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ISSN: 0165-8107
DOI: 10.1080/01658100701501109
CASE REPORT
Z. Kapoula INTRODUCTION
Laboratoire de Physiologie de la Vertigo is a common symptom due to either peripheral or central vestibu-
Perception et de lAction lar dysfunction.7 However, some patients may lack typical signs of vestibular
(LPPA), IRIS Group, UMR 7152, dysfunction but still manifest vertigo symptoms. Anoh-Tanon et al.1 reported
CNRS-College de France, 11,
that about 5% of children consulting the ENT service for vertigo and headaches
place M. Berthelot, 75005,
had normal vestibular function; they suggested that vertigo in such cases can be
Paris, France
a symptom of ocular disorders. De Haller et al.7 also diagnosed visual vertigo
based on the history and clinical examination in 11 from 242 vertigo or dizzi-
Address correspondence to Dr. Qing
Yang, IRIS Group, LPPA, UMR 7152, ness patients (4.5%). The symptoms immediately improved either on cessation
CNRSCollege de France, 11, place M. of the visual input or upon closure of the eyes. They suggested that the visual
Berthelot, 75005, Paris, France. Tel:
(331) 44.27.16.36; E-mail:
vertigo could result from a mismatch between vestibular, proprioceptive and
yangqing165@hotmail.fr visual inputs (neuro-ophthalmological examination was normal in all cases).
93
In addition to vestibular eye movements, saccade in the control of eye movements have not been entirely
and vergence are important for exploration of 3D space matured and this conceals oculomotor abnormalities.
and for high quality 3D vision. Saccades are rapid However, for adults as cortical areas have been matured
eye movements during which both eyes rotate in the and the oculomotor plasticity has been accomplished,
same direction; vergence is the slow eye movement in their deficit of eye movements may be different from
opposite direction for the two eyes allowing to adjust children despite the similarity of vertigo symptoms.
the angle of visual axes according to the depth of the The main goal of this study is to explore whether
object of interest. Under natural conditions, most shifts similar deficits exist in adults with a complaint of ver-
of the line of sight are to objects that lie in different tigo but without vestibular abnormalities. First, latency,
direction and different depths. Such gaze shifts require accuracy and speed characteristics of different types of
a combination of a saccade and vergence movement. eye movements are compared within subjects to con-
The spatial and temporal characteristics of saccades and firm the differences known to exist in normal adults.
vergence movements are different, indicating different Secondly, for all the above mentioned parameters com-
control mechanisms albeit interacting. For example, parisons are made with values of the same types of
the latency of saccades is longer to near targets than to movements from control adult subjects of similar age
distant targets and the latency of convergence is longer studied in the same conditions by our group.25,26
than that of divergence; combined saccade-vergence
movements have longer latencies than pure saccades or METHODS
vergence movements such as required when the targets
are aligned along the median plane.19,24,26 Another im-
Patients
portant characteristic for combined saccade-vergence Six subjects, aged 2856 years old (means 40.5 11.8
movements is that the saccade component is slower years), 2 males and 4 females, were recruited presenting
(in speed) than the pure saccade while the vergence complaints of vertigo. All subjects were recruited in
component is faster than pure vergence.5,6,10,25,27 Stud- the hospital and underwent vestibular, ophthalmology
ies of the variety of naturally made eye movements and orthoptic examination. They were addressed to
in adults with vertigo symptoms are non-existent. In us because no vestibular dysfunction was found and
children with vertigo but normal vestibular function, the orthoptic examination revealed abnormalities
saccade and vergence eye movements have been (see Table 1). Vestibular testing was extensive for some
studied by Bucci et al.;3,4 they reported abnormally of the subjects including caloric test, canal and otolith
long latencies for saccades and vergence, particularly examination, off vertical axis rotation with a computer
for convergence, and for saccades combined with controlled rotating chair in the dark.2123 Conven-
convergence or divergence; reduced accuracy, long tional hearing tests (tonal and speech audiometric
duration and low speed for vergence relative to techniques) were also performed to examine the inner
normal children of matched age. Bucci et al.2 showed ear function. The common symptoms reported by
poor binocular coordination of saccades in children all these patients were severe headaches and vertigo,
with vertigo. often after prolonged computer use (5 of them were
Thus, there is evidence that pseudo-vestibular employed as secretaries). Subject S3 had orthoptic
syndrome, e.g. vertigo symptoms are associated with training several years ago, subject S2 had such training
abnormalities of saccades and mostly of vergence. recently and subject S5 started taking medication lectil
Bucci et al.3,4 proposed some mechanisms by which 16 (betahistine, against vertigo) a week before our
such abnormalities could interfere actually with the oculomotor testing. No other subject took medication.
optimal adjustment of VOR gain according to the All these subjects were regularly follow-up by the
viewing distance, thereby leading to incomplete visual ophthalmology service due to their persisting vergence
stabilization and thus to vertigo. Such hypothesis is in abnormalities. The investigation adhered to the tenets
line with electrophysiological and behavioral studies of the Declaration of Helsinki and was approved by
showing the modulation of VOR by viewing distance.16 the institutional human experimentation committee.
For children studied by Bucci et al.,3,4 cortical areas Informed consent was obtained from each subject after
such as the parietal cortex and the frontal lobe involved the nature of the procedure had been explained.
Q. Yang et al. 94
TABLE 1A Clinical characteristics of subjects
Subject Visual Stereoacuity NPC Heterophoria Divergence Convergence Main clinical
(years) acuity (TNO) (cm) (pD) (pD) pD materials
Visual Display called for a pure vergence eye movement, along the
median plane. When it was at the same circle it called
The visual display consisted of LEDs (each LED on
for a pure saccade (left or right), and when it was lateral
2.9 mm of diameter) placed at two isovergence circles:
and on the other circle the required eye movement was
one at 20 cm from the subject, and the other at 150 cm.
a combined saccade and vergence eye movement. Note
At each viewing distance three LEDs were used; one
that our use of saccades both to near and to distant
at the center and the other at 20 . At 20 cm, the
targets allowed us to keep target direction and depth
required mean vergence angle for fixating any of these
unpredictable for all trials. All target LEDs for saccades
three LEDs was 17 ; at 150 cm such angle was 2.3 .
were at 20 . All targets along the median plane required
a change in ocular vergence of 15 ; similarly, combined
Oculomotor Tasks movements required a saccade of 20 and a vergence of
In a dark room the subject was seated in an adapted- 15 . In each block, the three types of eye movements
chair with a head and chin support. He/she viewed were interleaved randomly. Each block contained 72
binocularly and faced the 3D visual display of the trials, i.e. 12 trials per type of movement, saccades to
LEDs. The distance between the subject and the close distant targets, saccades to near targets, convergence,
isovergence surface was at 20 cm. The visual display of divergence, combined convergent movements and
the LEDs was placed at eye level to avoid vertical eye combined divergent movements. For each subject, two
movements. blocks were run, separated by a rest of few minutes; cal-
Each trial started by lighting a fixation LED at the ibrations were repeated at the beginning of each block.
center of one of the circles (distant or close). After For calibration the subject made a sequence of sac-
a 1.5 s fixational period the central LED was turned cades to a LED target jumping from zero to 10 ,
off and a target-LED appeared for 1 s. When the 20 . During each of these trials, the target remained
target-LED was on the center of the other circle it at each location for 2 s; the subject was instructed to
TABLE 1B Normal values of near point of convergence (NPC), of heterophoria and of the range of divergence and convergence
amplitudes at far and close viewing distance measured in adults
Heterophoria
Stereoacuity NPC (cm) (Dp) Divergence (Dp) Convergence (Dp)
Q. Yang et al. 96
FIGURE 1 Examples of eye movements. (A) saccades (to left or to right); (B) vergence ( convergence or divergence); (C) combined
convergent movements (with saccades to left or to right); (D) combined divergent movements (with saccades to left or to right). On the
right side of each figure shown the excursion of the target. The arrows i and e indicate the onset and the end of eye movements,
respectively. Time at 0 ms indicates the target onset.
Q. Yang et al. 98
difference of latency for any components of combined divergent) and they are regrouped. The Wilcoxon test
eye movements between the two adult groups (all U > showed significantly higher mean velocity for conver-
25, p > 0.05). At the individual level, inspection of gence than for divergence (Z = 1.99, p < 0.05). To test
the data in Figure 2, shows that the above conclusion the saccade-vergence interaction, i.e. the well-known
applies for the majority of subjects except subject S5 acceleration of vergence by saccades in combined
who was taken a drug against vertigo. movements [24], we will compare pure vergence with
In summary, vertigo subjects have longer latencies vergence components of combined movements, pure
of the majority of eye movements than for controls. saccades with saccade components of combined move-
Because of such slowing the normal differences between ments. Contrary to what is known in controls [24],
types of movements appear less for the group of vertigo there was no significant difference of mean velocities
subjects. between vergence and vergence components of com-
Accuracy bined movements (Z = 0.31, p = 0.75 for convergence
and Z = 0.94, p = 0.35 for divergence). Similar to
Differences According to Type controls, adults with vertigo still showed significantly
of Movement higher mean velocities for pure saccades than saccade
Figure 3 presents individual and group mean gains components of combined movements (Z = 2.2, p <
(eye-movement amplitude/target amplitude) together 0.05). Thus, in subjects with vertigo the saccade did
with standard errors for pure movements (saccade or not accelerate vergence but it was itself slowed.
vergence, A) and combined movements (B) in adults
with vertigo. As there was no significant difference in Comparison with Normal Adults
the accuracy between saccades to distant targets and to The nonparametric U-Mann-Whitney test was used
near targets, nor between the two saccade components to compare mean velocities between adults with vertigo
of combined movements (convergent and divergent) and control adults (mean values indicated by horizontal
they were grouped. The Wilcoxon test showed that lines in Fig. 4). Relative to controls, adults with vertigo
the mean gain (saccade amplitude/target amplitude) of showed significantly lower mean velocities for conver-
saccade components of combined movements was sig- gence (U = 0, p < 0.001), for divergence (U = 14,
nificantly reduced relative to pure saccades (Z = 2.2, p < p < 0.05), and for convergence components (U =11,
0.05), but there was no difference between convergence p < 0.01) or divergence components (U = 0, p < 0.001)
and divergence (Z = 0.73, p = 0.46), nor between pure of combined movements. There was no statistically sig-
vergence and corresponding vergence components of nificant difference of mean velocity for pure saccades
combined eye movements (both Z < 0.73, p > 0.05). (U = 27, p = 0.16), for saccade components of com-
bined movements (U = 32, p = 0.31).
Comparison with Normal Adults
The nonparametric U-Mann-Whitney test showed
DISCUSSION
no significant difference of gains of any type of eye
movements between adults with vertigo and control To summarize, the data show that adults with vertigo
adults (All U > 27, p > 0.05). without abnormal vestibular function or other pathol-
ogy present abnormalities in their eye movements,
Mean Velocity mainly in their temporal-dynamics parameters (laten-
cies, speed). Two types of abnormalities are seen. Firstly,
Differences According to Type one does not observe several of the specific characteris-
of Movement tics of eye movements described previously in controls.
Figure 4 presents individual and group mean veloc- Vertigo adults show no longer latency for convergence
ities together with standard errors for pure movements than for divergence nor longer latency for correspond-
(saccades or vergence, A) and combined movements ing components of combined movements than for
(B) in adults with vertigo. There was no significant dif- pure movements (saccades or vergence); they show no
ference of mean velocities between saccades to distant higher speed for vergence combined with saccades than
targets and to near targets, nor between two saccade for vergence alone. Secondly, relative to values from
components of combined movements (convergent and control adults, they show longer latencies of saccades
to distant targets, for divergence and convergence vertigo a similar difference exists, and is even more ac-
(tendency), slower speed for convergence, divergence centuated than in control adults (63 vs 17 ms). Yang
and vergence components of combined movements. et al.24 considered that this difference between viewing
These findings will be discussed further next. distances could be due to facilitation of oculomotor
or attention disengagement at close. The same factors
Latency could explain the prolongation of latency for saccades
to distant targets in adults with vertigo. Relative to con-
Saccades to Distant-Near Targets trol adults, adults with vertigo showed longer latency
Latency of saccades is longer to distant targets than for saccades to distant targets but not for saccades to
to near targets in normal adults.24,26 For adults with near targets. It seems that initiating saccades to distant
targets is more difficult in adults with vertigo and the fa- vergence and divergence relative to control adults hide
cilitation of disengagement of oculomotor fixation and the difference; convergence tended to have longer la-
visual attention to near targets allow them to maintain tency than divergence but did not reach statistical sig-
normal behavior. nificance (252 vs 240 ms, Z = 0.73, p = 0.46). The
examination of individual data in this study showed
Convergence-Divergence that two vertigo subjects showed longer latency for di-
Control adults studied in same conditions showed vergence. The more solid result of clinical relevance
longer latency of convergence than of divergence.24 is the increase of latencies for both convergence and
Adults with vertigo showed no difference of latency divergence for adults with vertigo compared to con-
between convergence and divergence. A possible rea- trols. These results are compatible with the study in
son was that the increase of latencies for both con- children with vertigo,4 which also showed increased