Abstract
Background and objective
Deafferentation caused by cochlear pathology (which can be hidden from the audiogram) activates forms of neural plasticity in auditory pathways, generating tinnitus and its associated conditions including hyperacusis. This article discusses tinnitus mechanisms and suggests how these mechanisms may relate to those involved in normal auditory information processing.
Materials and methods
Research findings from animal models of tinnitus and from electromagnetic imaging of tinnitus patients are reviewed which pertain to the role of deafferentation and neural plasticity in tinnitus and hyperacusis.
Results
Auditory neurons compensate for deafferentation by increasing their input/output functions (gain) at multiple levels of the auditory system. Forms of homeostatic plasticity are believed to be responsible for this neural change, which increases the spontaneous and driven activity of neurons in central auditory structures in animals expressing behavioral evidence of tinnitus. Another tinnitus correlate, increased neural synchrony among the affected neurons, is forged by spike-timing-dependent neural plasticity in auditory pathways. Slow oscillations generated by bursting thalamic neurons verified in tinnitus animals appear to modulate neural plasticity in the cortex, integrating tinnitus neural activity with information in brain regions supporting memory, emotion, and consciousness which exhibit increased metabolic activity in tinnitus patients.
Discussion and conclusion
The latter process may be induced by transient auditory events in normal processing but it persists in tinnitus, driven by phantom signals from the auditory pathway. Several tinnitus therapies attempt to suppress tinnitus through plasticity, but repeated sessions will likely be needed to prevent tinnitus activity from returning owing to deafferentation as its initiating condition.
Zusammenfassung
Hintergrund und Ziel
Über eine Deafferenzierung durch pathologische Veränderungen der Cochlea (die sich im Audiogramm nicht zeigen muss) werden Formen der neuronalen Plastizität in auditorischen Signalwegen aktiviert, die Tinnitus und damit einhergehende Erkrankungen einschließlich Hyperakusis verursachen. In dem vorliegenden Beitrag werden Tinnitusmechanismen erörtert und Konzepte vorgestellt, wie diese Mechanismen mit denen normaler auditorischer Informationsverarbeitung in Zusammenhang stehen können.
Material und Methoden
Dargelegt werden Forschungsergebnisse aus Tiermodellen des Tinnitus und von elektromagnetischen Untersuchungen mit Bildgebung an Tinnituspatienten, die die Bedeutung der Deafferenzierung und der neuronalen Plastizität bei Tinnitus und Hyperakusis unterstreichen.
Ergebnisse
Auditorische Neuronen kompensieren eine Deafferenzierung durch Erhöhung ihrer Eingangs-Ausgangs-Funktionen (Verstärkung, „gain“) auf mehreren Ebenen des auditorischen Systems. Formen der homöostatischen Plastizität sollen für diese neuronalen Veränderungen verantwortlich sein, so dass die spontane und gesteuerte Aktivität von Neuronen in zentralen auditorischen Strukturen bei solchen Tieren erhöht wird, deren Verhalten Hinweise auf das Vorliegen eines Tinnitus gibt. Ein weiteres Tinnituskorrelat ist die erhöhte neuronale Synchronizität unter den betroffenen Neuronen. Diese entsteht durch Erregungszeitmuster-(„spike-timing“)abhängige neuronale Plastizität in den auditorischen Signalwegen, d. h. die Verstärkung einer synaptischen Verbindung erfolgt in Abhängigkeit von der relativen zeitlichen Differenz der Erregung von Neuronen zueinander. Langsame Oszillationen, die durch wiederholte Aktionspotenziale („bursts“) thalamischer Neuronen erzeugt werden und die bei Tieren mit Tinnitus in Zusammenhang gebracht wurden, scheinen die neuronale Plastizität im Kortex zu modulieren. Dabei wird die neuronale Tinnitusaktivität mit Informationen aus Hirnarealen verflochten, die Gedächtnis, Gefühle und Bewusstsein unterstützen und bei Tinnituspatienten eine erhöhte metabolische Aktivität aufweisen.
Diskussion und Schlussfolgerung
Letzterer Vorgang könnte durch transiente auditorische Ereignisse auch in der normalen Hörverarbeitung induziert werden, angeregt durch Phantomsignale aus der Hörbahn jedoch bei Tinnitus persistierend. Bei verschiedenen Ansätzen zur Tinnitustherapie wird versucht, den Tinnitus über Anregungen von Plastizitätsveränderungen zu supprimieren. Aber es erscheinen wahrscheinlich wiederholte Behandlungseinheiten notwendig, um zu verhindern, dass die durch Deafferenzierung ausgelöste Tinnitusaktivität wiederkehrt.
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Abbreviations
- A1:
-
Primary auditory cortex
- A2:
-
Nonprimary auditory cortex
- ABR:
-
Auditory brainstem response
- AM:
-
Amplitude modulation
- ANF:
-
Auditory nerve fiber
- CN:
-
Cochlear nucleus
- DCN:
-
Dorsal cochlear nucleus
- EEG:
-
Electroencephalography
- EFR:
-
Envelope following response
- HSR:
-
High spontaneous rate (ANFs)
- IC:
-
Inferior colliculus
- HL:
-
Hearing level
- HP:
-
Homeostatic plasticity
- HT:
-
High threshold (ANFs)
- IHC:
-
Inner hair cell
- LT:
-
Low threshold (ANFs)
- OHC:
-
Outer hair cell
- PTS:
-
Permanent threshold shift
- SFR:
-
Spontaneous firing rate
- SPL:
-
Sound pressure level
- STDP:
-
Spike-timing-dependent plasticity
- TTS:
-
Temporary threshold shift
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Acknowledgements
This article derives from an invited presentation to the 18th Annual Tinnitus Symposium, Charité University Hospital Berlin, on 3 December 2016. The author acknowledges the support of the Natural Sciences and Engineering Research Council of Canada.
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L.E. Roberts declares that he has no competing interests.
The research studies reviewed in this article were approved by the ethics committees of the host institutions in accordance with accepted practices and the Declaration of Helsinki.
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Roberts, L.E. Neural plasticity and its initiating conditions in tinnitus. HNO 66, 172–178 (2018). https://doi.org/10.1007/s00106-017-0449-2
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DOI: https://doi.org/10.1007/s00106-017-0449-2