Vestibular function after vestibular neuritis

Recently we showed that when a patient comes to the vestibular

clinic with acute vertigo and nausea, the clinician, by using the

results of new objective measures of peripheral vestibular function

can be confi dent it is an acute attack of vestibular neuritis rather than

an acute attack of M é ni è re ’ s disease or an acute attack of labyrinthitis

(Manzari et al, 2011, 2013). But how can the recovery of the patient

after vestibular neuritis be measured? That is the crucial question

for vestibular compensation. Here we show that measures at regular

intervals by the new simple objective measurement of horizontal

semicircular canal function, the video head impulse test (vHIT;

MacDougall et al, 2009), provide the answer. The results from two

extreme patients raise important questions about the mechanism of

recovery after unilateral vestibular loss.

The new tests are (1) the vHIT test of semicircular canal func-

tion, (2) the ocular vestibular-evoked myogenic potential (oVEMP),

and (3) the cervical vestibular evoked myogenic potential (cVEMP).

The video head impulse test (vHIT) is a clinically realistic way of

measuring semicircular canal function quickly and accurately in a

way which is well tolerated by patients, even during intense nau-

sea. Simultaneous measures in the same person by both vHIT and

scleral search coils have shown that the accuracy of vHIT matches

the search coil technique in testing dynamic semicircular canal func-

tion (MacDougall et al, 2009; 2013). The ocular vestibular evoked

myogenic potential (oVEMP) tests predominantly utricular function,

and the cervical vestibular evoked myogenic potential (cVEMP) tests

predominantly saccular function (Curthoys, 2010, 2012).

Vestibular evoked myogenic potentials (VEMPs) are small poten-

tials in response to sound and vibration stimulation recorded by sur-

face electrodes on the skin above activated muscles. Physiological

evidence shows that air-conducted sound and bone-conducted vibra-

tion activates otolithic receptors and afferent neurons and results in:

A short latency inhibitory potential (the cVEMP p13-n23) 1.

recorded over the ipsilateral tensed sternocleidomastoid muscles

predominantly due to saccular input, and

A short latency excitatory potential (the oVEMP n10) recorded 2.

over inferior oblique eye muscles beneath the contralateral eye

as the patient looks upward, predominantly due to utricular input.

The oVEMP is a crossed , ascending, excitatory, utriculo-ocular

response. The cVEMP p13-n23 is an uncrossed , descending,

inhibitory, sacculo-collic response.

There is now a wealth of physiological and clinical evidence support-

ing the use of these VEMPs as indicators of the state of peripheral

utricular and saccular function (see Curthoys, 2012 for a review).

Design and Methods

To test saccular function, the cVEMP p13-n23 was measured to

repeated short-tone bursts of 500-Hz bone conducted vibration

(BCV) each lasting 7 milliseconds, at a rate of 4/s, for 50 pre-

sentations. To test utricular function the oVEMP n10 to the same

stimuli was measured. The stimuli were delivered by a Bruel and

Clinical note

Vestibular function after vestibular neuritis

L. Manzari * , A.M. Burgess † , H.G. MacDougall † & I.S. Curthoys †

* MSA ENT Academy Center, Cassino (FR), Italy, and † Vestibular Research Laboratory, School of Psychology, The University of Sydney, NSW, Australia

Abstract Objective: To measure horizontal semicircular canal function over days, weeks, and months after an acute attack of vestibular neuritis. Design: The video head impulse test (vHIT)

was used to measure the eye movement response to small unpredictable passive head turns at intervals after the attack. Study sample: Two patients diagnosed with acute right unilateral

vestibular neuritis. Results: There was full restoration of horizontal canal function in one patient (A) as shown by the return of the slow phase eye velocity response to unpredict-

able head turns, while in the other patient (B) there was little or no recovery of horizontal canal function. Instead this second patient generated covert saccades during head turns.

Conclusion: Despite the objective evidence of their very different recovery patterns, both patients reported, at the fi nal test, being happy and feeling well recovered, even though in one

of the patients there was clear absence of horizontal canal function. The results indicate covert saccades seem a successful way of compensating for loss of horizontal canal function

after unilateral vestibular neuritis. Factors other than recovery of the slow phase eye velocity are signifi cant for patient recovery.

Key Words: Vestibular; labyrinth; vestibular neuritis; head impulse test; vestibular compensation; saccades

Correspondence: Ian S. Curthoys, Vestibular Research Laboratory, School of Psychology, University of Sydney, Sydney. NSW 2006, Australia. E-mail: [email protected].

edu.au

(Received 19 January 2013; accepted 22 May 2013)

ISSN 1499-2027 print/ISSN 1708-8186 online © 2013 British Society of Audiology, International Society of Audiology, and Nordic Audiological Society

DOI: 10.3109/14992027.2013.809485

International Journal of Audiology 2013; Early Online: 1–6

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Kjaer minishaker 4810 to the midline of the forehead at the hairline

(a location called Fz). In both cases the stimuli were generated and

the responses averaged using a Chartr EP 200 averager (Otometrics,

Denmark).

The vHIT system consists of a pair of lightweight, tightly-fi tting

goggles on which is mounted a very small, light, fast, fi re-wire cam-

era and a half silvered mirror which refl ects the image of the patient ’ s

eye into the camera. A small sensor on the goggles measures head

movement. The whole goggle system is lightweight (about 60 g) and

must be secured tightly to the head to minimize slippage, because

any slippage of the goggles relative to the eye will be registered as

a movement of the eye and so generate artifactual data. The eye

movement is recorded at 250 Hz. The stimuli are brief, passive,

unpredictable, horizontal head turns to the left or right through an

angle of about 10 – 20 ° in 0.5 s, delivered by the clinician while the

patient is asked to keep fi xating a target spot on the wall. Head turns

towards the affected ear cause a reduced slow phase compensatory

eye velocity response with the consequence that the eyes are taken,

with the head, off target and a saccade is necessary to regain fi xa-

tion on the target spot as per instructions. These saccades may occur

after the end of the head turn when head velocity has returned to

zero (overt saccades), or actually during the head turn itself when

the head velocity is greater than zero (and such saccades are called

covert saccades because they are almost impossible for the clinician

to detect by visual inspection) (Weber et al, 2008, 2009).

vHIT provides two indicators of semicircular canal functional

state: (1) the VOR gain which is the ratio of slow phase compensa-

tory eye velocity to head velocity, and (2) the saccade pattern —

whether saccades occur during the head movement (covert saccades)

or after it (overt saccades). By using vHIT at intervals after the acute

attack, the clinician can follow the dynamic function of the horizon-

tal semicircular canal during vestibular neuritis or labyrinthitis, and

determine whether the dynamic function of the canal does or does

not recover.

Vestibular neuritis patients Two patients, one man (identifi ed as A) and one woman (B), both aged

36, were referred for the fi rst time to our tertiary referral neurotological

center (MSA ENT Center, Cassino, Italy) respectively on the 23rd Jan-

uary 2012 and 10th June 2011. On the basis of the results of a battery of

objective tests of otolithic and semicircular canal function (see below)

both patients were diagnosed as having right-sided vestibular neuritis.

They both came to the clinic with acute vestibular syndrome (long

lasting rotatory vertigo, nausea, pallor, and vomiting). The patients did

not remember closed cranial trauma, and the anamnesis showed no

notable systemic disease such as diabetes or cardiovascular problems.

There were no cochlear symptoms, such as tinnitus or fullness or acute

hearing loss either before, during, or after the onset of the acute vertigo,

so it was presumed that they were not patients with M é ni è re ’ s disease

or involvement of the cochlea or labyrinthitis.

At the time of the fi rst visit all symptoms reported by the patients

were evaluated with a standardized set of tests including bed-side

examination (Table 1). Otoscopy fi ndings were normal. Both patients

were submitted to instrumental audio vestibular tests: audiometry,

tympanometry with stapedial refl exes, and auditory brainstem response

which were all normal for the patient ’ s age. Vestibular sense organ

testing showed marked losses. Firstly, Fitzgerald – Hallpike caloric

testing showed hyporesponsiveness of the right horizontal canal of

the affected ear. The pattern of horizontal, torsional, and vertical eye

movement components were measured with three-dimensional infrared

video-oculography (50-Hz sampling; Torsio VNG Ulmer; Synapsys,

Marseille, France) during spontaneous nystagmus; during head shaking

nystagmus; during the Dix-Hallpike manoeuvre, and during the head

roll manoeuvre for positional and positioning nystagmus. At the time

of the acute attack, both patients showed spontaneous nystagmus with

horizontal and torsional components; the horizontal quick phase being

directed toward the left (healthy) side. There was no evidence of BPPV

or positional nystagmus.

Both patients were referred to a tertiary radiology center for a

magnetic resonance imaging scan (MRI) of the posterior cranial

fossa using paramagnetic contrast enhancement. In both patients

radiologic evaluation revealed normal and symmetrical eighth

cranial nerves and normal signal from midbrain and posterior

cranial fossa.

The patients received oral steroids in the fi rst period of the disease,

seven days at least. It was recommended to resume daily activities as

soon as possible. A specifi c vestibular rehabilitation training was not

recommended. Over the next months the same patients were tested

on repeated occasions even when the acute subjective symptoms had

completely disappeared.

Abbreviations

BCV Bone-conducted vibration

cVEMP Cervical vestibular evoked myogenic potential

oVEMP Ocular vestibular evoked myogenic potential

SCM Sternocleidomastoid muscle

vHIT Video head impulse test

VOR Vestibulo-ocular refl ex

Table 1. Summary of clinical data of patients.

Neurotological evaluation

Audiometry

PTA scores

Patient Affected ear Gender Age, years

Spontaneous nystagmus

Head-shaking nystagmus

Canal paresis

Vibration-induced nystagmus MRI Right ear Left ear

A R M 36 Ny L/H Ny L/H 56% Ny L/H Normal 10.00 dB 10.00 dB

B R F 37 Ny L/H Ny L/H 67% Ny L/H Normal 10.00 dB 10.00 dB

L: left; R: right; F: female; M: male; dB: decibel; Ny: nystagmus; L/H: nystagmus with the horizontal quick-phase component to the left. Spontaneous

nystagmus: nystagmus that appears while the patient is in darkness without a fi xation light. Head-shaking nystagmus: nystagmus that appears after vigorous

horizontal headshaking for about 15 seconds at a frequency of about 2 Hz. Vibration-induced Nystagmus: nystagmus that appears after bone-conducted

vibration is applied to the mastoid bone while the patient is in darkness. MRI: magnetic resonance imaging scan. PTA scores (pure-tone audiometry average

scores): 500, 1000, 2000, 3000 Hz (considered frequencies).

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Vestibular function after vestibular neuritis 3

p13n23n10

R eye

L eye

R eye

L eye8 May 2012

R eye

L eye23 Jan 2012

R eye

L eye15 June 2012

10 ms

R SCM

L SCM

R SCM

L SCM8 May 2012

R SCM

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23 Jan 2012

R SCM

L SCM

15 June 2012

10 ms

–+

10 μV

10 June 2011 10 June 2011

–+

100 μV

oVEMPs cVEMPs

Patient A

Patient B

Figure 1. Records of oVEMP (left column) and cVEMP (right

column) responses for patients A (upper panel) and B (lower panel),

tested by 500-Hz BCV at Fz at the acute phase (top row) and after

recovery (bottom row). The approximate epoch of the oVEMP n10

potentials are marked by a yellow bar, and similarly the epoch of

the cVEMP p13 and n23 are marked by a blue bar. The p13 and

n23 responses are indicated by short vertical tick marks. In the fi rst

session of 23 Jan 2012, patient A shows reduced otolith function in

the right ear (both reduced utricular function shown by oVEMP n10

beneath the left eye, and reduced saccular function shown by cVEMP

p13-n23 over the right SCM). By the second session of 15 June

2012, the saccular function in the right ear had recovered, as shown

by a detectable p13-n23 response in the right SCM, approximately

symmetrical with the p13-n23 response in the left SCM. In the same

ear, utricular function as shown by n10 in the left eye was still small.

In the fi rst session of 10 June 2011, patient B shows absent saccular

and utricular function in the right ear, similar to the fi rst session for

patient A. By the second session of 8 May 2012 neither utricular nor

saccular function in the right ear had recovered in this patient, as

shown by absent n10 responses in the left eye and absent p13-n23

responses in the right SCM.

Results

In both patients 500-Hz BCV at Fz caused asymmetrical cVEMP

responses with reduced or absent p13-n23 potential over the ipsilat-

eral (right) contracted sternocleidomastoid (SCM) muscle, but with

potentials in the normal range for the Cassino clinic (130 � 65 μ V

(SD) n � 54; (Manzari et al, 2012) over the contralateral SCM, and

so it was concluded that the saccular afferents in the right inferior

vestibular nerve were affected in both patients (Figure 1).

The objective test of utricular function — the n10 component of

the ocular vestibular evoked myogenic potential (the oVEMP n10)

to the same 500-Hz Fz BCV stimulus — showed absent n10 potentials

beneath the left eye (the contralesional eye), in both patients with

n10s beneath the right eye being in the normal range for the Cassino

clinic (5.7 � 2.6 μ V (SD), n � 54; Manzari et al, 2012) — resulting

in an oVEMP n10 asymmetry ratio (AR) of 100% for both patients

(Figure 1), indicating that the utricular afferents in the right superior

vestibular nerve were affected in both patients.

This result indicates that the utricular afferents in the right superior

vestibular nerve were affected since the oVEMP is a crossed response

(Iwasaki et al, 2007). Testing horizontal canal function (described

below) showed reduced horizontal canal function for rightwards head

rotations. The combination of the reduced right horizontal canal func-

tion, the reduced right utricular function, and the reduced right saccular

function, in the absence of any cochlear symptoms, led to the diagnosis

of right vestibular neuritis for both patients.

At the time of the fi rst visit dynamic horizontal canal function was

tested by vHIT and the results of that test are shown in the uppermost

panels of Figures 2 and 3. For both patients vHIT showed a clearly

impaired right horizontal VOR gain when their head was abruptly,

unpredictably, passively turned to the right, whereas similar head turns

to the left (the healthy side) had normal VOR gain. At testing on this

fi rst occasion during the ipsilesional rightward passive head turns,

patients also showed a series of overt saccades and some covert sacca-

des and these saccades also confi rm inadequate right horizontal canal

VOR dynamic function (Weber et al, 2008). After the fi rst evaluation

both patients were regularly retested at the Cassino clinic (at the dates

shown on the panels in the fi gures) to evaluate the time course of the

recovery of the dynamic VOR from the acute neuritis. Both patients

were evaluated until they themselves declared they were ‘ cured ’ and

that subjectively their balance felt normal. For Patient A the time

to reach this stage was short — only about fi ve months, whereas for

Patient B the time was much longer (about 11 months) before the

patient declared herself fully recovered. In contrast to these subjective

reports of good recovery, the objective measures of semicircular canal

function by vHIT showed two totally different pictures of recovery of

dynamic semicircular canal function. In the fi rst case (A) there was

complete recovery – full restoration of horizontal canal function with

normal slow phase eye velocity and VOR gain close to 1.0 — whereas

in the second case (B) there was a complete absence of any recovery

of horizontal canal function.

Discussion

What factor(s) could explain this very similar subjective evaluation,

in light of the very different objective evidence? The results suggest

that saccades may play a major role in the recovery. In response

to the passive, unpredictable head rotation with high acceleration,

patient B showed a pattern of saccades evolving from a combina-

tion of overt and covert saccades at the acute stage (10 June 2011)

to covert saccades only at testing 11 months later (8 May 2012;

Figure 3). This patient, like many others, generated very small covert

saccades during the passive high acceleration head movements; and

these may hold the key to understanding compensation of vestibulo-

ocular symptoms in some patients.

Two distinct neural circuits underlie the generation of horizontal

eye movements: one for slow phase eye movements and the other for

generating quick phases and saccades (for a review, see Curthoys,

2002). There are interconnections between these circuits but each

can be considered separately. Slow phase eye velocity in response to

head turns is generated by the direct three neuron pathway: receptor/

vestibular nucleus/abducens motoneurons/eye muscles.

Quick phases and saccades are generated by a separate neural

circuit involving a network of burst neurons and pause neurons in

the brainstem close to abducens nucleus. The quick phase circuit can

be triggered by vestibular input (and so generate the quick phase of

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GAIN

Left Lateral Right Lateral




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n 18

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Left: mean 1.19 SD 0.03 n 18

2012/01/23

2012/02/27

2012/03/28

Time (ms) Time (ms)

Time (ms) Time (ms)

Time (ms) Time (ms)

Time (ms) Time (ms)

deg/ s deg/ s

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6000 100 200 300 400 500 6000 100 200 300 400 500

6000 100 200 300 400 500 6000 100 200 300 400 500

6000 100 200 300 400 500 6000 100 200 300 400 500

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EyeHead

Figure 2. Objective measures of horizontal semicircular canal function at four testing occasions for patient A with acute unilateral (right)

vestibular neuritis: occasion 1 (23 Jan 2012) and at succeeding times thereafter. Each panel shows superimposed time series of head velocity

(blue) and the corresponding eye velocity (orange) for the tests of horizontal canal dynamic function using vHIT. The signs of head velocity

for leftward impulses and of eye velocity for rightward impulses have been inverted to allow for easier comparison. Each panel also shows

the horizontal VOR gains versus peak head velocity for the head-impulse data shown in that panel. Closed circles: leftward impulses; open

circles: rightward impulses. The mean and 95% confi dence intervals for gains in leftward and rightward impulses are shown at the right of

each Gain plot. Normal horizontal VOR gains are about 0.7 – 1.0 (MacDougall et al, 2009). For rotations to the affected side, eye velocity

is substantially less than the corresponding head velocity during the head turn so the VOR is signifi cantly less than for head turns to the

healthy side. There is a shower of saccades at the end of the head turn (black arrow). On each succeeding testing occasion, for head turns

to the affected side the slow phase eye velocity improves and the corrective saccades reduce in frequency and size until at the fi nal test,

VOR gain is 1.03 (in the normal range) and there are virtually no corrective saccades and it is concluded that horizontal semicircular canal

function has been fully restored after the neuritis.

vestibular nystagmus during prolonged canal activation) but can also

be triggered by other inputs, e.g. descending axons from the superior

colliculus causing voluntary saccades. There is evidence that input

from neck afferents can also trigger this quick phase neural circuit

(Barmack et al, 1989). In healthy subjects these two neural circuits

interact so that prolonged semicircular canal input from a maintained

acceleration results in slow phase compensatory eye movements, inter-

rupted by the quick return phases of vestibular nystagmus. In both of

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Vestibular function after vestibular neuritis 5

3

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0.130.56

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18

Figure 3. The corresponding records for patient B who was also diagnosed with an acute (right) vestibular neuritis on occasion 1 (10

June 2011) and then tested at succeeding times thereafter. In this patient also the eye velocity is substantially less than head velocity on

occasion 1, but in contrast to patient A, the eye velocity response during the head impulse does not change over the succeeding tests and

at the fi nal test on 8 May 2012 the VOR gain remained at 0.46, about the same (slightly smaller) than the original VOR gain of 0.56. In

the later tests there is a shift of the saccadic pattern so that the saccades tend to be much more clustered and to be initiated during the head

turn (i.e. before the head velocity has returned to zero) and so are classifi ed as covert saccades. This is strong evidence that the slow phase

eye velocity to high acceleration head impulses does not change over time, and so we conclude that the neuritis has caused long term and

probably permanent damage. There is evidence of changes in the pattern of saccades. At the last test this patient reported good balance

function and considered that they had recovered.

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the patients here the horizontal slow phase mechanism was disabled at

the acute stage (as shown by the very low gain VOR) most probably

because of the acute damage to the superior vestibular nerve. However

the quick phase mechanism was unaffected as shown by the saccades

at each head turn. Over time in Patient A the slow phase mechanism

returned (the VOR gain increased) and as it did so the quick phases

become progressively smaller. In Patient B there is no recovery of the

slow phase at all, so even after many months it is just the saccades

which are present in response to the head turn. However the temporal

location of these saccades has moved so they occur during the head

movement and so are termed covert saccades.

Why are covert saccades so potentially valuable? Firstly because

they achieve the goal of keeping fi xation on the target and they do

so by effectively bypassing the neural circuits generating the slow

phase eye velocity (which are non-functional because of the reduced

or absent vestibular input) and instead use the independent neural

circuits for saccade generation. Secondly because visual perception

is attenuated — effectively blanked — by a process called saccadic

suppression during and after the saccade (Matin, 1974).

The major question remains ‘ what triggers covert saccades? ’ Why

do we suggest that these covert saccades may be produced by neck

afferent input (Macdougall & Curthoys, 2012)? Because one patient

with known surgical bilateral complete vestibular loss produced

covert saccades with exactly correct direction for 300 successive head

rotations (Weber et al, 2009). This is simply too high a success rate

to attribute it to anticipation or prediction. We have suggested the

covert saccades could be produced by neck afferents being triggered

at the very start of the head turn (Macdougall & Curthoys, 2012).

We stress that this is NOT the cervico-ocular refl ex which acts to

generate slow compensatory eye movements in response to neck input

(Yakushin et al, 2011) but a saccade which is triggered by activation

of neck receptors at the start of the head turn. Given their total loss

of vestibular input and the improbability of generating 300 successive

saccades in the correct direction by means of anticipation or prediction

we consider neck afferent input as a likely cause of covert saccades.

It is of particular interest that in both patients the measures of

otolithic function show unilateral loss of utricular function at the

acute stage and no recovery. Neither of these patients was troubled

by the unilaterally absent utricular input. Just as many patients with

total loss of all vestibular function from one ear may recover com-

pletely and resume normal life styles and be perfectly happy, so these

tests are showing that patients with isolated loss of individual ves-

tibular sense organs can also recover and resume normal lifestyles.

It may be thought that caloric tests delivered to these two patients

at comparable intervals would have given a similar result. In our

experience patients must be persuaded to have one caloric test and

are very reluctant to commit to successive calorics. Furthermore the

caloric test measures horizontal canal function and only the slow

phase eye velocity, and could not have shown the shift in response

towards covert saccades which we think to be of special signifi cance

for the successful compensation of patient B in the face of absent

horizontal canal function.

Conclusions

Tracking vestibular function from patients presented with acute

vestibular neuritis, over days, weeks, and months after the acute

attack, using the vHIT test and other new tests of vestibular

function, provides very useful information about their vestibular

compensation, and highlights the apparent value of covert saccades

in vestibular compensation.

Acknowledgements

We are grateful for the support of NH & MRC of Australia (1046826)

and of the Garnett Passe and Rodney Williams Memorial Foundation.

Ian Curthoys is funded by project grants from the National Health

and Medical Research Council of Australia and the Garnett Passe and

Rodney Williams Memorial Foundation. Ann Burgess and Hamish G.

MacDougall are funded by a project grant from the National Health

and Medical Research Council of Australia and the Garnett Passe and

Rodney Williams Memorial Foundation, respectively.

Declaration of interest : Hamish G. MacDougall and Ian Curthoys

are unpaid consultants to GN Otometrics, Taastrup, Denmark. The

authors have no other funding, fi nancial relationships, or confl icts

of interest to disclose.

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Vestibular function after vestibular neuritis