Inhibition of Experimental Tinnitus With High Frequency Stimulation of the Rat Medial Geniculate Body

Zwieten, Gusta van; Janssen, Marcus L.F.; Smit, Jasper V.; Janssen, A. Miranda L.; Roet, Milaine; Jahanshahi, Ali; Stokroos, Robert J.; Temel, Yasin

doi:10.1111/ner.12795

Cited by 19 publications

(44 citation statements)

References 75 publications

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“…One of the disadvantages is habituation, i.e., when repeated, unconditioned reflexes diminish in amplitude (Lobarinas et al 2013 ; Longenecker and Galazyuk 2011 ). This issue was addressed by administering fewer trials and by randomly varying the inter-stimulus interval (van Zwieten et al 2019a , b ). Based on the assumption that tinnitus pathogenesis relies on malfunctioning of a vast network of primary auditory and non-auditory structures (Llinas et al 1999 ; Rauschecker et al 2010 ), it has also been criticized that the GPIAS model does not take hyperacusis and emotional factors such as stress into account (Brozoski and Bauer 2016 ; Kleinjung and Langguth 2020 ).…”

Section: The Mgb In Tinnitus Pathologymentioning

confidence: 99%

“…It actively shapes information processing between subcortical and cortical areas (Bartlett 2013 ; De Ridder et al 2015 ; Llinas et al 1999 ). Animal research provides first indications of successful tinnitus treatment by invasively stimulating the MGB in rats (van Zwieten et al 2019b ). The MGB should hence not only be considered a major gateway station for auditory signals transmitted to the cerebral cortex, but also as a crucial component in developing a better understanding of tinnitus pathology (Leaver et al 2011 ; Moller 2003 ).…”

Section: Introductionmentioning

confidence: 99%

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Auditory thalamus dysfunction and pathophysiology in tinnitus: a predictive network hypothesis

et al. 2021

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Tinnitus is the perception of a ‘ringing’ sound without an acoustic source. It is generally accepted that tinnitus develops after peripheral hearing loss and is associated with altered auditory processing. The thalamus is a crucial relay in the underlying pathways that actively shapes processing of auditory signals before the respective information reaches the cerebral cortex. Here, we review animal and human evidence to define thalamic function in tinnitus. Overall increased spontaneous firing patterns and altered coherence between the thalamic medial geniculate body (MGB) and auditory cortices is observed in animal models of tinnitus. It is likely that the functional connectivity between the MGB and primary and secondary auditory cortices is reduced in humans. Conversely, there are indications for increased connectivity between the MGB and several areas in the cingulate cortex and posterior cerebellar regions, as well as variability in connectivity between the MGB and frontal areas regarding laterality and orientation in the inferior, medial and superior frontal gyrus. We suggest that these changes affect adaptive sensory gating of temporal and spectral sound features along the auditory pathway, reflecting dysfunction in an extensive thalamo-cortical network implicated in predictive temporal adaptation to the auditory environment. Modulation of temporal characteristics of input signals might hence factor into a thalamo-cortical dysrhythmia profile of tinnitus, but could ultimately also establish new directions for treatment options for persons with tinnitus.

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Section: The Mgb In Tinnitus Pathologymentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Auditory thalamus dysfunction and pathophysiology in tinnitus: a predictive network hypothesis

et al. 2021

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“…The medial geniculate body, which is a potential target for tinnitus treatment [60], may be associated with tinnitus in VM patients. Despite having a primary role in auditory signaling from the cochlear nucleus, the medial division of the medial geniculate body receives projections from the spinal cord [61] and vestibular nuclei [62,63].…”

Section: Possible Cortical Pathway Responsible For Tinnitusmentioning

confidence: 99%

Differences in characteristics between definite vestibular migraines, migraines with vestibular symptoms that do not meet vestibular migraine criteria, and migraines without vestibular symptoms: A cross-sectional study through the lens of central sensitization

Toriyama¹,

Hanaoka

Horiuchi

2021

Preprint

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Background: The demographic and clinical characteristics of vestibular migraine (VM) based on the International Classification of Headache Disorders (ICHD)-III beta are not well documented, and the underlying pathophysiology remains largely unknown. Based on evidence that central sensitization is involved in VM pathogenesis, we hypothesized that cutaneous allodynia (CA), which is a clinical manifestation of central sensitization, and interictal widespread pressure hyperalgesia (IWPH), which may be an accelerator for central sensitization, are more frequently associated with VM patients compared with non-VM patients. The aim of this study was as follows: 1) to assess differences in demographic and clinical characteristics among VM patients, patients with migraine with vestibular symptoms not meeting VM criteria (MwVS), and patients with migraine without vestibular symptoms (MwoVS); and 2) to evaluate whether VM patients were more frequently associated with CA/IWPH compared with the other two groups.Methods: This cross-sectional study enrolled consecutive migraine patients, aged 18–65. The comprehensive interview form included diagnostic questions of migraine and VM, demographic characteristics, migraine-specific variables, migraine-associated symptoms, and CA. IWPH occurrence was investigated using a manual tender point survey and clinical parameters were compared.Results: A total of 245 episodic migraineurs (mean age = 39.5 ± 11.3 years, 81.2% women) were enrolled. Based on ICHD-III beta criteria, 65 (26.5%), 74 (30.2%), and 106 (43.3%) patients were assigned to the VM group, MwVS group, or MwoVS group, respectively. Pairwise comparisons demonstrated no significant differences between the VM and MwVS groups, except for higher occurrence of headache disability in the VM group. Compared with the MwoVS group, the VM group was significantly associated with aura, severe disability, depression, tinnitus, sleep disorders, multimodal CA, and IWPH.Conclusions: There were no significant differences in clinical features between VM and MwVS groups, except for disability, which was possibly caused by criteria selection bias. VM and MwVS may be on the same disease process spectrum. Widespread multimodal CA, including clinical manifestations of thalamic sensitization, was significantly associated with VM patients compared with MwoVS patients, which indicates that thalamic sensitization may play a key role VM pathogenesis. Furthermore, IWPH may enhance susceptibility to thalamic sensitization.

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“…HFS (100 Hz, 60 µs, 100 µA, bipolar, monophasic square-wave pulses) was applied with a stimulator (DS8000, World Precision Instruments, Sarasota, Florida) connected to a constant-current isolator (DLS100, WPI, Sarasota, Florida). These stimulation parameters were based on previous experiments [20]. Regular and irregular external auditory sound sequences were repeated, each being preceded by HFS, again using a counterbalanced design.…”

Section: Deep Brain Stimulationmentioning

confidence: 99%

“…DBS has recently emerged as a promising treatment option for tinnitus [15][16][17]. High-frequency stimulation (HFS) applied to the auditory pathway has been shown to effectively reduce tinnitus-like behavior in rats [18][19][20]. The exact working mechanisms of DBS remain elusive, although complex inhibitory and distant excitatory effects have been described [15,21].…”

Section: Introductionmentioning

confidence: 99%

The effect of noise trauma and high-frequency stimulation on thalamic sensory gating in rodents

Zare

Zwieten

Kotz

et al. 2020

Preprint

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BackgroundThe medial geniculate body (MGB) of the thalamus plays a central role in tinnitus pathophysiology. Breakdown of sensory gating in this part of the auditory thalamus is a potential mechanism underlying tinnitus. The alleviation of tinnitus-like behavior by high-frequency stimulation (HFS) of the MGB might mitigate dysfunctional sensory gating. ObjectiveThe study aims at exploring the role of the MGB in sensory gating as a mandatory relay area in auditory processing in noise-exposed and control subjects, and to assess the effect of MGB HFS on this function. Methods Noise-exposed rats and controls were tested. Continuous auditory sequences were presented to allow assessment of sensory gating effects associated with pitch, binary grouping, and temporal regularity. Evoked potentials (EP) were recorded from the MGB and acquired before and after HFS (100 Hz). Results Noise-exposed rats showed differential modulation of MGB EP amplitudes, confirmed by significant main effects of stimulus type, pair position and temporal regularity. Noiseexposure selectively abolished the effect of temporal regularity on EP amplitudes. A significant three-way interaction between HFS phase, temporal regularity and rat condition (noise-exposed, control) revealed that only noise-exposed rats showed significantly reduced EP amplitudes following MGB HFS. Conclusion This is the first report that shows thalamic filtering of incoming auditory signals based on different sound features. Noise-exposed rats further showed higher EP amplitudes in most conditions and did not differentiate the temporal regularity. Critically, MGB HFS was effective in reducing amplitudes of the EP responses in noise-exposed animals. Highlights▪ EP findings indicate sensory gating in the MGB in rats. ▪ Noise exposure alters EP amplitudes in the MGB. ▪ HFS selectively suppresses EP responses in noise-exposed animals.Abbreviations deep brain stimulation (DBS), evoked potentials (EP), high-frequency stimulation (HFS), linear mixed-effects model (LMEM), medial geniculate body (MGB), sensory gating (SG)

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Inhibition of Experimental Tinnitus With High Frequency Stimulation of the Rat Medial Geniculate Body

Abstract: High frequency stimulation of the MGB has a direct and residual suppressing effect on tinnitus in this animal model. Low frequency stimulation of the MGB did not inhibit tinnitus.

Cited by 19 publications

References 75 publications

Auditory thalamus dysfunction and pathophysiology in tinnitus: a predictive network hypothesis

Auditory thalamus dysfunction and pathophysiology in tinnitus: a predictive network hypothesis

Differences in characteristics between definite vestibular migraines, migraines with vestibular symptoms that do not meet vestibular migraine criteria, and migraines without vestibular symptoms: A cross-sectional study through the lens of central sensitization

The effect of noise trauma and high-frequency stimulation on thalamic sensory gating in rodents

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