. 10.1007/s11682-019-00218-0 [Epub ahead of print].
- McFerran D. J., Stockdale D., Holme R., Large C. H., Baguley D. M. (2019). Why is there no cure for tinnitus? Front. Neurosci. 13:802. 10.3389/fnins.2019.00802
- Meyer M., Neff P., Liem F., Kleinjung T., Weidt S., Langguth B., et al. (2016). Differential tinnitus-related neuroplastic alterations of cortical thickness and surface area. Hear. Res. 342 1–12. 10.1016/j.heares.2016.08.016
- Mishra S., Roy T. S., Wadhwa S. (2018). Morphological and morphometrical maturation of ventral cochlear nucleus in human foetus. J. Chem. Neuroanat. 93 38–47. 10.1016/j.jchemneu.2017.03.002
- Pecorari G., Riva G., Bruno G., Naqe N., Nardo M., Albera A., et al. (2020). Recurrences in sudden sensorineural hearing loss: a long-term observational study. Am. J. Audiol. 29 18–22. 10.1044/2019_AJA-19-00061
- Poeppl T. B., Langguth B., Lehner A., Frodl T., Rupprecht R., Kreuzer P. M., et al. (2018). Brain stimulation-induced neuroplasticity underlying therapeutic response in phantom sounds. Hum. Brain Mapp. 39 554–562. 10.1002/hbm.23864
- Rauschecker J. P., Leaver A. M., Muhlau M. (2010). Tuning out the noise: limbic-auditory interactions in tinnitus. Neuron 66 819–826. 10.1016/j.neuron.2010.04.032
- Schecklmann M., Lehner A., Poeppl T. B., Kreuzer P. M., Rupprecht R., Rackl J., et al. (2013). Auditory cortex is implicated in tinnitus distress: a voxel-based morphometry study. Brain Struct. Funct. 218 1061–1070. 10.1007/s00429-013-0520-z
- Schecklmann M., Pregler M., Kreuzer P. M., Poeppl T. B., Lehner A., Cronlein T., et al. (2015). Psychophysiological associations between chronic tinnitus and sleep: a cross validation of tinnitus and insomnia questionnaires. Biomed. Res. Int. 2015:461090. 10.1155/2015/461090
- Scott-Wittenborn N., Karadaghy O. A., Piccirillo J. F., Peelle J. E. (2017). A methodological assessment of studies that use voxel-based morphometry to study neural changes in tinnitus patients. Hear Res. 355 23–32. 10.1016/j.heares.2017.09.002
- Shore S. E., Roberts L. E., Langguth B. (2016). Maladaptive plasticity in tinnitus–triggers, mechanisms and treatment. Nat. Rev. Neurol. 12 150–160. 10.1038/nrneurol.2016.12
- Simoes J., Neff P., Schoisswohl S., Bulla J., Schecklmann M., Harrison S., et al. (2019). Toward personalized tinnitus treatment: an exploratory study based on internet crowdsensing. Front. Public Health 7:157. 10.3389/fpubh.2019.00157
- Tae W. S., Yakunina N., Lee W. H., Ryu Y. J., Ham H. K., Pyun S. B., et al. (2018). Changes in the regional shape and volume of subcortical nuclei in patients with tinnitus comorbid with mild hearing loss. Neuroradiology 60 1203–1211. 10.1007/s00234-018-2093-2
- van der Loo E., Congedo M., Vanneste S., Van De Heyning P., De Ridder D. (2011). Insular lateralization in tinnitus distress. Auton. Neurosci. 165 191–194. 10.1016/j.autneu.2011.06.007
- Vanneste S., De Ridder D. (2012). The auditory and non-auditory brain areas involved in tinnitus. An emergent property of multiple parallel overlapping subnetworks. Front. Syst. Neurosci. 6:31. 10.3389/fnsys.2012.00031
- Vanneste S., Heyning P. V., Ridder D. D. (2011). Contralateral parahippocampal gamma-band activity determines noise-like tinnitus laterality: a region of interest analysis. Neuroscience 199 481–490. 10.1016/j.neuroscience.2011.07.067
- Vanneste S., Plazier M., der Loo E., de Heyning P. V., Congedo M., De Ridder D. (2010). The neural correlates of tinnitus-related distress. Neuroimage 52 470–480. 10.1016/j.neuroimage.2010.04.029
- Xia M., Wang J., He Y. (2013). BrainNet viewer: a network visualization tool for human brain connectomics. PLoS One 8:e68910. 10.1371/journal.pone.0068910
- Zeman F., Koller M., Figueiredo R., Aazevedo A., Rates M., Coelho C., et al. (2011). Tinnitus handicap inventory for evaluating treatment effects: which changes are clinically relevant? Otolaryngol. Head Neck Surg. 145 282–287. 10.1177/0194599811403882
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