Exp Brain Res (2004) 157: 286295
DOI 10.1007/s00221-004-1842-0
RESEARCH ARTICLES
Maria Pia Bucci . Zo Kapoula . Qing Yang .
Dominique Brmond-Gignac . Sylvette Wiener-Vacher
Speed-accuracy of saccades, vergence and combined eye
movements in children with vertigo
Received: 7 July 2003 / Accepted: 22 December 2003 / Published online: 13 March 2004
# Springer-Verlag 2004
Abstract Vergence abnormalities could lead to inap-
propriate vestibulo-ocular reflex (VOR), causing vertigo
and imbalance (Brandt 1999). Indeed, a recent study by
Anoh-Tanon et al. (2000) reported the existence of a
population of children with symptoms of vertigo in the
absence of vestibular dysfunction but with abnormal
vergence findings in orthoptic tests. The purpose of this
study was to examine in such children the accuracy,
duration and mean velocity of vergence and saccades;
additionally, for a few subjects, the effect of orthoptic
vergence training on these parameters was also investi-
gated. LEDs were used to stimulate saccades, pure
vergence along the median plane and combined saccade-
vergence movements. Movements from both eyes were
recorded with a photoelectric device (Bouis). The results
show that children with vertigo perform saccades as
normal subjects of comparable age. In contrast, vergence,
particularly convergence, shows abnormalities: poor ac-
curacy, long duration and low speed. During combined
movements, the well known reciprocal interaction be-
M. P. Bucci . Z. Kapoula . Q. Yang
Laboratoire de Physiologie de la Perception et de 1lAction,
LPPA, CNRS-College de France,
11 place M. Berthelot,
75005 Paris, France
D. Brmond-Gignac
Hpital Robert Debr, service dOphtalmologie,
48 Bld. Srurier,
75019 Paris, France
S. Wiener-Vacher
Hpital Robert Debr, service dORL,
48 Bld. Srurier,
75019 Paris, France
M. P. Bucci (*)
Laboratoire de Physiologie de la Perception et de 1lAction,
UMR 9950, CNRS-College de France,
11 place Marcelin Berthelot,
75005 Paris, France
e-mail: maria-pia.bucci@college-de-france.fr
Tel.: +33-1-44271636
Fax: +33-1-44271382
tween the saccade and the vergence is present only for
saccades combined with divergence; for saccades com-
bined with convergence such interaction is abnormal: the
saccade is slowed down by the convergence but the
convergence is not accelerated by the saccade. Orthoptic
training improves significantly the accuracy of all eye
movements; such improvement was significant for all
types of eye movements except for divergence (pure and
combined). Furthermore, convergence remains abnormal
and the lack of acceleration by the saccade persists. These
specific convergence deficits could be of both subcortical
and cortical origin. Orthoptic training improves the
accuracy presumably via visual attentional mechanisms,
but cannot completely override deficits related to subcor-
tical deficiencies.
Keywords Accuracy . Duration . Speed . Saccade .
Vergence . Combined movements . Vertigo
Introduction
For the visual exploration of the natural environment,
humans make at least three types of eye movements:
saccades (rapid eye movements to change fixation
horizontally or vertically), vergence eye movements (to
adjust the angle of visual axes according to the distance of
the object of interest), and combined saccade-vergence
movements; the latter are the most common movements
used for exploring the natural world. During natural
activity humans move the eyes and the head together, and
the vestibulo-ocular system stabilizes the image of interest
on the fovea compensating the head movements. The
vestibulo-ocular reflex (VOR) should be adjusted accu-
rately to the distance between the eyes and the target, and
vergence is one of the signals that the brain can use for
distance adjustment (Leigh and Zee 1999). If the vergence
command is not accurate the VOR will be inappropriate;
consequently the image on the fovea will not be well
stabilized; such visual instability can cause vertigo and
headache (Brandt 1999). Anoh-Tanon et al. (2000) showed

that about 5% of children consulting the ENT service for
vertigo and headaches symptoms have normal vestibular
functions but orthoptic vergence abnormalities; however,
objective studies on vergence eye movement character-
istics in children with or without vertigo are rather scarce.
Several studies examined latency of saccades in a large
population of normal subjects (Fischer et al. 1997; Munoz
et al. 1998; Fukushima et al. 2000; Klein and Foerster
2001) and they showed that its latency in children is longer
than in adults and that it shortens with age. Moreover,
Yang et al. (2002) showed that latency of eye movements
in natural space (saccades and vergence), particularly
those of vergence, is long in young children, reaching
adult values at the age of 1012 years. All these results
suggest that the central/cortical circuitry involved in the
initiation of eye movements is not completely developed
until 1012 years.
In contrast, a recent study by our group (Yang and
Kapoula 2004) explored children from the age of 4.5 years
and showed that saccades, vergence and combined
movements are similarly accurate (close to 90% of the
amplitude of the movement) in children from the age of
4.5 years and in adults; divergence is the slowest
movement to execute for both children and adults.
Moreover, these authors did not found a significant
difference in the peak velocity of all types of eye
movements between children and adults. Their observa-
tions indicate early maturation of all distinct brainstem
structures controlling these movements and their interac-
tion; this contrasts with the prior study on latencies (Yang
et al. 2002), which indicates slow progressive develop-
ment of the cortical structures controlling the initiation of
eye movements.
A recent study by Bucci et al. (2004) reported that in
children with vertigo in the absence of measurable
vestibular dysfunction, latency of eye movements is
abnormally long, particularly that of convergence; this
could be due to central/cortical impairment of the
structures controlling the triggering of eye movements.
The purpose of the present study is to examine whether
children with vertigo with no abnormal findings of
vestibular function present abnormal trajectories of eye
movements, particularly of vergence. Indeed, given the
complaints and the orthoptic findings for reduced vergence
amplitudes (as measured clinically by the bar prism) one
could expect deficiency (inaccuracy and/or slowness)
particularly for convergence movements.
Finally, a reciprocal interaction between saccades and
vergence for combined movements in direction and depth
is well known for adults (Zee et al. 1992; Collewijn et al.
1995): the saccade is slowed down by the vergence while
the vergence is accelerated by the saccade; it seems also
that vergence acceleration is higher for convergence than
for divergence (Collewijn et al. 1995). A similar dynamic
interaction has also been observed by Yang and Kapoula
(2004) for normal children. To assess eventual vergence
abnormalities in children with vertigo this study examines
the speed-accuracy characteristics of isolated saccades,
vergence and combined eye movements.
287
The second goal of the study is to explore eventual
effects of orthoptic training on the spatiotemporal
characteristics of eye movements.
Methods
Subject characteristics
Eight young subjects participated in the study. The investigation
adhered to the principles of the Declaration of Helsinki and was
approved by the Human Experimentation Committee of our
institute. Subjects age ranged between 8 and 16 years (11.75
2.91). Subjects were admitted to the ENT and ophthalmology
service of the childrens hospital because they complained of vertigo
and headache. With vertigo we indicate subjective symptoms
experienced by all our children; more precisely, children felt the
environment moving around them or being in imbalance. Such
symptoms were usually brief, lasting less than 1 min; however, they
occurred several times during the day. Other than these symptoms,
no children had neurologic problems, and they did not receive any
medication. All children underwent a complete vestibular and
orthoptic examination (see below).
Vestibular examination
The vestibular testing included a clinical vestibular examination and
vestibulo-ocular response recording (see Wiener-Vacher et al. 1996,
for details). Briefly, the vestibular clinical examination included a
caloric test (irrigation of each ear with 30 and 44C warm water).
Hearing examinations were also performed to assess the function of
the inner ear. The electro-oculography (EOG) was used for
recording the VOR responses to horizontal semi-circular canal and
otolith stimulations. More precisely, the canal VOR was elicited by
rotatory impulsions about a vertical axis (acceleration and deceler-
ation were at 40/s, separated by a rotation at 60/s). The otolith
VOR was induced by inclining the chair by 9 with respect to
gravity. The results of all these tests were normal for all children
participating in this study.
Orthoptic examination before and after orthoptic training
All children had normal binocular vision (60 s of arc or better),
which was evaluated with the TNO random dot test for stereoscopic
depth discrimination. No child wore spectacles. Orthoptic evaluation
of vergence (made by using prisms, and the Maddox rod and
synoptophore technique) revealed for all subjects vergence abnorm-
alities: the distant near point of convergence was on average 9
2 cm, exophoria (i.e. latent deviation of one eye when the other eye
is covered) at near viewing was on average 82 pD; and there was a
limited range of fusional vergence (at near: 207 pD and 104 pD
respectively for convergence and divergence).
Orthoptic training (12 sessions, 3 times per week) was prescribed
for all children. It consisted of several eye movement exercises (e.g.
converging and diverging the eyes to follow a small pen-light or a
letter moving in depth) in order to improve the range of vergence
fusional amplitude (see for details www. childrensvision.com).
After this training a second orthoptic clinical examination was
done for all children. Clinical signs of vergence disorders
disappeared: the near point of convergence became normal (5
1 cm) and the exophoria at near vision decreased, reaching normal
values (32 pD). Finally, the range of vergence at near viewing also
increased after training (375 pD and 156 pD for convergence and
divergence respectively). Most importantly, for all children, subjec-
tive symptoms of vertigo and headache disappeared.
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Eye movements recording
A PC directed the stimulation of LEDs; data collection was directed
by REX, software developed for real-time experiments and visual
display run on the PC. Horizontal eye movements from both eyes
were recorded simultaneously with a photoelectric device (Ocul-
ometer, Bouis). This system has an optimal resolution of 2 of arc
and a linear range at 20 (Bach et al. 1983). Eye-position signals
were low-pass filtered with a cutoff frequency of 200 Hz and
digitized with a 12-bit analogue-to-digital converter and each
channel was sampled at 500 Hz.
Eye movements were recorded before the orthoptic vergence
training in all eight subjects, and after training in four of them (S3,
S5, S6 and S7).
Visual display
one at the center, two at 10 and two at 20; fixation to any of
these LEDs required a vergence angle of 2.3. In a dark room the
subject was seated in an adapted chair with the head stabilized by a
forehead and chin support facing the visual display. Subjects viewed
the LEDs binocularly and were asked to move their eyes to the LED
as soon and accurately as possible.
Oculomotor testing
Calibration task
The calibration task was done at the beginning and at the end of
each block of the main experiment (see below): a standard saccade
paradigm was used to elicit visually guided saccades to the LED
presented at 10 and 20 at the far isovergence surface. These
saccades were used to extract the calibration factor for each eye.

Target-LEDs were placed at eye level on two isovergence circles at

different distances from the subject: one at 20 cm and the other at
150 cm from the subject. On the circle close to the subject three
LEDs were placed: one at the center and the other at 20. The
required mean vergence angle for fixating any of these three LEDs
was 17. On the circle far from the subject, five LEDs were placed:
Saccades, vergence and combined movements
Each trial started by lighting a fixation LED at the center of one of
the two circles (far or close). After a 2.5 s fixational period the

Fig. 1AF Typical recordings

of the different types of eye
movements. The saccade trace is
the average of the position of the
two eyes (LE+RE/2); the ver-
gence trace is the difference
between the two eyes (LERE).
Pure saccade to the right (A) and
to the left (B); convergence (C)
and divergence (D) movements
along the median plane. Com-
bined movements: (E) saccade
to the left combined with con-
vergence; (F) saccades to the
right combined with divergence
component. The arrows indicate
the beginning and the end of the
movement. Dashed lines indi-
cate target position. The target-
LED appears at time zero

central LED was turned off and a target-LED appeared for 2 s.
When the target-LED was on the center of the other circle it called
for a pure vergence eye movement, along the median plane. When it
was at the same circle it called for a pure saccade of 20 (left or
right), and, when it was lateral and on the other circle, the required
eye movement was a combined saccade and vergence eye move-
ment. The required saccade amplitude was 20, and the required
vergence change along the median plane or along lateral axes (for
combined movements) was 15. In each block, the three types of
trials were interleaved randomly. Each block contained four
saccades at far, four pure convergence and four pure divergence
movements, four saccades combined with divergence, and four
saccades combined with convergence. Four blocks were run; each of
them was separated by a rest of a few minutes.
Data analysis
Calibration and analysis methods are similar to those used in prior
studies (Kapoula et al. 2001; Yang et al. 2002). Briefly, a linear
function was used to calibrate the individual eye position signals.
From these two signals, we calculated the conjugate signal [(left eye
+right eye)/2] and the vergence signal (left eyeright eye). Markers
were placed at different points on eye position signals automatically
by the computer, and were verified afterwards by an investigator.
The onset of the conjugate saccadic component was defined as the
time when the eye velocity reached 5% of the saccadic peak
velocity; the offset of these signal was defined as the time when the
eye velocity dropped below 10/s. The onset and the offset of the
vergence signals (for pure vergence movements and for the vergence
component of the combined movements) were defined as the time
point when the eye velocity exceeded or dropped 5/s. These criteria
are standard and similar to those used by other authors (e.g. Takagi
et al. 1995). Eye movements that were in the wrong direction or
Fig. 2 Mean gain (amplitude of the movement/target excursion),
duration and mean velocity (amplitude of the movement/duration) of
pure movements: saccades (A), convergence (B) and divergence (C)
for each subject tested. Vertical lines indicate the standard deviation.
Group means are based on eight subjects. Horizontal line on the
289
contaminated by blinks were rejected. The mean percentage of the
rejected eye movements was about 6%.
For all types of eye movements we measured the gain, that is the
ratio of the amplitude of the total movement over the target
excursion amplitude, the duration and the mean velocity (amplitude
of the movement/duration). Analysis of variance (ANOVA) was
performed with subjects as random factor and as a fixed factor the
individual means of the gain (amplitude of the movement/amplitude
of the target excursion), of the duration and of mean velocity for
different types of eye movements. Such analysis was performed for
the before and after training comparison.
To evaluate eventual abnormalities of various parameters, data
were compared to values of children without vertigo of similar age,
studied by our group under the same conditions (see Yang and
Kapoula 2004). A statistical comparison with normal children was
done using Students t-test.
Results
Qualitative observations
Figure 1 shows examples of trajectories of three different
types of eye movements recorded (saccades, vergence and
combined movements). Saccades to the right (Fig. 1A) as
well as to the left (Fig. 1B) show mild undershoot of the
target and a small corrective saccade is made for reducing
the error. In contrast, convergence and divergence move-
ments (Fig. 1C, D) are highly hypometric (their amplitude
is only 10, while the target required 15); note also the
slowness of these movements. For the combined move-
group means corresponds to the mean value found in normal
subjects of comparable age (Yang and Kapoula 2004). Asterisks
indicate that the group mean value is significantly different from
normal value
290
ments (Fig. 1E, F) the saccade component shows also
hypometria relative to the targets lateral eccentricity,
particularly when these movements are combined with
convergence (Fig. 1E). The convergence component is
hypometric, only 9 of amplitude instead of the 15
required by the target in depth. In contrast, the divergence
component during combined movements is performed
accurately. Note the remarkable acceleration of divergence
when combined with the saccade (see Fig. 1F), and the
absence of a similar phenomenon for combined conver-
gence movements (Fig. 1E). Next we will present
quantitative data of the accuracy, of the duration and of
the mean velocity of all these types of eye movements.
Quantitative data
Pure movements
Figure 2 shows the gain (amplitude of the movement/
target-LED excursion), the duration and the mean velocity
for pure saccades (A), pure convergence (B) and pure
divergence (C).
All subjects perform accurate saccades, the gain ranging
between 0.85 and 1 and with a group mean value of 0.91
0.09. The duration of saccades is short, 100 ms; the
mean group value is 899 ms. The speed of saccades
measured by the mean velocity (amplitude of the move-
ment/duration) is quite similar over all subjects; it ranges
between 175 and 245 deg/s with a mean value of 209
29 deg/s. All these values are very similar to the mean
values observed in normal children of comparable age
reported by Yang and Kapoula (2004) and indicated in the
figure by horizontal lines on the group mean (gain: 0.91
0.09; duration: 8011 ms, mean velocity: 22011 deg/s).
Fig. 3 Mean gain (amplitude of the movement/target excursion), duration and mean velocity (amplitude of the movement/duration) of the
saccade (A) and of the convergence component (B) of combined movements. Other notations as in Fig. 2
In contrast, the accuracy of pure vergence movements is
poor and more variable between the subjects; the gain
ranges from 0.51 to 0.90 for convergence and from 0.40 to
0.90 for divergence movements. The mean group value is
0.730.15 and 0.670.21 for convergence and divergence
respectively and these values are significantly smaller than
the gain of pure saccades (F(1,7)=5.89, p<0.02, and F
(1,7)=5.76, p<0.03 respectively). Importantly, these gain
values are significantly lower (t-test, p<0.01) than those
observed in normal children (0.920.09 and 0.870.10, for
convergence and divergence, respectively) by Yang and
Kapoula (2004).
The mean duration of vergence movements is very long:
57396 ms for convergence (range 427700 ms) and 617
82 ms for divergence (range 472720 ms) and they are
not statistically different (F(1,7)=1.00, p<0.33); both
durations are significantly longer than the duration of
pure saccades (F(1,14)=200, p<0.00001 and F(1,14)=304,
p<0.00001 for convergence and divergence, respectively).
Duration of both convergence and divergence movements
is longer than those observed in normal children (304
61 ms and 47093 ms, respectively); moreover, only the
duration of convergence is significantly longer in our
subjects than in normals (t-test, p<0.01).
Consistently with the duration data, the speed of
convergence and divergence is variable over the subjects
(1428 deg/s for convergence and 1222 deg/s for
divergence movements respectively). The mean value is
209 deg/s for convergence and 176 deg/s for divergence
and they are not significantly different (F(1,7)=165,
p=0.21), while, in normals convergence is significantly
faster than divergence. With respect to the speed of
normals (467 deg/s and 265 deg/s for convergence and
divergence, respectively) the speed of convergence is

significantly slower (t-test, p<0.01), and that of divergence
tends toward significance (t-test, p<0.06).
In conclusion, subjects with vertigo perform normal
saccades. In contrast, vergence movements, particularly
convergence, are abnormal, with poor accuracy, long
duration and low speed.
Combined movements
Figure 3 shows the gain, the duration and the mean
velocity for both saccade (A) and convergence (B)
components of combined movements. The gain of the
saccade component is low (it ranges between 0.44 and
0.80) and the mean group value is 0.640.14; this gain is
significantly lower than that of pure saccades
(F(1,7)=18.91, p<0.0007). This gain is slightly lower than
that reported in normal children (0.800.12) by Yang and
Kapoula (2004) and not statistically different.
The mean duration of the saccade component of
movements combined with convergence is 9722 ms
(range 66131 ms) and the mean velocity is 14033 deg/s
(range 98200 deg/s); moreover, the speed of the saccade
component of combined movements is significantly lower
than that observed for pure saccades (F(1,7)=14.67,
p<0.0018). Both the duration and the mean velocity of
the saccade component of movements combined with
convergence even more slowly, and are not significantly
different to the values reported for normals by Yang and
Kapoula (duration: 8511 ms, and mean velocity: 164
15 deg/s). At least for this component, the dynamic
properties observed in normals during combined move-
ments seem to exist (that is, the saccade is slower when
combined with convergence than when done alone).
Fig. 4 Mean gain (amplitude of the movement/target excursion), duration and mean velocity (amplitude of the movement/duration) of the
saccade (A) and of the divergence component (B) of combined movements. Other notations as in Fig. 2
291
In contrast, the performance of the convergence com-
ponent of combined movements is highly different from
that in normals: indeed, the value of gain, duration and
mean velocity in subjects with vertigo is significantly
lower (t-test, p<0.01) than that of normal subjects (that is,
gain: 0.920.09, duration: 272100 ms; mean velocity: 50
8 deg/s). The gain of the convergence component ranges
between 0.40 and 0.84; the group mean value is only 0.57
0.17 and it is significantly smaller than that recorded for
pure convergence movements (F(1,7)=5.43, p<0.05). The
mean duration of convergence components of combined
movements is 496100 ms (range 298642 ms), and even
if it is shorter with respect to the duration of the
corresponding pure convergence movements it is not
statistically different (F(1,7)=2.47, p=0.13). The speed of
the convergence component of combined movements is 19
10 deg/s (the range is 929 deg/s). This value is not
significantly different to the speed of pure convergence
movements (F(1,7)=0.95, p=0.34). The absence of a
significant difference in the speed with respect to pure
movements suggests that during combined movements in
subjects with vertigo, differently to normals, the vergence
is not accelerated by the saccade.
Figure 4 shows the gain, the duration and the mean
velocity for both saccade (A) and divergence (B)
components of combined movements. Differently to
movements combined with convergence, the performance
of both the saccade and the divergence components of
combined movements is very similar to normals. The
mean group gain is 0.790.05 (it ranges between 0.70 and
0.89) and, as for normal subjects, the gain, when measured
at the offset of the primary saccade, is significantly lower
than that of pure saccades (F(1,7)=8.65, p<0.01). The
duration of these movements is 12514 ms (range 110
148 ms), very similar to that observed in normals (115
292

59 ms); and, as normals, it is significantly longer than
that of the corresponding pure saccades (F(1,7)=22.81,
p<0.0003). The speed of the saccadic components is 127
13 deg/s (range 101147 deg/s), and it is very similar to
that observed in normals (12211 deg/s). Moreover, the
mean velocity of the saccadic component of combined
movements is significantly slower than that of pure
saccades (F(1,7)=44.79, p<0.00001), suggesting that the
presence of the saccade-divergence interaction is similar to
that reported for normals (Collewijn et al. 1995) and for
adults and children (Yang and Kapoula 2004).
The gain of divergence during combined movements is
0.930.12, ranging between 0.71 and 1. Note that such a
gain value is significantly higher than that observed for
pure divergence (F(1,7)=6.69, p<0.02). The mean duration
of divergence components of combined movements is 573
107 ms (range 382720 ms), and this is shorter than the
duration of pure divergence, but not statistically different
to it (F(1,7)=1.09, p=0.31). The mean velocity of the
divergence component of combined movements is 26
8 deg/s (the range is between 21 and 34 deg/s), and this
value is significantly faster than that of pure divergence
movements (F(1,7)=12.70, p<0.003), suggesting once more
that the saccade-divergence dynamic interaction during
combined movements is reciprocal and normal.
In conclusion, combined movements for subjects with
vertigo show a normal reciprocal interaction between
saccade and divergence but unilateral interaction for
saccades combined with convergence, i.e., the saccade is
slowed by the convergence and convergence is not
accelerated by the saccade. The accuracy, the speed and
the duration of both saccade and divergence component of
combined movements is normal; in contrast the conver-
gence component is abnormally inaccurate and of low
speed.
Additional observations: effect of training
Figure 5 shows the mean value of the gain, of the duration
and of the mean velocity for the four subjects before and
after training for pure movementssaccades, convergence
and divergence(A), for saccades combined with con-
vergence (B) and for saccades combined with divergence
(C).
After training, an improvement of the gain can be
observed for all types of eye movements. The gain is
significantly higher than that measured before training for
pure saccades and pure convergence (F(1,3)=6.95, p<0.05
and F(1,3)=6.85, p<0.05, respectively). The gain increased
also for pure divergence; however, the change is not
statistically different (F(1,3)=2.87, p=0.14) from that
observed before training, maybe due to the subject
variability. Indeed, remember that subject S5 already had
a normal gain before training (see Fig. 2B). In contrast,
after training for both components of saccades combined
with convergence the gain increased significantly
(F(1,3)=20.88, p<0.0038 and F(1,3)=22.53, p<0.0032,
respectively).
Finally, the gain of the saccade component of move-
ments combined with divergence increases significantly
with respect to that recorded before training (F(1,3)=6.57,

Fig. 5 Group mean (on four

subjects) of the gain, duration
and mean velocity before and
after orthoptic vergence training
for pure movements (A: sac-
cades, convergence and diver-
gence), for saccades combined
with convergence (B) and for
saccades combined with diver-
gence (C). A significant before-
after training change is shown
by an asterisk. The horizontal
lines indicate the values re-
corded in normal subjects of
matched age (Yang and Kapoula
2004); crosses indicate a signif-
icant difference from normal
value

p<0.0427). In contrast, the mean value of the gain of the
divergence component increases only a small amount;
indeed, two of the four subjects examined performed quite
well with such types of movements already before
training. Furthermore, it is important to note that after
training the accuracy of all types of eye movement reaches
normal values (horizontal lines on the after training group
mean).
After training, the duration decreases for pure saccades
by a small amount (10 ms); vergence movements show a
larger decrease of the duration: 70 ms and 55 ms for
convergence and divergence, respectively. The duration of
the saccade components of movements combined with
convergence and divergence decreases very little (10
20 ms), while the decrease of duration of vergence
components is larger: about 100 ms for the convergence
component and 37 ms for the divergence component.
None of these changes, however, is significantly different.
Moreover, the duration of convergence pure as well as
combined remains significantly longer with respect to
normals (t-test, p<0.01).
The mean velocity after training increases for all types
of movements studied; however, such an increase is
statistically different only for the saccade component of
movements combined with convergence (F(1,3)=5.73,
p<0.05). Finally, it is important to observe that while the
mean velocity of the saccades and divergence (pure and
combined) recorded after training is not significantly
different from normal values, the velocity of the conver-
gence (pure or combined) in subjects with vertigo remains
abnormally low (t-test, p<0.01).
In conclusion, the major effect of training is a signif-
icant improvement of the accuracy of saccades and
convergence (pure or combined). In terms of speed,
however, the changes are less remarkable and convergence
remains abnormal.
Discussion
The main findings of this study are the following: (1)
children with vertigo perform normal saccades; in contrast,
vergence movements, particularly convergence, are ab-
normal in terms of accuracy, duration and speed; (2) the
reciprocal interaction between the saccades and the
vergence system normally present during combined
movements exists also in children with vertigo but only
for saccades combined with divergence; in contrast
saccades combined with convergence show deceleration
of the saccade by the convergence, but not acceleration of
the convergence by the saccade; (3) orthoptic vergence
training improves the accuracy of all types of eye
movements; the duration and the speed of such eye
movements does not change; furthermore, the duration and
the speed of convergence (pure and combined) remains
abnormal. Next we will discuss in more detail each of
these findings.
293
Saccades
The first finding of this study is that children with vertigo
and vergence abnormalities perform saccade eye move-
ments as normal subjects (Collewijn et al. 1988; Kapoula
and Robinson 1986; Yang and Kapoula 2004): the gain
measure approaches 1 for all subjects examined; as
normals, saccades undershoot the target and they are
followed by small corrective saccades. The duration and
the mean velocity of saccades are also similar to that
observed from studies examining a large population of
normal adults as well as in children of comparable age
(Fioravanti et al. 1995; Munoz et al. 1998; Yang and
Kapoula 2004). Indeed, Fioravanti et al. (1995) pointed
out that the accuracy and the duration of saccades in
children older than 8 years are similar to that of adults.
Moreover, Munoz et al. (1998) examined the metric and
the dynamic of saccades in a large population of normal
subjects whose age ranged between 5 and 79 years. They
found that saccades are accurate except for the youngest
children (58 years), who make hypometric saccades; the
duration is significantly longer only in older subjects and
the peak velocity did not change significantly across age.
Similarly, the study by Yang and Kapoula (2004) showed
that normal children (>8 years old) performed saccades as
normal adults. Our observations in children with vertigo
older than 8 years are in agreement with these studies.
Vergence
In contrast to saccades, vergence movements along the
median plane are severely impaired in our children. First,
we found that the accuracy of both convergence and
divergence is poor in these subjects relative to that
observed in normal adults (Zee et al. 1992; Collewijn et al.
1995), as well as in normal children of similar age and
adults using the same experimental condition in the study
of Yang and Kapoula (2004) beyond 0.90 for both
convergence and divergence. Moreover, the duration of
vergence movements, particularly convergence, is abnor-
mally long. Indeed, in our subjects, the duration of
convergence is significantly longer than that reported in
normals by Yang and Kapoula (2004), where a similar
amplitude of convergence was elicited. The mean velocity
of convergence is abnormally low, significantly lower than
that observed in normals by Yang and Kapoula (2004). We
suggest that such poor vergence accuracy could be caused
by a reduced ability of our subjects to localize the target in
depth correctly. This hypothesis is in agreement with the
clinical observations of Riddell et al. (1990). Indeed, these
authors observed that the performances in clinical tests
assessing spatial discrimination (a synoptophore based
vergence test, the Dunlop test) were significantly worse in
children with poor vergence control than in normals. We
believe that such impairment in the localization of the
target could cause difficulty in the preparation and in the
execution of vergence movements, leading to both abnor-
294
mal longer latency (as shown in our previous study, Bucci
et al. 2004) and inaccurate vergence movements.
On the other hand, in children with vertigo vergence
was abnormally slow with low velocity. This finding is
compatible with the hypothesis of dysfunction of the
cortical and/or subcortical circuitry that controls the
execution of such movements. Indeed, Mays (1984) and
Mays et al. (1996) found in the mesencephalic reticular
formation of monkeys, distinct convergence and diver-
gence burst neurons discharging in relation to vergence
velocity. More recently, Gamlin and Yoon (2000) and
Gamlin (2002) provided evidence that the activity of
neurons in the prearcuate area, close to the frontal eye field
of monkeys, was related to vergence dynamic. On the
basis of these studies, we suggest that the slowness of
vergence, particularly convergence observed in children
with vertigo, could have both a subcortical and a cortical
origin.
Combined saccade-vergence movements
Our subjects performed differently combined movements
according to the type of vergence, convergence or
divergence associated with saccades. The performance of
saccade components of movements combined with con-
vergence or divergence is similar to that observed in
normal children and adults; indeed, the accuracy, the
duration and the mean velocity of the saccade components
are in the normal range (Collewijn et al. 1995; Yang and
Kapoula 2004). Moreover, the finding of a significant
slowness of the saccade components with respect to the
corresponding pure saccades suggests that the known
interaction between the saccade and the vergence system
during combined movements reported by Collewijn et al.
(1995) is also present in children with vertigo.
The performance of the convergence and divergence
components is different; indeed, the divergence compo-
nent has normal accuracy, normal duration and normal
mean velocity; most importantly its mean velocity is
significantly higher than that of pure divergence. This
means that, in children with vertigo, the reciprocal
interaction between the saccade and the divergence system
during combined movements exists as in normals. In
contrast, the convergence components of combined move-
ments are abnormal in terms of accuracy, duration and
mean velocity. Furthermore, the convergence of combined
movements is not accelerated by the saccade as occurs in
normals; indeed, the mean velocity of the convergence
component in children with vertigo does not change with
respect to that of pure convergence movements.
Relatively little is known about the neuronal circuitry
controlling combined movements. Zee et al. (1992)
proposed a model in which combined eye movements
could be produced by a coactivation of the two distinct
oculomotor systems, that of the saccade and that of the
vergence. The omnipause neurons (OPN) could gate the
activity of a specific pool of neurons, the so-called
saccade-related-vergence bursters responsible for generat-
ing both saccade and vergence command. According to
these authors, slow vergence is not controlled by these
burst neurons. In line with this hypothesis, Chaturvedi and
van Gisbergen (2000) showed that the superior colliculus
(SC) via the OPN controls the saccade and the vergence
response during combined movements. Indeed, when the
target called for combined movement, electrical stimula-
tion of the rostral region of the superior colliculus of
monkeys inactivated the saccadic and the vergence system
in a different way: the saccade was completely stopped
while a residual slow vergence response persisted.
Chaturvedi and van Gisbergen (2000) suggested that the
neural circuit controlling the slow vergence command is
distinct from that of the fast vergence command activated
during combined movements. According to all these
studies, we suggest that the lack of acceleration of
convergence during combined movements in children
with vertigo could be due to impairment in the distinct
neural circuitry responsible for producing such fast
command. In other words, the behavioral deficit could
indicate the presence of a subtle specific deficiency in the
subcortical circuitry.
Effect of orthoptic vergence training
Orthoptic vergence training is widely used by clinicians
for improving vergence capabilities (von Noorden 2002);
however, only the study of van Leeuwen et al. (1999),
limited to one subject, reported objective measures on the
accuracy of vergence movements after orthoptic training.
The present study extends the study of van Leeuwen et
al. (1999), showing that not only vergence but also
saccades can improve after orthoptic training. Moreover,
our results show that after training only the accuracy of
different types of eye movements improves, reaching
normal values. Such a finding is compatible with the
hypothesis that training could reinforce the visual percep-
tion of the target in the natural space as showed by Fischer
and Hartnegg (2000). Indeed, these authors reported that a
daily training of visual tasks (saccades as well as fixation)
in dyslexic children improved both the ability in the
detection of the orientation of the target and the
performance of saccades (latency as well as the percentage
of errors decreased significantly). Furthermore, in our
previous study (Bucci et al. 2004) we observed after
training a decrease of the latency of eye movements, and
we suggested that visual attention mechanisms could
facilitate, after training, the initiation of eye movements. In
a similar way we suggest that attentional mechanisms
could also be responsible for a better target perception and
its localization in the natural space, leading to the
execution of more accurate eye movements.
Our results show also that the training does not improve
either the duration of eye movements or the mean velocity
of vergence, suggesting that there is no change in the
subcortical structures controlling the dynamics of these
movements. The significant slowness of convergence pure
and combined with saccades that persists even after

training suggests that children with vertigo have a specific
problem in the subcortical circuitry responsible for the
execution of such movements.
Consequences of vergence abnormalities on the VOR
adjustment
An important characteristic of the visual system is that
single vision is possible when the target is stable on the
retina. During rapid head movements, the VOR induces
compensatory eye movements allowing the stabilization of
the target of the retina. Several studies (see Leigh and Zee
1999 for review) have shown that the gain of the VOR is
modulated by the viewing distance and the vergence angle.
Snyder et al. (1992) reported that during vergence eye
movements the change in the gain of the VOR anticipates
the vergence, suggesting the possibility for predictive
control of vergence combined with the control of the VOR
system. Furthermore, Coenen (1998) suggested that the
cerebellum could prepare by learning a predictive ver-
gence signal for the VOR gain. On the basis of these
studies, we could assume that abnormalities of vergence
can lead to inappropriate VOR adjustment and thereby
poor gaze stabilization and thereby vertigo (Brandt 1999).
Our after training findings show a complete disappear-
ance of vertigo symptoms for all subjects; however, only
vergence accuracy improved significantly while its speed
did not change after training. According to these results we
can propose the hypothesis that the vergence signal for a
correct VOR adjustment is the final vergence angle rather
than the speed of vergence itself. However, further studies
combining VOR and vergence are needed.
Acknowledgements. This study was supported by INSERM
(contract no. 4M105E) and by Disfonctionnement Cognitif (MRT
Cognitique). Dr. M.P. Bucci was supported by EDF and FRM; Dr.
Q. Yang was supported by CNRS-K.C. WONG.
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