Skip to main content

Advertisement

SpringerLink
Log in

The Importance of Aging in Gray Matter Changes Within Tinnitus Patients Shown in Cortical Thickness, Surface Area and Volume

  • Original Paper
  • Published:
Brain Topography Aims and scope Submit manuscript

Abstract

Aging and sensorineural hearing loss are known to be involved in the development of chronic tinnitus. This study explores the structural changes of gray matter using surface base methods and focuses more specifically on changes in cortical thickness in 127 tinnitus patients. The linear relationships between cortical thickness and behavioral measures including aging, tinnitus loudness, tinnitus duration, tinnitus distress, and hearing loss were analyzed. Three dimensional T1-weighted MR images were acquired and cortical gray matter volumes were segmented using FreeSurfer on Talairach space. The results showed that cortical thickness and volume are negatively correlated to age in widespread regions of frontal cortices, and positively to bilateral entorhinal cortex and left rostral anterior cingulate cortex. The cortical thickness changes related to hearing loss overlap with those related to normal aging. The gray matter volumes of bilateral amygdalae, hippocampi, nuclei accumbens, and thalami are all significantly negatively correlated to age. Tinnitus-related distress level and subjective loudness were negatively correlated only to the thalamic volume. The results suggest that the primary factor of long-term structural changes in chronic tinnitus patients is age and age related hearing loss, rather than hearing loss per se. Tinnitus related factors such as subjective tinnitus loudness, tinnitus duration, and the level of chronic tinnitus related distress were not correlated to important morphometric changes in this study.

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
Fig. 5

Similar content being viewed by others

References

  • Abbena E, Salamon S, Gray A (2006) Modern differential geometry of curves and surfaces with Mathematica. CRC Press, Boca Raton

    Google Scholar 

  • Aldhafeeri FM, Mackenzie I, Kay T, Alghamdi J, Sluming V (2012) Neuroanatomical correlates of tinnitus revealed by cortical thickness analysis and diffusion tensor imaging. Neuroradiology 54:883–892. doi:10.1007/s00234-012-1044-6

    Article  PubMed  Google Scholar 

  • Allen JS, Bruss J, Brown CK, Damasio H (2005) Normal neuroanatomical variation due to age: the major lobes and a parcellation of the temporal region. Neurobiol Aging 26:1245–1260

    Article  PubMed  Google Scholar 

  • Audiology BSO (2008) Recommended procedure: pure tone air and bone conduction threshold audiometry with and without masking and determination of uncomfortable loudness levels

  • Boyen K, Langers DR, de Kleine E, van Dijk P (2012) Gray matter in the brain: differences associated with tinnitus and hearing loss. Hear Res. doi:10.1016/j.heares.2012.02.010

    PubMed  Google Scholar 

  • Boyen K, Langers DR, de Kleine E, van Dijk P (2013) Gray matter in the brain: differences associated with tinnitus and hearing loss. Hear Res 295:67–78

    Article  PubMed  Google Scholar 

  • Brozoski T, Odintsov B, Bauer C (2012) Gamma-aminobutyric acid and glutamic acid levels in the auditory pathway of rats with chronic tinnitus: a direct determination using high resolution point-resolved proton magnetic resonance spectroscopy (H-MRS). Front Syst Neurosci 6:9. doi:10.3389/fnsys.2012.00009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chao L, Knight R (1997) Prefrontal deficits in attention and inhibitory control with aging. Cereb Cortex 7:63–69

    Article  CAS  PubMed  Google Scholar 

  • Chung DY, Gannon RP, Mason K (1984) Factors affecting the prevalence of tinnitus. Audiology 23:441–452

    Article  CAS  PubMed  Google Scholar 

  • Collins DL, Neelin P, Peters TM, Evans AC (1994) Automatic 3D intersubject registration of MR volumetric data in standardized Talairach space. J Comput Assist Tomogr 18:192–205

    Article  CAS  PubMed  Google Scholar 

  • Crippa A, Lanting CP, van Dijk P, Roerdink JB (2010) A diffusion tensor imaging study on the auditory system and tinnitus. Open Neuroimaging J 4:16–25. doi:10.2174/1874440001004010016

    Article  Google Scholar 

  • Dale AM, Fischl B, Sereno MI (1999) Cortical surface-based analysis: I. Segmentation and surface reconstruction. Neuroimage 9:179–194

    Article  CAS  PubMed  Google Scholar 

  • De Ridder D, Fransen H, Francois O, Sunaert S, Kovacs S, Van De Heyning P (2006) Amygdalohippocampal involvement in tinnitus and auditory memory. Acta Otolaryngol 126:50–53

    Article  Google Scholar 

  • De Ridder D, Vanneste S, Congedo M (2011) The distressed brain: a group blind source separation analysis on tinnitus. PLoS One 6:e24273. doi:10.1371/journal.pone.0024273

    Article  PubMed  PubMed Central  Google Scholar 

  • Eggermont JJ, Roberts LE (2004) The neuroscience of tinnitus. Trends Neurosci 27:676–682

    Article  CAS  PubMed  Google Scholar 

  • Elgoyhen AB, Langguth B, De Ridder D, Vanneste S (2015) Tinnitus: perspectives from human neuroimaging. Nat Rev Neurosci 16:632–642. doi:10.1038/nrn4003

    Article  CAS  PubMed  Google Scholar 

  • Fischl B, Dale AM (2000) Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc Natl Acad Sci 97:11050–11055

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fischl B, Sereno MI, Dale AM (1999) Cortical surface-based analysis: II: inflation, flattening, and a surface-based coordinate system. Neuroimage 9:195–207

    Article  CAS  PubMed  Google Scholar 

  • Fischl B et al (2002) Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 33:341–355

    Article  CAS  PubMed  Google Scholar 

  • Fjell AM et al (2009) One-year brain atrophy evident in healthy aging. J Neurosci 29:15223–15231

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fjell AM, McEvoy L, Holland D, Dale AM, Walhovd KB, AsDN Initiative (2014) What is normal in normal aging? Effects of aging, amyloid and Alzheimer’s disease on the cerebral cortex and the hippocampus. Prog Neurobiol 117:20–40

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gates GA, Mills JH (2005) Presbycusis. The Lancet 366:1111–1120

    Article  Google Scholar 

  • Gilles A, De Ridder D, Van Hal G, Wouters K, Kleine Punte A, Van de Heyning P (2012) Prevalence of leisure noise-induced tinnitus and the attitude toward noise in university students. Otol Neurotol 33:899–906. doi:10.1097/MAO.0b013e31825d640a

    PubMed  Google Scholar 

  • Hagler DJ, Saygin AP, Sereno MI (2006) Smoothing and cluster thresholding for cortical surface-based group analysis of fMRI data. Neuroimage 33:1093–1103

    Article  PubMed  PubMed Central  Google Scholar 

  • Helfer TM (2011) Noise-induced hearing injuries, active component, U.S. Armed Forces, 2007–2010. MSMR 18:7–10

    PubMed  Google Scholar 

  • Hiller W, Goebel G (1992) A psychometric study of complaints in chronic tinnitus. J Psychosom Res 36:337–348

    Article  CAS  PubMed  Google Scholar 

  • Hiller W, Goebel G, Rief W (1994) Reliability of self-rated tinnitus distress and association with psychological symptom patterns. Br J Clin Psychol 33(Pt 2):231–239

    Article  PubMed  Google Scholar 

  • Huang Q, Tang J (2010) Age-related hearing loss or presbycusis. Eur Arch Otorhinolaryngol 267:1179–1191

    Article  PubMed  Google Scholar 

  • Husain FT, Medina RE, Davis CW, Szymko-Bennett Y, Simonyan K, Pajor NM, Horwitz B (2011) Neuroanatomical changes due to hearing loss and chronic tinnitus: a combined VBM and DTI study. Brain Res 1369:74–88. doi:10.1016/j.brainres.2010.10.095

    Article  CAS  PubMed  Google Scholar 

  • Hutton C, Draganski B, Ashburner J, Weiskopf N (2009) A comparison between voxel-based cortical thickness and voxel-based morphometry in normal aging. Neuroimage 48:371–380

    Article  PubMed  PubMed Central  Google Scholar 

  • Kaltenbach JA, Afman CE (2000) Hyperactivity in the dorsal cochlear nucleus after intense sound exposure and its resemblance to tone-evoked activity: a physiological model for tinnitus. Hear Res 140:165–172

    Article  CAS  PubMed  Google Scholar 

  • Kreuzer PM, Landgrebe M, Vielsmeier V, Kleinjung T, De Ridder D, Langguth B (2014) Trauma-associated tinnitus. J Head Trauma Rehabil 29:432–442. doi:10.1097/HTR.0b013e31829d3129

    Article  PubMed  Google Scholar 

  • Landgrebe M et al (2009) Structural brain changes in tinnitus: grey matter decrease in auditory and non-auditory brain areas. Neuroimage 46:213–218. doi:10.1016/j.neuroimage.2009.01.069

    Article  PubMed  Google Scholar 

  • Langguth B, Kreuzer PM, Kleinjung T, De Ridder D (2013) Tinnitus: causes and clinical management. Lancet Neurol 12:920–930. doi:10.1016/S1474-4422(13)70160-1

    Article  PubMed  Google Scholar 

  • Leaver AM, Renier L, Chevillet MA, Morgan S, Kim HJ, Rauschecker JP (2011) Dysregulation of limbic and auditory networks in tinnitus. Neuron 69:33–43. doi:10.1016/j.neuron.2010.12.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin FR, Ferrucci L, Metter EJ, An Y, Zonderman AB, Resnick SM (2011) Hearing loss and cognition in the Baltimore Longitudinal Study of Aging. Neuropsychology 25:763

    Article  PubMed  PubMed Central  Google Scholar 

  • MacDonald D, Kabani N, Avis D, Evans AC (2000) Automated 3-D extraction of inner and outer surfaces of cerebral cortex from MRI. NeuroImage 12:340–356

    Article  CAS  PubMed  Google Scholar 

  • Mahoney CJ, Rohrer JD, Goll JC, Fox NC, Rossor MN, Warren JD (2011) Structural neuroanatomy of tinnitus and hyperacusis in semantic dementia. J Neurol Neurosurg Psychiatry 82:1274–1278. doi:10.1136/jnnp.2010.235473

    Article  PubMed  PubMed Central  Google Scholar 

  • McCombe A, Baguley D, Coles R, McKenna L, McKinney C, Windle-Taylor P (2001) Guidelines for the grading of tinnitus severity: the results of a working group commissioned by the British Association of Otolaryngologists, Head and Neck Surgeons, 1999. Clin Otolaryngol Allied Sci 26:388–393

    Article  CAS  PubMed  Google Scholar 

  • Meeus O, Blaivie C, Van de Heyning P (2007) Validation of the Dutch and the French version of the Tinnitus Questionnaire. B-Ent 3(Suppl 7):11–17

    PubMed  Google Scholar 

  • Meeus O, Heyndrickx K, Lambrechts P, De Ridder D, Van de Heyning P (2009) Phase-shift treatment for tinnitus of cochlear origin. Eur Arch Otorhinolaryngol. doi:10.1007/s00405-009-1145-y

    PubMed  Google Scholar 

  • Meeus O, De Ridder D, Van de Heyning P (2011) Administration of the combination clonazepam-Deanxit as treatment for tinnitus. Otol Neurotol. doi:10.1097/MAO.0b013e31820e737c

    PubMed  Google Scholar 

  • Melcher JR, Knudson IM, Levine RA (2012) Subcallosal brain structure: correlation with hearing threshold at supra-clinical frequencies (>8 kHz), but not with tinnitus. Hear Res 295:79–86. doi:10.1016/j.heares.2012.03.013

    Article  PubMed  Google Scholar 

  • Mirz F, Gjedde A, Ishizu K, Pedersen CB (2000a) Cortical networks subserving the perception of tinnitus–a PET study. Acta Otolaryngol Suppl 543:241–243

    Article  CAS  PubMed  Google Scholar 

  • Mirz F, Gjedde A, Sdkilde-Jrgensen H, Pedersen CB (2000b) Functional brain imaging of tinnitus-like perception induced by aversive auditory stimuli. NeuroReport 11:633–637

    Article  CAS  PubMed  Google Scholar 

  • Mühlau M et al (2006) Structural brain changes in tinnitus. Cereb Cortex 16:1283–1288

    Article  PubMed  Google Scholar 

  • Muhr P, Rosenhall U (2010) Self-assessed auditory symptoms, noise exposure, and measured auditory function among healthy young Swedish men. Int J Audiol 49:317–325. doi:10.3109/14992020903431280

    Article  PubMed  Google Scholar 

  • Nondahl DM, Cruickshanks KJ, Huang G-H, Klein BE, Klein R, Tweed TS, Zhan W (2012) Generational differences in the reporting of tinnitus. Ear Hear 33:640

    Article  PubMed  PubMed Central  Google Scholar 

  • Pakkenberg B, Gundersen HJG (1997) Neocortical neuron number in humans: effect of sex and age. J Comp Neurol 384:312–320

    Article  CAS  PubMed  Google Scholar 

  • Pardo JV et al (2007) Where the brain grows old: decline in anterior cingulate and medial prefrontal function with normal aging. Neuroimage 35:1231–1237

    Article  PubMed  PubMed Central  Google Scholar 

  • Pereira JB, Ibarretxe-Bilbao N, Marti MJ, Compta Y, Junqué C, Bargallo N, Tolosa E (2012) Assessment of cortical degeneration in patients with Parkinson’s disease by voxel-based morphometry, cortical folding, and cortical thickness. Hum Brain Mapp 33:2521–2534

    Article  PubMed  Google Scholar 

  • Pilgramm M, Rychlick R, Lebisch H, Siedentop H, Goebel G, Kirchhoff D (1999) Tinnitus in the Federal Republic of Germany: a representative epidemiological study. In: Proceedings of the sixth international tinnitus seminar, 1999. The Tinnitus and Hyperacusis Society Cambridge, United Kingdom, pp 64–67

  • Salat DH et al (2004) Thinning of the cerebral cortex in aging. Cereb Cortex 14:721–730

    Article  PubMed  Google Scholar 

  • Salvi RJ, Wang J, Ding D (2000) Auditory plasticity and hyperactivity following cochlear damage. Hear Res 147:261–274

    Article  CAS  PubMed  Google Scholar 

  • Schecklmann M et al (2013) Auditory cortex is implicated in tinnitus distress: a voxel-based morphometry study. Brain Struct Funct 218:1061–1070. doi:10.1007/s00429-013-0520-z

    Article  CAS  PubMed  Google Scholar 

  • Schlee W, Mueller N, Hartmann T, Keil J, Lorenz I, Weisz N (2009) Mapping cortical hubs in tinnitus. BMC Biol 7:80. doi:10.1186/1741-7007-7-80

    Article  PubMed  PubMed Central  Google Scholar 

  • Shargorodsky J, Curhan GC, Farwell WR (2010) Prevalence and characteristics of tinnitus among US adults. Am J Med 123:711–718. doi:10.1016/j.amjmed.2010.02.015

    Article  PubMed  Google Scholar 

  • Smits M, Kovacs S, de Ridder D, Peeters RR, van Hecke P, Sunaert S (2007) Lateralization of functional magnetic resonance imaging (fMRI) activation in the auditory pathway of patients with lateralized tinnitus. Neuroradiology 49:669–679. doi:10.1007/s00234-007-0231-3

    Article  PubMed  Google Scholar 

  • Sobel ME (1987) Direct and indirect effects in linear structural equation models. Sociol Methods Res 16:155–176

    Article  Google Scholar 

  • Tisserand DJ, Pruessner JC, Arigita EJS, van Boxtel MP, Evans AC, Jolles J, Uylings HB (2002) Regional frontal cortical volumes decrease differentially in aging: an MRI study to compare volumetric approaches and voxel-based morphometry. Neuroimage 17:657–669

    Article  PubMed  Google Scholar 

  • van der Loo E, Congedo M, Vanneste S, De Heyning PV, De Ridder D (2011) Insular lateralization in tinnitus distress. Auton Neurosci 165:191–194. doi:10.1016/j.autneu.2011.06.007

    Article  PubMed  Google Scholar 

  • Van Essen DC (2005) A population-average, landmark-and surface-based (PALS) atlas of human cerebral cortex. Neuroimage 28:635–662

    Article  PubMed  Google Scholar 

  • Van Essen DC, Drury HA, Dickson J, Harwell J, Hanlon D, Anderson CH (2001) An integrated software suite for surface-based analyses of cerebral cortex. J Am Med Inf Assoc 8:443–459

    Article  Google Scholar 

  • Vanneste S, Plazier M, der Loo E, de Heyning PV, Congedo M, De Ridder D (2010) The neural correlates of tinnitus-related distress. Neuroimage 52:470–480. doi:10.1016/j.neuroimage.2010.04.029

    Article  PubMed  Google Scholar 

  • Vanneste S, de Heyning PV, Ridder DD (2011) Contralateral parahippocampal gamma-band activity determines noise-like tinnitus laterality: a region of interest analysis. Neuroscience 199:481–490

    Article  CAS  PubMed  Google Scholar 

  • Vanneste S, Van De Heyning P, De Ridder D (2015) Tinnitus: a large VBM-EEG correlational study. PLoS One 10:e0115122. doi:10.1371/journal.pone.0115122

    Article  PubMed  PubMed Central  Google Scholar 

  • Winkler AM et al (2010) Cortical thickness or grey matter volume? The importance of selecting the phenotype for imaging genetics studies. NeuroImage 53:1135–1146. doi:10.1016/j.neuroimage.2009.12.028

    Article  PubMed  Google Scholar 

  • Winkler AM et al (2012) Measuring and comparing brain cortical surface area and other areal quantities. Neuroimage 61:1428–1443

    Article  PubMed  PubMed Central  Google Scholar 

  • Yoo HB, De Ridder D, Vanneste S (2015) White matter changes in tinnitus: is it all age and hearing loss? Brain connectivity 6(1):84–93

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Lab for Clinical & Integrative Neuroscience, School of Behavioral and Brain Sciences, The University of Texas at Dallas, W 1966 Inwood Rd., Dallas, TX, 75235, USA

    Hye Bin Yoo & Sven Vanneste

  2. Department of Surgical Sciences, Section of Neurosurgery, Dunedin School of Medicine, University of Otago, Dunedin, New Zealand

    Dirk De Ridder

Authors
  1. Hye Bin Yoo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dirk De Ridder
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sven Vanneste
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sven Vanneste.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yoo, H.B., De Ridder, D. & Vanneste, S. The Importance of Aging in Gray Matter Changes Within Tinnitus Patients Shown in Cortical Thickness, Surface Area and Volume. Brain Topogr 29, 885–896 (2016). https://doi.org/10.1007/s10548-016-0511-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10548-016-0511-5

Keywords

Search

Navigation