Linking Vestibular Function and Subcortical Gray Matter Volume Changes in a Longitudinal Study of Aging Adults

Emerging evidence suggests a relationship between impairments of the vestibular (inner ear balance) system and alterations in the function and the structure of the central nervous system (CNS) in older adults. However, it is unclear whether age-related vestibular loss is associated with volume loss in brain regions known to receive vestibular input. To address this gap, we investigated the association between vestibular function and the volumes of four structures that process vestibular information (the hippocampus, entorhinal cortex, thalamus, and basal ganglia) in a longitudinal study of 97 healthy, older participants from the Baltimore Longitudinal Study of Aging. Vestibular testing included cervical vestibular-evoked myogenic potentials (cVEMP) to measure saccular function, ocular VEMP (oVEMP) to measure utricular function, and video head impulse tests to measure the horizontal semicircular canal vestibulo-ocular reflex (VOR). Participants in the sample had vestibular and brain MRI data for a total of one (18.6%), two (49.5%), and three (32.0%) visits. Linear mixed-effects regression was used to model regional volume over time as a function of vestibular physiological function, correcting for age, sex, intracranial volume, and intersubject random variation in the baseline levels and rates of change of volume over time. We found that poorer saccular function, characterized by lower cVEMP amplitude, is associated with reduced bilateral volumes of the basal ganglia and thalamus at each time point, demonstrated by a 0.0714 cm3 ± 0.0344 (unadjusted p = 0.038; 95% CI: 0.00397–0.139) lower bilateral-mean volume of the basal ganglia and a 0.0440 cm3 ± 0.0221 (unadjusted p = 0.046; 95% CI: 0.000727–0.0873) lower bilateral-mean volume of the thalamus for each 1-unit lower cVEMP amplitude. We also found a relationship between a lower mean VOR gain and lower left hippocampal volume (β = 0.121, unadjusted p = 0.018, 95% CI: 0.0212–0.222). There were no significant associations between volume and oVEMP. These findings provide insight into the specific brain structures that undergo atrophy in the context of age-related loss of peripheral vestibular function.

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Linking vestibular function and sub-cortical grey matter volume changes in a longitudinal study of aging adults

10.1101/2020.11.17.20233684 ◽

2020 ◽

Author(s):

Dominic Padova ◽

J. Tilak Ratnanather ◽

Qian-Li Xue ◽

Susan M. Resnick ◽

Yuri Agrawal

Keyword(s):

Older Adults ◽

Longitudinal Study ◽

Basal Ganglia ◽

Spatial Cognition ◽

Vestibular Function ◽

Brain Regions ◽

Vestibular Input ◽

Vestibular Loss ◽

Age Related ◽

Over Time

AbstractEmerging evidence suggests a relationship between impairments of the vestibular (inner ear balance) system and decline in visuospatial cognitive performance in older adults. However, it is unclear whether age-related vestibular loss is associated with volume loss in brain regions known to receive vestibular input. To address this gap, we investigated the association between vestibular function and the volumes of four structures that process vestibular information (the hippocampus, entorhinal cortex, thalamus, and basal ganglia) in a longitudinal study of 97 healthy, older participants from the Baltimore Longitudinal Study of Aging. Vestibular testing included cervical vestibular-evoked myogenic potentials (cVEMP) to measure saccular function, ocular VEMP (oVEMP) to measure utricular function, and video head-impulse tests to measure the horizontal semi-circular canal vestibulo-ocular reflex (VOR). Participants in the sample had vestibular and brain MRI data for a total of 1 (18.6%), 2 (49.5%) and 3 (32.0%) visits. Linear mixed-effects regression was used to model regional volume over time as a function of vestibular physiological function, correcting for age, sex, intracranial volume, and inter-subject random variation in the baseline levels of and rates of change of volume over time. We found that poorer saccular function, characterized by lower cVEMP amplitude, is associated with reduced bilateral volumes of the thalamus and basal ganglia at each time point, demonstrated by a 0.0714 cm3 ± 0.0344 (p=0.038; 95% CI: 0.00397-0.139) lower bilateral-mean volume of the basal ganglia and a 0.0440 cm3 ± 0.0221 (p=0.046; 95% CI: 0.000727-0.0873) lower bilateral-mean volume of the thalamus for each 1 unit lower cVEMP amplitude. There were no significant associations between volume and oVEMP or mean VOR gain. These findings provide insight into the potential neural substrates for the observed link between age-related vestibular loss and spatial cognition.Comprehensive SummaryHumans rely on their vestibular, or inner ear balance, system to manage everyday life. In addition to sensing head motion and head position with respect to gravity, the vestibular system helps to maintain balance and gaze stability. Furthermore, the evidence is mounting that vestibular function is linked to spatial cognition: the capacity to mentally represent the world and navigate through it. Yet, the exact processes by which vestibular function enables spatial cognition are unclear. One promising mechanism is through changes of the sizes and shapes of the brain anatomies that support spatial cognitive function. The intuition is that, as vestibular function declines with aging, less vestibular information is distributed throughout the brain, leading to a loss of neurons in areas that receive those inputs. In support of this putative mechanism, recent discoveries underscore the association of vestibular impairment with spatial cognitive declines and with atrophy of brain areas that support spatial cognition, the hippocampus and entorhinal cortex, in older adults. This work investigates the extent over time to which age-related vestibular loss contributes to the atrophy of four brain regions that receive vestibular input and subserve spatial cognition: the hippocampus, entorhinal cortex, thalamus, and basal ganglia. Using data from a cohort of healthy, older adults between 2013 and 2017 from the Baltimore Longitudinal Study of Aging, we assessed regional brain volume as a function of vestibular function, while accounting for common confounds of brain volume change (e.g. age, sex, head size). We found that poor vestibular function is associated with significantly reduced volumes of the thalamus and basal ganglia. Notably, this study is one of the first to demonstrate relationships between age-related vestibular loss and brain atrophy in brain regions that receive vestibular input and promote spatial cognition. But more research is needed to understand the observed connection between vestibular function, neuroanatomy, and spatial cognition. Which brain areas suffer from age-related vestibular loss? How and in what sequence are they affected? As the world’s aging population—and likely the prevalence of age-related vestibular impairment—increases, answering questions like these becomes increasingly important. One day, these answers will provide targets for preemptive interventions, like physical or cognitive pre-habilitation, to stave off malignant cognitive changes before they occur and progress into clinical significance.

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Vestibular implantation and longitudinal electrical stimulation of the semicircular canal afferents in human subjects

Journal of Neurophysiology ◽

10.1152/jn.00171.2013 ◽

2015 ◽

Vol 113 (10) ◽

pp. 3866-3892 ◽

Cited By ~ 35

Author(s):

James O. Phillips ◽

Leo Ling ◽

Kaibao Nie ◽

Elyse Jameyson ◽

Christopher M. Phillips ◽

...

Keyword(s):

Electrical Stimulation ◽

Eye Movements ◽

Human Subjects ◽

Vestibular Function ◽

Slow Phase ◽

Vestibular Loss ◽

Stimulation Current ◽

Eye Velocity ◽

Over Time ◽

Stimulation Of

Animal experiments and limited data in humans suggest that electrical stimulation of the vestibular end organs could be used to treat loss of vestibular function. In this paper we demonstrate that canal-specific two-dimensionally (2D) measured eye velocities are elicited from intermittent brief 2 s biphasic pulse electrical stimulation in four human subjects implanted with a vestibular prosthesis. The 2D measured direction of the slow phase eye movements changed with the canal stimulated. Increasing pulse current over a 0–400 μA range typically produced a monotonic increase in slow phase eye velocity. The responses decremented or in some cases fluctuated over time in most implanted canals but could be partially restored by changing the return path of the stimulation current. Implantation of the device in Meniere's patients produced hearing and vestibular loss in the implanted ear. Electrical stimulation was well tolerated, producing no sensation of pain, nausea, or auditory percept with stimulation that elicited robust eye movements. There were changes in slow phase eye velocity with current and over time, and changes in electrically evoked compound action potentials produced by stimulation and recorded with the implanted device. Perceived rotation in subjects was consistent with the slow phase eye movements in direction and scaled with stimulation current in magnitude. These results suggest that electrical stimulation of the vestibular end organ in human subjects provided controlled vestibular inputs over time, but in Meniere's patients this apparently came at the cost of hearing and vestibular function in the implanted ear.

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Video Head Impulse Testing (vHIT) and the Assessment of Horizontal Semicircular Canal Function

Journal of the American Academy of Audiology ◽

10.3766/jaaa.14083 ◽

2015 ◽

Vol 26 (05) ◽

pp. 518-523 ◽

Cited By ~ 5

Author(s):

Kristal M. Riska ◽

Owen Murnane ◽

Faith W. Akin ◽

Courtney Hall

Keyword(s):

Semicircular Canal ◽

Objective Assessment ◽

Vestibular Function ◽

Vestibular Evoked Myogenic Potentials ◽

Head Impulse Test ◽

Clinical Test ◽

Horizontal Semicircular Canal ◽

Head Impulse ◽

New Instrument ◽

Qualitative Test

Background: Vestibular function (specifically, horizontal semicircular canal function) can be assessed across a broad frequency range using several different techniques. The head impulse test is a qualitative test of horizontal semicircular canal function that can be completed at bedside. Recently, a new instrument (video head impulse test [vHIT]) has been developed to provide an objective assessment to the clinical test. Questions persist regarding how this test may be used in the overall vestibular test battery. Purpose: The purpose of this case report is to describe vestibular test results (vHIT, rotational testing, vestibular evoked myogenic potentials, and balance and gait performance) in an individual with a 100% unilateral caloric weakness who was asymptomatic for dizziness, vertigo or imbalance. Data Collection and/or Analysis: Comprehensive assessment was completed to evaluate vestibular function. Caloric irrigations, rotary chair testing, vHIT, and vestibular evoked myogenic potentials were completed. Results: A 100% left-sided unilateral caloric weakness was observed in an asymptomatic individual. vHIT produced normal gain with covert saccades. Conclusions: This case demonstrates the clinical usefulness of vHIT as a diagnostic tool and indicator of vestibular compensation and functional status.

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Vestibular evoked myogenic potentials in response to laterally directed skull taps

Journal of Vestibular Research ◽

10.3233/ves-2002-12104 ◽

2002 ◽

Vol 12 (1) ◽

pp. 35-45 ◽

Cited By ~ 2

Author(s):

Krister Brantberg ◽

Arne Tribukait

Keyword(s):

Vestibular Function ◽

Normal Subjects ◽

Short Latency ◽

The Other ◽

Vestibular Evoked Myogenic Potentials ◽

Vestibular Loss ◽

Skin Electrodes ◽

Function Loss ◽

Relaxation Responses ◽

Muscular Responses

In recent years it has been demonstrated that loud clicks generate short latency vestibular evoked myogenic potentials (VEMP). It has also been demonstrated that midline forehead skull tap stimulation evokes similar VEMP. In the present study, the influence of skull tap direction on VEMP was studied in 13 normal subjects and in five patients with unilateral vestibular loss. Gentle skull taps were delivered manually above each ear on the side of the skull. The muscular responses were recorded over both sternocleidomastoid muscles using skin electrodes. Among the normals, laterally directed skull taps evoked “coordinated contraction-relaxation responses”, i.e. skull taps on one side evoked a negative-positive “inverted” VEMP on that side and a positive-negative "normal" VEMP on the other side. Among patients with unilateral vestibular function loss, skull taps above the lesioned ear evoked similar coordinated contraction-relaxation responses. However, skull taps above the healthy ear did not evoke that type of response. These findings suggest that laterally directed skull taps activate mainly the contralateral labyrinth.

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Abstract 043: Leisure-Time Physical Activity in Adulthood and Region of Interest (ROI) Brain Volumes: The Atherosclerosis Risk in Communities Neurocognitive Study (ARIC-NCS)

Circulation ◽

10.1161/circ.137.suppl_1.043 ◽

2018 ◽

Vol 137 (suppl_1) ◽

Author(s):

Priya Palta ◽

A R Sharrett ◽

Kelly R Evenson ◽

Clifford R Jack ◽

Pamela L Lutsey ◽

...

Keyword(s):

Physical Activity ◽

Cognitive Impairment ◽

Life Table ◽

Brain Mri ◽

Late Life ◽

Intracranial Volume ◽

Reverse Causality ◽

Cross Sectional ◽

Brain Volumes ◽

Age Related

Introduction: Several studies report late-life physical activity (PA) to be associated with less brain atrophy. Associations of PA and subclinical brain markers evaluated at older ages may be subject to reverse causality due to comorbidity, age-related changes in lifestyle, or incipient cognitive impairment. Therefore, we aimed to compare late-life cross-sectional estimates of PA and ROI brain volumes to those using prospective PA measures from mid- to late-life. Methods: Participants (n=1549, mean age: 75, 39% male, 20% Black) with repeat assessments of PA from visit 1 (1987-1989) and a brain magnetic resonance imaging (MRI) in 2011-2013 were included. Total volume of PA in metabolic equivalent-min/week was estimated using the Baecke Physical Activity Questionnaire and classified as no, low, middle or high at each visit. Based on visit 1 and 3 (1993-1995) PA assessments, a subset of participants (n=663) were further categorized as habitually inactive or having habitually low, middle, or high PA in mid-life. Brain MRI using 3D-1.5T equipment quantified ROI volumes following a standardized protocol. Weighted linear regression adjusted for intracranial volume, demographics, select cardiovascular risk factors and ApoE4 estimated the standardized difference in ROI volumes. Results: Compared to no PA, high PA was associated with larger ROI brain volumes cross-sectionally in late-life (Table). High mid-life PA was only modestly associated with larger frontal cortical and deep gray matter volumes in late-life (Table). Habitually high PA in mid-life was not associated with less atrophy across brain regions in late-life. Conclusions: Our results do not support a causal interpretation of the cross-sectional associations between PA and brain volumes reported in late-life. Drawing on long-term population-based data, this study provides novel information on the associations of PA across life epochs with brain health, which can inform translational and intervention efforts to reduce age-related cognitive impairment.

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Preservation of tap vestibular evoked myogenic potentials despite resection of the inferior vestibular nerve

Journal of Vestibular Research ◽

10.3233/ves-2004-14404 ◽

2004 ◽

Vol 14 (4) ◽

pp. 347-351 ◽

Cited By ~ 3

Author(s):

Krister Brantberg ◽

Tiit Mathiesen

Keyword(s):

Bone Conduction ◽

Vestibular Function ◽

Vestibular Nerve ◽

Vestibular Evoked Myogenic Potentials ◽

Nerve Function ◽

Sound Stimulation ◽

Vestibular Loss ◽

Vestibular Neurectomy ◽

Inferior Vestibular Nerve ◽

Healthy Side

Sound and skull-tap induced vestibular evoked myogenic potentials (VEMP) were studied in a 43-year-old man following inferior vestibular neurectomy. Surgery was performed because of a small acoustic neuroma. Postoperative caloric testing suggested sparing of superior vestibular nerve function on the operated side. In response to sound stimulation there were no VEMP on the operated side, irrespective of whether sounds were presented by air- or bone-conduction. This suggests sound-induced VEMP to be critically dependent on inferior vestibular nerve function and this is in agreement with present knowledge. However, VEMP were obtained in response to forehead skull taps, i.e. positive-negative VEMP not only on the healthy side but also on the operated side. This suggests remnant vestibular function on the operated side of importance for forehead skull tap VEMP, because with complete unilateral vestibular loss there are no (positive-negative) VEMP on the lesioned side. Thus, forehead skull-tap VEMP depend, at least partly, on the superior vestibular nerve function.

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Aging, Vestibular Function, and Balance: Proceedings of a National Institute on Aging/National Institute on Deafness and Other Communication Disorders Workshop

The Journals of Gerontology Series A ◽

10.1093/gerona/glaa097 ◽

2020 ◽

Vol 75 (12) ◽

pp. 2471-2480

Author(s):

Yuri Agrawal ◽

Daniel M Merfeld ◽

Fay B Horak ◽

Mark S Redfern ◽

Brad Manor ◽

...

Keyword(s):

Older Adults ◽

Research Agenda ◽

Balance Control ◽

Vestibular Function ◽

Communication Disorders ◽

Knowledge Gaps ◽

Vestibular Loss ◽

Balance Impairment ◽

Age Related ◽

Key Questions

Abstract Balance impairment and falls are among the most prevalent and morbid conditions affecting older adults. A critical contributor to balance and gait function is the vestibular system; however, there remain substantial knowledge gaps regarding age-related vestibular loss and its contribution to balance impairment and falls in older adults. Given these knowledge gaps, the National Institute on Aging and the National Institute on Deafness and Other Communication Disorders convened a multidisciplinary workshop in April 2019 that brought together experts from a wide array of disciplines, such as vestibular physiology, neuroscience, movement science, rehabilitation, and geriatrics. The goal of the workshop was to identify key knowledge gaps on vestibular function and balance control in older adults and develop a research agenda to make substantial advancements in the field. This article provides a report of the proceedings of this workshop. Three key questions emerged from the workshop, specifically: (i) How does aging impact vestibular function?; (ii) How do we know what is the contribution of age-related vestibular impairment to an older adult’s balance problem?; and more broadly, (iii) Can we develop a nosology of balance impairments in older adults that can guide clinical practice? For each of these key questions, the current knowledge is reviewed, and the critical knowledge gaps and research strategies to address them are discussed. This document outlines an ambitious 5- to 10-year research agenda for increasing knowledge related to vestibular impairment and balance control in older adults, with the ultimate goal of linking this knowledge to more effective treatment.

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Skull Vibration-Induced Nystagmus Test in a Human Model of Horizontal Canal Plugging

Audiology Research ◽

10.3390/audiolres11030028 ◽

2021 ◽

Vol 11 (3) ◽

pp. 301-312

Author(s):

Georges Dumas ◽

Christol Fabre ◽

Anne Charpiot ◽

Lea Fath ◽

Hella Chaney-Vuong ◽

...

Keyword(s):

Semicircular Canal ◽

Vestibular Function ◽

Human Model ◽

Vestibular Evoked Myogenic Potentials ◽

Head Impulse Test ◽

Slow Phase ◽

Caloric Test ◽

Horizontal Semicircular Canal ◽

Horizontal Canal ◽

Tertiary Referral Center

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.

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Nightly Hypoxia Does Not Seem to Lead to Otolith Dysfunction in Patients With Obstructive Sleep Apnea

Ear Nose & Throat Journal ◽

10.1177/0145561320922126 ◽

2020 ◽

pp. 014556132092212

Author(s):

Richard Birk ◽

Miriam Dietz ◽

Jörg Ulrich Sommer ◽

Boris A. Stuck ◽

Karl Hörmann ◽

...

Keyword(s):

Obstructive Sleep Apnea ◽

Sleep Apnea ◽

Vestibular Function ◽

Oxygen Desaturation ◽

Vestibular Evoked Myogenic Potentials ◽

Head Impulse Test ◽

Apnea Hypopnea Index ◽

Horizontal Semicircular Canal ◽

Respiratory Parameters ◽

Obstructive Sleep

Objectives: Obstructive sleep apnea (OSA) is a common sleep disorder, which is associated with recurrent oxygen desaturation during sleep. It has already been shown that nocturnal hypoxia may lead to cochlear dysfunction in patients with OSA. Less is known whether hypoxia during sleep also impacts vestibular function in those patients. Thus, the aim of the presented study was to assess a potential vestibulotoxic effect of nightly desaturations with hypoxia in patients with OSA by investigating a possible correlation between respiratory parameters and vestibular function tests. Methods: A total of 56 patients were included in the study and underwent a fully attended cardiorespiratory polysomnography (PSG). Vestibular function was assessed using video head impulse test to evaluate horizontal semicircular canal function and cervical vestibular evoked myogenic potentials (cVEMPs) and ocular vestibular evoked myogenic potentials (oVEMPs) to measure otolith function. Descriptive data analysis was conducted and correlation analysis between selected PSG parameters and the results of vestibular testing was performed using Kendall τ coefficient. Results: A significant correlation between vestibular function and respiratory polysomnographic parameters could not be demonstrated in the study ( P > .05) but cVEMP and oVEMP results showed a trend toward a correlation with oxygen desaturation indices and apnea–hypopnea index. Additionally, otolith hypofunction was more prevalent in patients with hypertension as well as OSA. Conclusion: The results of our study show that there is no significant correlation between vestibular function and sleep apnea parameters, although otolith dysfunction might be more prevalent in patients with OSA and hypertension.

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Visualizing the neuroanatomical changes in Han Chinese adulthood: A pseudo-longitudinal study based on age-related large-scale statistical Chinese brain atlases

Brain Science Advances ◽

10.1177/2096595820902583 ◽

2019 ◽

Vol 5 (2) ◽

pp. 106-116

Author(s):

Lin Shi ◽

Peipeng Liang ◽

Andy Li ◽

Raymond Wong ◽

Yishan Luo ◽

...

Keyword(s):

Longitudinal Study ◽

Large Scale ◽

Brain Mri ◽

Temporal Cortex ◽

Occipital Cortex ◽

Han Chinese ◽

Brain Atlas ◽

Age Related ◽

Multiple Regions ◽

Brain Atlases

Objective: Understanding how brain changes over lifetime provides the basis for new insights into neurophysiology and neuropathology. In this study, we carried out a pseudo-longitudinal study based on age-related Chinese brain atlases (i.e., Chinese2020) constructed from large-scale volumetric brain MRI data collected in normal Han Chinese adults at varying ages. Methods: In order to quantify the deformation and displacement of brains for each voxel as age increases, optical flow algorithm was employed to compute motion vectors between every two consecutive brain templates of the age-related brain atlas, i.e., Chinese2020. Results: Dynamic age-related neuroanatomical changes in a standardized brain space were shown. Overall, our results demonstrate that brain inward deformation (mainly due to atrophy) can appear in adulthood and this trend generally accelerates as age increases, affecting multiple regions including frontal cortex, temporal cortex, parietal cortex, and cerebellum, whereas occipital cortex is least affected by aging, and even showed some degree of outward deformation in the midlife. Conclusion: Our findings indicated more complicated age-related changes instead of a simple trend of brain volume decrease, which may be in line with the recently increasing interests in the age-related cortical complexity with other morphometry measures.

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