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The Neural Bases of Tinnitus: Lessons from Deafness and Cochlear Implants

Marlies Knipper, Pim van Dijk, Holger Schulze, Birgit Mazurek, Patrick Krauss, Verena Scheper, Athanasia Warnecke, Winfried Schlee, Kerstin Schwabe, Wibke Singer, Christoph Braun, Paul H. Delano, Andreas J. Fallgatter, Ann-Christine Ehlis, Grant D. Searchfield, Matthias H.J. Munk, David M. Baguley and Lukas Rüttiger
Journal of Neuroscience 16 September 2020, 40 (38) 7190-7202; DOI: https://doi.org/10.1523/JNEUROSCI.1314-19.2020
Marlies Knipper
1University of Tübingen, Department of Otolaryngology, Head and Neck Surgery, Tübingen Hearing Research Center, Molecular Physiology of Hearing, 72076 Tübingen, Germany
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  • ORCID record for Marlies Knipper
Pim van Dijk
2Department of Otorhinolaryngology/Head and Neck Surgery, University of Groningen, University Medical Center Groningen, 9700 AB Groningen, The Netherlands
3Graduate School of Medical Sciences (Research School of Behavioural and Cognitive Neurosciences), University of Groningen, 9700 AB Groningen, The Netherlands
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Holger Schulze
4Experimental Otolaryngology, Neuroscience Laboratory, University Hospital Erlangen, Friedrich-Alexander University Erlangen-Nürnberg, 91054 Erlangen, Germany
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Birgit Mazurek
5Charité–Universitätsmedizin Berlin, Tinnituszentrum, 10117 Berlin, Germany
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Patrick Krauss
4Experimental Otolaryngology, Neuroscience Laboratory, University Hospital Erlangen, Friedrich-Alexander University Erlangen-Nürnberg, 91054 Erlangen, Germany
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Verena Scheper
6Department of Otorhinolaryngology, Head and Neck Surgery, Hannover Medical School, 30625 Hannover, Germany
7Cluster of Excellence “Hearing4all” of the German Research Foundation, 30625 Hannover, Germany
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Athanasia Warnecke
6Department of Otorhinolaryngology, Head and Neck Surgery, Hannover Medical School, 30625 Hannover, Germany
7Cluster of Excellence “Hearing4all” of the German Research Foundation, 30625 Hannover, Germany
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Winfried Schlee
8Department of Psychiatry and Psychotherapy, University of Regensburg, 93053 Regensburg, Germany
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Kerstin Schwabe
6Department of Otorhinolaryngology, Head and Neck Surgery, Hannover Medical School, 30625 Hannover, Germany
7Cluster of Excellence “Hearing4all” of the German Research Foundation, 30625 Hannover, Germany
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Wibke Singer
1University of Tübingen, Department of Otolaryngology, Head and Neck Surgery, Tübingen Hearing Research Center, Molecular Physiology of Hearing, 72076 Tübingen, Germany
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Christoph Braun
9MEG Center, University Hospital Tübingen, 72076 Tübingen, Germany
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Paul H. Delano
10Departments of Otolaryngology and Neuroscience, Faculty of Medicine, University of Chile, 15782 Santiago, Chile
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Andreas J. Fallgatter
11Department of Psychiatry, University of Tübingen, 72076 Tübingen, Germany
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Ann-Christine Ehlis
11Department of Psychiatry, University of Tübingen, 72076 Tübingen, Germany
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Grant D. Searchfield
12Eisdell Moore Centre, Audiology Section, University of Auckland, 1546 Auckland, New Zealand
13Brain Research New Zealand, Centre for Brain Research, University of Auckland, 1142 Auckland, New Zealand
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Matthias H.J. Munk
11Department of Psychiatry, University of Tübingen, 72076 Tübingen, Germany
14Department of Biology, Technical University Darmstadt, 64287 Darmstadt, Germany
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David M. Baguley
15Hearing Sciences, Division of Clinical Neuroscience, School of Medicine, University of Nottingham, NG15DU Nottingham, United Kingdom
16NIHR Nottingham Biomedical Research Centre, University of Nottingham, NG72UH Nottingham, United Kingdom
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Lukas Rüttiger
1University of Tübingen, Department of Otolaryngology, Head and Neck Surgery, Tübingen Hearing Research Center, Molecular Physiology of Hearing, 72076 Tübingen, Germany
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Abstract

Subjective tinnitus is the conscious perception of sound in the absence of any acoustic source. The literature suggests various tinnitus mechanisms, most of which invoke changes in spontaneous firing rates of central auditory neurons resulting from modification of neural gain. Here, we present an alternative model based on evidence that tinnitus is: (1) rare in people who are congenitally deaf, (2) common in people with acquired deafness, and (3) potentially suppressed by active cochlear implants used for hearing restoration. We propose that tinnitus can only develop after fast auditory fiber activity has stimulated the synapse formation between fast-spiking parvalbumin positive (PV+) interneurons and projecting neurons in the ascending auditory path and coactivated frontostriatal networks after hearing onset. Thereafter, fast auditory fiber activity promotes feedforward and feedback inhibition mediated by PV+ interneuron activity in auditory-specific circuits. This inhibitory network enables enhanced stimulus resolution, attention-driven contrast improvement, and augmentation of auditory responses in central auditory pathways (neural gain) after damage of slow auditory fibers. When fast auditory fiber activity is lost, tonic PV+ interneuron activity is diminished, resulting in the prolonged response latencies, sudden hyperexcitability, enhanced cortical synchrony, elevated spontaneous γ oscillations, and impaired attention/stress-control that have been described in previous tinnitus models. Moreover, because fast processing is gained through sensory experience, tinnitus would not exist in congenital deafness. Electrical cochlear stimulation may have the potential to reestablish tonic inhibitory networks and thus suppress tinnitus. The proposed framework unites many ideas of tinnitus pathophysiology and may catalyze cooperative efforts to develop tinnitus therapies.

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The Journal of Neuroscience: 40 (38)
Journal of Neuroscience
Vol. 40, Issue 38
16 Sep 2020
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The Neural Bases of Tinnitus: Lessons from Deafness and Cochlear Implants
Marlies Knipper, Pim van Dijk, Holger Schulze, Birgit Mazurek, Patrick Krauss, Verena Scheper, Athanasia Warnecke, Winfried Schlee, Kerstin Schwabe, Wibke Singer, Christoph Braun, Paul H. Delano, Andreas J. Fallgatter, Ann-Christine Ehlis, Grant D. Searchfield, Matthias H.J. Munk, David M. Baguley, Lukas Rüttiger
Journal of Neuroscience 16 September 2020, 40 (38) 7190-7202; DOI: 10.1523/JNEUROSCI.1314-19.2020

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The Neural Bases of Tinnitus: Lessons from Deafness and Cochlear Implants
Marlies Knipper, Pim van Dijk, Holger Schulze, Birgit Mazurek, Patrick Krauss, Verena Scheper, Athanasia Warnecke, Winfried Schlee, Kerstin Schwabe, Wibke Singer, Christoph Braun, Paul H. Delano, Andreas J. Fallgatter, Ann-Christine Ehlis, Grant D. Searchfield, Matthias H.J. Munk, David M. Baguley, Lukas Rüttiger
Journal of Neuroscience 16 September 2020, 40 (38) 7190-7202; DOI: 10.1523/JNEUROSCI.1314-19.2020
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