Reviewing the Role of the Efferent Vestibular System in Motor and Vestibular Circuits

Mathews, Miranda A.; Camp, Aaron J.; Murray, Andrew

doi:10.3389/fphys.2017.00552

Cited by 42 publications

(27 citation statements)

References 166 publications

(280 reference statements)

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“…It has been shown that cochlear efferents have to be stimulated at least at 10 Hz to facilitate their normally low probability of release (Ballestero et al, 2011), and it is a reasonable assumption that the same is required for vestibular efferents. Vestibular efferents in mouse brainstem slices (Leijon and Magnusson, 2014;Mathews et al, 2015Mathews et al, , 2017 have spontaneous resting discharges of up to 5 spikes/s. The main input to efferent neurons is provided by the vestibular nuclei, and the spontaneous activity of vestibular nuclei neurons is ϳ5 times higher in alert mice (57.5 Ϯ 4.2 spike/s) (Beraneck and Cullen, 2007) compared Figure 8.…”

Section: Discussionmentioning

confidence: 99%

Efferent Inputs Are Required for Normal Function of Vestibular Nerve Afferents

2019

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A group of vestibular afferent nerve fibers with irregular-firing resting discharges are thought to play a prominent role in responses to fast head movements and vestibular plasticity. We show that, in C57BL/6 mice (either sex, 4-5 weeks old), normal activity in the efferent vestibular pathway is required for function of these irregular afferents. Thermal inhibition of efferent fibers results in a profound inhibition of irregular afferents' resting discharges, rendering them inadequate for signaling head movements. In this way, efferent inputs adjust the contribution of the peripheral irregular afferent pathway that plays a critical role in peripheral vestibular signaling and plasticity.

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Section: Discussionmentioning

confidence: 99%

Efferent Inputs Are Required for Normal Function of Vestibular Nerve Afferents

2019

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“…Several studies have provided evidence for α9 * nAChRs/SK in bird and mammalian crista hair cells (Li and Correia, 2011 ; Zhou et al, 2013 ; Yu et al, 2014 ; Poppi et al, 2015 ), but the relationship among hair cell location, α9 * nAChRs expression and corresponding efferent-mediated afferent responses in these species has not been resolved (Dickman and Correia, 1993 ; Lustig et al, 1999 ; Li and Correia, 2011 ). Furthermore, using efferent-mediated response in vestibular afferents to map out α9 * nAChRs in hair cells is particularly challenging in mammals since afferents are invariably excited by efferent stimulation (Goldberg and Fernández, 1980 ; Marlinski et al, 2004 ; Holt et al, 2015b ; Mathews et al, 2017 ). Our data demonstrate that α9 * nAChR-mediated changes in hair cell currents and voltages vary across the neuroepithelium, being larger in type II hair cells in the torus region than those in the central zone, while no apparent ACh responses were observed in hair cells from the planum region.…”

Section: Discussionmentioning

confidence: 99%

“…Vestibular efferent neurons (VENs) branch extensively to produce many presynaptic varicosities abutting hair cells, and both bouton and calyceal afferent processes (Smith and Rasmussen, 1968 ; Sans and Highstein, 1984 ; Lysakowski and Goldberg, 1997 ; Purcell and Perachio, 1997 ; Jordan et al, 2013 ). VENs, upon stimulation, may inhibit and/or excite the background discharge of vestibular afferents by activating acetylcholine receptors (AChRs) at each of these synaptic contacts (Goldberg and Fernández, 1980 ; Rossi et al, 1980 ; Highstein and Baker, 1985 ; Brichta and Goldberg, 2000b ; Boyle et al, 2009 ; Mathews et al, 2017 ). Pharmacological data indicate that the subsequent activation of both nicotinic (nAChRs) and muscarinic ACh receptors (mAChRs) on hair cells and afferents underlie many of these efferent-mediated inhibitory and excitatory responses (Guth et al, 1998 ; Holt et al, 2011 , 2017 ).…”

Section: Introductionmentioning

confidence: 99%

Confirming a Role for α9nAChRs and SK Potassium Channels in Type II Hair Cells of the Turtle Posterior Crista

Parks

Contini

Jordan

et al. 2017

Front. Cell. Neurosci.

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In turtle posterior cristae, cholinergic vestibular efferent neurons (VENs) synapse on type II hair cells, bouton afferents innervating type II hair cells, and afferent calyces innervating type I hair cells. Electrical stimulation of VENs releases acetylcholine (ACh) at these synapses to exert diverse effects on afferent background discharge including rapid inhibition of bouton afferents and excitation of calyx-bearing afferents. Efferent-mediated inhibition is most pronounced in bouton afferents innervating type II hair cells near the torus, but becomes progressively smaller and briefer when moving longitudinally through the crista toward afferents innervating the planum. Sharp-electrode recordings have inferred that efferent-mediated inhibition of bouton afferents requires the sequential activation of alpha9-containing nicotinic ACh receptors (α9*nAChRs) and small-conductance, calcium-dependent potassium channels (SK) in type II hair cells. Gradations in the strength of efferent-mediated inhibition across the crista likely reflect variations in α9*nAChRs and/or SK activation in type II hair cells from those different regions. However, in turtle cristae, neither inference has been confirmed with direct recordings from type II hair cells. To address these gaps, we performed whole-cell, patch-clamp recordings from type II hair cells within a split-epithelial preparation of the turtle posterior crista. Here, we can easily visualize and record hair cells while maintaining their native location within the neuroepithelium. Consistent with α9*nAChR/SK activation, ACh-sensitive currents in type II hair cells were inward at hyperpolarizing potentials but reversed near −90 mV to produce outward currents that typically peaked around −20 mV. ACh-sensitive currents were largest in torus hair cells but absent from hair cells near the planum. In current clamp recordings under zero-current conditions, ACh robustly hyperpolarized type II hair cells. ACh-sensitive responses were reversibly blocked by the α9nAChR antagonists ICS, strychnine, and methyllycaconitine as well as the SK antagonists apamin and UCL1684. Intact efferent terminals in the split-epithelial preparation spontaneously released ACh that also activated α9*nAChRs/SK in type II hair cells. These release events were accelerated with high-potassium external solution and all events were blocked by strychnine, ICS, methyllycaconitine, and apamin. These findings provide direct evidence that activation of α9*nAChR/SK in turtle type II hair cells underlies efferent-mediated inhibition of bouton afferents.

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“…In addition, the proposed algorithm is also able to generate nerve fiber orientation fields for various nerve volume shapes present in the vestibular model (like the IAC). It should also be noted that no fibers of the vestibular efferent system were considered in our model, since its distinct functional role in motor and vestibular coordination is not clear yet and varies significantly between species (Marianelli et al, 2015 ; Mathews et al, 2017 ).…”

Section: Discussionmentioning

confidence: 99%

Model-based Vestibular Afferent Stimulation: Modular Workflow for Analyzing Stimulation Scenarios in Patient Specific and Statistical Vestibular Anatomy

et al. 2017

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Our sense of balance and spatial orientation strongly depends on the correct functionality of our vestibular system. Vestibular dysfunction can lead to blurred vision and impaired balance and spatial orientation, causing a significant decrease in quality of life. Recent studies have shown that vestibular implants offer a possible treatment for patients with vestibular dysfunction. The close proximity of the vestibular nerve bundles, the facial nerve and the cochlear nerve poses a major challenge to targeted stimulation of the vestibular system. Modeling the electrical stimulation of the vestibular system allows for an efficient analysis of stimulation scenarios previous to time and cost intensive in vivo experiments. Current models are based on animal data or CAD models of human anatomy. In this work, a (semi-)automatic modular workflow is presented for the stepwise transformation of segmented vestibular anatomy data of human vestibular specimens to an electrical model and subsequently analyzed. The steps of this workflow include (i) the transformation of labeled datasets to a tetrahedra mesh, (ii) nerve fiber anisotropy and fiber computation as a basis for neuron models, (iii) inclusion of arbitrary electrode designs, (iv) simulation of quasistationary potential distributions, and (v) analysis of stimulus waveforms on the stimulation outcome. Results obtained by the workflow based on human datasets and the average shape of a statistical model revealed a high qualitative agreement and a quantitatively comparable range compared to data from literature, respectively. Based on our workflow, a detailed analysis of intra- and extra-labyrinthine electrode configurations with various stimulation waveforms and electrode designs can be performed on patient specific anatomy, making this framework a valuable tool for current optimization questions concerning vestibular implants in humans.

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Reviewing the Role of the Efferent Vestibular System in Motor and Vestibular Circuits

Cited by 42 publications

References 166 publications

Efferent Inputs Are Required for Normal Function of Vestibular Nerve Afferents

Efferent Inputs Are Required for Normal Function of Vestibular Nerve Afferents

Confirming a Role for α9nAChRs and SK Potassium Channels in Type II Hair Cells of the Turtle Posterior Crista

Model-based Vestibular Afferent Stimulation: Modular Workflow for Analyzing Stimulation Scenarios in Patient Specific and Statistical Vestibular Anatomy

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