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G
H
FIGURE 6–22. continued G. Image of plate “F” inverted to show actual plot of eye velocity data with respect to
chair velocity depicting a 45-degree phase-lead (re: chair velocity). H. Enhanced section illustrating the 12.5-second
eye-velocity lead time with respect to chair velocity and the conversion calculation to phase degrees. continues
178
6. Sinusoidal Harmonic Acceleration (SHA) Testing 179
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I
FIGURE 6–22. continued I. Final data plot of eye velocity data depicting a 45° VOR phase lead with respect
to chair velocity data or a 45° VOR phase lag with respect to chair acceleration.
Understanding Phase-Matching
for Low Frequency Stimuli
between detection of acceleration and the production of the ocular motor [velocity] output. This is
certainly true for frequencies that we experience
This exact phase velocity-matching of the VOR
is essential, as it continuously strives to respond
in a pure compensatory manner, always attempting to achieve response unity (gain of 1.0), as well
as striving to produce a precisely timed response
that is not only opposite to head movement, but
occurs with little or no delay in relation to the
velocity of head movement. So, given the inherent or “naturally” occurring 90° delay between
acceleration and velocity, the vestibular system
actually does an incredible job at “matching” eye
velocity to head movement velocity, all because of
this intrinsic 90°
central processing time needed
in daily life (1 to 5 Hz), and is generally true for
those SHA frequencies near or greater than 0.1 Hz
(between 0.08 and 1.28 Hz). For these frequen-
cies, the temporal relationship between the peak
eye velocity response and the peak chair velocity
stimulus does, in fact, approach unity, (although
precisely 180° out of phase from one another as
the slow-phase vestibular response is opposite in
direction to that of chair [head] movement). This
perfect temporal relationship of being precisely
180° out of phase is assigned a phase shift of “0°”
for reasons related to how the phase shift is calcu-
lated. (See VOR phase calculation below.)
180 Rotational Vestibular Assessment
The idea of perfect “phase-matching,” however, is frequency dependent. The exact phase
“velocity-matching” is not the case for the lower
frequencies applied during SHA testing (0.01,
0.02, and to a lesser extent 0.04 Hz). To understand this, we are back to recalling that: (1) the
cupulae are accelerometers and the detection of
low-frequency rotational stimuli is increasingly
poorer below 0.1 Hz, and (2) the subsequent afferent neural response is therefore concomitantly
weak. Because the afferent response is considerably weaker than that produced during higher frequency accelerations, there is concomitantly less
neural information to be “managed” by the central
processors. This central processing is composed of
a sub-network of commissural fibers and cerebellar neurons that comprises a neural feedback loop
that mediates and augments vestibular afferent
input. We have discussed this “neural feedback
loop” before as the neural integrator and subsequent velocity storage mechanism. The neural
integrator and velocity storage mechanisms are
critical and normal processes that provide much
needed augmentation of the weak afferent input
produced by low-frequency stimuli to sufficient
levels, which is required to deliver an appropriate VOR output. Without such intervention, the
low frequency stimulation (rotation in our case)
is simply not sufficient enough to elicit an efficient ocular response and the typical VOR gain of
the system for such low-frequency stimuli would
likely be significantly weak, and, possibly even,
unappreciable (Hirsch, 1986). Consequently, loss
of the velocity storage mechanism due to peripheral or central pathology can lead to a significant
reduction of VOR gain for low frequency stimuli
(to be discussed later in this chapter).
So What Is Happening with “PhaseMatching” for Low Frequency Stimuli?
Is It a Phase-Lag or a Phase Lead?
Actually it is both. It merely depends on whether
you reference the recorded eye velocity response in
relation to chair acceleration or chair velocity. With
such impuissant stimuli delivered during low
frequency SHA testing, the afferent neural drive
from the periphery is (in the simplest of terms)
insufficient to drive the secondary interneuron
processing that occurs in response to higher fre-
quency stimuli (Hirsch, 1986). As a result, the
secondary interneuron 90° lag time between the
detection of acceleration and the processing of the
compensatory vestibular slow-phase eye veloc-
ity is shortened. This can graphically be depicted
(see Figures 6–22E–I). Referring back to Figure
6–22D, the phase-matched eye velocity response
is occurring with the inherent 90° phase lag from
the detection of acceleration. However, by shortening the lag time due to the less robust low-frequency stimuli, the ocular response occurs with
less than the standard 90° (velocity-matching) lag
time. That is, peak eye velocity is occurring earlier
than the peak chair velocity. This is illustrated in
Figure 6–22E. This can easily be interpreted as a
phase-lead in relation to chair velocity. This can be
uncomfortable to think about, as it would seem
that the eye “movement” is actually leading chair
“movement.” In reality, the eyes are not moving
earlier than the chair, they are simply responding
with less lag time in relation to a weaker acceleration stimulus. This is the fundamental confusion
with understanding phase lead. We are not plotting eye displacement against chair displacement.
We are plotting velocity against velocity — and
velocity is very different from displacement (or
movement). Since we plot eye velocity to chair
velocity, it would “appear” that the eyes are, in
fact, leading the chair. However, if we were to plot
eye velocity to that of chair acceleration, we would
see that the eye response is simply responding with
less secondary interneuron processing lag time
(i.e., not using the full 90
degrees of central processing time for perfect velocity-matching). When
analyzing the normative data provided in Figure 6–23, one can see that the average phase
lead for healthy (normal) vestibular systems is
approximately 40 and 20 degrees for 0.01 and
0.02 Hz, respectively. In others words, in lieu of
the 90-degree central processing time present at
higher frequencies, there is a reduced but, normal
phase lag of only 60 and 70 degrees postacceleration at 0.01 and 0.02 Hz, respectively. It is not until
0.08 Hz and above, that a “perfectly matched”
phase lead of near zero degrees (90-degree lag
time from acceleration) is achieved. In fact, phase
lead sys-tematically increases with decreasing frequency below 0.08 Hz, reaching a 90° full phase
lead around 0.005 Hz (i.e., near or at the caloric frequency) (Wall, 1990).
6. Sinusoidal Harmonic Acceleration (SHA) Testing 181
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SHA Phase
75
70
65
60
55
50
45
40
35
30
25
20
15
VOR Phase
10
5
0
-5
-10
-15
-20
-25
0.01 Hz
0.02 Hz
0.04 Hz
0.08 Hz
0.16 Hz
Frequency
0.32 Hz
0.64 Hz
1.28 Hz
2.0 Hz
FIGURE 6–23. VOR Phase normative reference
range in degrees for 0.01 to 2.0 Hz. Diamonds represent mean VOR phase for each frequency. Error bars
denote ± standard deviations from the mean.
A Historical Point of View
for Plotting VO
Interestingly, at one time, eye velocity data
was actually plotted against chair acceleration
data; however, it soon became conventional
to plot chair velocity against eye velocity. This
is primarily because it makes more sense to
plot and compare similar measures (°/sec
versus °/sec rather than °/sec versus °/sec
It is true that a low-frequency phase-lead (or
lag with respect to acceleration) is physiologically
normal for acceleration stimuli less than 0.04 Hz.
The reduction in the precision of phase matching can best be illustrated by comparing the VOR
phase response against chair velocity across all
the SHA frequencies (Figure 6–24). The progressively increasing VOR phase lead below 0.04 Hz
R Phase
2
).
FIGURE 6–24. Average cycle slow-phase nystagmus plot data for all octave frequencies (0.01 to 0.64 Hz).
Dashed line marks the approximate peak of the chair velocity data, whereas red solid line marks the approximate
peak of the slow-phase nystagmus data. Note the advancing phase lead below 0.04 Hz.
182 Rotational Vestibular Assessment
can clearly be seen in this comparison of VOR
responses by frequency. However, some have
argued that there is seldom, if ever, a functional
component that accompanies such a naturally
occurring physiologic “deficiency,” as our visual
system is uniquely designed to compensate for
this phase mismatch (Goldberg et al., 2012; Leigh
& Zee, 2006). Honrubia, Jenkins, Baloh, Yee, and
Lau (1984) also argued that velocity storage is
likely inconsequential because visual input alone
can provide eye stabilization at low frequencies
of head motion. Conversely, others have argued
of its functional importance. Jacobson, McCaslin,
Patel, Barin, and Ramadan (2004) have argued
that velocity storage and its role in augmenting
the vestibular system’s sensitivity to low fre-
Calculating the VOR Response Phase from Sinusoidal Accelerations
Similar to calculating VOR gain, responses from each period are combined and
averaged together to form a single “average” slow-phase VOR response plot. These
averaged VOR slow-phase responses are then plotted against the averaged chair
stimulus (single line as the chair stimulus should contain no noise to average out).
Before we begin reviewing an example, it is a good to recall that because phase
is calculated from gain, a thorough analysis of the signal to noise ratio (spectral
purity) in the response must be considered whenever low gain (below 0.15) is
present. Figure 6–25 depicts data from an “average response plot” showing averaged data in both the rightward and leftward rotations. A best-fit line is calculated
through the averaged slow-phase VOR data. Although we talk about phase shift
in terms of the temporal relationship between peak eye velocity data to peak chair
velocity, the VOR phase is actually calculated from the difference between the
point in time where the best-fit line and the chair velocity plot crosses 0° velocity.
Since rotational cycles repeat themselves every 360 degrees, phase is, therefore,
quency stimuli is intrinsically vital to an efficient
vestibular response and its proper integration for
subjective postural stability, particularly during
low-frequency stance/postural sway (Jacobson et
al., 2004). When a peripheral or central vestibular disorder disrupts velocity storage to where a
significant-to-near theoretical maximum 90° VOR
phase-lead occurs (i.e., zero phase-lag with respect
to acceleration), the consequential phase mismatch becomes subtlety recognized by our central nervous system. When this happens, patients
will often complain of poor postural stability, particularly at rest or when standing still, as these
“postural resting movements” more closely match
the low-frequency accelerations where such VOR
phase abnormalities would predominate.
FIGURE 6–25. Average slow phase nystagmus data plotted against
average chair velocity data, with a peak velocity at 60°/sec. Yellow
best-fit line is plotted through the average of the slow phase eye
velocity data.
6. Sinusoidal Harmonic Acceleration (SHA) Testing 183
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expressed in terms of degrees. In Figure 6–26, the best-fit line identifies a peak
slow-phase eye velocity response crossing 0° velocity at 40 seconds, whereas the
chair velocity data crosses 0° velocity at 50 seconds. This difference in phase shift
(time) is then divided by the time needed to complete one full cycle at the respective
frequency. This difference is then multiplied by 360 degrees, which expresses the
VOR phase shift in terms of degrees. That is, the VOR phase shift for this example
would then be 10 seconds divided by 100 seconds (the time required to complete a
full cycle at 0.01 Hz) multiplied by 360 degrees. This would yield a VOR phase lead
of 36 degrees. A VOR phase lead of 36° means that only 54° of central processing occurred following detection of chair acceleration. So we can think of this as
either a 36° VOR phase lead with respect to chair velocity or a 54° VOR phase lag
with respect to chair acceleration. Again, a phase lead of 0° means that there was
a full 90° of central processing that occurred following detection of acceleration.
A
FIGURE 6–26. Individual graphs illustrate the phase lead calculation for a VOR response
to a 0.01 Hz SHA stimulus. A. The top panel depicts the entirety of the 0.01 Hz raw averaged
response showing both the nystagmus tracing and the plot of the slow phase eye velocity.
The boxed insert and bottom panel depict a magnified look at the response between 30
to 60 seconds. The change over from right-beating to left-beating nystagmus can be more
easily visualized in relation to the timing of the chair as it transitions from rightward to leftward rotation. continues
184 Rotational Vestibular Assessment
B
FIGURE 6–26. continued B. The inset box and bottom panel provide a magnified view of
the transition point between rightward and leftward rotation, and the point in time where the
best-fit line eye-velocity data crosses zero velocity (40 seconds) in relation to the point in
time where the chair transitions from rightward to leftward rotation (50 seconds). The VOR
phase lead can clearly be seen in this example. The calculation of VOR phase is shown.
A perfect compensatory response would then calculate as 0°, as a time difference
of zero divided by the total cycle time multiplied by 360 would equal “0.” Figure
6–27 shows the calculation of a 14.4° phase lead for a 0.02 Hz rotational stimulus.
As a point of nomenclature, a phase lead exists whenever the VOR gain best
fit line crosses 0° velocity before the chair velocity crosses 0°. This could be 75°
or 20°. Both examples are considered phase leads (re: chair velocity). However,
when comparing against normative reference ranges for 0.01 Hz the former would
be classified as a significantly prolonged phase lead, whereas the later would be
considered a significantly shortened phase lead. It is not considered a phase lag
until the VOR phase best-fit line crosses 0° velocity after the chair velocity crosses
0°. Figure 6–27 compares a prolonged VOR phase lead and a VOR phase lag.
Figure 6–28 illustrates the graphical differences between a prolonged phase lead,
a shortened phase lead and a phase lag with respect to normative data.
A
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B
FIGURE 6–27. Magnified view of a close-up comparison of a VOR phase lead response
(A) against a VOR phase lag response (B). Most VOR phase lag responses do not exhibit
a lag of more than 1 to 2 seconds, which is often in stark comparison to some phase leads,
which can extend well beyond a few seconds.
185
A
B
FIGURE 6–28. A. Differentiation between VOR phase leads and
VOR phase lags. Green dashed line represents 0° VOR phase. Any
data points above this line represent a phase lead. Any data points
below this line represent a phase lag. Data points lying within the yellow shaded area are not a phase lag, they are a significantly reduced
phase lead. Whereas the data points from 0.16 Hz to 0.32 Hz that
are below 0° (circled in blue) represent a true phase lag (albeit within
normal limits). B. Depicts significantly prolonged VOR phase leads for
the low-to-mid frequencies. continues
186
6. Sinusoidal Harmonic Acceleration (SHA) Testing 187
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C
FIGURE 6–28. continued C. Depicts significantly reduced VOR
phase leads from 0.01 to 0.04 Hz, VOR phase leads that are within
normal limits from 0.08 to 0.32 Hz, and a significantly prolonged VOR
phase lead at 0.64 Hz. Abnormal VOR phase lags (below 0°), particularly for the low frequencies, are extremely rare.
VOR Phase Interpretation
Now that we have a better understanding of how
VOR phase is processed, let us consider how it is
interpreted. Because VOR phase is a measure of
the timing in the processing of the compensatory
ocular response to vestibular stimulation, it is a
measure of both the peripheral and central processing that occurs within the vestibular nerve
and the central processors (i.e., the neural integrator and velocity storage mechanism). As such, a
loss or reduction in afferent neural drive, or a loss
in the efficiency of the velocity storage mechanism or the secondary interneuron commissural
network, will cause abnormalities in VOR phase.
When a VOR phase abnormality is observed,
it is nearly always a significant prolongation in the
phase lead (when compared against chair velocity).
This is most often due to a reduction of peripheral
input secondary to peripheral pathology and subsequent loss of central processing that is normally
present from the detection of acceleration to the
output of ocular velocity (i.e., the 90° processing
time needed for velocity-matching of the compensatory ocular response to head movement) (Hon-
rubia, Baloh, Yee, & Jenkins, 1980). A reduction in
VOR gain due to a peripheral vestibulopathy (or,
less frequently, a central pathology) will produce a
shorter lag-time from the detection of acceleration,
which is plotted as even a greater phase lead with
respect to chair velocity. The primary loss of central processing time leading to longer phase leads
is thought to be secondary to a reduction in the
number of neural synapses leading to a decrease
in neural processing within the neural integrator
and velocity storage mechanism (Honrubia et al.,
1980). Because of this, abnormalities in VOR phase
most often occur in the low frequencies during
SHA testing, where this central augmentation process is almost entirely dependent upon the velocity storage mechanism. In fact, a low-frequency
VOR phase lead in the presence of normal (compensated) VOR gain is the most common SHA
abnormality (Stockwell & Bojrab, 1997b). Conversely, given the greater velocity-matching efficiency of the VOR to acceleration stimuli >0.1 Hz,
as well as the low demand placed on the velocity
storage mechanism for higher frequencies, VOR
phase abnormalities for the mid-to-high frequencies during SHA testing are far less common.
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