1
|
Curthoys IS, Zee DS, Dumas G, Pastras CJ, Dlugaiczyk J. Skull vibration induced nystagmus, velocity storage and self-stability. Front Neurol 2025; 16:1533842. [PMID: 39968451 PMCID: PMC11832403 DOI: 10.3389/fneur.2025.1533842] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/25/2024] [Accepted: 01/17/2025] [Indexed: 02/20/2025] Open
Abstract
In this paper we give an introduction to the area, followed by brief reviews of the neural response to sound and vibration, and then the velocity storage integrator, before putting forward our hypothesis about the neural input to the velocity storage integrator. Finally we discuss some of the implications of our hypothesis. There are two pathways conveying neural information from the vestibular periphery (the semicircular canals and the otoliths) to central neural mechanisms-a direct and an indirect pathway. Within the indirect pathway there is a unique neural mechanism called the velocity storage integrator (VSI) which is part of a neural network generating prolonged nystagmus, afternystagmus and the sensation of self-motion and its converse self-stability. It is our hypothesis that only neural input from primary afferent neurons with irregular resting discharge projects in the direct pathway, whereas the primary afferent input in the indirect pathway consists of neurons with regular resting discharge. The basis for this hypothesis is that vibration is a selective stimulus for vestibular neurons with irregular resting discharge. 100 Hz mastoid vibration, while capable of generating nystagmus (skull vibration induced nystagmus SVIN), is ineffective in generating afternystagmus (in the condition of an encased labyrinth) which is a marker of the action of the VSI, leading to the conclusion that irregular afferents bypass the indirect pathway and the VSI. In order to present this hypothesis we review the evidence that irregular neurons are selectively activated by sound and vibration, whereas regular neurons are not so activated. There are close similarities between the temporal characteristics of the irregular afferent neural response to vibration and the temporal characteristics of SVIN. SVIN is a simple clinical indicator of whether a patient has an imbalance between the two vestibular labyrinths and our hypothesis ties SVIN to irregular primary vestibular neurons.
Collapse
Affiliation(s)
- Ian S. Curthoys
- Vestibular Research Laboratory, School of Psychology, The University of Sydney, Sydney, NSW, Australia
| | - David S. Zee
- Departments of Neurology, Neuroscience, Ophthalmology, Otolaryngology-Head and Neck Surgery, The Johns Hopkins University School of Medicine, The Johns Hopkins Hospital, Baltimore, MD, United States
| | - Georges Dumas
- Department of Oto-Rhino-Laryngology Head and Neck Surgery, University Hospital, Grenoble, France
- Research Unit DevAH — Development, Adaptation and Handicap, Faculty of Medicine, University of Lorraine, Vandoeuvre-lès-Nancy, France
| | - Christopher J. Pastras
- Faculty of Science and Engineering, School of Engineering, Macquarie University, Sydney, NSW, Australia
| | - Julia Dlugaiczyk
- Department of Otorhinolaryngology, Head and Neck Surgery & Interdisciplinary Center for Vertigo, Balance and Ocular Motor Disorders, University Hospital Zurich (USZ), University of Zurich (UZH), Zurich, Switzerland
| |
Collapse
|
2
|
Kjærsgaard JB, Hougaard DD, Kingma H. Thirty years with cervical vestibular myogenic potentials: a critical review on its origin. Front Neurol 2025; 15:1502093. [PMID: 39911743 PMCID: PMC11794123 DOI: 10.3389/fneur.2024.1502093] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/26/2024] [Accepted: 12/17/2024] [Indexed: 02/07/2025] Open
Abstract
Myogenic potentials generated by acoustic stimulation of the vestibular system have been reported since 1964. This examination became better known as cervical vestibular evoked myogenic potentials (cVEMPs) and gained increasing clinical application since the nineties. Since its discovery, the saccule has been conceived as the most likely vestibular end-organ driving these myogenic potentials of the neck. As findings from both animal and human studies for a long time uniformly provided evidence supporting this theory, cVEMP assessment has become synonymous with evaluation of saccular and inferior vestibular nerve function. This review of the basic evidence supporting this conclusion, questions if cVEMP may be considered as being predominantly or even exclusively driven by the activation of any single vestibular end-organ. We conclude that the results of this review show that contributions from the crista ampullaris of all three ipsilateral semicircular canals, as well as the ipsilateral utricle cannot be ruled out in clinically conducted cVEMP assessments.
Collapse
Affiliation(s)
- Jonas Bruun Kjærsgaard
- Department of Otolaryngology, Head & Neck Surgery and Audiology, Aalborg University Hospital, Aalborg, Denmark
- Department of Clinical Medicine, Aalborg University, Aalborg, Denmark
| | - Dan Dupont Hougaard
- Department of Otolaryngology, Head & Neck Surgery and Audiology, Aalborg University Hospital, Aalborg, Denmark
- Department of Clinical Medicine, Aalborg University, Aalborg, Denmark
| | - Herman Kingma
- Department of Otolaryngology, Head & Neck Surgery and Audiology, Aalborg University Hospital, Aalborg, Denmark
- Department of Clinical Medicine, Aalborg University, Aalborg, Denmark
| |
Collapse
|
3
|
Han D, Carr CE. Auditory pathway for detection of vibration in the tokay gecko. Curr Biol 2024; 34:4908-4919.e3. [PMID: 39368471 PMCID: PMC11537832 DOI: 10.1016/j.cub.2024.09.016] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/07/2024] [Revised: 09/05/2024] [Accepted: 09/09/2024] [Indexed: 10/07/2024]
Abstract
Otolithic endorgans such as the saccule were thought to be strictly vestibular in amniotes (reptiles, birds, and mammals), with little evidence supporting the auditory function found in fish and amphibians (frogs and salamanders). Here, we demonstrate an auditory role for the saccule in the tokay gecko (Gekko gecko). The nucleus vestibularis ovalis (VeO) in the hindbrain exclusively receives input from the saccule and projects to the auditory midbrain, the torus semicircularis, via an ascending pathway parallel to cochlear pathways. Single-unit recordings show that VeO is exquisitely sensitive to low-frequency vibrations. Moreover, VeO is present in other lepidosaurs, including snakes and Sphenodon. These findings indicate that the ancestral auditory function of the saccule is likely preserved at least in the lepidosaurian lineage of amniotes and mediates sensitive encoding of vibration. VIDEO ABSTRACT.
Collapse
Affiliation(s)
- Dawei Han
- Department of Biology, University of Maryland, College Park, MD 20742, USA
| | - Catherine E Carr
- Department of Biology, University of Maryland, College Park, MD 20742, USA.
| |
Collapse
|
4
|
Kimura A. Cross-modal sensitivities to auditory and visual stimulations in the first-order somatosensory thalamic nucleus. Eur J Neurosci 2024; 60:5621-5657. [PMID: 39192569 DOI: 10.1111/ejn.16510] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/10/2024] [Revised: 07/15/2024] [Accepted: 08/06/2024] [Indexed: 08/29/2024]
Abstract
The ventral posterolateral nucleus (VPL), being categorized as the first-order thalamic nucleus, is considered to be dedicated to uni-modal somatosensory processing. Cross-modal sensory interactions on thalamic reticular nucleus cells projecting to the VPL, on the other hand, suggest that VPL cells are subject to cross-modal sensory influences. To test this possibility, the effects of auditory or visual stimulation on VPL cell activities were examined in anaesthetized rats, using juxta-cellular recording and labelling techniques. Recordings were obtained from 70 VPL cells, including 65 cells responsive to cutaneous electrical stimulation of the hindpaw. Auditory or visual alone stimulation did not elicit cell activity except in three bi-modal cells and one auditory cell. Cross-modal alterations of somatosensory response by auditory and/or visual stimulation were recognized in 61 cells with regard to the response magnitude, latency (time and jitter) and/or burst spiking properties. Both early (onset) and late responses were either suppressed or facilitated, and de novo cell activity was also induced. Cross-modal alterations took place depending on the temporal interval between the preceding counterpart and somatosensory stimulations, the intensity and frequency of sound. Alterations were observed mostly at short intervals (< 200 ms) and up to 800 ms intervals. Sounds of higher intensities and lower frequencies were more effective for modulation. The susceptibility to cross-modal influences was related to cell location and/or morphology. These and previously reported similar findings in the auditory and visual thalamic nuclei suggest that cross-modal sensory interactions pervasively take place in the first-order sensory thalamic nuclei.
Collapse
Affiliation(s)
- Akihisa Kimura
- Department of Physiology, Wakayama Medical University, Wakayama, Japan
| |
Collapse
|
5
|
Hegemann SCA, Bery AK, Kheradmand A. Focused Update on Clinical Testing of Otolith Organs. Audiol Res 2024; 14:602-610. [PMID: 39051195 PMCID: PMC11270297 DOI: 10.3390/audiolres14040051] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/16/2024] [Revised: 06/19/2024] [Accepted: 07/01/2024] [Indexed: 07/27/2024] Open
Abstract
Sensing gravity through the otolith receptors is crucial for bipedal stability and gait. The overall contribution of the otolith organs to eye movements, postural control, and perceptual functions is the basis for clinical testing of otolith function. With such a wide range of contributions, it is important to recognize that the functional outcomes of these tests may vary depending on the specific method employed to stimulate the hair cells. In this article, we review common methods used for clinical evaluation of otolith function and discuss how different aspects of physiology may affect the functional measurements in these tests. We compare the properties and performance of various clinical tests with an emphasis on the newly developed video ocular counter roll (vOCR), measurement of ocular torsion on fundus photography, and subjective visual vertical or horizontal (SVV/SVH) testing.
Collapse
Affiliation(s)
- Stefan C. A. Hegemann
- Balance Clinic Zurich, Nüschelerstrasse 49, CH-8001 Zurich, Switzerland
- Faculty of Medicine, University of Zurich, CH-8005 Zurich, Switzerland
| | - Anand Kumar Bery
- Department of Neurology, School of Medicine, The Johns Hopkins University, Baltimore, MD 21287, USA; (A.K.B.); (A.K.)
| | - Amir Kheradmand
- Department of Neurology, School of Medicine, The Johns Hopkins University, Baltimore, MD 21287, USA; (A.K.B.); (A.K.)
- Department of Otolaryngology-Head and Neck Surgery, School of Medicine, The Johns Hopkins University, Baltimore, MD 21287, USA
- Department of Neuroscience, School of Medicine, The Johns Hopkins University, Baltimore, MD 21287, USA
| |
Collapse
|
6
|
Fröhlich L, Löffler LB. [Practical instructions for recording vestibular evoked myogenic potentials]. HNO 2024; 72:377-388. [PMID: 38536466 DOI: 10.1007/s00106-024-01446-7] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Accepted: 02/13/2024] [Indexed: 04/26/2024]
Abstract
Recording of vestibular evoked myogenic potentials (VEMPs) is a well-established method for functional diagnostics of the otolith organs. VEMPs are vestibular reflexes of the sacculus und utriculus to acoustic stimulation by air-conducted sound or bone-conducted vibration and are recorded by surface electrodes from the cervical (cVEMP) and ocular (oVEMP) muscles. The results of VEMP recordings are part of the neuro-otologic test battery and enable diagnosis of various vestibular disorders or differentiation between non-vestibular and peripheral vestibular vertigo. However, the methods for recording VEMPs vary substantially, although recording and stimulation parameters as well as methods of data analysis have a significant influence on the results. This article provides an overview of recommended parameters as well as practical instructions for the recording, analysis, and interpretation of VEMPs.
Collapse
Affiliation(s)
- Laura Fröhlich
- Klinik und Poliklinik für Hals-Nasen-Ohren-Heilkunde, Universitätsklinikum Bonn (UKB), Venusberg-Campus 1, 53127, Bonn, Deutschland.
| | - Lea Babette Löffler
- Hals‑, Nasen‑, Ohrenheilkunde, Kopf- und Halschirurgie, Heinrich-Braun-Klinikum gemeinnützige GmbH, Zwickau, Deutschland
| |
Collapse
|
7
|
Xie H, Liang M, Mo Y, Schmidt C, Wang C, Chien JH. Comparison Between Effects of Galvanic and Vibration-Based Vestibular Stimulation on Postural Control and Gait Performance in Healthy Participants: A Systematic Review of Cross-Sectional Studies. Ann Biomed Eng 2024; 52:757-793. [PMID: 38148425 DOI: 10.1007/s10439-023-03425-5] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/20/2023] [Accepted: 12/08/2023] [Indexed: 12/28/2023]
Abstract
Electricity and vibration were two commonly used physical agents to provide vestibular stimulation in previous studies. This study aimed to systematically review the effects of galvanic (GVS) and vibration-based vestibular stimulation (VVS) on gait performance and postural control in healthy participants. Five bioscience and engineering databases, including MEDLINE via PubMed, CINAHL via EBSCO, Cochrane Library, Scopus, and Embase, were searched until March 19th, 2023. Studies published between 2000 and 2023 in English involving GVS and VVS related to gait performance and postural control were included. The procedure was followed via the Preferred Reporting Items for Systematic reviews and Meta-Analyses guidelines. The methodological quality of included studies was assessed using the NIH study quality assessment tool for observational cohort and cross-sectional studies. A total of 55 cross-sectional studies met the inclusion criteria and were included in this study. Five studies were good-quality while 49 were moderate-quality and 1 was poor-quality. There were 50 included studies involving GVS and 5 included studies involving VVS. GVS and VVS utilized different physical agents to provide vestibular stimulation and demonstrated similar effects on vestibular perception. Supra-threshold GVS and VVS produced vestibular perturbation that impaired gait performance and postural control, while sub-threshold GVS and VVS induced stochastic resonance phenomenon that led to an improvement. Bilateral vestibular stimulation demonstrated a greater effect on gait and posture than unilateral vestibular stimulation. Compared to GVS, VVS had the characteristics of better tolerance and fewer side effects, which may substitute GVS to provide more acceptable vestibular stimulation.
Collapse
Affiliation(s)
- Haoyu Xie
- Department of Rehabilitation Medicine, The First Affiliated Hospital of Sun Yat-Sen University, Guangzhou, Guangdong, China
| | - Meizhen Liang
- Department of Rehabilitation Medicine, The First Affiliated Hospital of Sun Yat-Sen University, Guangzhou, Guangdong, China
| | - Yujia Mo
- Chan Division of Occupational Science and Occupational Therapy, University of Southern California, Los Angeles, CA, USA
| | - Cindy Schmidt
- Leon S. McGoogan Health Sciences Library, University of Nebraska Medical Center, Omaha, NE, USA
| | - Chuhuai Wang
- Department of Rehabilitation Medicine, The First Affiliated Hospital of Sun Yat-Sen University, Guangzhou, Guangdong, China.
| | | |
Collapse
|
8
|
Obeidat FS, Alghwiri AA, Bell SL. Vestibular evoked myogenic potential (VEMP) test-retest reliability in adults. J Vestib Res 2024; 34:39-48. [PMID: 38108368 DOI: 10.3233/ves-230029] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/19/2023]
Abstract
BACKGROUND The technique of measuring ocular vestibular evoked myogenic potentials (oVEMP) in response to Mini-shaker vibration is relatively new, there is a limited normative data to define the presence or absence of a response in the literature. OBJECTIVE To determine the test-retest reliability of cervical and ocular VEMPs (cVEMP and oVEMP, respectively) to air-conducted sound (ACS) and bone-conducted vibration (BCV) stimulation and to determine normative ranges for the responses. METHODS Twenty normal-hearing individuals (40 ears) and 20 hearing impaired volunteers with normal balance function (40 ears) were examined in this study. ACS cVEMP and BCV oVEMP (using a Mini-shaker) were recorded from both groups to assess the test-retest reliability and to collect normative VEMP data for P1/N1 latencies and amplitudes from 20 normal hearing individuals. To test reliability, VEMP recordings were repeated within the same session. RESULTS The test-retest reliability for all the cVEMP parameters showed excellent reliability whereas oVEMP parameters showed between fair and excellent reliability depending on the parameter tested. Normative data for VEMP P1/N1 latencies and amplitudes were established. CONCLUSIONS Normative data and test-retest reliability for BCV oVEMP using the Mini-shaker at 100 Hz were established in our study for the first time in the literature. Responses appear reliable.
Collapse
Affiliation(s)
- Faten S Obeidat
- Department of Hearing and Speech Sciences, School of Rehabilitation Sciences, University of Jordan, Amman, Jordan
| | - Alia A Alghwiri
- Department of Physiotherapy, School of Rehabilitation Sciences, University of Jordan, Amman, Jordan
| | - Steven L Bell
- Institute of Sound and Vibration Research, University of Southampton, Southampton, UK
| |
Collapse
|
9
|
Pastras CJ, Curthoys IS. Vestibular Testing-New Physiological Results for the Optimization of Clinical VEMP Stimuli. Audiol Res 2023; 13:910-928. [PMID: 37987337 PMCID: PMC10660708 DOI: 10.3390/audiolres13060079] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/18/2023] [Revised: 11/05/2023] [Accepted: 11/07/2023] [Indexed: 11/22/2023] Open
Abstract
Both auditory and vestibular primary afferent neurons can be activated by sound and vibration. This review relates the differences between them to the different receptor/synaptic mechanisms of the two systems, as shown by indicators of peripheral function-cochlear and vestibular compound action potentials (cCAPs and vCAPs)-to click stimulation as recorded in animal studies. Sound- and vibration-sensitive type 1 receptors at the striola of the utricular macula are enveloped by the unique calyx afferent ending, which has three modes of synaptic transmission. Glutamate is the transmitter for both cochlear and vestibular primary afferents; however, blocking glutamate transmission has very little effect on vCAPs but greatly reduces cCAPs. We suggest that the ultrafast non-quantal synaptic mechanism called resistive coupling is the cause of the short latency vestibular afferent responses and related results-failure of transmitter blockade, masking, and temporal precision. This "ultrafast" non-quantal transmission is effectively electrical coupling that is dependent on the membrane potentials of the calyx and the type 1 receptor. The major clinical implication is that decreasing stimulus rise time increases vCAP response, corresponding to the increased VEMP response in human subjects. Short rise times are optimal in human clinical VEMP testing, whereas long rise times are mandatory for audiometric threshold testing.
Collapse
Affiliation(s)
- Christopher J. Pastras
- Faculty of Science and Engineering, School of Engineering, Macquarie University, Sydney, NSW 2109, Australia;
| | - Ian S. Curthoys
- Vestibular Research Laboratory, School of Psychology, The University of Sydney, Sydney, NSW 2006, Australia
| |
Collapse
|
10
|
Raciti FM, Morales Y, Snapp HA, Rajguru SM. A reliable and reproducible protocol for sound-evoked vestibular myogenic potentials in rattus norvegicus. Front Integr Neurosci 2023; 17:1236642. [PMID: 37731913 PMCID: PMC10508189 DOI: 10.3389/fnint.2023.1236642] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/08/2023] [Accepted: 08/21/2023] [Indexed: 09/22/2023] Open
Abstract
Introduction Cervical vestibular evoked myogenic potentials (cVEMPs) provide an objective measure of the integrity of the sacculo-collic pathway leading to their widespread use as a clinical tool in the diagnostic vestibular test battery. Though the application of cVEMPs in preclinical models to assess vestibular function, as performed in relevant clinical populations, remains limited. The present study aimed to establish a rodent model of cVEMP with standardized methods and protocols, examine the neural basis of the responses, and characterize and validate important features for interpretation and assessment of vestibular function. Methods We compared air-conducted sound (ACS)-evoked VEMPs from the sternocleidomastoid muscles in naïve Brown Norway rats. A custom setup facilitated repeatable and reliable measurements which were carried out at multiple intensities with ACS between 1 and 16 kHz and over 7 days. The myogenic potentials were identified by the presence of a positive (P1)-negative (N1) waveform at 3-5 ms from the stimulus onset. Threshold, amplitude, and latency were compared with intensity- and frequency-matched responses within and between animals. Results cVEMP responses were repeatedly evoked with stimulus intensities between 50-100 dB SPL with excellent test-retest reliability and across multiple measurements over 7 days for all frequencies tested. Suprathreshold, cVEMP responses at 90 dB SPL for 6-10 kHz stimuli demonstrated significantly larger amplitudes (p < 0.01) and shorter latencies (p < 0.001) compared to cVEMP responses for 1-4 kHz stimuli. Latency of cVEMP showed sex-dependent variability, but no significant differences in threshold or amplitude between males and females was observed. Discussion The results provide a replicable and reliable setup, test protocol, and comprehensive characterization of cVEMP responses in a preclinical model which can be used in future studies to elucidate pathophysiological characteristics of vestibular dysfunctions or test efficacy of therapeutics.
Collapse
Affiliation(s)
- Federica M. Raciti
- Department of Otolaryngology, University of Miami, Miami, FL, United States
- Department of Biomedical Engineering, University of Miami, Miami, FL, United States
| | - Yasniary Morales
- Department of Otolaryngology, University of Miami, Miami, FL, United States
- Department of Biomedical Engineering, University of Miami, Miami, FL, United States
| | - Hillary A. Snapp
- Department of Otolaryngology, University of Miami, Miami, FL, United States
- Department of Biomedical Engineering, University of Miami, Miami, FL, United States
| | - Suhrud M. Rajguru
- Department of Otolaryngology, University of Miami, Miami, FL, United States
- Department of Biomedical Engineering, University of Miami, Miami, FL, United States
- Bruce W. Carter Department of Veterans Affairs Medical Center, Miami, FL, United States
| |
Collapse
|
11
|
Pastras CJ, Curthoys IS, Rabbitt RD, Brown DJ. Using macular velocity measurements to relate parameters of bone conduction to vestibular compound action potential responses. Sci Rep 2023; 13:10204. [PMID: 37353559 PMCID: PMC10290084 DOI: 10.1038/s41598-023-37102-3] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/29/2022] [Accepted: 06/15/2023] [Indexed: 06/25/2023] Open
Abstract
To examine mechanisms responsible for vestibular afferent sensitivity to transient bone conducted vibration, we performed simultaneous measurements of stimulus-evoked vestibular compound action potentials (vCAPs), utricular macula velocity, and vestibular microphonics (VMs) in anaesthetized guinea pigs. Results provide new insights into the kinematic variables of transient motion responsible for triggering mammalian vCAPs, revealing synchronized vestibular afferent responses are not universally sensitive to linear jerk as previously thought. For short duration stimuli (< 1 ms), the vCAP increases magnitude in close proportion to macular velocity and temporal bone (linear) acceleration, rather than other kinematic elements. For longer duration stimuli, the vCAP magnitude switches from temporal bone acceleration sensitive to linear jerk sensitive while maintaining macular velocity sensitivity. Frequency tuning curves evoked by tone-burst stimuli show vCAPs increase in proportion to onset macular velocity, while VMs increase in proportion to macular displacement across the entire frequency bandwidth tested between 0.1 and 2 kHz. The subset of vestibular afferent neurons responsible for synchronized firing and vCAPs have been shown previously to make calyceal synaptic contacts with type I hair cells in the striolar region of the epithelium and have irregularly spaced inter-spike intervals at rest. Present results provide new insight into mechanical and neural mechanisms underlying synchronized action potentials in these sensitive afferents, with clinical relevance for understanding the activation and tuning of neurons responsible for driving rapid compensatory reflex responses.
Collapse
Affiliation(s)
- Christopher J Pastras
- Faculty of Science and Engineering, School of Engineering, Macquarie University, Sydney, NSW, 2109, Australia.
- School of Medical Sciences, The University of Sydney, Sydney, NSW, 2050, Australia.
| | - Ian S Curthoys
- Vestibular Research Laboratory, School of Psychology, The University of Sydney, Sydney, NSW, 2050, Australia
| | - Richard D Rabbitt
- Departments of Biomedical Engineering, Otolaryngology and Neuroscience Program, University of Utah, Salt Lake City, UT, 84112, USA
| | - Daniel J Brown
- School of Pharmacy and Biomedical Sciences, Curtin University, Bentley, WA, 6102, Australia
| |
Collapse
|
12
|
Curthoys IS, Smith CM, Burgess AM, Dlugaiczyk J. A Review of Neural Data and Modelling to Explain How a Semicircular Canal Dehiscence (SCD) Causes Enhanced VEMPs, Skull Vibration Induced Nystagmus (SVIN), and the Tullio Phenomenon. Audiol Res 2023; 13:418-430. [PMID: 37366683 PMCID: PMC10294846 DOI: 10.3390/audiolres13030037] [Citation(s) in RCA: 2] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/02/2023] [Revised: 05/24/2023] [Accepted: 05/30/2023] [Indexed: 06/28/2023] Open
Abstract
Angular acceleration stimulation of a semicircular canal causes an increased firing rate in primary canal afferent neurons that result in nystagmus in healthy adult animals. However, increased firing rate in canal afferent neurons can also be caused by sound or vibration in patients after a semicircular canal dehiscence, and so these unusual stimuli will also cause nystagmus. The recent data and model by Iversen and Rabbitt show that sound or vibration may increase firing rate either by neural activation locked to the individual cycles of the stimulus or by slow changes in firing rate due to fluid pumping ("acoustic streaming"), which causes cupula deflection. Both mechanisms will act to increase the primary afferent firing rate and so trigger nystagmus. The primary afferent data in guinea pigs indicate that in some situations, these two mechanisms may oppose each other. This review has shown how these three clinical phenomena-skull vibration-induced nystagmus, enhanced vestibular evoked myogenic potentials, and the Tullio phenomenon-have a common tie: they are caused by the new response of semicircular canal afferent neurons to sound and vibration after a semicircular canal dehiscence.
Collapse
Affiliation(s)
- Ian S. Curthoys
- Vestibular Research Laboratory, School of Psychology, University of Sydney, Sydney, NSW 2006, Australia
| | - Christopher M. Smith
- Center for Anatomy and Functional Morphology, Icahn School of Medicine at Mount Sinai, Annenberg Building, Room 12-90, 1468 Madison Ave., New York, NY 10029, USA;
| | - Ann M. Burgess
- Vestibular Research Laboratory, School of Psychology, University of Sydney, Sydney, NSW 2006, Australia
| | - Julia Dlugaiczyk
- Department of Otorhinolaryngology, Head and Neck Surgery & Interdisciplinary Center of Vertigo, Balance and Ocular Motor Disorders, University Hospital Zurich (USZ), University of Zurich (UZH), CH-8091 Zürich, Switzerland
| |
Collapse
|
13
|
Argaet EC, Kwok BYC, Bradley J, Young AS, Nham B, Calic Z, Taylor RL, Pogson JM, Reid N, Kong JHK, Flanagan S, Halmagyi GM, Rosengren SM, Welgampola MS. Subjective visual horizontal correlates better with ocular than with cervical vestibular evoked myogenic potentials. Clin Neurophysiol 2023; 152:1-10. [PMID: 37257318 DOI: 10.1016/j.clinph.2023.04.011] [Citation(s) in RCA: 4] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/26/2022] [Revised: 04/03/2023] [Accepted: 04/24/2023] [Indexed: 06/02/2023]
Abstract
OBJECTIVE To examine the relationship between widely used otolith function tests: the Subjective Visual Horizontal (SVH) and Vestibular Evoked Myogenic Potentials (VEMP). METHODS A retrospective analysis was performed on 301 patients who underwent SVH, ocular and cervical VEMP (oVEMP and cVEMP) tests on the same day. Correlations between the mean SVH tilt and amplitude asymmetry ratios for bone-conducted (BC) oVEMP and air-conducted (AC) cVEMP were examined. Diagnoses included vestibular neuritis, stroke, vestibular migraine, Meniere's disease, sudden sensorineural hearing loss (SSNHL) and vestibular schwannoma. RESULTS SVH results were concordant with the oVEMP in 64% of cases and the cVEMP in 51%. Across all patients, SVH demonstrated a significant moderate correlation with BC oVEMP amplitude asymmetry ratios (r = 0.55, p < 0.001) and a weak correlation with AC cVEMP amplitude asymmetry ratios (r = 0.35, p < 0.001). A stronger correlation between SVH and oVEMPs was observed in patients with vestibular neuritis (r = 0.67, p < 0.001) and SSNHL (r = 0.76, p = 0.001). CONCLUSIONS SVH correlates better with oVEMP than cVEMP symmetry. SIGNIFICANCE This finding reinforces the hypothesis of a common utricular origin for both SVH and oVEMPs which is distinct from the saccular origin of cVEMPs.
Collapse
Affiliation(s)
- Emma C Argaet
- Institute of Clinical Neurosciences, Royal Prince Alfred Hospital, Central Clinical School, University of Sydney, Sydney, Australia
| | - Belinda Y C Kwok
- Institute of Clinical Neurosciences, Royal Prince Alfred Hospital, Central Clinical School, University of Sydney, Sydney, Australia
| | - Justine Bradley
- Institute of Clinical Neurosciences, Royal Prince Alfred Hospital, Central Clinical School, University of Sydney, Sydney, Australia
| | - Allison S Young
- Institute of Clinical Neurosciences, Royal Prince Alfred Hospital, Central Clinical School, University of Sydney, Sydney, Australia
| | - Benjamin Nham
- Institute of Clinical Neurosciences, Royal Prince Alfred Hospital, Central Clinical School, University of Sydney, Sydney, Australia
| | - Zeljka Calic
- Department of Neurophysiology, Liverpool Hospital, Sydney, Australia.
| | - Rachael L Taylor
- Institute of Clinical Neurosciences, Royal Prince Alfred Hospital, Central Clinical School, University of Sydney, Sydney, Australia.
| | - Jacob M Pogson
- Institute of Clinical Neurosciences, Royal Prince Alfred Hospital, Central Clinical School, University of Sydney, Sydney, Australia.
| | - Nicole Reid
- Institute of Clinical Neurosciences, Royal Prince Alfred Hospital, Central Clinical School, University of Sydney, Sydney, Australia.
| | - Jonathan H K Kong
- Department of Otolaryngology, Royal Prince Alfred Hospital, Sydney, Australia; Discipline of Surgery, Sydney Medical School, University of Sydney, Sydney, Australia; Department of Otolaryngology, Head and Neck Surgery, Macquarie University Hospital, Sydney, Australia
| | - Sean Flanagan
- Department of Otolaryngology, St Vincent's Hospital, Sydney, Australia
| | - Gabor M Halmagyi
- Institute of Clinical Neurosciences, Royal Prince Alfred Hospital, Central Clinical School, University of Sydney, Sydney, Australia.
| | - Sally M Rosengren
- Institute of Clinical Neurosciences, Royal Prince Alfred Hospital, Central Clinical School, University of Sydney, Sydney, Australia.
| | - Miriam S Welgampola
- Institute of Clinical Neurosciences, Royal Prince Alfred Hospital, Central Clinical School, University of Sydney, Sydney, Australia.
| |
Collapse
|
14
|
Xie H, Song H, Schmidt C, Chang WP, Chien JH. The effect of mechanical vibration-based stimulation on dynamic balance control and gait characteristics in healthy young and older adults: A systematic review of cross-sectional study. Gait Posture 2023; 102:18-38. [PMID: 36871475 DOI: 10.1016/j.gaitpost.2023.02.013] [Citation(s) in RCA: 4] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 10/22/2022] [Revised: 02/16/2023] [Accepted: 02/21/2023] [Indexed: 03/07/2023]
Abstract
BACKGROUND A good dynamic balance control and stable gait played an important role in the daily ambulation, especially for older adults with sensorimotor degeneration. This study aimed to systematically review the effects and potential mechanisms of mechanical vibration-based stimulation (MVBS) on dynamic balance control and gait characteristics in healthy young and older adults. METHOD Five bioscience and engineering databases, including MEDLINE via PubMed, CINAHL via EBSCO, Cochrane Library, Scopus, and Embase, were searched until September 4th, 2022. Studies published between 2000 and 2022 in English and Chinese involving mechanical vibration related to gait and dynamic balance were included. The procedure was followed via the preferred reporting items for systematic reviews and meta-analysis method. The methodological quality of included studies was assessed using the NIH study quality assessment tool for observational cohort and cross-sectional studies. RESULTS A total of 41 cross-sectional studies met the inclusion criteria and were included in this study. Eight studies were good-quality while 26 were moderate-quality and 7 were poor-quality. There were six categories of MVBS at various frequencies and amplitudes utilized in included studies, including plantar vibration, focal muscle vibration, Achilles tendon vibration, vestibular vibration, cervical vibration, and vibration on nail of hallux. SIGNIFICANCE Different types of MVBS targeting different sensory systems affected the dynamic balance control and gait characteristics differently. MVBS could be used to provide improvement or perturbation to specific sensory systems, to induce different sensory reweight strategies during gait.
Collapse
Affiliation(s)
- Haoyu Xie
- Division of Physical Therapy Education, College of Allied Health Professions, University of Nebraska Medical Center, Omaha, NE, USA
| | - Huiyan Song
- Department of Rehabilitation Medicine, West China Hospital, Sichuan University, Chengdu, Sichuan, China
| | - Cindy Schmidt
- Leon S. McGoogan Health Sciences Library, University of Nebraska Medical Center, Omaha, NE, USA
| | - Wen-Pin Chang
- Department of Occupational Therapy, Rocky Mountain University of Health Professions, Provo, UT, USA
| | | |
Collapse
|
15
|
Shi T, Beaulieu MO, Saunders LM, Fabian P, Trapnell C, Segil N, Crump JG, Raible DW. Single-cell transcriptomic profiling of the zebrafish inner ear reveals molecularly distinct hair cell and supporting cell subtypes. eLife 2023; 12:82978. [PMID: 36598134 PMCID: PMC9851615 DOI: 10.7554/elife.82978] [Citation(s) in RCA: 44] [Impact Index Per Article: 22.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/25/2022] [Accepted: 01/04/2023] [Indexed: 01/05/2023] Open
Abstract
A major cause of human deafness and vestibular dysfunction is permanent loss of the mechanosensory hair cells of the inner ear. In non-mammalian vertebrates such as zebrafish, regeneration of missing hair cells can occur throughout life. While a comparative approach has the potential to reveal the basis of such differential regenerative ability, the degree to which the inner ears of fish and mammals share common hair cells and supporting cell types remains unresolved. Here, we perform single-cell RNA sequencing of the zebrafish inner ear at embryonic through adult stages to catalog the diversity of hair cells and non-sensory supporting cells. We identify a putative progenitor population for hair cells and supporting cells, as well as distinct hair and supporting cell types in the maculae versus cristae. The hair cell and supporting cell types differ from those described for the lateral line system, a distributed mechanosensory organ in zebrafish in which most studies of hair cell regeneration have been conducted. In the maculae, we identify two subtypes of hair cells that share gene expression with mammalian striolar or extrastriolar hair cells. In situ hybridization reveals that these hair cell subtypes occupy distinct spatial domains within the three macular organs, the utricle, saccule, and lagena, consistent with the reported distinct electrophysiological properties of hair cells within these domains. These findings suggest that primitive specialization of spatially distinct striolar and extrastriolar hair cells likely arose in the last common ancestor of fish and mammals. The similarities of inner ear cell type composition between fish and mammals validate zebrafish as a relevant model for understanding inner ear-specific hair cell function and regeneration.
Collapse
Affiliation(s)
- Tuo Shi
- Department of Stem Cell Biology and Regenerative Medicine, Keck School of Medicine, University of Southern CaliforniaLos AngelesUnited States
- Caruso Department of Otolaryngology-Head and Neck Surgery, Keck School of Medicine, University of Southern CaliforniaLos AngelesUnited States
| | - Marielle O Beaulieu
- Department of Otolaryngology-Head and Neck Surgery, University of WashingtonSeattleUnited States
| | - Lauren M Saunders
- Department of Genome Sciences, University of WashingtonSeattleUnited States
| | - Peter Fabian
- Department of Stem Cell Biology and Regenerative Medicine, Keck School of Medicine, University of Southern CaliforniaLos AngelesUnited States
| | - Cole Trapnell
- Department of Genome Sciences, University of WashingtonSeattleUnited States
| | - Neil Segil
- Department of Stem Cell Biology and Regenerative Medicine, Keck School of Medicine, University of Southern CaliforniaLos AngelesUnited States
- Caruso Department of Otolaryngology-Head and Neck Surgery, Keck School of Medicine, University of Southern CaliforniaLos AngelesUnited States
| | - J Gage Crump
- Department of Stem Cell Biology and Regenerative Medicine, Keck School of Medicine, University of Southern CaliforniaLos AngelesUnited States
| | - David W Raible
- Department of Otolaryngology-Head and Neck Surgery, University of WashingtonSeattleUnited States
- Department of Genome Sciences, University of WashingtonSeattleUnited States
- Department of Biological Structure, University of WashingtonSeattleUnited States
| |
Collapse
|
16
|
Han Y, Bai Y, Liu Q, Zhao Y, Chen T, Wang W, Ni G. Assessing vestibular function using electroencephalogram rhythms evoked during the caloric test. Front Neurol 2023; 14:1126214. [PMID: 36908620 PMCID: PMC9996014 DOI: 10.3389/fneur.2023.1126214] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/17/2022] [Accepted: 01/31/2023] [Indexed: 02/25/2023] Open
Abstract
Introduction The vestibular system is responsible for motion perception and balance preservation in the body. The vestibular function examination is useful for determining the cause of associated symptoms, diagnosis, and therapy of the patients. The associated cerebral cortex processes and integrates information and is the ultimate perceptual site for vestibular-related symptoms. In recent clinical examinations, less consideration has been given to the cortex associated with the vestibular system. As a result, it is crucial to increase focus on the expression of the cortical level while evaluating vestibular function. From the viewpoint of neuroelectrophysiology, electroencephalograms (EEG) can enhance the assessments of vestibular function at the cortex level. Methods This study recorded nystagmus and EEG data throughout the caloric test. Four phases were considered according to the vestibular activation status: before activation, activation, fixation suppression, and recovery. In different phases, the distribution and changes of the relative power of the EEG rhythms (delta, theta, alpha, and beta) were analyzed, and the correlation between EEG characteristics and nystagmus was also investigated. Results The results showed that, when the vestibule was activated, the alpha power of the occipital region increased, and the beta power of the central and top regions and the occipital region on the left decreased. The changes in the alpha and beta rhythms significantly correlate with nystagmus values in left warm stimulation. Discussion Our findings offer a fresh perspective on cortical electrophysiology for the assessment of vestibular function by demonstrating that the relative power change in EEG rhythms can be used to assess vestibular function.
Collapse
Affiliation(s)
- Yutong Han
- Academy of Medical Engineering and Translational Medicine, Tianjin University, Tianjin, China.,Tianjin Key Laboratory of Brain Science and Neuroengineering, Tianjin, China
| | - Yanru Bai
- Academy of Medical Engineering and Translational Medicine, Tianjin University, Tianjin, China.,Tianjin Key Laboratory of Brain Science and Neuroengineering, Tianjin, China
| | - Qiang Liu
- Key Laboratory of Auditory Speech and Balance Medicine, Tianjin, China.,Institute of Otolaryngology of Tianjin, Tianjin, China.,Key Medical Discipline of Tianjin (Otolaryngology), Tianjin, China
| | - Yuncheng Zhao
- Tianjin Key Laboratory of Brain Science and Neuroengineering, Tianjin, China.,Department of Biomedical Engineering, College of Precision Instruments and Optoelectronics Engineering, Tianjin University, Tianjin, China
| | - Taisheng Chen
- Key Laboratory of Auditory Speech and Balance Medicine, Tianjin, China.,Institute of Otolaryngology of Tianjin, Tianjin, China.,Key Medical Discipline of Tianjin (Otolaryngology), Tianjin, China
| | - Wei Wang
- Key Laboratory of Auditory Speech and Balance Medicine, Tianjin, China.,Institute of Otolaryngology of Tianjin, Tianjin, China.,Key Medical Discipline of Tianjin (Otolaryngology), Tianjin, China
| | - Guangjian Ni
- Academy of Medical Engineering and Translational Medicine, Tianjin University, Tianjin, China.,Tianjin Key Laboratory of Brain Science and Neuroengineering, Tianjin, China
| |
Collapse
|
17
|
Macena Duarte VO, Neves-Lobo IF, Samelli AG. Effects of noise on the vestibular system of normal-hearing workers. Work 2022; 73:1217-1225. [DOI: 10.3233/wor-211088] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/15/2022] Open
Abstract
BACKGROUND: Studies in noise-exposed animals have shown changes in vestibular structures. Likewise, studies in humans have been suggesting that noise can damage the vestibular system, even with normal assessment results. OBJECTIVE: To assess the vestibular system of workers exposed to noise and to compare with individuals not exposed. METHODS: Twenty normal-hearing male adults were divided in the study group (SG), exposed to occupational noise, and control group (CG). We conducted the following procedures: medical history, Dizziness Handicap Inventory (DHI), Dix-Hallpike maneuver, and electronystagmography (eye and caloric tests). RESULTS: The DHI score did not differ between groups. The Dix-Hallpike maneuver was normal for both groups. All individuals had normal responses in the eye tests. 50% of the SG had hyperreflexia in the caloric tests, with a significant difference between the groups. There was a trend towards a statistical significance in the absolute values of angular speed of the slow component in the cold-air test, which were higher in the SG. There was a significant difference between the groups in the relative values of labyrinthine preponderance, which were higher in the SG. CONCLUSION: Our findings showed that 70% of the workers exposed to occupational noise had vestibular alterations identified with electronystagmography, whereas 100% of the individuals in the CG had normal results in the vestibular assessment. Moreover, only 20% of the sample in both groups had vestibular complaints, indicating the presence of subclinical vestibular changes in 50% of the individuals exposed to occupational noise.
Collapse
Affiliation(s)
- Victor Octávio Macena Duarte
- Department of Physical Therapy, Speech-Language-Hearing Pathology, and Occupational Therapy, Faculty of Medicine (FMUSP), University of São Paulo, São Paulo, Brazil
| | - Ivone Ferreira Neves-Lobo
- Department of Physical Therapy, Speech-Language-Hearing Pathology, and Occupational Therapy, Faculty of Medicine (FMUSP), University of São Paulo, São Paulo, Brazil
| | - Alessandra Giannella Samelli
- Department of Physical Therapy, Speech-Language-Hearing Pathology, and Occupational Therapy, Faculty of Medicine (FMUSP), University of São Paulo, São Paulo, Brazil
| |
Collapse
|
18
|
A Single Fast Test for Semicircular Canal Dehiscence—oVEMP n10 to 4000 Hz—Depends on Stimulus Rise Time. Audiol Res 2022; 12:457-465. [PMID: 36136853 PMCID: PMC9498918 DOI: 10.3390/audiolres12050046] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/07/2022] [Revised: 08/14/2022] [Accepted: 08/21/2022] [Indexed: 11/17/2022] Open
Abstract
As previously reported, a single test measuring oVEMP n10 to 4000 Hz stimuli (bone-conducted vibration (BCV) or air-conducted sound (ACS)) provides a definitive diagnosis of semicircular canal dehiscence (SCD) in 22 CT-verified patients, with a sensitivity of 1.0 and specificity of 1.0. This single short screening test has great advantages of speed, minimizing testing time, and the exposure of patients to stimulation. However, a few studies of the 4000 Hz test for SCD have reported sensitivity and specificity values which are slightly less than reported previously. We hypothesized that the rise time of the stimulus is important for detecting the oVEMP n10 to 4000 Hz, similarly to what we had shown for 500 and 750 Hz BCV. We measured oVEMP n10 in 15 patients with CT-verified SCD in response to 4000 Hz ACS or BCV stimuli with rise times of 0, 1, and 2 ms. As a result, increasing the rise time of the stimulus reduced the oVEMP n10 amplitude. This outcome is expected from the physiological evidence of guinea pig primary vestibular afferents, which are activated by sound or vibration. Therefore, for clinical VEMP testing, short rise times are optimal (preferably 0 ms).
Collapse
|
19
|
Bouisset N, Villard S, Legros A. Vestibular Extremely Low-Frequency Magnetic and Electric Stimulation Effects on Human Subjective Visual Vertical Perception. Bioelectromagnetics 2022; 43:355-367. [PMID: 35801487 PMCID: PMC9541167 DOI: 10.1002/bem.22417] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/13/2021] [Revised: 05/25/2022] [Accepted: 06/18/2022] [Indexed: 11/08/2022]
Abstract
Electric fields from both extremely low‐frequency magnetic fields (ELF‐MF) and alternating current (AC) stimulations impact human neurophysiology. As the retinal photoreceptors, vestibular hair cells are graded potential cells and are sensitive to electric fields. Electrophosphene and magnetophosphene literature suggests different impacts of AC and ELF‐MF on the vestibular hair cells. Furthermore, while AC modulates the vestibular system more globally, lateral ELF‐MF stimulations could be more utricular specific. Therefore, to further address the impact of ELF‐MF‐induced electric fields on the human vestibular system and the potential differences with AC stimulations, we investigated the effects of both stimulation modalities on the perception of verticality using a subjective visual vertical (SVV) paradigm. For similar levels of SVV precision, the ELF‐MF condition required more time to adjust SVV, and SVV variability was higher with ELF‐MF than with AC vestibular‐specific stimulations. Yet, the differences between AC and ELF‐MF stimulations were small. Overall, this study highlights small differences between AC and ELF‐MF vestibular stimulations, underlines a potential utricular contribution, and has implications for international exposure guidelines and standards. © 2022 Bioelectromagnetics Society.
Collapse
Affiliation(s)
- Nicolas Bouisset
- Human Threshold Research and Bioelectromagnetics Group, Imaging, Lawson Health Research Institute, London, Canada.,Department of Kinesiology, Western University, London, Canada
| | - Sébastien Villard
- Human Threshold Research and Bioelectromagnetics Group, Imaging, Lawson Health Research Institute, London, Canada.,Department of Kinesiology, Western University, London, Canada
| | - Alexandre Legros
- Human Threshold Research and Bioelectromagnetics Group, Imaging, Lawson Health Research Institute, London, Canada.,Department of Kinesiology, Western University, London, Canada.,Department of Medical Biophysics, Western University, London, Canada.,Department of Medical Imaging, Western University, London, Canada.,Euromov Digital Heath in Motion, Univ Montpellier, IMT Mines Ales, Montpellier, France.,EuroStim, Montpellier, France
| |
Collapse
|
20
|
Clinard CG, Piker EG, Romero DJ. Inter-trial coherence as a measure of synchrony in cervical vestibular evoked myogenic potentials. J Neurosci Methods 2022; 377:109628. [PMID: 35618165 DOI: 10.1016/j.jneumeth.2022.109628] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/08/2021] [Revised: 05/11/2022] [Accepted: 05/18/2022] [Indexed: 11/16/2022]
Abstract
BACKGROUND Cervical vestibular evoked myogenic potentials (cVEMPs) are surface-recorded responses that reflect saccular function. Analysis of cVEMPs has focused, nearly exclusively, on time-domain waveform measurements such as amplitude and latency of response peaks, but synchrony-based measures have not been previously reported. NEW METHOD Time-frequency analyses were used to apply an objective response-detection algorithm and to quantify response synchrony. These methods are new to VEMP literature and have been adapted from previous auditory research. Air-conducted cVEMPs were elicited using a 500Hz tone burst in twenty young, healthy participants. RESULTS Time-frequency characteristics of cVEMPs and time-frequency boundaries for response energy were established. An inter-trial coherence analysis approach revealed highly synchronous responses with representative inter-trial coherence values of approximately 0.7. COMPARISON WITH EXISTING METHODS Inter-trial coherence measures were highly correlated with conventional amplitude measures in this group of young, healthy adults (R2 = 0.91 - 0.94), although the frequencies at which these measures had their largest magnitude were unrelated (R2 =.02). Conventional measures of peak-to-peak amplitude and latency were consistent with previous literature. Interaural asymmetry ratios were comparable between amplitude- and synchrony-based measures. CONCLUSIONS Synchrony-based time-frequency analyses were successfully applied to cVEMP data and this type of analysis may be helpful to differentiate synchrony from amplitude in populations with disrupted neural synchrony.
Collapse
Affiliation(s)
- Christopher G Clinard
- Department of Communication Sciences and Disorders, 235 MLK Jr. Way, MSC 4304, HBS 1024, James Madison University, Harrisonburg, VA, 22807 USA.
| | - Erin G Piker
- Department of Communication Sciences and Disorders, 235 MLK Jr. Way, MSC 4304, HBS 1024, James Madison University, Harrisonburg, VA, 22807 USA
| | - Daniel J Romero
- Department of Hearing and Speech Sciences, 1215 21(st) Avenue South, Medical Center East, Vanderbilt University, Nashville, TN, 37232 USA
| |
Collapse
|
21
|
Skull Vibration-Induced Nystagmus and High Frequency Ocular Vestibular-Evoked Myogenic Potentials in Superior Canal Dehiscence. Audiol Res 2022; 12:202-211. [PMID: 35447743 PMCID: PMC9030186 DOI: 10.3390/audiolres12020023] [Citation(s) in RCA: 4] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/16/2021] [Revised: 04/07/2022] [Accepted: 04/13/2022] [Indexed: 11/16/2022] Open
Abstract
Background: Although diagnostic criteria have been established for superior canal dehiscence syndrome, cases in which the diagnosis is not easy are frequent. On those occasions, some tests such as vibration-induced nystagmus or vestibular-evoked myogenic potentials can offer invaluable help due to their high sensitivity and specificity. Methods: We studied 30 patients showing superior canal dehiscence or “near-dehiscence” in a CT scan. Skull vibration-induced nystagmus and high frequency ocular vestibular-evoked myogenic potentials are performed in each patient. The aim of the study is to determine how useful both tests are for detection of superior canal dehiscence or near-dehiscence. Results: Of the 60 temporal bones studied, no dehiscence was the result in 22, near-dehiscence in 17 and a definite finding in 21. In 10/30 patients, there was no SVIN (Skull vibration induced nystagmus) during otoneurological testing, while in 6/30, induced nystagmus was mainly horizontal, and in 14/30 there was vertical up-beating. All patients had a positive oVEMP (Ocular vestibular evoked myiogenic potentials) at 0.5 kHz in both ears and the HFoVEMP (High frequency ocular vestibular evoked myiogenic potentials) response was positive in 25/60 (41.6%) of the ears studied and in 19/30 of the patients evaluated (in 6 it was positive in both ears). Up-beat SVIN will point to a SCD (Superior Canal Dehiscence) mainly when HFoVEMP are present, and when this is negative there is a high probability that it is not a SCD. Conclusions: When SVIN and HFoVEMP results are added (or combined), they not only improve the possibilities of detecting SCD, but also the affected side.
Collapse
|
22
|
Clinard CG, Lawlor KJ, Thorne AP, Piker EG. Nonlinearity in bone-conducted amplitude-modulated cervical vestibular evoked myogenic potentials: Harmonic distortion products. J Neurophysiol 2022; 127:791-800. [PMID: 35171737 DOI: 10.1152/jn.00347.2021] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/22/2022] Open
Abstract
Otolith organs of the balance system, the saccule and utricle, encode linear acceleration. Integrity of the saccule is commonly assessed using cervical vestibular evoked myogenic potentials (cVEMPs) arising from an inhibitory reflex along the vestibulospinal pathway. Conventional approaches to eliciting these responses use brief, transient sounds to elicit onset responses. Here we used long-duration amplitude-modulated (AM) tones to elicit cVEMPs (AMcVEMPs) and analyzed their spectral content for evidence of nonlinear processing consistent with known characteristics of vestibular hair cells. Twelve young adults (ages 21-25) with no hearing or vestibular pathologies participated in this study. AMcVEMPs were elicited by bone-conducted AM tones with a 500 Hz carrier frequency. Eighteen modulation frequencies were used between 7 and 403 Hz. All participants had robust distortion products at harmonics of the modulation frequency. Total harmonic distortion ranged from approximately 10 to 80%. AMcVEMPs contain harmonic distortion products consistent with vestibular hair cell nonlinearities, and this new approach to studying the otolith organs may provide a non-invasive, in vivo method to study nonlinearity of vestibular hair cells in humans.
Collapse
Affiliation(s)
- Christopher G Clinard
- Communication Sciences and Disorders, James Madison University, Harrisonburg, VA, United States
| | - Kerri J Lawlor
- Communication Sciences and Disorders, James Madison University, Harrisonburg, VA, United States
| | - Andrew P Thorne
- Communication Sciences and Disorders, James Madison University, Harrisonburg, VA, United States
| | - Erin G Piker
- Communication Sciences and Disorders, James Madison University, Harrisonburg, VA, United States
| |
Collapse
|
23
|
Curthoys IS. The Neural Basis of Skull Vibration Induced Nystagmus (SVIN). Audiol Res 2021; 11:557-566. [PMID: 34698054 PMCID: PMC8544221 DOI: 10.3390/audiolres11040050] [Citation(s) in RCA: 4] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/16/2021] [Revised: 10/09/2021] [Accepted: 10/11/2021] [Indexed: 11/16/2022] Open
Abstract
I list a summary of the major clinical observations of SVIN in patients with total unilateral vestibular loss (TUVL) and show how basic results from neurophysiology can explain these clinical observations. The account integrates results from single neuron recordings of identified semicircular canal and otolith afferent neurons in guinea pigs in response to low frequency skull vibration with evidence of the eye movement response in cats to selective semicircular canal stimulation (both individual and combined) and a simple model of nystagmus generation to show how these results explain most of the major characteristics of SVIN.
Collapse
Affiliation(s)
- Ian S Curthoys
- Vestibular Research Laboratory, School of Psychology, The University of Sydney, Sydney, NSW 2006, Australia
| |
Collapse
|
24
|
Gattie M, Lieven EVM, Kluk K. Weak Vestibular Response in Persistent Developmental Stuttering. Front Integr Neurosci 2021; 15:662127. [PMID: 34594189 PMCID: PMC8477904 DOI: 10.3389/fnint.2021.662127] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/31/2021] [Accepted: 06/14/2021] [Indexed: 11/24/2022] Open
Abstract
Vibrational energy created at the larynx during speech will deflect vestibular mechanoreceptors in humans (Todd et al., 2008; Curthoys, 2017; Curthoys et al., 2019). Vestibular-evoked myogenic potential (VEMP), an indirect measure of vestibular function, was assessed in 15 participants who stutter, with a non-stutter control group of 15 participants paired on age and sex. VEMP amplitude was 8.5 dB smaller in the stutter group than the non-stutter group (p = 0.035, 95% CI [−0.9, −16.1], t = −2.1, d = −0.8, conditional R2 = 0.88). The finding is subclinical as regards gravitoinertial function, and is interpreted with regard to speech-motor function in stuttering. There is overlap between brain areas receiving vestibular innervation, and brain areas identified as important in studies of persistent developmental stuttering. These include the auditory brainstem, cerebellar vermis, and the temporo-parietal junction. The finding supports the disruptive rhythm hypothesis (Howell et al., 1983; Howell, 2004) in which sensory inputs additional to own speech audition are fluency-enhancing when they coordinate with ongoing speech.
Collapse
Affiliation(s)
- Max Gattie
- Manchester Centre for Audiology and Deafness (ManCAD), The University of Manchester, Manchester, United Kingdom
| | - Elena V M Lieven
- Child Study Centre, The University of Manchester, Manchester, United Kingdom.,The ESRC International Centre for Language and Communicative Development (LuCiD), The University of Manchester, Manchester, United Kingdom
| | - Karolina Kluk
- Manchester Centre for Audiology and Deafness (ManCAD), The University of Manchester, Manchester, United Kingdom
| |
Collapse
|
25
|
Nakul E, Bartolomei F, Lopez C. Vestibular-Evoked Cerebral Potentials. Front Neurol 2021; 12:674100. [PMID: 34621231 PMCID: PMC8490637 DOI: 10.3389/fneur.2021.674100] [Citation(s) in RCA: 6] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/28/2021] [Accepted: 08/20/2021] [Indexed: 11/30/2022] Open
Abstract
The human vestibular cortex has mostly been approached using functional magnetic resonance imaging and positron emission tomography combined with artificial stimulation of the vestibular receptors or nerve. Few studies have used electroencephalography and benefited from its high temporal resolution to describe the spatiotemporal dynamics of vestibular information processing from the first milliseconds following vestibular stimulation. Evoked potentials (EPs) are largely used to describe neural processing of other sensory signals, but they remain poorly developed and standardized in vestibular neuroscience and neuro-otology. Yet, vestibular EPs of brainstem, cerebellar, and cortical origin have been reported as early as the 1960s. This review article summarizes and compares results from studies that have used a large range of vestibular stimulation, including natural vestibular stimulation on rotating chairs and motion platforms, as well as artificial vestibular stimulation (e.g., sounds, impulsive acceleration stimulation, galvanic stimulation). These studies identified vestibular EPs with short latency (<20 ms), middle latency (from 20 to 50 ms), and late latency (>50 ms). Analysis of the generators (source analysis) of these responses offers new insights into the neuroimaging of the vestibular system. Generators were consistently found in the parieto-insular and temporo-parietal junction-the core of the vestibular cortex-as well as in the prefrontal and frontal areas, superior parietal, and temporal areas. We discuss the relevance of vestibular EPs for basic research and clinical neuroscience and highlight their limitations.
Collapse
Affiliation(s)
- Estelle Nakul
- Centre National de la Recherche Scientifique (CNRS), Laboratoire de Neurosciences Cognitives (LNC), FR3C, Aix Marseille Univ, Marseille, France
| | - Fabrice Bartolomei
- Institut de Neurosciences des Systèmes, Inserm, Aix Marseille Univ, Marseille, France
- Service de Neurophysiologie Clinique, Hôpital Timone, Aix Marseille Univ, Marseille, France
| | - Christophe Lopez
- Centre National de la Recherche Scientifique (CNRS), Laboratoire de Neurosciences Cognitives (LNC), FR3C, Aix Marseille Univ, Marseille, France
| |
Collapse
|
26
|
Maheu M, Elblidi A, Saliba I. Investigating Performance of cVEMP and oVEMP in the Identification of Superior Canal Dehiscence in Relation to Dehiscence Location and Size. Audiol Res 2021; 11:452-462. [PMID: 34562880 PMCID: PMC8482095 DOI: 10.3390/audiolres11030042] [Citation(s) in RCA: 8] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/26/2021] [Revised: 08/19/2021] [Accepted: 09/07/2021] [Indexed: 01/18/2023] Open
Abstract
Compare the sensitivity and specificity of cVEMP (500 Hz), oVEMP (500 Hz and 4 kHz) in the identification of SSCD. A secondary objective was to identify the influence of dehiscence size and location on cVEMP and oVEMP responses. Methods: Individuals with unilateral (n = 16) and bilateral (n = 10) scan confirmed SSCD were assessed using air-conducted cVEMP and oVEMP Results: For cVEMP, an amplitude cutoff of 286.9 μV or a threshold cutoff of 67.5 dBnHL revealed, respectively, a sensitivity of 75% and 70.6% and a specificity of 69.4% and 100%. For oVEMP (500 Hz), an amplitude cutoff of 10.8 μV or a threshold cutoff of 77.5 dBnHL revealed a sensitivity of 83.33% and a specificity of 87.5% and 80%, respectively. oVEMP (4 kHz), an amplitude cutoff of 3.1 μV, revealed a high specificity of 100% but a low sensitivity of 47.2%. A positive correlation was noted between the length of the SSCD and the cVEMP and oVEMP (500 Hz) thresholds and cVEMP amplitude. Conclusions: Our results support the use of oVEMP in the identification of SSCD. The presence of oVEMP (500 Hz) with an amplitude higher or equal to 10.8 μV, a threshold lower or equal to 77.5 dBnHL or oVEMP (4 kHz) amplitude of 3.1 μV represents the most useful to identify SSCD.
Collapse
Affiliation(s)
- Maxime Maheu
- Faculty of Medicine, School of Speech Language Pathology and Audiology, University of Montreal, Montreal, QC H3N 1X7, Canada
- Centre de Recherche Interdisciplinaire en Réadaptation, Institut Universitaire sur la Réadaptation en Déficience Physique de Montréal (IURDPM), Pavillon Laurier, CIUSSS du Centre-Sud-de-l’Île-de-Montréal, Montreal, QC H2H 1C4, Canada
| | - Ahlem Elblidi
- Montreal University Hospital Center (CHUM), Montreal, QC H2X 3E4, Canada;
| | - Issam Saliba
- Montreal University Hospital Center (CHUM), Montreal, QC H2X 3E4, Canada;
- Department of Surgery, Division of Otorhinolaryngology-Head & Neck Surgery, University of Montreal, Montreal, QC H3C 3J7, Canada
| |
Collapse
|
27
|
Curthoys IS, Grant JW, Pastras CJ, Fröhlich L, Brown DJ. Similarities and Differences Between Vestibular and Cochlear Systems - A Review of Clinical and Physiological Evidence. Front Neurosci 2021; 15:695179. [PMID: 34456671 PMCID: PMC8397526 DOI: 10.3389/fnins.2021.695179] [Citation(s) in RCA: 6] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/14/2021] [Accepted: 07/12/2021] [Indexed: 12/04/2022] Open
Abstract
The evoked response to repeated brief stimuli, such as clicks or short tone bursts, is used for clinical evaluation of the function of both the auditory and vestibular systems. One auditory response is a neural potential - the Auditory Brainstem Response (ABR) - recorded by surface electrodes on the head. The clinical analogue for testing the otolithic response to abrupt sounds and vibration is the myogenic potential recorded from tensed muscles - the vestibular evoked myogenic potential (VEMP). VEMPs have provided clinicians with a long sought-after tool - a simple, clinically realistic indicator of the function of each of the 4 otolithic sensory regions. We review the basic neural evidence for VEMPs and discuss the similarities and differences between otolithic and cochlear receptors and afferents. VEMPs are probably initiated by sound or vibration selectively activating afferent neurons with irregular resting discharge originating from the unique type I receptors at a specialized region of the otolithic maculae (the striola). We review how changes in VEMP responses indicate the functional state of peripheral vestibular function and the likely transduction mechanisms allowing otolithic receptors and afferents to trigger such very short latency responses. In section "ELECTROPHYSIOLOGY" we show how cochlear and vestibular receptors and afferents have many similar electrophysiological characteristics [e.g., both generate microphonics, summating potentials, and compound action potentials (the vestibular evoked potential, VsEP)]. Recent electrophysiological evidence shows that the hydrodynamic changes in the labyrinth caused by increased fluid volume (endolymphatic hydrops), change the responses of utricular receptors and afferents in a way which mimics the changes in vestibular function attributed to endolymphatic hydrops in human patients. In section "MECHANICS OF OTOLITHS IN VEMPS TESTING" we show how the major VEMP results (latency and frequency response) follow from modeling the physical characteristics of the macula (dimensions, stiffness etc.). In particular, the structure and mechanical operation of the utricular macula explains the very fast response of the type I receptors and irregular afferents which is the very basis of VEMPs and these structural changes of the macula in Menière's Disease (MD) predict the upward shift of VEMP tuning in these patients.
Collapse
Affiliation(s)
- Ian S. Curthoys
- Vestibular Research Laboratory, School of Psychology, The University of Sydney, Sydney, NSW, Australia
| | - John Wally Grant
- Department of Biomedical Engineering and Mechanics, Virginia Tech, Blacksburg, VA, United States
| | - Christopher J. Pastras
- The Menière’s Research Laboratory, Sydney Medical School, The University of Sydney, Sydney, NSW, Australia
| | - Laura Fröhlich
- Department of Otorhinolaryngology, Head and Neck Surgery, Martin Luther University Halle-Wittenberg, Halle, Germany
| | - Daniel J. Brown
- School of Pharmacy and Biomedical Sciences, Curtin University, Bentley, WA, Australia
| |
Collapse
|
28
|
Dumas G, Fabre C, Charpiot A, Fath L, Chaney-Vuong H, Perrin P, Schmerber S. Skull Vibration-Induced Nystagmus Test in a Human Model of Horizontal Canal Plugging. Audiol Res 2021; 11:301-312. [PMID: 34202582 PMCID: PMC8293257 DOI: 10.3390/audiolres11030028] [Citation(s) in RCA: 4] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/05/2021] [Revised: 06/17/2021] [Accepted: 06/21/2021] [Indexed: 01/22/2023] Open
Abstract
Background/Aim: the aim of this study was to assess the skull vibration-induced nystagmus test (SVINT) results and vestibular residual function after horizontal semicircular canal (HSCC) plugging. Methods: In this retrospective chart review performed in a tertiary referral center, 11 patients who underwent unilateral horizontal semicircular canal plugging (uHSCCP) for disabling Menière’s disease (MD) were included. The skull vibration-induced nystagmus (SVIN) slow-phase velocity (SPV) was compared with the results of the caloric test (CaT), video head impulse test (VHIT), and cervical vestibular-evoked myogenic potentials (cVEMP) performed on the same day. Results: Overall, 10 patients had a strong SVIN beating toward the intact side (Horizontal SVIN-SPV: 8.8°/s ± 5.6°/s), 10 had a significant or severe ipsilateral CaT hypofunction, 10 had an ipsilateral horizontal VHIT gain impairment, and 3 had altered cVEMP on the operated side. Five had sensorineural hearing worsening. SVIN-positive results were correlated with CaT and horizontal VHIT (HVHIT) results (p < 0.05) but not with cVEMP. SVIN-SPV was correlated with CaT hypofunction in % (p < 0.05). Comparison of pre- and postoperative CaT % hypofunction showed a significant worsening (p = 0.028). Conclusion: SVINT results in a human model of horizontal canal plugging are well correlated with vestibular tests exploring horizontal canal function, but not with cVEMP. SVINT always showed a strong lesional nystagmus beating away from the lesion side. SVIN acts as a good marker of HSCC function. This surgical technique showed invasiveness regarding horizontal canal vestibular function.
Collapse
Affiliation(s)
- Georges Dumas
- Department of Oto-Rhino-Laryngology, Head and Neck Surgery, University Hospital, 38043 Grenoble, France; (G.D.); (C.F.)
- EA 3450 DevAH, Development, Adaptation and Handicap, Faculty of Medicine, University of Lorraine, 54500 Vandoeuvre-lès-Nancy, France;
| | - Christol Fabre
- Department of Oto-Rhino-Laryngology, Head and Neck Surgery, University Hospital, 38043 Grenoble, France; (G.D.); (C.F.)
| | - Anne Charpiot
- Service d’ORL et CCF, Aveue Molière, Hôpital de Hautepierre, Hôpitaux Universitaires de Strasbourg, CEDEX, 67098 Strasbourg, France; (A.C.); (L.F.); (H.C.-V.)
| | - Lea Fath
- Service d’ORL et CCF, Aveue Molière, Hôpital de Hautepierre, Hôpitaux Universitaires de Strasbourg, CEDEX, 67098 Strasbourg, France; (A.C.); (L.F.); (H.C.-V.)
| | - Hella Chaney-Vuong
- Service d’ORL et CCF, Aveue Molière, Hôpital de Hautepierre, Hôpitaux Universitaires de Strasbourg, CEDEX, 67098 Strasbourg, France; (A.C.); (L.F.); (H.C.-V.)
| | - Philippe Perrin
- EA 3450 DevAH, Development, Adaptation and Handicap, Faculty of Medicine, University of Lorraine, 54500 Vandoeuvre-lès-Nancy, France;
| | - Sébastien Schmerber
- Department of Oto-Rhino-Laryngology, Head and Neck Surgery, University Hospital, 38043 Grenoble, France; (G.D.); (C.F.)
- BrainTech Lab INSERM UMR 2015, 38043 Grenoble, France
- Otologie, Neuro-Otologie, Implants Auditifs, Centre d’Implantation Cochléaire des Alpes, Clinique Universitaire Oto-Rhino-Laryngologie, Université Grenoble Alpes, INSERM UMR 1205, CHU A. Michallon BP 217, CEDEX 09, 38043 Grenoble, France
- Correspondence: ; Tel.: +33-4-76-76-56-62
| |
Collapse
|
29
|
Halmágyi GM, Curthoys IS. Vestibular contributions to the Romberg test: Testing semicircular canal and otolith function. Eur J Neurol 2021; 28:3211-3219. [PMID: 34160115 DOI: 10.1111/ene.14942] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/11/2021] [Accepted: 05/20/2021] [Indexed: 12/26/2022]
Abstract
Normal stance relies on three sensory inputs: vision, proprioception and vestibular function. The Romberg test, trying to stand with feet together and eyes closed, is familiar to every medical student as a test of distal proprioceptive impairment. It remains the best known of Romberg's many remarkable contributions to clinical neurology. In Romberg's time almost nothing was known about the function of the vestibular system. We now know that standing with the eyes closed on a compliant rather than a firm surface is more a test of vestibular than proprioceptive function. Peripheral vestibular function tests in clinical use today all rely on measurements of oligosynaptic brainstem reflexes. Short-latency eye rotations in response to rapid, brief head rotations (head impulses) give an accurate, robust and reproducible measure of the function of any and each of the six semicircular canals. Short-latency evoked potentials from sternomastoid and inferior oblique muscles in response to loud clicks or skull taps (vestibular evoked myogenic potentials) give an accurate and reproducible measure of the function of each and any of the four otolith organs. In the present paper, we briefly review what is now known about the anatomy and physiology of the peripheral receptors and brainstem pathways mediating these reflexes and examine how this knowledge can help interpret the Romberg test.
Collapse
Affiliation(s)
- Gábor M Halmágyi
- Neurology Department, Royal Prince Alfred Hospital and the University of Sydney, Sydney, NSW, Australia
| | - Ian S Curthoys
- School of Psychology, University of Sydney, Sydney, NSW, Australia
| |
Collapse
|
30
|
Outer Hair Cell Glutamate Signaling through Type II Spiral Ganglion Afferents Activates Neurons in the Cochlear Nucleus in Response to Nondamaging Sounds. J Neurosci 2021; 41:2930-2943. [PMID: 33574178 DOI: 10.1523/jneurosci.0619-20.2021] [Citation(s) in RCA: 25] [Impact Index Per Article: 6.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/13/2020] [Revised: 01/24/2021] [Accepted: 02/04/2021] [Indexed: 11/21/2022] Open
Abstract
Cochlear outer hair cells (OHCs) are known to uniquely participate in auditory processing through their electromotility, and like inner hair cells, are also capable of releasing vesicular glutamate onto spiral ganglion (SG) neurons: in this case, onto the sparse Type II SG neurons. However, unlike glutamate signaling at the inner hair cell-Type I SG neuron synapse, which is robust across a wide spectrum of sound intensities, glutamate signaling at the OHC-Type II SG neuron synapse is weaker and has been hypothesized to occur only at intense, possibly damaging sound levels. Here, we tested the ability of the OHC-Type II SG pathway to signal to the brain in response to moderate, nondamaging sound (80 dB SPL) as well as to intense sound (115 dB SPL). First, we determined the VGluTs associated with OHC signaling and then confirmed the loss of glutamatergic synaptic transmission from OHCs to Type II SG neurons in KO mice using dendritic patch-clamp recordings. Next, we generated genetic mouse lines in which vesicular glutamate release occurs selectively from OHCs, and then assessed c-Fos expression in the cochlear nucleus in response to sound. From these analyses, we show, for the first time, that glutamatergic signaling at the OHC-Type II SG neuron synapse is capable of activating cochlear nucleus neurons, even at moderate sound levels.SIGNIFICANCE STATEMENT Evidence suggests that cochlear outer hair cells (OHCs) release glutamate onto Type II spiral ganglion neurons only when exposed to loud sound, and that Type II neurons are activated by tissue damage. Knowing whether moderate level sound, without tissue damage, activates this pathway has functional implications for this fundamental auditory pathway. We first determined that OHCs rely largely on VGluT3 for synaptic glutamate release. We then used a genetically modified mouse line in which OHCs, but not inner hair cells, release vesicular glutamate to demonstrate that moderate sound exposure activates cochlear nucleus neurons via the OHC-Type II spiral ganglion pathway. Together, these data indicate that glutamate signaling at the OHC-Type II afferent synapse participates in auditory function at moderate sound levels.
Collapse
|
31
|
Metabolic changes in the brain and blood of rats following acoustic trauma, tinnitus and hyperacusis. PROGRESS IN BRAIN RESEARCH 2021; 262:399-430. [PMID: 33931189 DOI: 10.1016/bs.pbr.2020.09.002] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 12/27/2022]
Abstract
It has been increasingly recognized that tinnitus is likely to be generated by complex network changes. Acoustic trauma that causes tinnitus induces significant changes in multiple metabolic pathways in the brain. However, it is not clear whether those metabolic changes in the brain could also be reflected in blood samples and whether metabolic changes could discriminate acoustic trauma, hyperacusis and tinnitus. We analyzed brain and serum metabolic changes in rats following acoustic trauma or a sham procedure using metabolomics. Hearing levels were recorded before and after acoustic trauma and behavioral measures to quantify tinnitus and hyperacusis were conducted at 4 weeks following acoustic trauma. Tissues from 11 different brain regions and serum samples were collected at about 3 months following acoustic trauma. Among the acoustic trauma animals, eight exhibited hyperacusis-like behavior and three exhibited tinnitus-like behavior. Using Gas chromatography-mass spectrometry and multivariate statistical analysis, significant metabolic changes were found in acoustic trauma animals in both the brain and serum samples with a number of metabolic pathways significantly perturbated. Furthermore, metabolic changes in the serum were able to differentiate sham from acoustic trauma animals, as well as sham from hyperacusis animals, with high accuracy. Our results suggest that serum metabolic profiling in combination with machine learning analysis may be a promising approach for identifying biomarkers for acoustic trauma, hyperacusis and potentially, tinnitus.
Collapse
|
32
|
Batuecas-Caletrío A, Martínez-Carranza R, García Nuñez GM, Fernández Nava MJ, Sánchez Gómez H, Santacruz Ruiz S, Pérez Guillén V, Pérez-Fernández N. Skull vibration-induced nystagmus in vestibular neuritis. Acta Otolaryngol 2020; 140:995-1000. [PMID: 32865143 DOI: 10.1080/00016489.2020.1809706] [Citation(s) in RCA: 4] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 10/23/2022]
Abstract
BACKGROUND As described by Dumas, an 80-100 Hz vibration applied to the mastoid produces a horizontal nystagmus, with quick phases beating away from the affected side in patients with unilateral vestibular loss (UVL). AIM/OBJECTIVES To elucidate the characteristics of skull vibration-induced nystagmus (SVIN) in patients suffering from vestibular neuritis and how these characteristics are related to information provided by the video head impulse test (vHIT). MATERIAL AND METHODS Sixty-three patients were enrolled to perform a vHIT to measure the gain in both ears. SVIN was induced with stimulation at 30 Hz, 60 Hz, and 100 Hz. The slow phase velocity (SPV) of the SVIN was measured. RESULTS The SVIN test was positive in 25/63 patients at 30 Hz, 36/63 at 60 Hz and 46/63 at 100 Hz. Mean gain difference between both ears to obtain a positive SVIN at 30 Hz was observed to be 0.38 ± 0.25, decreasing to 0.35 ± 0.23 at 60 Hz, and 0.31 ± 0.24 at 100 Hz (p = .025). We found a significant positive linear correlation between the gain asymmetry measured using horizontal vHIT and SPV in SVIN at 100 Hz. CONCLUSIONS AND SIGNIFICANCE There is a close relationship between the difference in the gains of both ears as measured using VHIT and the SPV of the nystagmus induced by SVIN at 100 Hz.
Collapse
Affiliation(s)
- Angel Batuecas-Caletrío
- Otoneurology Unit, Department of Otorhinolaryngology, University Hospital of Salamanca, IBSAL, Salamanca, Spain
| | - Ramón Martínez-Carranza
- Otoneurology Unit, Department of Otorhinolaryngology, University Hospital of Salamanca, IBSAL, Salamanca, Spain
| | - Gianni Mercy García Nuñez
- Otoneurology Unit, Department of Otorhinolaryngology, University Hospital of Salamanca, IBSAL, Salamanca, Spain
| | - Maria José Fernández Nava
- Otoneurology Unit, Department of Otorhinolaryngology, University Hospital of Salamanca, IBSAL, Salamanca, Spain
| | - Hortensia Sánchez Gómez
- Otoneurology Unit, Department of Otorhinolaryngology, University Hospital of Salamanca, IBSAL, Salamanca, Spain
| | - Santiago Santacruz Ruiz
- Otoneurology Unit, Department of Otorhinolaryngology, University Hospital of Salamanca, IBSAL, Salamanca, Spain
| | - Vanesa Pérez Guillén
- Otoneurology Unit, Department of Otorhinolaryngology, Hospital Universitario La Fe, Valencia, Spain
| | | |
Collapse
|
33
|
Curthoys IS, Manzari L. A Simple Specific Functional Test for SCD: VEMPs to High Frequency (4,000Hz) Stimuli-Their Origin and Explanation. Front Neurol 2020; 11:612075. [PMID: 33329372 PMCID: PMC7720427 DOI: 10.3389/fneur.2020.612075] [Citation(s) in RCA: 4] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/30/2020] [Accepted: 10/29/2020] [Indexed: 12/13/2022] Open
Affiliation(s)
- Ian S Curthoys
- Vestibular Research Laboratory, School of Psychology, The University of Sydney, Darlington, NSW, Australia.,MSA ENT Academy Center, Cassino, Italy
| | - Leonardo Manzari
- Vestibular Research Laboratory, School of Psychology, The University of Sydney, Darlington, NSW, Australia.,MSA ENT Academy Center, Cassino, Italy
| |
Collapse
|
34
|
Fröhlich L, Curthoys IS, Kösling S, Obrist D, Rahne T, Plontke SK. Cervical and Ocular Vestibular-Evoked Myogenic Potentials in Patients With Intracochlear Schwannomas. Front Neurol 2020; 11:549817. [PMID: 33192980 PMCID: PMC7655125 DOI: 10.3389/fneur.2020.549817] [Citation(s) in RCA: 9] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/07/2020] [Accepted: 09/22/2020] [Indexed: 12/14/2022] Open
Abstract
Objective: To evaluate ocular and cervical vestibular evoked myogenic potentials (oVEMPs and cVEMPs) in patients with solely intracochlear localization of an intralabyrinthine schwannoma (ILS). Study Design: Retrospective analysis of a series of cases. Setting: Monocentric study at a tertiary referral center. Patients: Patients with intracochlear schwannoma (ICS) and VEMP measurements. Outcome Measures: Signed asymmetry ratio (AR) of cVEMPs and oVEMPs to air conducted sound with AR cut-offs considered to be asymmetrical when exceeding ±30% for cVEMPs and ±40% for oVEMPs with respect to the side affected by the tumor (reduced amplitudes on the affected side indicated by negative values, enhanced amplitudes by positive values); VEMP amplitudes and latencies; tumor localization in the cochlear turn and scala. Results: Nineteen patients with a solely intracochlear tumor (ICS patients) [10 males, 9 females, mean age 57.1 (SD: 13.4) years] were included in the study. On the affected side, cVEMPs were absent or reduced in 47% of the patients, normal in 32%, and enhanced in 21%. Ocular VEMPs on the affected side were absent or reduced in 53% of the patients, normal in 32% and enhanced in 15%. Latencies for cVEMPs and oVEMPs were not significantly different between the affected and non-affected side. In all patients with enhanced VEMPs, the tumor was located in the scala tympani and scala vestibuli. Conclusions: As a new and unexpected finding, VEMP amplitudes can be enhanced in patients with intracochlear schwannoma, mimicking the third window syndrome.
Collapse
Affiliation(s)
- Laura Fröhlich
- Department of Otorhinolaryngology, Head and Neck Surgery, Martin Luther University Halle-Wittenberg, Halle (Saale), Germany
| | - Ian S Curthoys
- Vestibular Research Laboratory, School of Psychology, The University of Sydney, Sydney, NSW, Australia
| | - Sabrina Kösling
- Department of Radiology, Martin Luther University Halle-Wittenberg, Halle (Saale), Germany
| | - Dominik Obrist
- ARTORG Center for Biomedical Engineering Research, University of Bern, Bern, Switzerland
| | - Torsten Rahne
- Department of Otorhinolaryngology, Head and Neck Surgery, Martin Luther University Halle-Wittenberg, Halle (Saale), Germany
| | - Stefan K Plontke
- Department of Otorhinolaryngology, Head and Neck Surgery, Martin Luther University Halle-Wittenberg, Halle (Saale), Germany
| |
Collapse
|
35
|
Curthoys IS. The Anatomical and Physiological Basis of Clinical Tests of Otolith Function. A Tribute to Yoshio Uchino. Front Neurol 2020; 11:566895. [PMID: 33193004 PMCID: PMC7606994 DOI: 10.3389/fneur.2020.566895] [Citation(s) in RCA: 10] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/28/2020] [Accepted: 09/18/2020] [Indexed: 12/15/2022] Open
Abstract
Otolithic receptors are stimulated by gravitoinertial force (GIF) acting on the otoconia resulting in deflections of the hair bundles of otolithic receptor hair cells. The GIF is the sum of gravitational force and the inertial force due to linear acceleration. The usual clinical and experimental tests of otolith function have used GIFs (roll tilts re gravity or linear accelerations) as test stimuli. However, the opposite polarization of receptors across each otolithic macula is puzzling since a GIF directed across the otolith macula will excite receptors on one side of the line of polarity reversal (LPR at the striola) and simultaneously act to silence receptors on the opposite side of the LPR. It would seem the two neural signals from the one otolith macula should cancel. In fact, Uchino showed that instead of canceling, the simultaneous stimulation of the oppositely polarized hair cells enhances the otolithic response to GIF—both in the saccular macula and the utricular macula. For the utricular system there is also commissural inhibitory interaction between the utricular maculae in each ear. The results are that the one GIF stimulus will cause direct excitation of utricular receptors in the activated sector in one ear as well as indirect excitation resulting from the disfacilitation of utricular receptors in the corresponding sector on the opposite labyrinth. There are effectively two complementary parallel otolithic afferent systems—the sustained system concerned with signaling low frequency GIF stimuli such as roll head tilts and the transient system which is activated by sound and vibration. Clinical tests of the sustained otolith system—such as ocular counterrolling to roll-tilt or tests using linear translation—do not show unilateral otolithic loss reliably, whereas tests of transient otolith function [vestibular evoked myogenic potentials (VEMPs) to brief sound and vibration stimuli] do show unilateral otolithic loss. The opposing sectors of the maculae also explain the results of galvanic vestibular stimulation (GVS) where bilateral mastoid galvanic stimulation causes ocular torsion position similar to the otolithic response to GIF. However, GVS stimulates canal afferents as well as otolithic afferents so the eye movement response is complex.
Collapse
Affiliation(s)
- Ian S Curthoys
- Vestibular Research Laboratory, School of Psychology, The University of Sydney, Sydney, NSW, Australia
| |
Collapse
|
36
|
Tarnutzer AA, Bockisch CJ, Buffone E, Weber KP. Vestibular mapping in patients with unilateral peripheral-vestibular deficits. Neurology 2020; 95:e2988-e3001. [PMID: 32913014 DOI: 10.1212/wnl.0000000000010812] [Citation(s) in RCA: 16] [Impact Index Per Article: 3.2] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/31/2020] [Accepted: 07/10/2020] [Indexed: 01/16/2023] Open
Abstract
OBJECTIVE To test the hypothesis that patterns of semicircular canal (SCC) and otolith impairment in unilateral vestibular loss depend on the underlying disorders, we analyzed peripheral-vestibular function of all 5 vestibular sensors. METHODS For this retrospective case series, we screened the hospital video-head-impulse test database (n = 4,983) for patients with unilaterally impaired SCC function who also received ocular vestibular-evoked myogenic potentials and cervical vestibular-evoked myogenic potentials (n = 302). Frequency of impairment of vestibular end organs (horizontal/anterior/posterior SCC, utriculus/sacculus) was analyzed with hierarchical cluster analysis and correlated with the underlying etiology. RESULTS Acute vestibular neuropathy (AVN) (37.4%, 113 of 302), vestibular schwannoma (18.2%, 55 of 302), and acute cochleovestibular neuropathy (6.6%, 20 of 302) were most frequent. Horizontal SCC impairment (87.4%, 264 of 302) was more frequent (p < 0.001) than posterior (47.4%, 143 of 302) and anterior (37.8%, 114 of 302) SCC impairment. Utricular damage (58%, 175 of 302) was noted more often (p = 0.003) than saccular impairment (32%, 98 of 302). On average, 2.6 (95% confidence interval 2.48-2.78) vestibular sensors were deficient, with higher numbers (p ≤ 0.017) for acute cochleovestibular neuropathy and vestibular schwannoma than for AVN, Menière disease, and episodic vestibular syndrome. In hierarchical cluster analysis, early mergers (posterior SCC/sacculus; anterior SCC/utriculus) pointed to closer pathophysiologic association of these sensors, whereas the late merger of the horizontal canal indicated a more distinct state. CONCLUSIONS While the extent and pattern of vestibular impairment critically depended on the underlying disorder, more limited damage in AVN and Menière disease was noted, emphasizing the individual range of loss of function and the value of vestibular mapping. Likely, both the anatomic properties of the different vestibular end organs and their vulnerability to external factors contribute to the relative sparing of the vertical canals and the sacculus.
Collapse
Affiliation(s)
- Alexander A Tarnutzer
- From the Cantonal Hospital Baden (A.A.T.); Faculty of Medicine (A.A.T., C.J.B., K.P.W.), University of Zurich; Departments of Neurology (A.A.T., C.J.B., E.B., K.P.W.), Ophthalmology (C.J.B., K.P.W.), and Otorhinolaryngology (C.J.B.), University Hospital Zurich; and Clinical Neuroscience Center (A.A.T., C.J.B., K.P.W.), Zurich, Switzerland.
| | - Christopher J Bockisch
- From the Cantonal Hospital Baden (A.A.T.); Faculty of Medicine (A.A.T., C.J.B., K.P.W.), University of Zurich; Departments of Neurology (A.A.T., C.J.B., E.B., K.P.W.), Ophthalmology (C.J.B., K.P.W.), and Otorhinolaryngology (C.J.B.), University Hospital Zurich; and Clinical Neuroscience Center (A.A.T., C.J.B., K.P.W.), Zurich, Switzerland
| | - Elena Buffone
- From the Cantonal Hospital Baden (A.A.T.); Faculty of Medicine (A.A.T., C.J.B., K.P.W.), University of Zurich; Departments of Neurology (A.A.T., C.J.B., E.B., K.P.W.), Ophthalmology (C.J.B., K.P.W.), and Otorhinolaryngology (C.J.B.), University Hospital Zurich; and Clinical Neuroscience Center (A.A.T., C.J.B., K.P.W.), Zurich, Switzerland
| | - Konrad P Weber
- From the Cantonal Hospital Baden (A.A.T.); Faculty of Medicine (A.A.T., C.J.B., K.P.W.), University of Zurich; Departments of Neurology (A.A.T., C.J.B., E.B., K.P.W.), Ophthalmology (C.J.B., K.P.W.), and Otorhinolaryngology (C.J.B.), University Hospital Zurich; and Clinical Neuroscience Center (A.A.T., C.J.B., K.P.W.), Zurich, Switzerland
| |
Collapse
|
37
|
Clinard CG, Thorne AP, Piker EG. Effects of Tonic Muscle Activation on Amplitude-Modulated Cervical Vestibular Evoked Myogenic Potentials (AMcVEMPs) in Young Females: Preliminary Findings. J Assoc Res Otolaryngol 2020; 21:445-461. [PMID: 32761291 DOI: 10.1007/s10162-020-00766-z] [Citation(s) in RCA: 4] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/14/2019] [Accepted: 07/24/2020] [Indexed: 12/21/2022] Open
Abstract
Cervical vestibular evoked myogenic potentials (cVEMPs) are usually elicited by transient tonebursts, but when elicited by amplitude-modulated (AM) tones, they can provide new information about cVEMPs. Previous reports of cVEMPs elicited by AM tones, or AMcVEMPs, have not systematically examined the effects of tonic EMG activation on their response properties. Fourteen young, healthy female adults (ages 20-24) with clinically normal audiograms participated in this study. AMcVEMPs were elicited with bone-conducted 500 Hz tones amplitude modulated at a rate of 37 Hz and recorded for five different EMG targets ranging from 0 to 90 μV. Amplitude increased linearly as tonic EMG activation increased. Signal-to-noise ratio (SNR) was minimal at 0 μV, but robust and with equivalent values from 30 to 90 μV; phase coherence and EMG-corrected amplitude had findings similar to SNR across EMG target levels. Interaural asymmetry ratios for SNR and phase coherence were substantially lower than those for raw or corrected amplitude. AMcVEMP amplitude scaled with tonic EMG activation similar to transient cVEMPs. Signal-to-noise ratio, phase coherence, and EMG-corrected amplitude plateaued across a range of EMG values, suggesting that these properties of the response reach their maximum values at relatively low levels of EMG activation and that higher levels of EMG activation are not necessary to record robust AMcVEMPs.
Collapse
Affiliation(s)
- Christopher G Clinard
- Department of Communication Sciences and Disorders, James Madison University, 235 Martin Luther King Jr. Way, MSC 4304, Harrisonburg, VA, 22807, USA.
| | - Andrew P Thorne
- Department of Communication Sciences and Disorders, James Madison University, 235 Martin Luther King Jr. Way, MSC 4304, Harrisonburg, VA, 22807, USA
| | - Erin G Piker
- Department of Communication Sciences and Disorders, James Madison University, 235 Martin Luther King Jr. Way, MSC 4304, Harrisonburg, VA, 22807, USA
| |
Collapse
|
38
|
Matos R, Navarro M, Pérez-Guillén V, Pérez-Garrigues H. The role of vertical semicircular canal function in the vertical component of skull vibration-induced nystagmus. Acta Otolaryngol 2020; 140:639-645. [PMID: 32329666 DOI: 10.1080/00016489.2020.1751877] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.2] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 10/24/2022]
Abstract
Background: Generally, vertical component of the skull vibratory nystagmus (VCN) is ignored in the clinical practise. Thus, the relative contribution of the vestibular organs in the presence of VCN remains unknown.Objectives: To determine the association between vertical semicircular canal (vSCC) function and the presence of VCN.Material and methods: Comparisons were made between Video Head Impulse Test and SVINT (100 Hz) results at the time of the acute peripheral vestibular lesion (PVL) and at the post-acute phase in patients diagnosed PVL. Later on, a paired analysis was performed restricting the assessments to patients with vestibular explorations in both the acute and post-acute phases.Results: In an univariable analysis, larger mean total gain differences (TGD) between vSCC VOR gains, significantly related with the appearance of VCN in nystagmography in the acute phase (p = .001), unlike the post-acute phase (p = .46). After a multivariate analysis, mean TGD was the only predictive factor of the VCN (p = .013). In the paired analysis, we found an increase in the post-acute phase mean TGD, approaching zero value.Conclusions and significance: Global relation between all vertical canals has at least a contributory role in the presence of the vertical component of nystagmus in SVINT.
Collapse
Affiliation(s)
- Ricardo Matos
- Department of Otorhinolaryngology, Centro Hospitalar Universitário São João EPE, Porto, Portugal University of Porto Medical School, Porto, Portugal.,University of Porto Medical School, Porto, Portugal
| | - Marta Navarro
- Otoneurology Unit, ENT Department, Hospital "La Fe", Valencia, Spain
| | | | | |
Collapse
|
39
|
Abstract
BACKGROUND Vestibular evoked myogenic potentials (VEMPs) are increasingly being used for testing otolith organ function. OBJECTIVE This article provides an overview of the anatomical, biomechanical and neurophysiological principles underlying the evidence-based clinical application of ocular and cervical VEMPs (oVEMPs and cVEMPs). MATERIAL AND METHODS Systematic literature search in PubMed until April 2019. RESULTS Sound and vibration at a frequency of 500 Hz represent selective vestibular stimuli for the otolith organs. The predominant specificity of oVEMPs for contralateral utricular function and of cVEMPs for ipsilateral saccular function is defined by the different central projections of utricular and saccular afferents. VEMPs are particularly useful in the diagnosis of superior canal dehiscence and otolith organ specific vestibular dysfunction and as an alternative diagnostic approach in situations when video oculography is not possible or useful. CONCLUSION The use of VEMPs is a simple, safe, reliable and selective test of dynamic function of otolith organs.
Collapse
Affiliation(s)
- J Dlugaiczyk
- Deutsches Schwindel- und Gleichgewichtszentrum (DSGZ), Klinikum der Universität München, LMU München, Marchioninistraße 15, 81377, Munich, Germany.
| |
Collapse
|
40
|
D'Albora-Rivas R, Monaco-Hansen MJ. Audiovestibulograma: una forma práctica de ver todos los resultados. REVISTA ORL 2020. [DOI: 10.14201/orl.23458] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/11/2022] Open
Abstract
RESUMEN Introducción y objetivo: El oído (órgano cócleovestibular) es un órgano multifrecuen-ciaL. Por lo tanto, debe verse a este órgano como lo que es: una unidad embriológica, anatómica, fisiológica y clínica. Objetivo: desarrollar una cartilla audiovestibular don-de se puedan volcar los resultados obtenidos en los diferentes estudios que valoran al oído como un todo. Método: Se tomó como base la cartilla audiométrica y su sim-bología clásica, extendiendo su rango frecuencial y colocando los diferentes estu-dios a documentar: audiometría tonal liminal, impedanciometría, reflejo estapedial, electrococleografía, potenciales miogénicos vestibulares, test vibracional, video head impulse test, prueba rotatoria, prueba calórica y comandos oculomotores centrales. Discusión: Esta forma de presentación de datos, si bien no es completa, otorga la mayoría de los estudios de diagnóstico audiovestibulares. A primera vista genera sobrecarga de información al especialista, requiriendo un mínimo de entrenamiento. Conclusiones: Se trata de una cartilla de documentación única de los principales estudios cócleovestibulares, con sus respectivas referencias de normalidad, para ser presentada ante el especialista en una sola imagen requiriendo un mínimo de entre-namiento.
Collapse
|
41
|
Clinard CG, Piker EG, Thorne AP, Surface EN, Anderson AE, Beacham VA, Crouse MC, Whitney VH, Depaolis RA. Maximum Output and Low-Frequency Limitations of B71 and B81 Clinical Bone Vibrators: Implications for Vestibular Evoked Potentials. Ear Hear 2020; 41:847-854. [DOI: 10.1097/aud.0000000000000808] [Citation(s) in RCA: 9] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/25/2022]
|
42
|
Aghababaei Ziarati M, Taziki MH, Hosseini SM. Autonomic laterality in caloric vestibular stimulation. World J Cardiol 2020; 12:144-154. [PMID: 32431785 PMCID: PMC7215963 DOI: 10.4330/wjc.v12.i4.144] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.2] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 12/24/2019] [Revised: 03/12/2020] [Accepted: 03/26/2020] [Indexed: 02/06/2023] Open
Abstract
BACKGROUND Caloric stimulation of the vestibular system is associated with autonomic response. The lateralization in the nervous system activities also involves the autonomic nervous system.
AIM To compare the effect of the right and left ear caloric test on the cardiac sympathovagal tone in healthy persons.
METHODS This self-control study was conducted on 12 healthy male volunteers. The minimal ice water caloric test was applied for vestibular stimulation. This was done by irrigating 1 milliliter of 4 ± 2 °C ice water into the external ear canal in 1 s. In each experiment, only one ear was stimulated. For each ear, the pessimum position was considered as sham control and the optimum position was set as caloric vestibular stimulation of horizontal semicircular channel. The order of right or left caloric vestibular stimulation and the sequence of optimum or pessimum head position in each set were random. The recovery time between each calorie test was 5 min. The short-term heart rate variability (HRV) was used for cardiac sympathovagal tone metrics. All variables were compared using the analysis of variance.
RESULTS After caloric vestibular stimulation, the short-term time-domain and frequency-domain HRV indices as well as, the systolic and the diastolic arterial blood pressure, the respiratory rate and the respiratory amplitude, had no significant changes. These negative results were similar in the right and the left sides. Nystagmus duration of left caloric vestibular stimulations in the optimum and the pessimum positions had significant differences (e.g., 72.14 ± 39.06 vs 45.35 ± 35.65, P < 0.01). Nystagmus duration of right caloric vestibular stimulations in the optimum and the pessimum positions had also significant differences (e.g., 86.42 ± 67.20 vs 50.71 ± 29.73, P < 0.01). The time of the start of the nystagmus following caloric vestibular stimulation had no differences in both sides and both positions.
CONCLUSION Minimal ice water caloric stimulation of the right and left vestibular system did not affect the cardiac sympathovagal balance according to HRV indices.
Collapse
Affiliation(s)
- Mohammadreza Aghababaei Ziarati
- Department of Internal Medicine, Medical Faculty, Golestan University of Medical Sciences, Gorgan 4934174515, Golestan, Iran
| | - Mohammad Hosein Taziki
- Department of Otolaryngology, Medical Faculty, Golestan University of Medical Sciences, Gorgan 4934174515, Golestan, Iran
| | - Seyed Mehran Hosseini
- Department of Physiology, Medical Faculty, Golestan University of Medical Sciences, Gorgan 4934174515, Golestan, Iran
- Neuroscience Research Center, Faculty of Medicine, Golestan University of Medical Sciences, Gorgan 4934174515, Golestan, Iran
| |
Collapse
|
43
|
Dyball AC, Govender S, Taylor RL, Young AS, Welgampola MS, Rosengren SM. Bone-conducted vestibular and stretch reflexes in human neck muscles. Exp Brain Res 2020; 238:1237-1248. [PMID: 32279086 DOI: 10.1007/s00221-020-05798-8] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/10/2019] [Accepted: 03/24/2020] [Indexed: 12/01/2022]
Abstract
In normal humans, tapping the forehead produces a neck muscle reflex that is used clinically to test vestibular function, the cervical vestibular evoked myogenic potential (cVEMP). As stretch receptors can also be activated by skull taps, we investigated the origin of the early and late peaks of the bone-conducted cVEMP. In twelve normal participants, we differentially stimulated the vestibular and neck stretch receptors by applying vibration to the forehead (activating both vestibular and stretch receptors) and to the sternum (activating mainly stretch receptors). Patients with bilateral vestibulopathy (BVP; n = 26) and unilateral vestibular loss (uVL; n = 17) were also investigated for comparison. Comparison of peaks in normal subjects suggested that the early peaks were vestibular-dependent, while the later peaks had mixed vestibular and stretch input. The late peaks were present but small (1.1 amplitude ratio) in patients with BVP and absent VEMPs, confirming that they do not strictly depend on vestibular function, and largest in age-matched controls (1.5 amplitude ratio, p = 0.049), suggesting that there is an additional vestibular reflex at this latency (approx. 30 ms). Patients with uVL had larger late peaks on the affected than the normal side (1.4 vs 1.0 amplitude ratio, p = 0.034). The results suggest that the early responses in SCM to skull vibration in humans are vestibular-dependent, while there is a late stretch reflex bilaterally and a late vestibular reflex in the contralateral muscle.
Collapse
Affiliation(s)
- Alyssa C Dyball
- Audiology, Department of Linguistics, Macquarie University, Sydney, Australia
| | - Sendhil Govender
- Department of Neurological Sciences, Prince of Wales Hospital, Randwick, Sydney, Australia.,Neurology Department and Institute of Clinical Neurosciences, Royal Prince Alfred Hospital, Level 8, Missenden Rd, Camperdown, Sydney, NSW, 2050, Australia
| | - Rachael L Taylor
- Department of Physiology and Centre for Brain Research, The University of Auckland, Auckland, New Zealand
| | - Allison S Young
- Central Clinical School, Faculty of Medicine and Health, The University of Sydney, Sydney, Australia
| | - Miriam S Welgampola
- Neurology Department and Institute of Clinical Neurosciences, Royal Prince Alfred Hospital, Level 8, Missenden Rd, Camperdown, Sydney, NSW, 2050, Australia.,Central Clinical School, Faculty of Medicine and Health, The University of Sydney, Sydney, Australia
| | - Sally M Rosengren
- Neurology Department and Institute of Clinical Neurosciences, Royal Prince Alfred Hospital, Level 8, Missenden Rd, Camperdown, Sydney, NSW, 2050, Australia. .,Central Clinical School, Faculty of Medicine and Health, The University of Sydney, Sydney, Australia.
| |
Collapse
|
44
|
Longridge NS. Vestibular evoked myogenic potentials: what are they for? An opinion; a hypothesis. Acta Otolaryngol 2020; 140:1-3. [PMID: 32149556 DOI: 10.1080/00016489.2019.1704545] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/26/2019] [Accepted: 11/02/2019] [Indexed: 10/24/2022]
Affiliation(s)
- Neil S Longridge
- Division of Otolaryngology, Department of Surgery, Faculty of Medicine, University of British Columbia, Vancouver, Canada
| |
Collapse
|
45
|
Yacovino DA, Zanotti E, Hain TC. Is Cerebellar Ataxia, Neuropathy, and Vestibular Areflexia Syndrome (CANVAS) a Vestibular Ganglionopathy? J Int Adv Otol 2020; 15:304-308. [PMID: 31418719 DOI: 10.5152/iao.2019.7068] [Citation(s) in RCA: 11] [Impact Index Per Article: 2.2] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/06/2023] Open
Abstract
OBJECTIVES CANVAS is an acronym for cerebellar ataxia, neuropathy and vestibular areflexia syndrome. Limited autopsy data has suggested that CANVAS is caused by a focal dorsal root ganglionopathy that damages Scarpa's (vestibular) ganglion, but spares the Spiral (hearing) ganglion. If the vestibular areflexia of CANVAS is in fact due to ganglionopathy, then there should be global reduction of all vestibular responses. MATERIALS AND METHODS With this hypothesis in mind, a retrospective review of 5 subjects who met the clinical criteria for CANVAS was performed. Recent advances in vestibular testing have made it possible to quantify responses from all 5 vestibular end organs in the inner ear. Results of the Video head impulse test (VHIT), video oculography, caloric test and vestibular evoked myogenic potential (VEMP) were examined to determine if all 5 end organs are nonfunctional in CANVAS. RESULTS Severe reduction of function of the six semicircular canals and ocular VEMPs were observed. Only the cervical VEMPs were present and reproducible, consistent with either partial sparing of the inferior vestibular ganglia, specific embryologic resistance of the saccule to the degeneration or a mechanism for cervical VEMPs that does not require an intact vestibular ganglion. CONCLUSION Our results suggest that Scarpa´s ganglia dysfunction could be the mechanism for loss of semicircular canal and utricular function in CANVAS patients, but the preservation of the cervical VEMP response is unexplained.
Collapse
Affiliation(s)
- Dario Andres Yacovino
- Department of Neurology, Dr. César Milstein Hospital, Buenos Aires, Argentina ; Department of Neurology, Memory and Balance Clinic, Capital Federal, Argentina
| | - Estefania Zanotti
- Department of Neurology, Dr. César Milstein Hospital, Buenos Aires, Argentina
| | | |
Collapse
|
46
|
Physiology, clinical evidence and diagnostic relevance of sound-induced and vibration-induced vestibular stimulation. Curr Opin Neurol 2020; 33:126-135. [DOI: 10.1097/wco.0000000000000770] [Citation(s) in RCA: 19] [Impact Index Per Article: 3.8] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 02/07/2023]
|
47
|
Stewart CE, Bauer DS, Kanicki AC, Altschuler RA, King WM. Intense noise exposure alters peripheral vestibular structures and physiology. J Neurophysiol 2020; 123:658-669. [PMID: 31875485 PMCID: PMC7052639 DOI: 10.1152/jn.00642.2019] [Citation(s) in RCA: 9] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/08/2019] [Revised: 12/23/2019] [Accepted: 12/23/2019] [Indexed: 12/20/2022] Open
Abstract
The otolith organs play a critical role in detecting linear acceleration and gravity to control posture and balance. Some afferents that innervate these structures can be activated by sound and are at risk for noise overstimulation. A previous report demonstrated that noise exposure can abolish vestibular short-latency evoked potential (VsEP) responses and damage calyceal terminals. However, the stimuli that were used to elicit responses were weaker than those established in previous studies and may have been insufficient to elicit VsEP responses in noise-exposed animals. The goal of this study was to determine the effect of an established noise exposure paradigm on VsEP responses using large head-jerk stimuli to determine if noise induces a stimulus threshold shift and/or if large head-jerks are capable of evoking VsEP responses in noise-exposed rats. An additional goal is to relate these measurements to the number of calyceal terminals and hair cells present in noise-exposed vs. non-noise-exposed tissue. Exposure to intense continuous noise significantly reduced VsEP responses to large stimuli and abolished VsEP responses to small stimuli. This finding confirms that while measurable VsEP responses can be elicited from noise-lesioned rat sacculi, larger head-jerk stimuli are required, suggesting a shift in the minimum stimulus necessary to evoke the VsEP. Additionally, a reduction in labeled calyx-only afferent terminals was observed without a concomitant reduction in the overall number of calyces or hair cells. This finding supports a critical role of calretinin-expressing calyceal-only afferents in the generation of a VsEP response.NEW & NOTEWORTHY This study identifies a change in the minimum stimulus necessary to evoke vestibular short-latency evoked potential (VsEP) responses after noise-induced damage to the vestibular periphery and reduced numbers of calretinin-labeled calyx-only afferent terminals in the striolar region of the sacculus. These data suggest that a single intense noise exposure may impact synaptic function in calyx-only terminals in the striolar region of the sacculus. Reduced calretinin immunolabeling may provide insight into the mechanism underlying noise-induced changes in VsEP responses.
Collapse
Affiliation(s)
- C E Stewart
- Kresge Hearing Research Institute, Department of Otolaryngology-Head and Neck Surgery, University of Michigan, Ann Arbor, Michigan
| | - D S Bauer
- Kresge Hearing Research Institute, Department of Otolaryngology-Head and Neck Surgery, University of Michigan, Ann Arbor, Michigan
| | - A C Kanicki
- Kresge Hearing Research Institute, Department of Otolaryngology-Head and Neck Surgery, University of Michigan, Ann Arbor, Michigan
| | - R A Altschuler
- Kresge Hearing Research Institute, Department of Otolaryngology-Head and Neck Surgery, University of Michigan, Ann Arbor, Michigan
| | - W M King
- Kresge Hearing Research Institute, Department of Otolaryngology-Head and Neck Surgery, University of Michigan, Ann Arbor, Michigan
| |
Collapse
|
48
|
Devantier L, Hansen AK, Mølby-Henriksen JJ, Christensen CB, Lildal T, Pedersen M, Magnusson M, Borghammer P, Ovesen T. PET Visualized Stimulation of the Vestibular Organ in Menière's Disease. Front Neurol 2020; 11:11. [PMID: 32047473 PMCID: PMC6997538 DOI: 10.3389/fneur.2020.00011] [Citation(s) in RCA: 15] [Impact Index Per Article: 3.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/30/2019] [Accepted: 01/07/2020] [Indexed: 01/05/2023] Open
Abstract
Introduction: The cortical metabolic activity in patients with Menière's disease has not been investigated. The aim of this study was to investigate the 18F-FDG cerebral uptake in Menière's patients compared to healthy controls. Method: Eight patients with right-sided Menière's disease and fourteen healthy controls underwent a video head impulse test (vHIT), test of utricular function with ocular vestibular evoked myogenic potentials (oVEMP) and three 18F-FDG-based PET examinations of the brain. Participants were seated in a self-propelled chair, injected with 18F-FDG and then exposed to 35 min of chair motion stimulation, followed by a PET scan. Two types of natural vestibular stimuli were applied, predominantly toward the right horizontal semicircular canal (angular acceleration) and right utriculus (linear acceleration). For baseline scans, participants were injected with 18F-FDG while seated without movement. Results: Analyses of baseline scans revealed decreased 18F-FDG-uptake in the medial part of Heschl's gyrus in the left hemisphere in patients with Menière's disease compared to healthy controls. During angular vestibular stimulation there was also a significantly decreased 18F-FDG uptake in the intersection between the medial part of Heschl's gyrus and the parietal operculum in the left hemisphere and bilaterally in the posterior part of insula. During linear stimulation, Menière's patients showed decreased 18F-FDG uptake in the medial part of Heschl's gyrus in the right hemisphere and also bilaterally in the posterior insula. In addition, decreased 18F-FDG uptake was seen in the thalamus during vestibular stimulation. Conclusion: Heschl's gyrus, the posterior part of insula, and thalamus have previously been shown to be core areas for processing vestibular inputs. Patients with Menière's disease solely differed from the healthy controls with lower cortical activity in these areas at baseline and during natural vestibular stimulation.
Collapse
Affiliation(s)
- Louise Devantier
- Department of Clinical Medicine, Aarhus University, Aarhus, Denmark.,Department of Oto-Rhino-Laryngology, Regional Hospital West Jutland, Holsterbo, Denmark
| | - Allan K Hansen
- Department of Nuclear Medicine & PET Centre, Aarhus University Hospital, Aarhus, Denmark
| | | | | | - Tina Lildal
- Department of Clinical Medicine, Aarhus University, Aarhus, Denmark.,Department of Oto-Rhino-Laryngology, Regional Hospital West Jutland, Holsterbo, Denmark
| | - Michael Pedersen
- Department of Clinical Medicine, Aarhus University, Aarhus, Denmark.,Comparative Medicine Lab, Aarhus University, Aarhus, Denmark
| | - Måns Magnusson
- Department of Oto-Rhino-Laryngology, Lund University Hospital, Lund, Sweden
| | - Per Borghammer
- Department of Nuclear Medicine & PET Centre, Aarhus University Hospital, Aarhus, Denmark
| | - Therese Ovesen
- Department of Clinical Medicine, Aarhus University, Aarhus, Denmark.,Department of Oto-Rhino-Laryngology, Regional Hospital West Jutland, Holsterbo, Denmark
| |
Collapse
|
49
|
Dlugaiczyk J. [Evidence-based diagnostic use of VEMPs : From neurophysiological principles to clinical application. German version]. HNO 2019; 68:324-335. [PMID: 31578599 DOI: 10.1007/s00106-019-00757-4] [Citation(s) in RCA: 4] [Impact Index Per Article: 0.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/19/2022]
Abstract
BACKGROUND Vestibular evoked myogenic potentials (VEMPs) are increasingly being used for testing otolith organ function. OBJECTIVE This article provides an overview of the anatomical, biomechanical and neurophysiological principles of an evidence-based clinical application of ocular and cervical VEMPs (oVEMPs and cVEMPs). MATERIAL AND METHODS Systematic literature search in PubMed until April 2019. RESULTS Sound and vibration at a frequency of 500 Hz represent selective vestibular stimuli for the otolith organs. The predominant specificity of oVEMPs for contralateral utricular function and of cVEMPs for ipsilateral saccular function is defined by the different neuronal projections of the utricle and the saccule. VEMPs are particularly useful in the diagnosis of superior canal dehiscence and otolith organ-specific vestibular dysfunction and as an alternative diagnostic approach in situations when video oculography is not possible or useful. CONCLUSION The use of VEMPs is a simple, safe, reliable and selective test of dynamic function of otolith organs.
Collapse
Affiliation(s)
- J Dlugaiczyk
- Deutsches Schwindel- und Gleichgewichtszentrum (DSGZ), Klinikum der Universität München, LMU München, Marchioninistr. 15, 81377, München, Deutschland. .,Neurologische Klinik und Poliklinik, Klinikum der Universität München, LMU München, München, Deutschland.
| |
Collapse
|
50
|
Devantier L, Hansen AK, Mølby-Henriksen JJ, Christensen CB, Pedersen M, Hansen KV, Magnusson M, Ovesen T, Borghammer P. Positron emission tomography visualized stimulation of the vestibular organ is localized in Heschl's gyrus. Hum Brain Mapp 2019; 41:185-193. [PMID: 31520516 PMCID: PMC7268041 DOI: 10.1002/hbm.24798] [Citation(s) in RCA: 8] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/09/2019] [Revised: 08/12/2019] [Accepted: 09/04/2019] [Indexed: 11/10/2022] Open
Abstract
The existence of a human primary vestibular cortex is still debated. Current knowledge mainly derives from functional magnetic resonance imaging (fMRI) and positron emission tomography (PET) acquisitions during artificial vestibular stimulation. This may be problematic as artificial vestibular stimulation entails coactivation of other sensory receptors. The use of fMRI is challenging as the strong magnetic field and loud noise during MRI may both stimulate the vestibular organ. This study aimed to characterize the cortical activity during natural stimulation of the human vestibular organ. Two fluorodeoxyglucose (FDG)-PET scans were obtained after natural vestibular stimulation in a self-propelled chair. Two types of stimuli were applied: (a) rotation (horizontal semicircular canal) and (b) linear sideways movement (utriculus). A comparable baseline FDG-PET scan was obtained after sitting motion-less in the chair. In both stimulation paradigms, significantly increased FDG uptake was measured bilaterally in the medial part of Heschl's gyrus, with some overlap into the posterior insula. This is the first neuroimaging study to visualize cortical processing of natural vestibular stimuli. FDG uptake was demonstrated in the medial-most part of Heschl's gyrus, normally associated with the primary auditory cortex. This anatomical localization seems plausible, considering that the labyrinth contains both the vestibular organ and the cochlea.
Collapse
Affiliation(s)
- Louise Devantier
- Department of Clinical Medicine, Aarhus University, Aarhus, Denmark.,Department of Oto-Rhino-Laryngology, Regional Hospital West Jutland, Holstebro, Denmark
| | - Allan K Hansen
- Department of Nuclear Medicine & PET Centre, Aarhus University Hospital, Aarhus, Denmark
| | | | | | | | - Kim V Hansen
- Department of Nuclear Medicine & PET Centre, Aarhus University Hospital, Aarhus, Denmark
| | - Måns Magnusson
- Department of Oto-Rhino-Laryngology, Lund University Hospital, Lund, Sweden
| | - Therese Ovesen
- Department of Clinical Medicine, Aarhus University, Aarhus, Denmark.,Department of Oto-Rhino-Laryngology, Regional Hospital West Jutland, Holstebro, Denmark
| | - Per Borghammer
- Department of Nuclear Medicine & PET Centre, Aarhus University Hospital, Aarhus, Denmark
| |
Collapse
|