Differential cortical activation patterns: pioneering sub-classification of tinnitus with and without hyperacusis by combining audiometry, gamma oscillations, and hemodynamics
The ongoing controversies about the neural basis of tinnitus, whether linked with central neural gain or not, may hamper efforts to develop therapies. We asked to what extent measurable audiometric characteristics of tinnitus without (T) or with co-occurrence of hyperacusis (TH) are distinguishable...
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| Format: | Article |
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Frontiers Media S.A.
2024-01-01
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| Series: | Frontiers in Neuroscience |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fnins.2023.1232446/full |
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| author | Jakob Wertz Lukas Rüttiger Benjamin Bender Uwe Klose Robert S. Stark Konrad Dapper Konrad Dapper Jörg Saemisch Christoph Braun Wibke Singer Ernst Dalhoff Katharina Bader Stephan M. Wolpert Marlies Knipper Matthias H. J. Munk Matthias H. J. Munk |
| author_facet | Jakob Wertz Lukas Rüttiger Benjamin Bender Uwe Klose Robert S. Stark Konrad Dapper Konrad Dapper Jörg Saemisch Christoph Braun Wibke Singer Ernst Dalhoff Katharina Bader Stephan M. Wolpert Marlies Knipper Matthias H. J. Munk Matthias H. J. Munk |
| author_sort | Jakob Wertz |
| collection | DOAJ |
| description | The ongoing controversies about the neural basis of tinnitus, whether linked with central neural gain or not, may hamper efforts to develop therapies. We asked to what extent measurable audiometric characteristics of tinnitus without (T) or with co-occurrence of hyperacusis (TH) are distinguishable on the level of cortical responses. To accomplish this, electroencephalography (EEG) and concurrent functional near-infrared spectroscopy (fNIRS) were measured while patients performed an attentionally demanding auditory discrimination task using stimuli within the individual tinnitus frequency (fTin) and a reference frequency (fRef). Resting-state-fMRI-based functional connectivity (rs-fMRI-bfc) in ascending auditory nuclei (AAN), the primary auditory cortex (AC-I), and four other regions relevant for directing attention or regulating distress in temporal, parietal, and prefrontal cortex was compiled and compared to EEG and concurrent fNIRS activity in the same brain areas. We observed no group differences in pure-tone audiometry (PTA) between 10 and 16 kHz. However, the PTA threshold around the tinnitus pitch was positively correlated with the self-rated tinnitus loudness and also correlated with distress in T-groups, while TH experienced their tinnitus loudness at minimal loudness levels already with maximal suffering scores. The T-group exhibited prolonged auditory brain stem (ABR) wave I latency and reduced ABR wave V amplitudes (indicating reduced neural synchrony in the brainstem), which were associated with lower rs-fMRI-bfc between AAN and the AC-I, as observed in previous studies. In T-subjects, these features were linked with elevated spontaneous and reduced evoked gamma oscillations and with reduced deoxygenated hemoglobin (deoxy-Hb) concentrations in response to stimulation with lower frequencies in temporal cortex (Brodmann area (BA) 41, 42, 22), implying less synchronous auditory responses during active auditory discrimination of reference frequencies. In contrast, in the TH-group gamma oscillations and hemodynamic responses in temporoparietal regions were reversed during active discrimination of tinnitus frequencies. Our findings suggest that T and TH differ in auditory discrimination and memory-dependent directed attention during active discrimination at either tinnitus or reference frequencies, offering a test paradigm that may allow for more precise sub-classification of tinnitus and future improved treatment approaches. |
| first_indexed | 2024-03-08T17:06:10Z |
| format | Article |
| id | doaj.art-b02020f5b8f944cbac16e13bc5f4f9d2 |
| institution | Directory Open Access Journal |
| issn | 1662-453X |
| language | English |
| last_indexed | 2024-03-08T17:06:10Z |
| publishDate | 2024-01-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Neuroscience |
| spelling | doaj.art-b02020f5b8f944cbac16e13bc5f4f9d22024-01-04T04:44:08ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2024-01-011710.3389/fnins.2023.12324461232446Differential cortical activation patterns: pioneering sub-classification of tinnitus with and without hyperacusis by combining audiometry, gamma oscillations, and hemodynamicsJakob Wertz0Lukas Rüttiger1Benjamin Bender2Uwe Klose3Robert S. Stark4Konrad Dapper5Konrad Dapper6Jörg Saemisch7Christoph Braun8Wibke Singer9Ernst Dalhoff10Katharina Bader11Stephan M. Wolpert12Marlies Knipper13Matthias H. J. Munk14Matthias H. J. Munk15Department of Otolaryngology, Head and Neck Surgery, Tübingen Hearing Research Centre, University of Tübingen, Tübingen, GermanyDepartment of Otolaryngology, Head and Neck Surgery, Tübingen Hearing Research Centre, University of Tübingen, Tübingen, GermanyDepartment of Diagnostic and Interventional Neuroradiology, University of Tübingen, Tübingen, GermanyDepartment of Diagnostic and Interventional Neuroradiology, University of Tübingen, Tübingen, GermanyDepartment of Psychiatry and Psychotherapy, University of Tübingen, Tübingen, GermanyDepartment of Otolaryngology, Head and Neck Surgery, Tübingen Hearing Research Centre, University of Tübingen, Tübingen, GermanyDepartment of Biology, Technical University Darmstadt, Darmstadt, GermanyDepartment of Otolaryngology, Head and Neck Surgery, Tübingen Hearing Research Centre, University of Tübingen, Tübingen, GermanyMEG-Center, University of Tübingen, Tübingen, GermanyDepartment of Otolaryngology, Head and Neck Surgery, Tübingen Hearing Research Centre, University of Tübingen, Tübingen, GermanySection of Physiological Acoustics and Communication, Department of Otolaryngology, Head and Neck Surgery, University of Tübingen, Tübingen, GermanySection of Physiological Acoustics and Communication, Department of Otolaryngology, Head and Neck Surgery, University of Tübingen, Tübingen, GermanyDepartment of Otolaryngology, Head and Neck Surgery, Tübingen Hearing Research Centre, University of Tübingen, Tübingen, GermanyDepartment of Otolaryngology, Head and Neck Surgery, Tübingen Hearing Research Centre, University of Tübingen, Tübingen, GermanyDepartment of Psychiatry and Psychotherapy, University of Tübingen, Tübingen, GermanyDepartment of Biology, Technical University Darmstadt, Darmstadt, GermanyThe ongoing controversies about the neural basis of tinnitus, whether linked with central neural gain or not, may hamper efforts to develop therapies. We asked to what extent measurable audiometric characteristics of tinnitus without (T) or with co-occurrence of hyperacusis (TH) are distinguishable on the level of cortical responses. To accomplish this, electroencephalography (EEG) and concurrent functional near-infrared spectroscopy (fNIRS) were measured while patients performed an attentionally demanding auditory discrimination task using stimuli within the individual tinnitus frequency (fTin) and a reference frequency (fRef). Resting-state-fMRI-based functional connectivity (rs-fMRI-bfc) in ascending auditory nuclei (AAN), the primary auditory cortex (AC-I), and four other regions relevant for directing attention or regulating distress in temporal, parietal, and prefrontal cortex was compiled and compared to EEG and concurrent fNIRS activity in the same brain areas. We observed no group differences in pure-tone audiometry (PTA) between 10 and 16 kHz. However, the PTA threshold around the tinnitus pitch was positively correlated with the self-rated tinnitus loudness and also correlated with distress in T-groups, while TH experienced their tinnitus loudness at minimal loudness levels already with maximal suffering scores. The T-group exhibited prolonged auditory brain stem (ABR) wave I latency and reduced ABR wave V amplitudes (indicating reduced neural synchrony in the brainstem), which were associated with lower rs-fMRI-bfc between AAN and the AC-I, as observed in previous studies. In T-subjects, these features were linked with elevated spontaneous and reduced evoked gamma oscillations and with reduced deoxygenated hemoglobin (deoxy-Hb) concentrations in response to stimulation with lower frequencies in temporal cortex (Brodmann area (BA) 41, 42, 22), implying less synchronous auditory responses during active auditory discrimination of reference frequencies. In contrast, in the TH-group gamma oscillations and hemodynamic responses in temporoparietal regions were reversed during active discrimination of tinnitus frequencies. Our findings suggest that T and TH differ in auditory discrimination and memory-dependent directed attention during active discrimination at either tinnitus or reference frequencies, offering a test paradigm that may allow for more precise sub-classification of tinnitus and future improved treatment approaches.https://www.frontiersin.org/articles/10.3389/fnins.2023.1232446/fulltinnitushyperacusisrs-fMRIfNIRSEEGgamma oscillations |
| spellingShingle | Jakob Wertz Lukas Rüttiger Benjamin Bender Uwe Klose Robert S. Stark Konrad Dapper Konrad Dapper Jörg Saemisch Christoph Braun Wibke Singer Ernst Dalhoff Katharina Bader Stephan M. Wolpert Marlies Knipper Matthias H. J. Munk Matthias H. J. Munk Differential cortical activation patterns: pioneering sub-classification of tinnitus with and without hyperacusis by combining audiometry, gamma oscillations, and hemodynamics Frontiers in Neuroscience tinnitus hyperacusis rs-fMRI fNIRS EEG gamma oscillations |
| title | Differential cortical activation patterns: pioneering sub-classification of tinnitus with and without hyperacusis by combining audiometry, gamma oscillations, and hemodynamics |
| title_full | Differential cortical activation patterns: pioneering sub-classification of tinnitus with and without hyperacusis by combining audiometry, gamma oscillations, and hemodynamics |
| title_fullStr | Differential cortical activation patterns: pioneering sub-classification of tinnitus with and without hyperacusis by combining audiometry, gamma oscillations, and hemodynamics |
| title_full_unstemmed | Differential cortical activation patterns: pioneering sub-classification of tinnitus with and without hyperacusis by combining audiometry, gamma oscillations, and hemodynamics |
| title_short | Differential cortical activation patterns: pioneering sub-classification of tinnitus with and without hyperacusis by combining audiometry, gamma oscillations, and hemodynamics |
| title_sort | differential cortical activation patterns pioneering sub classification of tinnitus with and without hyperacusis by combining audiometry gamma oscillations and hemodynamics |
| topic | tinnitus hyperacusis rs-fMRI fNIRS EEG gamma oscillations |
| url | https://www.frontiersin.org/articles/10.3389/fnins.2023.1232446/full |
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