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

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An Erratum to this article was published on 14 January 2014

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.

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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

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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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Authors and Affiliations

  1. Department of Otorhinolaryngology-Head and Neck Surgery, Seoul National University Hospital, Yun-Kun Dong 28, Chong-No Gu, Seoul, 110-744, Korea

    Jae-Jin Song

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

    Dirk De Ridder

  3. Department of Translational Neuroscience, Faculty of Medicine, University of Antwerp, Antwerp, Belgium

    Dirk De Ridder, Paul Van de Heyning & Sven Vanneste

  4. Center for Mind/Brain Sciences, University of Trento, Trento, Italy

    Nathan Weisz

  5. Department of Clinical and Biological Psychology, University of Ulm, Ulm, Germany

    Winfried Schlee

  6. Brai²n, TRI & ENT, University Hospital Antwerp, Antwerp, Belgium

    Paul Van de Heyning

  7. School of Behavioral and Brain Sciences, The University of Texas at Dallas, Richardson, USA

    Sven Vanneste

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  1. Jae-Jin Song
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  2. Dirk De Ridder
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Correspondence to Jae-Jin Song.

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Song, JJ., De Ridder, D., Weisz, N. et al. Hyperacusis-associated pathological resting-state brain oscillations in the tinnitus brain: a hyperresponsiveness network with paradoxically inactive auditory cortex. Brain Struct Funct 219, 1113–1128 (2014). https://doi.org/10.1007/s00429-013-0555-1

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