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figure 6–5. Static compensation following a right peripheral vestibular lesion. See the text for
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the description of each step. Solid arrows identify the onset of head acceleration. continues
114
6. CLINICAL NEUROPHYSIOLOGY OF VESTIBULAR COMPENSATION 115
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figure 6–5. continued Hollow arrows identify the onset of the lesion. θ, θ′, and θ″ represent slow-
phase nystagmus intensities. The density of the dots represents the level of neural activity within
the vestibular nuclei. LSCC, lateral semicircular canal; ASCC, anterior semicircular canal; PSCC,
posterior semicircular canal.
The vestibular test findings at this stage of the
lesion should include significant right unilateral caloric
weakness and strong left-beating spontaneous nystagmus without fixation. The nystagmus is usually strong
enough that it is not fully suppressed and can be seen
with fixation also. This nystagmus is likely to follow
Alexander’s law (Hegemann, Straumann, & Bockisch,
2007), which means it is stronger with the gaze toward
the fast phases (left gaze in this case). The head impulse
test should show decreased VOR gain and presence
of consistent catch-up saccades for rightward head
impulses (Weber et al., 2008). The same findings are
likely to be present for leftward head impulses as well,
but they are not as prominent as those for rightward
head impulses. Rotation chair testing should show
decreased gain and increased phase at very low frequencies (Baloh, Jacobson, Beykirch, & Honrubia,
1989). Also, the asymmetry should be significant for
all frequencies, reflecting the presence of spontaneous nystagmus (Magnusson, Brantberg, Pyykkö, &
Schalén, 1989). However, the rotation chair findings
at the early stages of lesion should be interpreted
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cautiously because the same type of nonlinearity that
occurs with very fast head movements (Figure 6–2E)
can also happen in the rotation testing at the onset of
the lesion. As a result, eye velocities resemble a rectified sinusoid instead of a full sinusoid. Most of the
commercial rotation chair systems use a curve-fitting
technique to estimate the gain, phase, and asymmetry
parameters of the VOR eye movements. However, the
results at the early stages of lesion may be contaminated because the VOR eye velocities resemble a half
sinusoid instead of a full sinusoid. In fact, what is
assumed to be a reflection of vestibular compensation
in rotation testing may simply be due to the way the
test parameters are calculated (Rubin, 1984). Finally,
the responses in VEMP testing are assumed to originate from the otolith organs. Therefore, the findings
will depend on whether or not the damage involves the
vestibular nerve. Regardless, VEMP testing will not be
discussed here further because the findings are lesion
dependent similar to the caloric test and are unlikely to
change with compensation.
Cerebellar Clamping Stage
The neural asymmetry caused by peripheral vestibular
lesion (Figure 6–5B) is similar to the asymmetry caused
by head movement (Figure 6–5A), with one notable exception. The neural asymmetries between the
right and left neural firings that are induced by head
movements are temporary and do not persist for an
extended period of time. On the other hand, the asymmetries caused by a lesion are persistent. Therefore,
any prolonged and constant asymmetry is interpreted
as a sign of a malfunction within the VOR pathways
and results in the activation of the vestibular compensation process.
The first step in the vestibular compensation process is cerebellar clamping, in which the neural activity
from the intact side is reduced at the vestibular nuclei
level before it is relayed to the motor centers. This step
begins within hours if not minutes after the onset of
the lesion, and its effect is to reduce the asymmetry
and ease the patient’s symptoms. This is essentially
the same role that vestibular suppressants play when
they are prescribed during the early stages of a lesion
when the symptoms are likely to be severe. It should
be noted that although cerebellar clamping reduces
the static symptoms, it may have a short-term adverse
effect on the dynamic symptoms. The reason is that cerebellar clamping reduces the neural activity from the
intact side, which mimics bilateral impairment of the
VOR function.
The evidence for the cerebellar clamping stage
comes from the studies by Vibert and his colleagues
(Vibert et al., 1999). They studied guinea pigs that had
undergone a unilateral labyrinthectomy. If a secondary
vestibular nerve section was performed on the opposite side within the first three days after the labyrinthectomy, the impact was minimal. This suggests that
the neural activities were already reduced on the initially intact side due to cerebellar clamping and that
is why the effects of the subsequent deafferentation
were marginal.
The vestibular test findings at the cerebellar
clamping stage include significant spontaneous nystagmus without fixation. However, the intensity is
reduced compared with the intensity at the onset of
the lesion. This reflects the decrease in neural asymmetry and accompanies improvement in the patient’s
symptoms. The caloric test should continue to show a
significant right weakness, but at times the responses
can be bilaterally weak because of the strong clamping effect. The rotation test results should be similar to
those at the onset of the lesion, although the gain may
be abnormally low in low frequencies because of the
clamping effect. The rotation asymmetry should also
decrease because of the reduction of the spontaneous
nystagmus intensity. Similarly, the head impulse test
should be similar to those at the onset of the lesion.
Appearance of Neural Activity at the
Vestibular Nuclei of the Damaged Side
Shortly after the cerebellar clamping stage, the tonic
neural activity of the secondary vestibular neurons
begins to increase at the vestibular nuclei of the damaged side. Assuming that the peripheral vestibular
lesion is permanent, this neural activity cannot be originating from the primary vestibular neurons. Instead,
the most likely source for the increased neural activity
is the vestibular nuclei of the intact side that communicates with the other side through the commissural
fibers (Olabi, Bergquist, & Dutia, 2009). Simultaneous
with the increase of neural activity on the damaged
side, the clamping effect on the intact side is reduced
(Beraneck et al., 2004). The neural asymmetry is still
present but it is not as severe compared with the onset
of the lesion. Furthermore, the reduction in clamping
allows for the neural activity on the intact side to be
more representative of head movements. In short, the
patient still suffers from both static and dynamic symptoms but the severity of both is reduced.
The evidence for this stage of the compensation
also comes from the same series of studies by Vibert
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et al. (1999). They demonstrated that if the secondary
vestibular nerve section was performed more than
three days after the first labyrinthectomy, the guinea
pigs again experienced increase in the symptoms and
showed spontaneous nystagmus, but this time the nystagmus was in the opposite direction. This suggests an
increase in the neural activity of the vestibular nuclei
on the damaged side so that the subsequent nerve section created a secondary asymmetry in the opposite
direction. As the animals were labyrinthectomized, the
increase in the neural activity must have been generated centrally.
Again, the intensity of spontaneous nystagmus
continues to decline in the vestibular tests even though
the caloric weakness persists. In the rotation chair test,
the phase and gain parameters should improve, especially for low frequencies, and the asymmetry parameter should decrease as the spontaneous nystagmus
intensity declines (Allum & Honegger, 2013). Finally,
the head impulse test findings remain essentially
unchanged, with one possible exception. It is suggested
that the latency of catch-up saccades decreases with
compensation so that they occur during head impulses
(MacDougall et al., 2009). These catch-up saccades are
called covert saccades, as opposed to the overt saccades
that occur after the head impulse. Covert saccades are
assumed to be more efficient because they place the
eyes on the target and stabilize the vision more quickly
(MacDougall & Curthoys, 2012). Support for this viewpoint is emerging as the covert saccades have been
associated with functional improvement and better
visual acuity during head movements (Hermann et al.,
2018; Wettstein, Weber, Bockisch, & Hegemann, 2016).
Static Compensation
The process of increase in the neural activity of the
damaged side continues until it returns to its pre-lesion
level. At the same time, cerebellar clamping on the intact
side continues to decrease until it is completely lifted.
At this point, the patient has achieved static compensation because the neural asymmetry has disappeared
and the patient is no longer symptomatic as long as the
head remains stationary (Halmagyi et
Vestibular test findings continue the trend from
the previous step. Spontaneous nystagmus should disappear completely or its intensity should decrease to
an insignificant level. However, the caloric weakness
should persist as before. For rotation testing, the phase
parameter should stabilize at a level higher than its prelesion level and the gain parameter should stabilize at a
level lower than its pre-lesion level (Baloh et al., 1989).
al., 2010).
Similarly, the asymmetry parameter should drop to an
insignificant level along with the intensity of spontaneous nystagmus. The head impulse test findings should
be similar to those in the previous step but perhaps
exhibiting even more covert saccades than before.
Static compensation represents a significant milestone in the recovery from a peripheral vestibular
lesion. Therefore, it is worthwhile to better understand
the process:
1. In animals, if the mobility and visual stimulation
are restricted, static compensation is delayed and
recovery may never be complete (Zee, 2000). In
humans, static compensation seems to occur spontaneously as long as the compensation mechanisms
can be engaged at a critical time after the lesion
(Lacour et al., 2016). Furthermore, head–eye coordination exercises immediately after the lesion or
even before may expedite the recovery (Tjernstrom
et al., 2018).
2. Theoretically, static compensation requires com-
plete resolution of the neural asymmetry and disappearance of spontaneous nystagmus. In practice,
a small degree of asymmetry may persist indefinitely because the process of compensation continues until the asymmetry reaches a threshold that
it is no longer perceived by the patient as head
motion. The manifestation of this asymmetry is
the continued presence of spontaneous nystagmus
with the SPV that is below a certain threshold (typically 4 deg/sec).
3. Static compensation takes place regardless of
whether the lesion occurs suddenly or gradually.
For example, patients with a vestibular schwannoma usually do not experience many of the symptoms that are associated with the sudden loss of
peripheral vestibular function (Parietti-Winkler,
Gauchard, Simon, & Perrin, 2011). The reason is
that static compensation takes place incrementally
and without obvious signs as the tumor grows
gradually and impinges on the vestibular nerve
(Uehara et al., 2011).
4. Static compensation is most effective when the
lesion is stable. Patients with fluctuating lesions
such as Meniere’s disease may not compensate as
well as those with non-fluctuating lesions, especially if the attacks are frequent (Lacour et al.,
2009). In fact, patients with fluctuating lesions may
present an interesting pattern of response during
the compensation process. After damage to the hair
cells or nerve fibers, the compensation process is
expected to proceed with the cerebellar clamping
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stage regardless of whether the lesion is stable or
fluctuating (Figure 6–6A). However, if the function returns to the damaged labyrinth during the
clamping stage, such as after healing of the ruptured membrane in Meniere’s disease, suddenly
the asymmetry will be reversed (Figure 6–6B). The
patient must now undergo another phase of compensation to reverse the effect of cerebellar clamping and restore neural symmetry. In effect, the
compensation process extends the length of time
that the patient suffers from symptoms. That is
why one of the management options for Meniere’s
disease is to destroy the affected labyrinth and to
make the damage permanent. If the attacks of fluctuating lesions are not frequent, the ineffectiveness
of the compensation process may not have a longterm effect. However, in patients who suffer from
frequent attacks, the compensation mechanisms
may cease to respond because of their ineffectiveness and because they lengthen the symptoms.
The reversal of neural asymmetry in Figure 6–6
results in the reversal of spontaneous nystagmus
direction (McClure, Copp, & Lycett, 1981). This type of
nystagmus that beats toward the side of lesion is sometimes seen with fluctuating lesions. It is called recovery
nystagmus because it is due to the recovery of vestibular function on the affected side. Significant recovery
nystagmus is short-lived because the neural activity on
the clamped side is elevated rapidly until the asym-
metry is resolved. However, residual mild spontaneous
nystagmus beating toward the side of lesion may persist for the same reason that was discussed above. That
is, once the asymmetry decreases below a level that is
no longer perceived as head motion, the change in neural activities stops. This discussion also provides a clear
example that the direction of spontaneous nystagmus
does not always identify the side of lesion.
Dynamic Compensation
After static compensation, the patient no longer suffers
symptoms when the head is at rest but as soon as the
head moves, the patient may experience blurry vision
and loss of visual acuity. Figure 6–7 shows the underlying reason. If the head moves exactly the same way that
it did prior to the onset of the lesion (see Figure 6–5A),
the resulting neural asymmetry after static compensation is only half as large as that before the onset of the
lesion. Therefore, the head velocity is interpreted to
be only half as large as it actually is and the eyes are
moved only half as fast as they should (Figure 6–7A).
The difference between the head and eye velocities
causes retinal slip. When the retinal slip is not close to
zero, images do not stay stationary on the retina and
the patient experiences blurry vision (Fadaee & Migliaccio, 2016).
One possible method for improving VOR performance and minimizing retinal slip is to increase the
neural activity of the secondary vestibular neurons
A B
figure 6–6. Mechanism of recovery nystagmus in fluctuating lesions. Hollow arrows identify the
onset of restoration of neural activity after the lesion. Abbreviations are the same as in Figure 6–5.
6. CLINICAL NEUROPHYSIOLOGY OF VESTIBULAR COMPENSATION 119
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figure 6–7. A. Before dynamic compensation. B. After dynamic compensation. See the text for
the description of the process. Abbreviations are the same as in Figure 6–5.
from the pre-lesion level for the same head velocities.
There is no direct evidence that such an increase in the
VOR gain occurs but there are some compelling correlates. Recall the function of the VSM that behaves
as a storage tank with a small outlet. Increasing the
VOR gain can be accomplished by increasing the
outflow of the neural activity from the VSM (Figure
6–7B). Although this increases the VOR gain, it also
degrades the performance of the VOR for low frequencies, which is the main function of the VSM (Laurens,
Valko, & Straumann, 2011). The decline of VOR function in low frequencies is in fact evident in the rotation
chair results in which the phase parameter increases
and the gain parameter decreases in low frequencies
(Baloh et al., 1989).
Understanding the cause of dynamic symptoms
provides a clue as to why the compensation process
for these symptoms is far more challenging than static
compensation. As described before, the internal database that relates different patterns of neural activity to
various types of head movements is developed over
several years. After a unilateral vestibular lesion, the
database no longer provides an accurate measure of the
head movements and must be replaced. In addition to
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the length of time that seems to be required for reestablishing the relationship between neural firing patterns
and head movements, one should also recall that the
original database is developed during age periods in
which the sensory and motor mechanisms are at their
peak performance. Later in life when the incidence of
vestibular abnormalities is higher, patients often have
more difficulty with dynamic compensation because
of other confounding issues common to aging, such as
decline of acuity in the sensory and motor pathways.
This may also explain why some patients who successfully achieve dynamic compensation are susceptible to
episodes of decompensation (Katsarkas & Segal, 1988).
That is, a seemingly unrelated event may trigger a bout
of symptoms because the compensation mechanisms
seem to “forget” the new pattern of neural behavior
and revert to the original database.
If our understanding of the dynamic compensation process turns out to be accurate, the best method to
facilitate it is for the patient to be exposed to a variety
of head movements. The difference between the head
and eye velocities serves as an error signal so that the
retinal slip can be reduced gradually. However, some
have questioned the neural basis of dynamic compensation. Instead, they propose that dynamic compensation is achieved by other oculomotor mechanisms, such
as saccades, substituting for the VOR function (Curthoys, 2000). Although there is merit to the concept
of substitution for vestibular compensation, it fails to
explain some observations such as the change of gain
and phase parameters in the rotation test. Perhaps a
combination of neural changes and substitution is
a better model for describing the process of dynamic
compensation. Interestingly, regardless of whether the
aim is adaptation or substitution, the same type of exercises can be used to promote dynamic compensation.
More on this topic will follow.
Compensation After Vertical
Canal and Otolith Lesions
After a unilateral loss of vestibular function, most
patients exhibit imbalance and other postural control
deficits. These deficits are likely to be related to the
loss function in the vertical canals or the otolith organs.
However, postural control deficits seem to resolve more
quickly than oculomotor deficits. Perhaps incorporating the remaining function from the intact labyrinth
into the postural control mechanisms is more efficient
(Horak, 2010).
The oculomotor effects of vertical canal lesions are
similar to those described for the lateral canal lesions
(Aw et al., 1995). The only difference is that the spontaneous nystagmus has both vertical and torsional com-
ponents. Similarly, the static compensation process is
also the same as that described here. In fact, static compensation for vertical and torsional nystagmus seems
to require less time than that for the resolution of horizontal nystagmus. Although not much is known about
the dynamic compensation process for vertical canal
lesions, it is logical to expect that it is similar to the
process described above as long as the head–eye coordination exercises are performed in the plane of vertical canals (Schubert, Herdman, & Tusa, 2002).
As noted earlier, very little is known about the
effects of otolith lesions other than the fact that there
is a tonic torsion of the eyes toward the side of lesion
(Curthoys, 2000). Over time, the degree of torsion is
reduced, indicating some level of compensation similar
to the disappearance of spontaneous nystagmus (Furman, Hsu, Whitney, & Redfern, 2003). However, the
torsion does not resolve completely, which indicates
the necessity of some form of dynamic compensation
(Curthoys et al., 1991). If one accepts that view, then
exercises that stimulate the otoliths such as translational
head movements or eccentric rotation may be needed
for compensation (Akin, Hall, & Murnane, 2013).
The tests that document damage to the otoliths
include cervical and ocular VEMPs and eccentric rotation (Agrawal et al., 2013). In addition, subjective visual
vertical (SVV) testing can document the level of tonic
torsion that changes with the compensation of otolith
lesions. Caution must be taken in interpreting SVV
results because the test is also sensitive to some central
lesions (Klatt et al., 2019).
Compensation After Bilateral
Vestibular
Complete bilateral loss of peripheral vestibular function usually does not result in static symptoms because
of the absence of neural asymmetries. At the same time,
dynamic compensation based on the changes of neural behavior similar to those described for unilateral
lesions is not possible because of the complete loss of
vestibular input (McCall & Yates, 2011). Instead, the
compensation process involves substitution of other
sensorimotor mechanisms for the missing vestibular
system. However, compensation is usually incomplete
and sometimes ineffective because of the differences
in the operating frequency ranges of different sensory
mechanisms (Guinand et al., 2012). For example, the
neck receptors can provide information about head
movements but the frequency range is considerably
lower than the vestibular system. Interestingly, individuals with congenital loss of vestibular function
often can function at a level that their impairments
Lesions
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may not be obvious to casual observers. Obviously,
these individuals have developed alternative strategies that do not rely on the vestibular system. Although
it is possible, it is unlikely that most patients with
acquired bilateral vestibular loss can reach that level
of compensation.
The compensation process is more successful if
there is residual vestibular function. A combination of
substitution and reliance on the residual vestibular function can provide a moderate level of functional recovery.
When bilateral loss of function is present but is
more significant on one side, the patient undergoes
the same type of static and dynamic compensation
described for unilateral lesions. However, functional
recovery is not likely to be as successful for the same
reasons stated above.
Compensation After Central
Vestibular
Central abnormalities can cause vertigo and other balance symptoms. Some of these abnormalities, such as
those caused by vascular lesions or head trauma, can
affect peripheral vestibular pathways as well as the
central structures. For example, infarcts of some arteries are known to cause sudden hearing and vestibular
loss. For those lesions, vestibular compensation for the
peripheral component of the abnormality can proceed
as described before. However, if there is a simultaneous or pre-existing damage to the central compensation
mechanisms, then functional recovery may be difficult
or impossible to achieve. Animal studies have identified the cerebellar flocculus as an important site for
vestibular compensation (Aleisa, Zeitouni, & Cullen,
2007). Therefore, damage to this or the surrounding
areas in humans may have a similar adverse effect on
the compensation process.
In general, vestibular compensation is not as successful for central vestibular lesions compared with the
peripheral vestibular lesions (Brown et al., 2006). For
one thing, it is not known what type of activities may
be effective in promoting recovery in these patients.
Also, patients with central lesions constitute a nonhomogeneous group and the outcome may depend on
the type of lesion.
Lesions
CLINICAL TESTS OF
VESTIBULAR COMPENSATION
Clinical tests of compensation are necessary to document changes over time and to assess the effects of
rehabilitation. The SPV of spontaneous nystagmus is
an effective measure of static compensation. However,
assessing dynamic compensation is not as straightforward. Most of the current vestibular tests are site-oflesion tests. That is, the outcome of most vestibular
function tests, such as the caloric test, is the same before
and after dynamic compensation and give very little
information about the state and level of compensation
(Slattery, Sinks, & Goebel, 2011). For dynamic compensation, retinal slip seems to be the most effective
method for documenting the level of compensation.
However, most of the existing vestibular function tests
do not provide a direct measure of retinal slip. One
test that does provide an indirect measure of retinal
slip is the dynamic visual acuity (DVA) test (Mohammad et al., 2011). The bedside test of DVA in which the
patient is asked to read an eye chart with and without head movements is prone to a number of issues.
For example, the patient may attempt to read the chart
when the head comes to a momentary stop before
reversing direction. Computerized DVA tests either
during sinusoidal or impulsive head movements have
become available in recent years and are gaining more
widespread clinical use (Herdman et al., 1998; Sjogren,
Fransson, Karlberg, Magnusson, & Tjernstrom, 2018).
Dynamic posturography is another method for
evaluating dynamic compensation, but postural control
abnormalities after a unilateral vestibular lesion usually resolve very quickly and often do not correspond
to the patient’s dynamic symptoms (Furman, 1994).
Nonetheless, dynamic posturography can provide
an understanding of how patients use different sensory mechanisms to maintain their postural stability.
Effective use of available sensory inputs can improve
balance and may prevent the patient from acquiring
maladaptive strategies.
IMPLICATIONS FOR REHABILITATION
Most of the studies on rehabilitation and exercise
therapy for vestibular lesions have focused on unilateral peripheral lesions. As discussed earlier, static
compensation after a unilateral peripheral vestibular
lesion takes place spontaneously in most patients.
However, physical and exercise therapy can expedite
the recovery. The most effective approach for promoting dynamic compensation appears to be exercises that
are focused on head–eye coordination. These exercises
provide the central compensation mechanisms with
the error signal (retinal slip) that is necessary to either
cause adaption or substitution of the vestibular pathways (Herdman, 2013). These exercises should cover
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different head velocities and different planes of motion.
Furthermore, the exercises should involve visual, proprioceptive, and other sensorimotor mechanisms so
that the vestibular input can be properly integrated
within the balance control system (Lacour & BernardDemanze, 2014).
A review of the literature shows that in fact the
type of exercises described above is a common part
of the rehabilitation protocol for unilateral vestibular
lesions (Whitney & Sparto, 2011). These exercises are
usually referred to as X1 and X2 viewing exercises. For
a detailed discussion, see Chapter 19.
The same type of head–eye coordination exercises
can be used for bilateral vestibular lesions (Telian,
Shepard, Smith-Wheelock, & Hoberg, 1991). Although
the adaptive effects may not be significant, these
exercises can promote substitution of the missing or
reduced vestibular function in these patients (Porciuncula, Johnson, & Glickman, 2012). For example, during X1 viewing exercises, the patient moves his or her
head side to side while fixating on a stationary target.
This type of exercise in patients with bilateral vestibular lesions can promote the use of neck receptors to
control the eye movements. The success rate of exercise therapy in patients with bilateral lesions is not as
high as that of patients with unilateral lesions and often
depends on the residual vestibular function.
The rehabilitation protocols for other types of
lesions are still evolving because of our limited knowledge of the underlying physiology. It is assumed that
general conditioning exercises along with customized
protocols may be beneficial, but so far very few studies
have focused on these patients.
summary
Vestibular compensation is the process by which
patients achieve functional recovery after a vestibular
lesion. The process is most effective for stable unilateral
lesions in which the tonic neural activity is restored at
the vestibular nuclei to achieve static compensation,
and adaptive changes are made to the intact vestibular pathways to achieve dynamic compensation. Compensation for other types of lesions is possible but not
as effective.
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