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Figure 10–5. Illustrated is the use of a set of binocular infrared video goggle system..
movements that function independently of the peripheral vestibular system.
As one approaches the assessment of the ocular
motor system functioning independently of the peripheral vestibular system (during head still examinations),
four principal ocular control events are evaluated.
These include the following:
1. Saccade testing — This is the ability to move the
eyes in a rapid single movement to refixate a target
of interest onto the fovea (the most sensitive part of
the retina) for clear viewing.
2. Smooth pursuit tracking — This is the ability to
track the movement of a target of interest maintaining the image on the fovea with smooth continuous
eye movements, as opposed to tracking with the
use of repeated saccades.
3. Gaze stability — This refers to the ability to main-
tain gaze stable without the generation of other
eye movements (principally jerk nystagmus) while
looking straight ahead (primary), left, right, up,
and down.
4. Optokinetic nystagmus — This is the development
of reflexive eye movements in the form of jerk nystagmus during the visualization of moving objects
that fill 80% to 90% or greater of the visual field
of view. Ostensibly, the purpose for the generation
of the nystagmus is to assist clear visual viewing
when the head is in constant velocity motion, or
the head is still and objects of interest are moving
in a regular manner, or both are moving at constant velocities that are not equal, in which case the
the vestibulo-ocular reflex is normally inhibited in
order to maintain a clear visual view by preventing
the eyes from counter-rotating off the visual scene.
Saccade Testing
Technical Considerations
To assess saccadic eye movement, targets need to be
presented that require sudden rapid movements of the
eyes. In the past, this has been accomplished with the
use of fixed targets placed on a wall or screen such that
when the patient was seated at a particular distance
from the target plane, eye movements to each target
from the center would require a 10- to 15-degree subtended arc movement of the eyes. This task was used for
calibration of the system and for a cursory evaluation
of volitional saccades. With the use of computerized
systems, targets can now be presented via light bars or
through video projection systems. More importantly,
the task can be either that of presenting fixed position
targets or targets that appear randomly in different
positions in the horizontal or vertical planes. Also, it is
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possible to present the targets at random time intervals
together with the random location. Although fixed target location and timing are used for certain paradigms,
producing volitional saccades (predictable targets),
the use of random saccade testing is preferable in the
overall evaluation to elicit reflexive saccades (ability
to react when a target of interest suddenly appears at
a new location). Targets fixed or random are usually
presented within a ±30-degree range of subtended arc
movement of the eye. Saccade testing, specifically the
use of a broad bandpass filter of 10 to 100 Hz and a
sampling rate of a minimum of 60 Hz with 100 Hz or
higher, is now advised by the American National Standards Institute for ENG/VNG (ANSI, 2009).
It is also with this task that individual eye evalua-
tion is the preferred technique. This is secondary to the
need to recognize disorders involved with disconjugate
eye movements such as intranuclear ophthalmoplegia
(see case examples below). If using EOG for this task,
additional electrodes may need to be placed near the
medial canthus of each eye paired with those at the lateral canthus to obtain individual horizontal eye movements (refer to Figure 10–3 above).
Parameters for Saccade Testing Analysis
Refer to the bottom two panels of Figure 10–6 as each
of the analysis parameters are defined:
n Velocity — the plot on the left presents the
“main sequence plot.” This is a plot of the
peak velocity of the eye movement during
figure 10–6. Results of a normal random saccade test via individual eye video recordings on a 49-year-old female
diagnosed with unilateral vestibular hypofunction secondary to vestibular neuronitis. The top two panels provide
a sample of the traces showing the target in the dark line and the left and right recorded eye movements in the
lighter line. The left eye is in the top panel with the right eye in the second panel. The third and fourth panels give
the quantitative analysis for the saccade test. Each dot represents the analysis of a single saccade out of the total
of 30 presented for the test. From the left to the right in both the third and fourth panels the plots are for velocity
(main sequence plot), accuracy, and latency all as a function of the excursions of the eyes. The left eye analysis
is in panel three with the right eye analysis in the fourth panel.
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the trajectory from the initial point of regard
to the new eye location. Note that if the
sampling rate is less than 100 Hz, the plot is
more representative of the average velocity,
not truly peak velocity. The eye velocities
are plotted as a function of the excursion
distance of the eye in degrees of subtended
arc movement, not the movement of the
target.
n Accuracy — the center plot gives the percent-
age of the distance the eye moved in its first
single movement relative to that of the target
as a function of eye movement excursion. One
hundred percent indicates that the eye moved
the same distance as the target in a single
major excursion. Values over 100% indicate
an overshoot, whereas those under 100%
show an undershoot.
n Latency — the final plot to the right reflects the
lapsed time in milliseconds from the initiation
of the target movement to the initiation of
the eye movement, again as a function of eye
movement excursion.
In each of the plots, the abnormal region is defined
as two standard deviations below the mean in the main
sequence plot, two standard deviations above and
below the mean in the accuracy plot, and two standard deviations above the mean in the latency plot and
shown by the stippled region. These plots are typically
analyzed such that if 50% of the saccades sampled
for any of the three parameters are within the normal
range, the saccade test is considered normal. Agerelated normative data are not needed for routine clinical analysis of saccade testing by either fixed, random,
or remembered paradigms (Hain, 1993; Leigh & Zee,
2006; Shepard & Telian, 1996). A sample of normative
data for individual eye recordings (electro-oculography
techniques) from 46 subjects of age 19 to 49, 15 of age
50 to 69, 8 from 70 to 79, and 7 from 80 to 88 is shown
in Figure 10–7. In the figure the population responses
with means and two standard deviation ranges are
given for all three parameters discussed above. In the
main sequence plot in Figure 10–7, abduction velocities are lower than adduction velocities. This is a finding that has been reported previously (Boghen, Troost,
Daroff, Dell’Osso, & Birkett, 1974) again by the use of
EOG recording techniques. In this work it was determined that a consistent relationship between the peak
velocity and the size of the excursion of the saccade
was present — the larger the excursion of the saccade,
the higher the peak velocity up to about 500 degrees/
second. It was also demonstrated that the duration of
the saccade also lengthened with the increase in excursion up to about 100 ms. This duration is shorter than
that needed to obtain visual feedback, implying that
adjustments in the speed of the saccade and the final
destination of the eye movement cannot be adjusted
while the saccadic eye movement is in progress. Comparisons with other eye movement recording techniques suggest that this may be unique to the use of
EOG techniques, as use of scleral search coils and infrared reflections show the opposite (Leigh & Zee, 2006).
In a direct comparison between VOG and search coils
for saccade, smooth pursuit, and optokinetic nystagmus in both an artificial and human eye during roll
plane rotation, the mean differences between the VOG
and the search coil were 0.56, 0.78, and 0.18 degrees of
rotation for the roll, pitch, and yaw (horizontal) planes,
respectively (Imai et al., 2005). The implication from
this is that normative data for saccade testing need to
be those developed from the video recordings, but if
EOG techniques are used, then the normative ranges
for comparison should be those developed with the
EOG technique. It has not been demonstrated, irrespective of the recording technique, that age-related
normative ranges are needed for the clinical study
of saccades.
Interpretation of Saccade Testing
There are several protocols for testing saccadic activity. These are all well documented in the literature for
ENG or VNG applications (Jacobson, Newman, & Kartush, 1993; Leigh & Zee, 2006; Shepard & Telian, 1996).
Therefore, we concentrate our interpretation discussion
on what has become the most common protocol used
for routine clinical evaluation of saccadic eye movements, the random saccade paradigm. Recognize that,
in general, the interpretation of a fixed saccade paradigm will be like that detailed below for the random
saccade paradigm.
As indicated above, the parameters used for
analysis of a saccadic eye movement are the latency to
onset after the presentation of a target at a new location, the accuracy with which that movement is made,
and the peak velocity of the eye during the movement.
The combined use of these three allows for possible
suggestions of localization of involvement within the
CNS based on the neurologic substrate responsible for
the performance aspects of each of the three outcome
parameters. Saccade testing abnormalities do not occur
as a result of peripheral vestibular system lesions but
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a
figure 10–7. A. Shown are the individual eye data for a random saccade paradigm for the left eye of the 76
subjects with age distributions as given in the text. The graph on the top left gives latency to onset of saccade eye
movements, the top right plots percent accuracy, and the bottom graph shows the peak velocity all as a function
of the excursion of the eye. continues
reflect CNS lesion sites (Tables 10–1 to 10–3). A detailed
discussion of the current state of knowledge of the neural pathways responsible for saccade production is provided by Leigh and Zee (2006); only a brief summary
of the salient aspects of that information is presented
below. The neural substrate information is then used to
develop the interpretation suggestions given for abnormalities related to saccade velocity, accuracy, and laten-
cies or combinations of these parameters in Tables 10–1,
10–2, and 10–3, respectively.
For a horizontal or vertical reflexive saccade via
the random saccade paradigm, the initiation of the
movement results from the presentation of a target of
interest in a new location. The horizontal reflexive eye
movement that brings gaze to the new target is primarily engendered by excitatory burst neurons (EBNs) in
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b
figure 10–7. continued B. The right eye results for latency, accuracy, and velocity are given in the same orientation
as in part A. From Practical Management of the Balance Disorder Patient, by Shepard, N. T., and Telian, S. A., 1996,
pp. 100–103. Used with permission.
the paramedian pontine reticular formation (PPRF) in
the caudal pons (van Gisbergen, Robinson, & Gielen,
1981). For vertical and torsional saccades, the excitatory
burst neurons are part of the rostral interstitial nucleus
of the medial longitudinal fasciculus (riMLF) in the rostral mesencephalon (King & Fuchs, 1979; Vilis, Hepp,
Schwarz, & Henn, 1989). These premotor neurons initiate bursts of activity approximately 12 ms prior to the
actual initiation of the eye movement. However, while
the premotor neurons connect with cranial nerve nuclei
III and VI, the neural circuit also involves activity from
inhibitory and omnipause neurons in the brainstem
and midbrain areas in a complex network allowing for
the activity of the EBN to initiate eye movements (see
Chapter 3 in this text for a more detailed discussion)
with velocities proportional to the neural firing rate
(Leigh & Zee, 2006). There is a growing body of evidence that for both horizontal and vertical voluntary
saccades, areas other than simply frontal eye fields of
the frontal lobe and brainstem and midbrain circuits are
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table 10–1. Abnormalities of Saccade Velocity
• Slowing both eyes, all directions with full ocular
range-of-motion
Fatigue, medications, drowsiness
PPRF for horizontal movements and RIMLF for
vertical
Cerebral hemispheres, superior colliculus,
cerebellum
Early in myasthenia gravis especially with
repeated activity
movement and slowing as the target is
approached (
• Slowing either eye, restricted directions
For horizontal PPRF
For vertical RIMLF
For horizontal on adduction only (monocular
or binocular)
slowing (
Cranial nerves III, IV, VI, or muscle palsy
• Abnormally fast
Later in myasthenia gravis of ocular type (Leigh
&
Calibration errors
Restriction syndromes (see text for explanation)
INO)
Zee, 2006)
— glissades, initial fast
Leigh & Zee, 2006)
— MLF lesion on the side of the
involved. These include the superior colliculus, cerebellum, various regions of the frontal lobe, the posterior
parietal cortex, basal ganglia, and thalamus. A synthesis
of this literature is provided by Leigh and Zee (2006).
Primary control over the velocity of the saccadic
movement is engendered by the PPRF in the pons. Yet
not all saccadic slowing disorders are from the pons
region of the brainstem. A useful generality is that
global slowing (both eyes in both directions with full
ocular range of motion) could involve either the PPRF
or the riMLF (see Chapter 3 for complete discussion),
yet higher centers such as the superior colliculus and
cerebral hemispheres need to be considered. If the
slowing is restricted to involve only one eye or a single
direction, then slowing of abduction is most likely a
sixth nerve palsy with monocular slowing of adduction, which would be most likely internuclear ophthalmoplegia (INO) with an ipsilateral medial longitudinal
fasciculus (MLF) lesion (see Chapter 3 for a full discussion of the effects of lesions in these areas). See Table
10–1 for other considerations.
In the performance of saccade testing, more so
than during other portions of the ENG/VNG, individ-
table 10–2. Abnormalities of Accuracy
• Hypometria (undershoot)
Fatigue, medications, drowsiness
Bilateral — cerebellar dorsal vermis (Leigh &
Zee, 2006)
Unilateral — ipsilateral cerebellar/brainstem
Visual acuity or visual field cuts
Myasthenia gravis for large saccades
Brainstem burst neuron providing too short of a
burst
Cerebral hemispheric — contralateral to the
lesion more likely if the patient demonstrates
neglect (
•
Hypermetria (overshoot)
Cerebellar
Bilateral — cerebellar fastigial nucleus (Leigh &
Zee, 2006)
table 10–3. Abnormalities of Latency
• Both eyes in all directions
Fatigue, medication, drowsiness
Frontal eye fields, but likely for remembered
or antisaccade tasks as opposed to reflexive
random saccade paradigm
Visual deficits — severe reductions in acuity,
amblyopia (Ciuffreda, Kenyon, &
• Both eyes for fixed saccade paradigms — learned
or commanded tasks
Basal ganglia as in Parkinson’s and other
disorders of motor initiation where target
location and timing of movement is regular
Lasker & Zee, 1997; Lasker, Zee, & Hain, 1987)
(
• Abnormally short latency
Highly unusual — most likely patient anticipating
target movement, needs reinstruction
• Superior colliculus and pathways to reticular
formation in the brainstem (Leigh & Zee, 2006)
Meienberg, Harrer, & Wehren, 1986)
Stark, 1978)
ual eye recordings should be made if at all possible. It
is during saccade testing that disconjugate eye movements are accentuated. The hallmark eye movement
disorder causing disconjugate movement is that of
INO. In this disorder the adducting (moving toward
the midline) eye is abnormally slow. Recognition of the
condition immediately implies a lesion in the MLF on
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the side of the eye with the adduction slowing (Leigh
& Zee, 2006). Additionally, when INO is bilateral, there
is a presumptive diagnosis of multiple sclerosis until
proven otherwise. Video 10–1 shows the eye movements of a 44-year-old male with multiple sclerosis.
The eye movements were captured during VNG sac-
cade testing and illustrate bilateral INO. Figure 10–8
shows the recorded analysis for the eye movement in
Video 10–1. Video 10–2 shows the eye movements of
a 30-year-old male during random saccade testing,
with Figure 10–9 illustrating the recorded analysis for
Video 10–2. In this example, the eye movements and
figure 10–8. The recorded eye movement from individual eye recordings for the 44-year-old male in Video10–1
who was subsequently diagnosed with multiple sclerosis. The column of results on the left is for the right eye
with the right column representing the left eye. The top two panels indicate peak velocity; the middle two
show accuracy, and the bottom two are for latency all as a function of the excursion of the eyes. The larger
light color dots represent average performance for the parameter at the specific excursion with the small
black dots the performance for individual saccades. The velocity panels clearly show, as seen in the video,
slowing of each eye on adduction indicating bilateral INO. Additionally, abnormal slowing is noted for both
eyes dominantly on movements to the right. note that analysis is done based on needing 50% of the individual
saccades to be outside the normal range for a particular aspect of the study to be considered abnormal.
figure 10–9. Saccade performance from the 30-year-old male in Video 10–2 demonstrating left-side INO and
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subsequently diagnosed with a left-side brainstem stroke. See legend for Figure 10–8 for details of the figure layout. Additionally, the top two panels show samples of the raw eye movement for five saccades. The lighter trace
is the actual eye movements with the black trace the target movement. Right eye represented on the left and
left eye on the right. In the velocity plot for the left eye significant slowing is noted for adduction.
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analysis are consistent with left-side unilateral INO.
The patient was shown to have had an ischemic stroke
on the left involving the left MLF pathway.
Abnormally fast saccades typically occur as a
result of the saccade being prematurely halted before
reaching the target (restriction syndrome) (Leigh &
Zee, 2006). This can occur as a result of disease process that reduces the range of motion of an eye (such as
myasthenia gravis) or a mechanical restriction in range
of motion (such as trauma or a mass lesion), making the
saccade too fast for its actual recorded amplitude, though
likely normal velocity for its larger intended amplitude
(Leigh & Zee, 2006). During ENG or VNG testing, inaccurate calibration needs to be ruled out as a cause for
apparent abnormally fast saccade performance.
The cerebellum, specifically the dorsal vermis and
fastigial nucleus regions, are major contributors to the
accuracy with which saccades are performed (Leigh &
Zee, 2006). Yet although overshoot dysmetria (hypermetria) is considered a strong indication of cerebellar
involvement, the possibilities for involvement in the
presences of hypometric (undershoot dysmetria) saccades are considerably broader (Leigh & Zee, 2006).
Patients with severe visual acuity deficits, especially
macular degeneration, may perform the saccades to
targets by using multiple smaller saccades, because
during a random saccade task the target direction is
clear but placing the target on the fovea becomes difficult. Patients with visual field cuts that involve a
full or partial hemisphere (hemianopia) will produce
hypometric saccades. Here also combinations of brainstem and cerebellar lesion may result in mild to severe
undershooting of the target (Leigh & Zee, 2006).
Another aspect of saccade accuracy is related to
the mentioned ocular lateralpulsion introduced in the
section on gaze testing (a full discussion of the anatomy and examination findings is given in Chapter 3).
This directional bias of saccades is most commonly
ipsipulsion, with hypermetric saccades (overshoot) to
the lesion side and hypometric saccades to the contralateral side (undershoot).
The last attribute of a saccade is the length of time
to initiation of the eye movement (latency) once a target
of interest appears or a command is given to gaze at an
already existing target within the visual field. Lesions
in the PPRF or riMLF involving the burst neurons could
cause delays in the initiation of the eye movement
horizontally or vertically but this would represent an
unusual situation. The process to initiate the burst neuron activity involves multiple other central areas that
could result in delayed onset of burst neuron activity
and ultimately in an increase in latency for the desired
saccade. The involvement may be from visual acuity
problems, and amblyopia (Ciuffreda, Kenyon, & Stark,
1978) to visual eye fields in the frontal cortex (Leigh &
Zee, 2006). Likely more with latency than either velocity or accuracy, the state of the patient regarding medication, drowsiness, and attention highly influences the
results. It is with latency more so than with velocity or
accuracy that the paradigm differences between fixed
(volitional or commanded) saccades and the random
paradigm reflexive saccades are seen. Basal ganglia
involvement can cause increased latencies to fixed saccades yet show normal initiation timing with random
saccades (Leigh & Zee, 2006).
Once drugs, inattention, drowsiness, fatigue, and
impaired visual acuity are ruled out, then any abnormality with saccade performance must be considered
as a potential indicator of CNS or peripheral ocular
motor involvement. It would not be reasonable to consider peripheral vestibular system involvement as a
possible source for disruptions in any of the saccade
parameters discussed above.
When performing an antisaccade paradigm, the
primary means for analysis during an ENG or VNG is
percent error. This would be a ratio of the number of
saccadic eye movements that were made in the direction of the target movement to the number made in the
opposite direction (the desired response). With practice you should expect patients to be able to perform
the antisaccade task with a percent of error near zero
for an interval of 5 to 10 s. When overall performance
from the start to the end of the task was investigated
in a large number of young healthy male subjects, the
percent error has been noted to be 23% with a large
variance of 17% (Evdokimidis et al., 2002). If performance is such that correct sustained saccades cannot
be obtained for 5 to 10 s, then involvement in the eye
fields of the frontal cortex must be considered (Leigh
& Zee, 2006).
Pursuit Tracking/Smooth Pursuit Tracking
Technical Considerations
General filter setting would be the same as for saccade
testing with a low-pass filter at 100 Hz and a highpass filter, if used, at 3 to 10 Hz. Like saccade testing, a
60 Hz notch filter can be used as required. For pursuit
tracking, the issue of the sampling rate of the video or
electrode system is not as critical as in saccade testing
given the much slower eye velocity being captured.
Whereas many systems will provide for binocular individual eye recording, the simultaneous individual eye
recording is not as clinically revealing as with saccade
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evaluation. However, if this feature is available in the
video systems, it can be of use, as usually a selection of
either the right or the left eye can be used for analysis,
thus allowing for optimization of the analysis if a poor
recording was obtained for technical reasons for only
one eye.
What is critical with this evaluation is the use of
age-sensitive normative data. Changes in performance
of pursuit tracking can be seen starting in the third or
fourth decades of life (Paige, 1994). Figure 10–10 shows
the effects of age and the frequency of target presentation on the outcome parameter of pursuit velocity gain
(discussed below). A full set of normative data for individual eye electrode recordings for all outcome parameters as a function of age is reprinted in Table 10–4 for
reference (Shepard & Telian, 1996). The data given in
Table 10–4 are from subjects ranging in age from 20 to
80 years with 8 to 10 normal subjects in each decade.
These data are for horizontal smooth pursuit testing.
Statistical analysis showed significant differences at the
p = 0.05 level criteria for age grouping shown in the
table. For all the smooth pursuit frequencies, the excursion of the target was a 17.5-degree peak (movement to
either side of center). These data were developed using
the EOG technique. The authors are not aware of pub-
lished normative data as a function of age developed
using video recordings. It is the use of age-sensitive
normative data that improves the overall performance
of smooth pursuit testing, not by increasing sensitivity
but by increasing the specificity of the test.
Attention to the stimulus for smooth pursuit tracking by fixed velocity (ramp) or varying acceleration/
velocity (sinusoidal) target protocols (see below) can
maximize performance. The greater brightness of the
target and the large size of the target are both features
that improve performance (Hutton & Tegally, 2005).
Even if the visual field is filled with the stimulus, it
is the central portion of the fovea that dominates the
response (van den Berg & Collewijin, 1986; Van Die &
Collewijin, 1986).
For smooth pursuit tracking as well as for saccade testing, these are novel tasks for the patient. Even
though the ocular motor tasks are used throughout
an individual’s daily routines, they are not used in a
focused and isolated manner as when testing. Therefore, to achieve maximum performance, the tasks may
have to be repeated with coaching multiple times. It
is important not to accept the first trial for saccades or
pursuit tracking as adequate performance unless the
first trial is either normal or explainable by age-related
normative data.
figure 10–10. A modeling of smooth pursuit data
acquired from normal volunteers as a function of age
groupings (on the x-axis) and frequency of target movement (on the y-axis). The pursuit outcome parameter of
velocity gain (see text for explanation) for the left eye is
shown on the z-axis. The modeled data were developed
using a negative exponential weighting function. From
Practical Management of the Balance Disorder Patient
by Shepard, N. T., and Telian, S. A. Copyright © 1996.
Parameters for Analysis
Here as with saccades, the specifics of the analysis are
dependent on the manufacture of the equipment being
used, unless the facility has the capability to develop
its own computer sampling and analysis techniques.
That said, there are three parameters more commonly
seen with routine ENG/VNG analysis of smooth pursuit. These usually assume the use of a sinusoidal protocol (see discussion below). For this discussion, refer
to Table 10–4 and Figure 10–11.
Velocity gain is indirectly a measure of how sinusoidal the eye movement was in comparison to the target. The gain value is calculated by a ratio of peak eye
velocity divided by peak target velocity. Figure 10–11
presents a plot of the overall combined velocity gain
without regard to movement of the eye leftward or
rightward. Other examples of velocity gain displays
showing the individual gain for eye movements in each
direction are provided with the discussion of interpretation given below. If the eye tracked the target in a
perfect manner, the gain would be expected to be 1. As
saccadic disruptions in the eye movement occur, this
introduces discontinuities that reduce the sinusoidal
behavior of the eye movement and result in gain values
less than unity. The mathematical process to determine
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