vestibulo-ocular physiology underlying vestibular...

2004; 84:373-385.PHYS THER. Michael C Schubert and Lloyd B MinorHypofunctionVestibulo-ocular Physiology Underlying Vestibular

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Vestibulo-ocular PhysiologyUnderlying Vestibular Hypofunction

The vestibular system detects motion of the head and maintainsstability of images on the fovea of the retina as well as postural controlduring head motion. Signals representing angular and translationalmotion of the head as well as the tilt of the head relative to gravity aretransduced by the vestibular end organs in the inner ear. This sensoryinformation is then used to control reflexes responsible for maintain-ing the stability of images on the fovea (the central area of the retinawhere visual acuity is best) during head movements. Information fromthe vestibular receptors also is important for posture and gait. Whenvestibular function is normal, these reflexes operate with exquisiteaccuracy and, in the case of eye movements, at very short latencies.Knowledge of vestibular anatomy and physiology is important forphysical therapists to effectively diagnose and manage people withvestibular dysfunction. The purposes of this article are to review theanatomy and physiology of the vestibular system and to describe theneurophysiological mechanisms responsible for the vestibulo-ocularabnormalities in patients with vestibular hypofunction. [Schubert MC,Minor LB. Vestibulo-ocular physiology underlying vestibular hypofunc-tion. Phys Ther. 2004;84:373–385.]

Key Words: Anatomy, Clinical vestibular testing, Physiology, Vestibular rehabilitation, Vestibulo-ocular

reflex.

Michael C Schubert, Lloyd B Minor

Physical Therapy . Volume 84 . Number 4 . April 2004 373

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The vestibular system is responsible for sensingmotion of the head and maintains stability ofimages on the fovea of the retina and posturalcontrol during that motion. When functioning

normally, the vestibular receptors in the inner ear pro-vide an exquisitely accurate representation of themotion of the head in 3 dimensions. This information isthen used by the central vestibular pathways to controlreflexes and perceptions that are mediated by the ves-tibular system. Disorders of vestibular function result inabnormalities in these reflexes and lead to sensationsthat reflect abnormal information about motion fromthe vestibular receptors.1

Best visual acuity is obtained when images are projectedon the fovea of the retina. The fovea occupies a smallarea of the visual field, but movements of an image offthe fovea by as little as 1 degree can cause substantialdecreases in visual acuity.2 Stabilization of a visual targeton the fovea can be achieved by various systems, includ-ing the vestibular and smooth pursuit oculomotor sys-tems.3 Influences such as target velocity and distance aswell as velocity and frequency of head motion are thestimulus variables the brain uses to determine whichoculomotor system is recruited for gaze stability. Each ofthe oculomotor subsystems has a range in which itfunctions most efficiently.

Normal activities of daily life (such as running) can havehead velocities of up to 550°/s, head accelerations of upto 6,000°/s2, and frequency content of head motionfrom 0 to 20 Hz.4,5 Only the vestibular system can detecthead motion over this range of velocity, acceleration,and frequency.3 Additionally, the latency of thevestibulo-ocular reflex (VOR) has been reported to be asshort as 5 to 7 milliseconds.6,7 In contrast, ocular follow-ing mechanisms, such as smooth pursuit, generateslower eye velocities (�60°/s) and have relatively longlatencies (up to 100 milliseconds).8,9

The purposes of this article are to review the anatomyand physiology of the vestibular system and to describethe neurophysiological mechanisms responsible for thevestibulo-ocular abnormalities of people with vestibulardysfunction.

Anatomy and Physiology

Peripheral Vestibular AnatomyWithin the petrous portion of each temporal bone liesthe membranous vestibular labyrinth. Each labyrinthcontains 5 neural structures that detect head accelera-tion: 3 semicircular canals and 2 otolith organs (Fig. 1).The 3 semicircular canals (SCC) (lateral, posterior, andanterior) respond to angular acceleration and areorthogonal with respect to each other. Alignment of theSCCs in the temporal bone is such that each canal has acontralateral coplanar mate. The lateral canals form acoplanar pair, whereas the posterior and contralateralanterior SCC form coplanar pairs. The anterior aspect ofthe lateral SCC is inclined 30 degrees upward from aplane connecting the external auditory canal to thelateral canthus. The posterior and anterior SCCs areinclined about 92 and 90 degrees from the plane of thelateral SCC.10 Because the SCCs are not precisely ortho-gonal with earth vertical or earth horizontal, angularrotation of the head stimulates each canal to varyingdegrees.11

The SCCs are filled with endolymph that has a densityslightly greater than that of water. Endolymph contains ahigh concentration of potassium, with a lower concen-tration of sodium, and moves freely within each canal inresponse to the direction of the angular head rotation.12

The SCCs enlarge at one end to form the ampulla.Within the ampulla lies the cupula, a gelatinous barrierthat houses the sensory hair cells (Fig. 2A). The kinociliaand stereocilia of the hair cells are seated in the cristaampullaris (Fig. 2B). Deflection of the stereocilia causedby motion of the endolymph results in an opening (orclosing) of the transduction channels of hair cells, whichchanges the membrane potential of the hair cells.Deflection of the stereocilia toward the single kinociliain each hair cell leads to excitation (depolarization), and

MC Schubert, PT, PhD, is a postdoctoral fellow in the Department of Otolaryngology-Head and Neck Surgery, Johns Hopkins University, 710 RossBldg, 720 Rutland Ave, Baltimore, MD 21205 (USA) ([email protected]). Address all correspondence to Dr Schubert.

LB Minor, MD, is Professor, Department of Otolaryngology-Head and Neck Surgery, Johns Hopkins University.

Both authors provided concept/idea/research design and writing.

This article was received June 3, 2003, and was accepted October 21, 2003.

An understanding of the exquisite and

essential vestibular anatomy and

physiology is needed to effectively

diagnose and manage people with

vestibular dysfunction.

374 . Schubert and Minor Physical Therapy . Volume 84 . Number 4 . April 2004 by guest on April 15, 2014http://ptjournal.apta.org/Downloaded from



deflection of the stereocilia away from the kinocilia leadsto inhibition (hyperpolarization).

Hair cells are oriented in the lateral SCC so thatendolymph motion toward the ampulla causes excitation.In contrast, hair cells of the vertical SCCs (posterior andanterior) are oriented so that depolarization occurswhen endolymph moves away from the ampulla. Each ofthe SCCs responds best to motion in its own plane, withcoplanar pairs exhibiting a push-pull dynamic. Forexample, as the head is turned to the right, the hair cellsin the right lateral SCC are excited, whereas the haircells in the left lateral SCC are inhibited.13 The braindetects the direction of head movement by comparinginput from the coplanar labyrinthine mates.

The saccule and utricle make up the otolith organs ofthe membranous labyrinth. Sensory hair cells projectinto a gelatinous material that has calcium carbonatecrystals (otoconia) embedded in it, which provide theotolith organs with an inertial mass (Fig. 3). The utricleand the saccule have central regions known as thestriola, dividing the otolith organs into 2 parts. Thekinocilia of the utricular hair cells are oriented towardtheir striola, whereas the kinocilia of the saccular hair

cells are oriented away from theirstriola. Motion toward the kinociliacauses excitation. Utricular excitationoccurs during horizontal linear acceler-ation or static head tilt, and saccularexcitation occurs during vertical linearacceleration.

Vestibular Afferent PhysiologyIn primates, primary vestibular affer-ents of the healthy vestibular systemhave a resting firing rate that is typically70 to 100 spikes per second.13,14 Thedischarge regularity (determined bythe spacing of the interspike intervalsbetween action potentials [Fig. 4]) ofvestibular nerve afferents provides auseful marker for the information car-ried by these afferents. The coefficientof variation (standard deviation/meandischarge) of the interspike intervalprovides a useful measurement for clas-sifying afferents into irregularly andregularly discharging groups. Theinformation carried by irregular andregular afferents varies over the spec-tral range of frequency and accelera-tion that encompasses natural headmovements. Generally, irregular affer-ents are more sensitive to rotationsduring large head accelerations than

regular afferents are.14 The increased sensitivity of theirregular afferents may be more critical for the rapiddetection of head movements as well as initiation of theVOR.6,14 The regular afferents, in contrast, provide asignal that is proportional to head velocity over a widespectral range.14 In addition, the regular afferents maybe the primary source of input to the VOR for steady-state responses to sinusoidal rotations because tempo-rarily silencing the irregular afferents has no affect onthe VOR during low-frequency and small head acceler-ations.15

The cells bodies of vestibular nerve afferents are locatedin the superior or inferior divisions of Scarpa’s ganglia,which lie within the internal auditory canal near theemergence of the vestibular nerve into the cerebello-pontine angle.16 From the vestibular labyrinth, the affer-ent information travels ipsilateral in 1 of 2 branches ofthe vestibular nerve. The superior vestibular nerve inner-vates the lateral and anterior SCC as well as the utricle.The inferior vestibular nerve innervates the posteriorSCC and the saccule.17 It is estimated that between15,000 to around 25,000 vestibular nerve fibers exist inhumans.18–20 Variation of nerve fiber counts amongstudies appears to be a function of age, although rate of

Figure 1.Anatomy of the vestibular labyrinth. Structures include the utricle (Utr.), sacculus, anterior (orsuperior) semicircular canal (Sup.), posterior semicircular canal (Post.), and the lateralsemicircular canal (Lat.). Note the superior vestibular nerve innervating the anterior and lateralsemicircular canals as well as the utricle. The inferior vestibular nerve innervates the posteriorsemicircular canal and the saccule. The cell bodies of the vestibular nerves are located inScarpa’s ganglion (Gangl. Scarpae). Drawing from the Max Brodel Archives (No. 933).Reproduced with permission of the Department of Art as Applied to Medicine, Johns HopkinsUniversity.

Physical Therapy . Volume 84 . Number 4 . April 2004 Schubert and Minor . 375

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decline of the number of afferent fibers also appears tobe variable. The branches of the vestibular nerve traveltogether into the pontomedullary junction where theybifurcate. Primary vestibular afferents in the superiordivision of the vestibular nerve include axons that syn-apse in the superior and medial vestibular nuclei or theuvula, nodulus, flocculus, or fastigial nucleus of thecerebellum.21–24 Primary vestibular afferents from theinferior branch synapse with neurons in either themedial, lateral, or inferior vestibular nuclei, which, along

with the superior vestibular nuclei and other subnuclei,comprise the vestibular nuclear complex.17

Central Vestibular AnatomySecondary vestibular afferents have been identified asrelaying signals from the vestibular nuclei to the extra-ocular motor nuclei, the spinal cord, or the flocculus ofthe cerebellum.25 Central vestibular neurons differ interms of the inputs they receive from regular andirregular afferents. Those central vestibular neurons thatproject to the extraocular motor nuclei receive a major-ity of their monosynaptic inputs from regular afferents,whereas those that project to the spinal cord receive amajority of their inputs from irregular afferents.25,26

Those central vestibular neurons projecting to the floc-culus of the cerebellum receive relatively equal contri-butions from regular and irregular afferents.25

Many vestibular reflexes are controlled by processes thatexist primarily within the brain stem. Tracing tech-niques, however, have identified extensive connectionsbetween the vestibular nuclei and the reticular forma-tion,27 thalamus,28 and cerebellum.21 Vestibular path-ways appear to terminate in a unique cortical area. Instudies of primates, fibers terminating in the junction ofthe parietal and insular lobes have been identified andconsidered the location for a vestibular cortex.29–31

Recent evidence in studies of humans using functionalmagnetic resonance imaging appears to confirm theparietal and insular regions as the cortical location forprocessing vestibular information.32 Connections with

Figure 2.(A) The semicircular canals enlarge at one end to form the ampulla. Thecupula of the ampulla is a flexible barrier that partitions the canal. Thecrista ampullaris contains the sensory hair cells. The hair cells generateaction potentials in response to cupular deflection. (B) Cross-section ofcrista ampullaris showing kinocilia and stereocilia of hair cells project-ing into the cupula. Deflection of the stereocilia towards the kinociliacauses excitation; deflection in the opposite direction causes inhibition.Drawing adapted with permission from Patricia Wynne.

Figure 3.Otoconia are embedded in a gelatinous matrix and provide an inertialmass. Linear acceleration shifts the gelatinous matrix and excites orinhibits the vestibular afferents depending on the direction in which thestereocilia are deflected. Drawing adapted with permission from Patri-cia Wynne.




the vestibular cortex, thalamus, and reticular formationenable the vestibular system to contribute to the integra-tion of arousal and conscious awareness of the body andto discriminate between movement of self and theenvironment.33,34 The cerebellar connections help main-tain calibration of the VOR, contribute to posture dur-ing static and dynamic activities, and influence thecoordination of limb movements.

Vestibulo-ocular PhysiologyThe ability of the VOR to elicit rapid compensatory eyemovements that maintain stability of images on the foveadepends on relatively simple patterns of connectivity in

the central vestibular pathways. In its most basic form,the pathways controlling the VOR can be described as a3-neuron arc. In the case of the lateral SCC, primaryvestibular afferents from the lateral SCC synapse in theipsilateral medial and ventrolateral vestibular nuclei.Some of the secondary vestibular neurons receivinginnervation from the ipsilateral labyrinth have axonsthat decussate and synapse in the contralateral abducensnucleus, whereas others ascend ipsilaterally to the oculo-motor nucleus. Motoneurons from the abducensnucleus and the medial rectus subdivision of the oculo-motor nucleus then synapse at the neuromuscular junc-tion of the lateral rectus and medial rectus muscles,respectively. Similar patterns of connectivity exist for theanterior and posterior SCC and the eye muscles thatreceive innervations from them (Tab. 1).35 Figure 5illustrates the insertions of the ocular muscles.

The VOR has been tested across multiple frequenciesand velocities and shows velocity-dependent nonlineari-ties,6 which may correlate with unique afferent physiol-ogy. The gain of the VOR remains constant (linear)across multiple frequencies of sinusoidal rotations, withpeak velocities of �20°/s.6 For rotations at higher fre-quencies and velocities, the VOR gain rises withincreases in stimulus velocity (nonlinear). Similar effectsof stimulus frequency and velocity are seen in responsesto steps of acceleration. Therefore, it may be that theoutput of the VOR is the combined result of linear andnonlinear components.6 Adaptation experiments inwhich spectacles were used to modify the gain of theVOR support the notion that a linear component and anonlinear component may be responsible for mediatingthe VOR. Using different frequency and velocity profilesfor the adaptation stimulus, the nonlinear componenthas been shown to be adaptable only with high-frequency and high-velocity stimuli.36

Incidence and Prevalence of Dizziness in theUnited StatesThe incidence of dizziness in the United States isapproximately 5.5%, which means that more than 15million people develop the symptom each year.37 Thereported prevalence of dizziness as a medical complaintin community-dwelling adults varies based on their age,sex, and definition of the complaint (1%–35%).38–41

Researchers using specific definitions such as vertigo (anillusion of motion) have reported a prevalence of up to6.7%, which increases with age.39,40,42 When researchersused a broader definition that included light-headednessand disequilibrium, they reported a greater prevalenceof dizziness (25%–35%).38,41 Many of these patients mostlikely had nonvestibular causes of their dizziness. Dizzi-ness is one of the most common complaints reported inphysicians’ offices, with the prevalence increasing withage.43,44 For patients over 75 years of age, dizziness is the

Figure 4.Action potentials of regular and irregular vestibular afferents recorded insquirrel monkey. For these particular neurons, resting discharge rate is97 spikes per second for regular afferents and 98 spikes per second forirregular afferents. Note that the time between action potentials differslittle from one spike to the next for the regular afferent. In contrast, theinterspike interval is quite variable for the irregular afferent. Adaptedwith permission from Goldberg JM, Fernandez C. Physiology of periph-eral neurons innervating semicircular canals of the squirrel monkey, I:resting discharge and response to constant angular accelerations.J Neurophysiol. 1971;34:635–660.


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most common reason they see a physician.45 Regardlessof age, patients who experience dizziness report a signif-icant disability that reduces their quality of life.46–48

Furthermore, it has been reported that more than 70%of patients with initial reports of dizziness will not have aresolution of symptoms at a 2-week follow-up. Of thosepatients with persistent dizziness, 63% reported recur-rent symptoms continuing beyond 3 months.49

Distinguishing Between Vestibular andNonvestibular Causes of DizzinessClinicians who work with people who report dizzinessand imbalance have the difficult task of sorting throughpotential causes. Capturing a thorough history is a

critical component of the assessment. Many patients andclinicians use the imprecise term “dizziness” to describea vague sensation of light-headedness or a feeling thatthey have a tendency to fall. The imprecision of the termcan make clinical management decisions complicated.Generally, most complaints of being “dizzy” can becategorized as light-headedness, disequilibrium, vertigo,or oscillopsia.

Light-headedness is often defined as a feeling that faintingis about to occur and can be caused by nonvestibularfactors such as hypotension, hypoglycemia, or anxiety.50

Disequilibrium is defined as the sensation of being offbalance. Often, disequilibrium is associated with nonves-tibular problems such as decreased somatosensation orweakness in the lower extremities. Vertigo is defined as anillusion of movement. Vertigo tends to be episodic andtends to indicate pathology at one or more places alongthe vestibular pathways. Vertigo is common during theacute stage of a unilateral vestibular lesion, but also maymanifest itself through displaced otoconia (benign par-oxysmal positional vertigo [BPPV]) or acute brain stemlesions affecting the root entry zone of the peripheralvestibular neurons or the vestibular nuclei.50 Oscillopsia isthe experience that objects in the visual surround thatare known to be stationary are in motion. Oscillopsia canoccur in association with head movements in patientswith vestibular hypofunction because the vestibular sys-tem is not generating an adequate compensatory eyevelocity during a head rotation.51 A deficit such as thisin the VOR results in motion of images on the fovea andin a decline in visual acuity. The severity of gaze insta-bility, however, varies among people with vestibularhypofunction.51–54

Table 2 lists some of the more common causes associatedwith symptoms due to vestibular and nonvestibular diz-ziness and imbalance. Baloh50 provided a thoroughreview that distinguishes vestibular causes of dizzinessfrom nonvestibular causes.

Table 1.Innervation Pattern of Excitatory Input From the Semicircular Canals

Primary Afferent Secondary Neurona Extraocular Motoneuron Muscle

Lateral (right) Medial vestibular nucleus Right oculomotor nucleusb 3Right medial rectusLeft abducens nucleus 3Left lateral rectus

Anterior (or superior) (right) Lateral vestibular nucleus Left oculomotor nucleus 3Left inferior obliquenRight superior rectus

Posterior (or inferior) (right) Medial vestibular nucleus Left trochlear nucleus 3Right superior obliqueLeft oculomotor nucleus 3Left inferior rectus

a Ascending secondary neurons travel in the medial longitudinal fasciculus (MLF).b For the lateral semicircular canal, secondary neurons also travel in the ascending tract of Dieters.

Figure 5.Muscle insertions of the left eye. The 6 extraocular muscles insert into thesclera and can be considered as complementary pairs. The medial andlateral rectus muscles rotate the eyes horizontally, the superior andinferior rectus muscles principally rotate the eyes vertically, and thesuperior and inferior oblique muscles rotate the eyes torsionally withsome vertical component. By convention, the torsional rotation is notedas it relates to the superior poles of the eyes. The superior oblique musclerotates the eye downward and toward the nose [intorsion], whereas theinferior oblique muscle rotates the eye upward and away from the nose[extorsion]. The superior oblique muscle travels through the fibroustrochlea, which attaches to the anteromedial superior wall of the orbit.




Clinical Measures of Vestibular FunctionTo clinically assess vestibular dysfunction, first a carefulhistory is taken. The clinical examination then encom-passes assessment of eye movements, posture, and gait.Because of the direct relationship between vestibularreceptors in the inner ear and eye movements producedby VORs, the bedside examination of eye movementscan be of primary importance in defining and localizingvestibular pathology.

Clinical evaluation of the vestibulo-ocular system takesadvantage of 2 physiological principles: the high restingfiring rate and the inequality in firing rates within thecentral vestibular neurons for excitation and inhibition.The presence of a high resting firing rate means eachvestibular system can detect head motion through exci-tation or inhibition. During angular head rotations,ipsilateral vestibular afferents can be excited up to 400spikes per second.55 Such head movements also result ininhibition of peripheral afferents and of many centralvestibular neurons receiving innervation from the laby-rinth opposite the rotation. Because the resting dis-charge rate of these afferents and central vestibularneurons averages 70 to 100 spikes per second, inhibitorycutoff is more likely to occur than is excitationsaturation.

Head Thrust TestThe head thrust test is a widely accepted clinical tool thatis used to assess semicircular canal function.11,56–59 Thehead is flexed 30 degrees (to ensure cupular stimulationprimarily in the tested lateral SCC). Patients are asked tokeep their eyes focused on a target while their head ismanually rotated in an unpredictable direction using asmall-amplitude (5°–15°), high-acceleration (3,000–4,000°/s2) angular thrust. When the VOR is functioningnormally, the eyes move in the direction opposite to thehead movement and through the exact angle requiredto keep images stable on the fovea. In the case ofvestibular hypofunction, the eyes move less than therequired amount. At the end of the head movement, theeyes are not looking at the intended target and imageshave shifted on the fovea. A rapid, corrective saccade ismade to bring the target back on the fovea. The appear-ance of these corrective saccades indicates vestibular

hypofunction as evaluated by the head thrust test. Dur-ing a horizontal rotation toward the ear with vestibularhypofunction, corrective saccades occur because inhibi-tion of vestibular afferents and central vestibular neu-rons on the intact side (inhibitory cutoff) is less effectivein encoding the amplitude of a head movement thanexcitation is.

The head thrust test provides a sensitive indication ofvestibular hypofunction in patients with complete loss offunction in the affected labyrinth that occurs followingablative surgical procedures, such as labyrinth-ectomy.11,58,60 The test is less sensitive in detectinghypofunction in patients with incomplete loss offunction.61–64

Head-Shaking–Induced NystagmusNystagmus is an involuntary back-and-forth motion ofboth eyes. Any nystagmus due to vestibular stimulationor pathology is composed of slow and fast eye move-ments. The slow component (slow eye velocity) is pro-duce by the intact ear, which generates a normal VOR asa result of the asymmetry between the discharge rates ofcentral vestibular neurons on each side. The fast com-ponent is a resetting eye movement that brings the eyesclose to the center of the oculomotor range.65

The head-shaking–induced nystagmus (HSN) test is auseful aid in the diagnosis of people with asymmetry ofperipheral vestibular input to central vestibular regions.Patients undergoing the HSN test must have their visionblocked because fixation on a visual target can suppressnystagmus.66 Similar to the head thrust test, the headshould initially be flexed 30 degrees. Next, the head isoscillated horizontally for 20 cycles at a frequency of 2repetitions per second (2 Hz). Upon stopping the oscil-lation, people with symmetric peripheral vestibularinput will not have HSN. Typically, a person with aunilateral loss of peripheral vestibular function willmanifest a horizontal HSN, with the quick phases of thenystagmus directed toward the healthy ear and the slowphases directed toward the lesioned ear.65 Not allpatients with a unilateral vestibular loss will have HSN.Patients with a complete loss of vestibular functionbilaterally will not have HSN because neither system is

Table 2.Possible Causes of Vestibular and Nonvestibular Symptoms

Etiology Symptoms Possible Causes

Vestibular Oscillopsia with head movementVertigoImbalance

Unilateral vestibular hypofunction, bilateral vestibular hypofunction,benign paroxysmal positional vertigo, unilateral central lesionaffecting the vestibular nuclei

Nonvestibular Light-headednessDisequilibrium

Orthostatic hypotension, hypoglycemia, anxiety, panic disorder,lower-extremity somatosensory deficit, upper brain stem andmotor pathway lesions


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functioning and there is no asymmetry between thetonic firing rates.

Positional TestingPositional testing is commonly used to identify whetherotoconia have been displaced into the SCC, causingbenign paroxysmal positional vertigo (BPPV). The addi-tion of the otoconia into the endolymph makes thesemicircular canals sensitive to changes in head position.The abnormal signal results in nystagmus and vertigo,nausea with or without vomiting, and disequilibrium.Once the patients are in the provoking position, theresultant nystagmus indicates which semicircular canal isinvolved. Honrubia et al67 and Herdman68 have reviewedthe oculomotor signs and intervention associated withBPPV pathology.

Dynamic Visual AcuityDynamic visual acuity (DVA) is the measurement ofvisual acuity during self-generated horizontal motion ofthe head. A “bedside” and computerized form of the testcan be used to identify the functional significance of thevestibular hypofunction.69,70 Head velocities need to begreater than 100°/s at the time DVA is measured inorder to ensure that the vestibular afferents from thesemicircular canals on the contralateral side are driveninto inhibition and the letters are not identified with asmooth pursuit eye movement.

In people without vestibular problems, head movementresults in little or no change of visual acuity comparedwith the head still. For patients with vestibular hypofunc-tion, the VOR will not keep the eyes stable in spaceduring the rapid head movements. This results in adecrease in visual acuity during head motion comparedwith the head still. Dynamic visual acuity has been foundto correctly identify the side of lesion in patients withunilateral hypofunction for self-generated and unpre-dictable head motion.70,71

Laboratory Measures of Vestibular FunctionThe VOR is typically measured by monitoring eyemotion during stimulation of the peripheral vestibularsystem. The VOR gain is expressed as the ratio of eyevelocity to head velocity (eye velocity/head velocity).Under ideal conditions, when the eyes are not verged(adducting), the VOR gain is –1, implying a compensa-tory eye velocity equal to the head velocity and in theopposite direction. The VOR phase is a second usefulmeasure of the vestibular system and represents thetiming relationship for the eye and head position. Ide-ally, eye position should arrive at a point in time that isequal with the oppositely directed head position. Byconvention, this is described as zero phase shift (Fig. 6).

Semicircular Canal FunctionThe caloric test is the “gold standard” for identifyingperipheral unilateral vestibular hypofunction (UVH).72,73

By introducing a cold or warm stimulus in the externalauditory canal, a temperature gradient is created withthe temporal bone. The change in temperature is thegreatest for the lateral aspect of the temporal bone andthe least for the medial aspect. In the presence of gravity,this temperature gradient results in the convective flowof endolymph that deflects the cupula and generatesnystagmus. Direct hair cell stimulation as well as changesin pressure across the middle ear also cause cupulardeflection, contributing to the resulting nystagmus.74–76

The caloric test is particularly useful for determining theside of a deficit because each labyrinth is stimulatedseparately. Slow components of the nystagmus resultingfrom irrigations of the right ear are compared with slowcomponents of the nystagmus resulting from irrigationsof the left ear. The caloric test provides limited informa-tion, however, because only the lateral SCCs are stimu-lated and that stimulation corresponds to a frequency(0.025 Hz) that is much lower than the natural frequenciesof head movement (1–20 Hz).4,5 The rotary chair test isthe “gold standard” for identifying bilateral vestibularhypofunction (BVH) and the extent of central nervoussystem compensation due to vestibular hypofunction.73

The rotary chair test provides a physiological stimulusbecause rotating the patient causes endolymphatic flowin both lateral SCCs. Nystagmus should be generated forrotations in subjects without known pathology or impair-ments. Depending on the extent of the lesion, peoplewith vestibular hypofunction will demonstrate variedcompensatory slow eye velocities. The extent of pathol-ogy can be determined by comparing VOR gain andphase from rotations toward one ear with rotationstoward the opposite ear. In addition, VOR gain andphase of people without vestibular problems can becompared with that of people with suspected vestibularhypofunction. Rotary chair testing is limited becauseonly the lateral SCCs are routinely assessed to determineextent of pathology.

Otolith FunctionRecent advances in vestibular diagnostic testing haveextended the region of identifiable pathology to includethe otolith organs.77–79 The vestibular-evoked myogenicpotentials (VEMP) test has gained broad clinical use inrecent years.77 The VEMP test exposes patients to a seriesof loud (95 dB) clicks. During the sound application, theipsilateral sternocleidomastoid (SCM) muscle is assessedfor myogenic potentials. In people with healthy vestibu-lar function, an initial inhibitory potential (occurring ata latency of 13 milliseconds after the click) is followed byan excitatory potential (occurring at a latency of 21milliseconds after the click). For patients with vestibularhypofunction, the VEMPs are absent on the side of the




lesion. The pathway of the VEMP is believed to beassociated with the head-neck reflex that maintainsverticality of the head in relation to gravity (the vestibu-locollic reflex). The saccule has been implicated as thesite of afferent stimulation during VEMP testing becausesaccular afferents provide ipsilateral inhibitory disynap-tic input to the SCM muscle,80 are responsive to clicknoise,81–83 and are positioned close to the footplate ofthe stapes and, therefore, are subject to mechanicalstimulation.78,81

The subjective visual vertical (SVV) and subjective visualhorizontal (SVH) tests are used to assess otolith func-tion, though they cannot be used to uniquely detectsaccular or utricular pathology. With the SVV test,patients are asked to align a dimly lit luminous bar (in anotherwise darkened room) with what they perceive asbeing vertical. With the SVH test, patients are asked to

align a bar with what they perceive as being horizontal.Subjects without vestibular problems can align the barwithin 1.5 degrees of true vertical or horizontal, whereaspatients with UVH generally align the bar more than 2degrees of true vertical or horizontal with the bar tiltedtoward the lesioned side.79,84,85 Whether the SVV test orthe SVH test can detect chronic UVH is the subject ofdebate.85–87

Causes of Vestibular Hypofunction

UnilateralThe most frequent cause88 of UVH is vestibular neuro-nitis, which is commonly caused by the herpes simplexvirus. The superior vestibular nerve is more likely to beaffected than the inferior vestibular nerve.89–91 Lesscommon causes include Meniere disease and vestibularschwannoma on the eighth cranial nerve. The incidence

Figure 6.Simulated eye movements during low frequency sinusoidal head rotation Positive numbers along ordinate indicate rightward velocity rotation,whereas negative numbers indicate leftward velocity rotation. Dashed line placed at zero velocity is for reference. Arrow line styles match simulatedeye velocities. For people with healthy vestibular function, as the head rotates to the right at 10°/s, the eyes move to the left at 10°/s, and the eyeand head velocity reach zero at the same time (gain�1, zero phase shift). For people with bilateral reduced vestibular function, eye velocity maybe one half or less with respect to head velocity (5°/s in this example, gain�0.5) and the eyes cross zero velocity in advance of the head crossingzero velocity (eye position leads the head position – phase lead). VOR gain�eye velocity/head velocity.


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rates for these disorders are: 1,710 cases of vestibularneuronitis per million per year,88 500 cases of Menieredisease per million per year,92 and 11.5 cases of vestibu-lar schwannoma per million per year.93 Other patholog-ical events such as vascular lesions affecting the vestibu-lar nerve or traumatic brain injury also may damage thevestibular system unilaterally. Patients who sustain uni-lateral vestibular damage may experience vertigo, spon-taneous nystagmus, oscillopsia, postural instability, anddisequilibrium.

When the peripheral vestibular system is damaged uni-laterally, neuronal activity reaching the ipsilesional ves-tibular nuclei is reduced compared with that reachingthe contralateral vestibular nuclei. The brain interpretsthe asymmetry between resting firing rates as a headrotation toward the contralesional ear. This results inspontaneous nystagmus, with slow components directedtoward the lesioned ear and fast components directedtoward the intact ear. Resolution of spontaneous nystag-mus in the light typically occurs within 3 to 7 days butmay vary, and it can be a process as long as 2 months.94,95

Spontaneous nystagmus may always be present inthe dark after a unilateral loss of vestibular function.Regardless, resolution of spontaneous nystagmus inthe light or dark occurs when symmetry between theresting firing rates of both vestibular systems is reestab-lished.96 A number of authors97–100 have provided moredetail on the complex processes involved in vestibularcompensation.

BilateralThe most common cause of vestibular hypofunction onboth sides (BVH) is ototoxicity due to certain aminogly-coside antibiotics (gentamicin, streptomycin). The anti-biotics selectively damage the vestibular hair cells, oftenpreserving auditory function. It is estimated that 3% to4% of the population who receive gentamicin will sus-tain damage to both vestibular systems.101 For peoplewho receive gentamicin and renal dialysis concurrently,it is estimated that the likelihood of sustaining BVH isfrom 12.5% to 30%.102,103 Unfortunately, it appears thatpeople who are susceptible to ototoxicity have littleprotection from monitoring serum levels of these anti-bodies.104 Less common causes of BVH include menin-gitis, head trauma, tumors on each eighth cranial nerve(including bilateral vestibular schwannoma), transientischemic episodes of vessels supplying the vestibularsystem, and sequential unilateral vestibular neuroni-tis.105–107 Patients with BVH typically experience gaitataxia, postural instability, and oscillopsia.104

Vestibular RehabilitationVestibular rehabilitation refers to interventions such asadaptation exercises, habituation exercises, reposition-ing techniques, and exercise to improve muscle force,

gait, or balance. The beneficial effect of much of therehabilitation for people with vestibulospinal impair-ments as a result of vestibular hypofunction is welldocumented.108–110 Controlled studies have been usedto demonstrate improvements in dynamic visual acuityand to reduce complaints of oscillopsia as well as toreduce VOR gain asymmetry in people receiving vestib-ular adaptation exercises.110,111

Basic research may identify additional roles for programsof vestibular rehabilitation. The angular VOR has com-ponents that can be selectively modified based on thefrequency and velocity of head movements.36 Futurestudies may reveal unique head movement strategies thatoptimize performance and promote recovery of theVOR. These strategies might then be used in the designof interventions. Existing principles of vestibular neuro-physiology warrant vestibular rehabilitation that exposesthe damaged vestibular system to multiple head frequen-cies and velocities, thereby ensuring a broad range ofstimuli to which the system can adapt.

ConclusionsWhen receptors in the inner ear and central pathwaysare functioning normally, the vestibular system providesexquisitely accurate mechanisms for stabilizing gaze andposture. Disorders affecting the end organs in the laby-rinth or the central pathways cause decreases in theperformance of the system, including asymmetries inreflex responses. An understanding of vestibular anat-omy and physiology can reveal the reasons that thesedeficits occur. Further advances in research may lead todesign of more effective rehabilitation strategies.

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2004; 84:373-385.PHYS THER. Michael C Schubert and Lloyd B MinorHypofunctionVestibulo-ocular Physiology Underlying Vestibular

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