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Brain Structure and Function

, Volume 219, Issue 3, pp 1113–1128 | Cite as

Hyperacusis-associated pathological resting-state brain oscillations in the tinnitus brain: a hyperresponsiveness network with paradoxically inactive auditory cortex

  • Jae-Jin SongEmail author
  • Dirk De Ridder
  • Nathan Weisz
  • Winfried Schlee
  • Paul Van de Heyning
  • Sven Vanneste
Original Article

Abstract

Although hyperacusis, a hyperresponsiveness to non-noxious auditory stimuli, is a sound-evoked symptom, possible resting-state pathologic oscillations in hyperacusis brain have never been explored. By comparing 17 tinnitus participants with hyperacusis (T+H+) and 17 without hyperacusis (T+H−), we aimed to explore characteristic resting-state cortical activity of hyperacusis. The T+H+ and T+H− groups, strictly matched for all tinnitus sound characteristics to exclude tinnitus-related cortical changes, were compared using resting-state electroencephalography source-localized activity complemented by functional connectivity analyses. Correlation analysis revealed that hyperacusis questionnaire score was positively correlated with the orbitofrontal cortex (OFC) beta power, the right auditory cortex (AC) alpha1 power, and the dorsal anterior cingulate cortex (dACC) beta1 power. Compared to the T+H− group, the T+H+ group demonstrated increased beta power in the dACC and OFC, and increased alpha power in the right AC. Region of interest analyses including 17 normal controls further confirmed that these differences originated solely from relatively increased power of the T+H+ group, not from a relative power decrease of the T+H− group. Also, the T+H+ group showed increased connectivity between the OFC/dACC and the AC as compared to the T+H− group. The beta power increase in the OFC/dACC may indicate increased resting-state vigilance in tinnitus patients with hyperacusis. In addition, increased alpha power in the AC may reflect an adaptive top-down inhibition against sound stimuli probably mediated by the increased beta power of the OFC. The OFC/dACC, also frequently found to be activated in analogous diseases such as allodynia/hyperalgesia, may compose a hyperresponsiveness network.

Keywords

Hyperacusis Hyperalgesia Electroencephalography Neural networks 

Abbreviations

HQ

Hyperacusis questionnaire

qEEG

Quantitative electroencephalography

TQ

Tinnitus questionnaire

NRS

Numeric rating scale

sLORETA

Standardized low-resolution brain electromagnetic tomography

MNI

Montreal Neurological Institute

ROI

Region of interest

AC

Auditory cortex

A2

Secondary auditory cortex

A1

Primary auditory cortex

dACC

Dorsal anterior cingulate cortex

OFC

Orbitofrontal cortex

SnPM

Statistical non-parametric mapping

SMA

Supplementary motor area

dPMC

Dorsal premotor cortex

Notes

Acknowledgments

The authors thank Jan Ost, Bram Van Achteren, Bjorn Devree, Pieter van Looy and James Hartzell for their help in preparing this manuscript and thank Thomas Hartmann and Nadia Muller for their import comments. Also, the first author thanks Dr. DY Yoon for giving invaluable support to this study. This work was supported by Research Foundation Flanders (FWO), Tinnitus Research Initiative, The Neurological Foundation of New Zealand, TOP project University Antwerp, and the Korean Science and Engineering Foundation (KOSEF) grant funded by the Korean government (MOST) (No. 2012-0030102).

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Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Jae-Jin Song
    • 1
    Email author
  • Dirk De Ridder
    • 2
    • 3
  • Nathan Weisz
    • 4
  • Winfried Schlee
    • 5
  • Paul Van de Heyning
    • 3
    • 6
  • Sven Vanneste
    • 3
    • 7
  1. 1.Department of Otorhinolaryngology-Head and Neck SurgerySeoul National University HospitalSeoulKorea
  2. 2.Department of Surgical Sciences, Dunedin School of MedicineUniversity of OtagoDunedinNew Zealand
  3. 3.Department of Translational Neuroscience, Faculty of MedicineUniversity of AntwerpAntwerpBelgium
  4. 4.Center for Mind/Brain SciencesUniversity of TrentoTrentoItaly
  5. 5.Department of Clinical and Biological PsychologyUniversity of UlmUlmGermany
  6. 6.Brai²n, TRI & ENT, University Hospital AntwerpAntwerpBelgium
  7. 7.School of Behavioral and Brain SciencesThe University of Texas at DallasRichardsonUSA

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