A utricular origin of frequency tuning to low-frequency vibration in the human vestibular system?

doi:10.1016/j.neulet.2008.12.055

Neuroscience Letters

Volume 451, Issue 3, 27 February 2009, Pages 175-180

https://doi.org/10.1016/j.neulet.2008.12.055 Get rights and content

Abstract

Recent work has demonstrated that the human vestibular system displays a remarkable sensitivity to low-frequency vibration. To address the origin of this sensitivity we compared the frequency response properties of vestibular reflexes to 10 ms bursts of air-conducted sound and transmastoid vibration, which are thought to be differentially selective for the saccule and utricle, respectively. Measurements were made using two separate central pathways: vestibular evoked myogenic potentials (VEMPs), which are a manifestation of vestibulo-collic projections, and ocular vestibular evoked myogenic potentials (OVEMPs), which are a manifestation of vestibulo-ocular projections. For both response pathways air-conducted sound and vibration stimuli produced the same patterns of quite different tuning. Sound was characterised by a band-pass tuning with best frequency between 400 and 800 Hz whereas vibration showed a low-pass type response with a largest response at 100 Hz. Our results suggest that the tuning is at least in part due to properties of end-organs themselves, while the 100 Hz best frequency may be a specifically utricular feature.

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Acknowledgements

We thank Sendhil Govender for assistance in data collection. This work was supported by the National Health and Medical Research Council of Australia and the Garnett Passe and Rodney Williams Foundation.

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Cited by (105)

Why and when to refer patients for vestibular evoked myogenic potentials: A critical review
2019, Clinical Neurophysiology
Citation Excerpt :
The same frequency tuning changes have also been noted with oVEMPs (Singh and Barman, 2016). With regards to the frequency sensitivity itself, it is suggested that the phenomenon of frequency tuning in the vestibular end organs may be a result of an electrical resonance intrinsic to the hair cells (Ashmore, 1983; Todd et al., 2009). It is usually assessed by performing both c- and oVEMPs in the standard way, but separately using two different sound frequencies, namely 500 Hz and 1 kHz.
Cervical and ocular vestibular evoked myogenic potentials (cVEMPs and oVEMPs respectively) are now used by an increasing number of laboratories to evaluate otolith inner ear function and their pathways through the central nervous system. However, the literature is incomplete or unclear as to what information both c- and oVEMPs can add beyond what a good clinical examination can provide, and what other paramedical tests can provide also, and the present review aims to clarify what is known so far. The following review will describe what is known with regards to both c- and oVEMPs and their use. MEDLINE (accessed by PubMed, years 1994–2018) was searched with the following string: (“vestibular evoked myogenic potentials” [all fields]). Only articles published in English were evaluated. Both c- and oVEMPs are useful not only for confirming the presence of superior semicircular canal dehiscence (SSCD), but also for confirming the presence of acoustic neuromas when MRI is not available, bilateral vestibulopathies, inferior vestibular neuritis and vestibular dysfunction in inherited neuropathies. Further work is required, especially with respect to oVEMPs. The usefulness of both c- and oVEMPs goes beyond the confirmation of SSCDs, and is useful in many clinical cases.
Skull vibration induced nystagmus in patients with superior semicircular canal dehiscence
2019, Annales Francaises d'Oto-Rhino-Laryngologie et de Pathologie Cervico-Faciale
Optimiser la fréquence et la topographie des stimulations utilisées par le test de vibration osseux vestibulaire (TVOV) dans les déhiscences du canal semi-circulaire antérieur.
La comparaison 3D des composantes du nystagmus induit par vibration (NIV) a été effectuée chez 40 patients porteurs d’une déhiscence du canal semi-circulaire antérieur (27 unilatérales et 13 bilatérales), 18 patients avec un déficit vestibulaire sévère et un groupe témoin de 11 volontaires.
Dans les déhiscences unilatérales du canal semi-circulaire antérieur, les composantes torsionnelle et horizontale du NIV, obtenu au niveau du vertex dans 88 % des cas, battaient vers le côté lésé dans 95 % des cas, et pouvaient être observées jusqu’à la fréquence 800 Hz (la fréquence optimale se situant autour de 500 Hz). La vitesse de la phase lente du NIV était significativement plus importante après stimulation du vertex à 100 et 300 Hz (p = 0,04) qu’au niveau des mastoïdes. La composante verticale du NIV était le plus souvent supérieure qu’inférieure. Un NIV était significativement plus souvent observé dans les déhiscences unilatérales que bilatérales (p = 0,009) et avec une vitesse de phase lente (composante horizontale) plus importante (p = 0,008). Dans les déficits sévères unilatéraux vestibulaires la fréquence optimale était de 100 Hz et le NIV battait vers le côté intact. La stimulation mastoïdienne était significativement plus efficace que la stimulation du vertex à 60 et 100 Hz (p < 0,01).
Le TVOV révèle instantanément dans les déhiscences unilatérales du canal semi-circulaire antérieur un nystagmus caractéristique, principalement retrouvé au niveau du vertex, battant, pour les composantes torsionnelle et horizontale, vers le côté lésé et avec une sensibilité étendue vers les hautes fréquences. L’analyse des 3 composants du NIV suggère la stimulation conjointe du canal semi-circulaire antérieur et de l’utricule. Le TVOV agit comme un Weber vestibulaire, montre une asymétrie de la fonction vestibulaire et s’avère utile pour diagnostiquer la présence d’une déhiscence unilatérale du canal semi-circulaire antérieur.
Skull vibration induced nystagmus in patients with superior semicircular canal dehiscence
2019, European Annals of Otorhinolaryngology, Head and Neck Diseases
To establish optimum stimulus frequency and location of bone conducted vibration provoking a skull vibration induced nystagmus (SVIN) in superior semi-circular canal dehiscences.
SVIN 3D components in 40 patients with semi-circular canal dehiscence (27 unilateral and 13 bilateral) were compared with a group of 18 patients with severe unilateral vestibular loss and a control group of 11 volunteers.
In unilateral semi-circular canal dehiscences, SVIN torsional and horizontal components observed on vertex location in 88% beat toward the lesion side in 95%, and can be obtained up to 800 Hz (around 500 Hz being optimal). SVIN slow-phase-velocity was significantly higher on vertex stimulation at 100 and 300 Hz (P = 0.04) than on mastoids. SVIN vertical component is more often upbeating than downbeating. A SVIN was significantly more often observed in unilateral than bilateral semi-circular-canal dehiscences (P = 0.009) and with a higher slow phase velocity (P = 0.008). In severe unilateral vestibular lesions the optimal frequency was 100 Hz and SVIN beat toward the intact side. The mastoid stimulation was significantly more efficient than vertex stimulation at 60 and 100 Hz (P < 0.01).
SVIN reveals instantaneously in unilateral semi-circular canal dehiscences a characteristic nystagmus beating, for the torsional and horizontal components, toward the lesion side and with a greater sensitivity toward high frequencies on vertex stimulation. SVIN three components analysis suggests a stimulation of both superior semi-circular canal and utricle. SVIN acts as a vestibular Weber test, assessing a vestibular asymmetrical function and is a useful indicator for unilateral semi-circular canal dehiscence.
Effects of the stimulus phase on the air-conducted ocular vestibular evoked myogenic potential in healthy subjects
2017, Clinical Neurophysiology
Citation Excerpt :
It was also shown that the afferent units have a tuning curve after ACS and BCV with maximal responses between 500 and 1000 Hz (Curthoys et al., 2006, 2016; McCue and Guinan, 1994; Murofushi and Curthoys, 1997; Young et al., 1977). Although it was demonstrated that the responses also show tuning curves (Chihara et al., 2009; Park et al., 2010; Rauch et al., 2004; Taylor et al., 2012; Todd et al., 2000, 2009; Welgampola and Colebatch, 2001; Zhang et al., 2011) and the responses tend to occur spaced by 2 ms after stimulation with 500 Hz tone bursts (Lim et al., 2013), the effect of the stimulus phase in humans, however, is not as clear. Until this study was written, Govender et al. (2016a) were the only authors to the best of our knowledge who formally described the effect of ACS stimulus polarity in humans and, contrary to what would be expected from the animal studies, they did not find significant differences in latencies or amplitude of the responses.
The study aimed to examine the effect of the stimulus phase of air-conducted sound on ocular vestibular evoked myogenic potentials (oVEMPs).
oVEMPs were recorded after air-conducted sounds (500 Hz, 4 ms duration), presented with initial condensation (positive), rarefaction (negative), and alternant polarities from 12 healthy subjects.
Most responses showed a bifid n10 peak separated by ∼1.9 ms. The most prominent sub-peak after condensation was shorter than the most prominent sub-peak after rarefaction; however, the first sub-peak was shorter after the rarefaction stimuli. When a third sub-peak appeared, it occurred before the most prominent sub-peak after condensation and after the most prominent sub-peak after rarefaction. The latency difference between this third sub-peak and the closest sub-peak was shorter than the difference among the others sub-peaks, in both cases; the oVEMPs after alternating stimuli was an amalgam of the responses to the different stimuli.
The findings suggest that the negative to positive change of the stimulus was the main event responsible for the stimulation, and that when a third sub-peak appeared it was related to the initiation or the end of the stimulus.
These findings suggested that the oVEMP response, obtained by air conducted sound, was secondary to stimulation of the same type of afferent vestibular unit, independent of the stimulus polarity.
Vestibular-dependent inter-stimulus interval effects on sound evoked potentials of central origin
2016, Hearing Research
Todd et al. (2014ab) have recently demonstrated the presence of vestibular-dependent contributions to auditory evoked potentials (AEPs) when passing through the vestibular threshold as determined by vestibular evoked myogenic potentials (VEMPs), including a particular deflection labeled as an N42/P52 prior to the long-latency AEPs N1 and P2. In this paper we report the results of an experiment to determine the effect of inter-stimulus interval (ISI) and regularity on potentials recorded above and below VEMP threshold. Five healthy, right-handed subjects were recruited and evoked potentials were recorded to binaurally presented sound stimulation, above and below vestibular threshold, at seven stimulus rates with ISIs of 212, 300, 424, 600, 848, 1200 and 1696 ms. The inner five intervals, i.e. 300, 424, 600, 848, 1200 ms, were presented twice in both regular and irregular conditions. ANOVA on the global field power (GFP) were conducted for each of four waves, N42, P52, N1 and P2 with factors of intensity, ISI and regularity. Both N42 and P52 waves showed significant ANOVA effects of intensity but no other main effects or interactions. In contrast both N1 and P2 showed additional effects of ISI, as well as intensity, and evidence of non-linear interactions between ISI and intensity. A source analysis was carried out consistent with prior work suggesting that when above vestibular threshold, in addition to bilateral superior temporal cortex, ocular, cerebellar and cingulate sources are recruited. Further statistical analysis of the source currents indicated that the origin of the interactions with intensity may be the ISI sensitivity of the vestibular-dependent sources. This in turn may reflect a specific vestibular preference for stimulus rates associated with locomotion, i.e. rates close to 2 Hz, or ISIs close to 500 ms, where saccular afferents show increased gain and the corresponding reflexes are most sensitive.
Masseter vestibular-evoked myogenic potentials at different tone burst frequencies in healthy individuals
2023, Egyptian Journal of Otolaryngology

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A utricular origin of frequency tuning to low-frequency vibration in the human vestibular system?

Abstract

Section snippets

Acknowledgements

Clin. Neurophysiol.

Exp. Neurol.

Hear. Res.

Hear. Res.

Clin. Neurophysiol.

Clin. Neurophysiol.

Neurosci. Lett.

Hear. Res.

Neurological Anatomy in Relation to Clinical Medicine

Myogenic potentials generated by a click-evoked vestibulocollic reflex

J. Neurol. Neurosurg. Psychiatry

Bone conducted vibration selectively activates irregular primary otolithic vestibular neurons in the guinea pig

Exp. Brain Res.

Ocular counterrolling as an indicator of vestibular otolith function

Neurology

Acoustic responses recorded from the saccular bundle on the eighth nerve of the guinea pig

Hear. Res.

A model for electrical resonance and frequency tuning in saccular hair cells of the bull-frog, Rana catesbeiana

J. Physiol.