SACCADI C EYE-MOVEMENTS OF

CHILDREN WITH CEREBRAL PALSY

Mitsuko Katayama
Laszlo B. Tamas

2
m

mr4
00
I-

5
e

,c

2!

2
is

*5
P,

._

.5
E4
9

z
d

36

Oculomotor disorders are frequently

observed in cerebral-palsied children and
in many children with so-called minimal
brain damage (Abercrombie 1960;
Abercrombie et al. 1963; Ayres 1972,
1976; DeQuiros 1976; Funk and
Anderson 1977; Troost et al. 1986). The
most frequently described abnormality is
strabismus, which occurs in 40 to 60 per
cent of cases (Duckman 1979). Dyskinetic
strabismus, with fluctuating esotropia
and exotropia, may be the first sign of
cerebral palsy, and is present almost
exclusively in this disorder (Buckley and
Seaber 1981). A variety of other
abnormalities have been described, but
only Miyashita (1970) has attempted to
make a quantitative assessment of
oculomotor function in this population,
though that was only a preliminary
communication. It has been suggested
that these disorders may retard the
development
of
specific
learning
processes (Ayres 1972, 1976; DeQuiros
1976; Troost el al. 1986). For example,
DeQuiros and Schrager (1978) suggested
that when head-vestibular-ocular coordination fails a reading disability
results, whereas when eye-head-hand coordination fails a writing disability
occurs.
A number of therapeutic approaches
have been used to try to improve these

skills, often without a precise knowledge

of the degree of integrity of the many coordination systems involved. Our study
quantitatively assessed one of these
systems-the oculomotor-by analysing
saccadic horizontal eye-movements of
children with cerebral palsy.

Method
Sixteen consecutive children with cerebral
palsy treated at the Ottawa Crippled
Childrens Treatment Center were
selected for study because of a learning
disability which affected reading or
writing skills. None had mental
impairment, as shown by a verbal IQ
above 85 on the Wechsler Intelligence
Scale. The learning disability was
diagnosed and evaluated by a team
including a pediatrician, a teacher, a
psychologist
and an occupational
therapist. These children were also
required to have at least fair head and
body control in order to perform the tests.
Seven girls and nine boys between six and
13 years of age were tested. Six had
spastic diplegia, six spastic quadraparesis
and four hemiparesis. Clinical evaluation
by an ophthalmologist showed that five
children had strabismus and two had
refractive errors requiring glasses,
without other oculomotor or visual
abnormalities.

The children sat in a chair at the center

of radius of a semicircular target-board
lm away. With their heads mechanically
fixed, they looked straight ahead until one
of 13 target lights appeared on the screen,
prompting them quickly to gaze at the
target. After the light disappeared they
looked straight ahead again until
subsequent targets appeared. The 13
targets occurred to either side of center
and up to 40" laterally, which is near the
upper limit of normal eye-movements.
Each trial consisted of activating 24
targets in random order over two minutes.
Target activation was by a silent switching
system so that no warning was given to
the child about time of target
illumination.
Eye-movements
were
measured
by
standard
electrooculography, using small silver-silver
chloride electrodes at the outer canthus of
each eye, with a ground electrode on the
forehead. After amplification and
filtering (bandpass: DC to looHZ), eyemovements were recorded on magnetic
tape, along with target onset and location,
and audio.
Data analysis was performed off-line
and included measures of reaction time
(target onset to eye-movement onset),
saccade duration (eye-movement onset to
next fixation) and saccade amplitude
(angular movement during first saccade),
as well as qualitative analysis of types and
numbers of saccades per target
illumination. Saccade velocity was
calculated for movements of 40".
As we anticipated, performance of the
testing sometimes was limited by a child's
lack of compliance. Of the 16 children
tested, however, only four required a
repeat test. This study was approved by
the Canadian National Research Council
Advisory Committee on research on
human subjects and parental approval
was obtained in all cases.

Results
Saccade accuracy
Five of the 16 children required two or
more corrective eye-movements before
successfully fixing on the target (undershooting), one of whom required up to
eight separate saccades. However, only
one child under-shot more than half of
the time. The remaining 1 1 children

achieved accurate target fixation with no

more than one corrective saccade. Undershooting could occur on gazing to one or
both sides, with laterality showing no
clear relationship to the type or side of the
children's predominant motor involvement. It tended to occur when targets
were at the outer limits of the fields of
testing.

Reaction times
Reaction times averaged 241ms over-all,
with 209ms for targets up to 20" and
273ms for those between 20 and 40".
Again, no relationship emerged between
reaction time for eye-movements to a
given side and the type or laterality of
motor involvement. Only two children
had average reaction times well above
300ms, and both of these were able to
perform eye-movements within a more
normal range (200to 300ms) at least onethird of the time, suggesting that poor
compliance or inattention may have been
the reason for the prolongation.

p(j^
r-

s5

3
L,

Saccade velocity
The mean over-all saccade velocity was
452"/second. Eight children's velocities
were less than 400"/second and this
subgroup had a mean velocity of
283"/second (range:170 to 379). Such
slow saccades were observed on looking
t o the left in five cases, to the right in one,
and to either side in only two cases. Four
children had saccade velocities under
300"/second. All five children with
strabismus and four of the five with
significant under-shooting also belonged
to the slow-saccade group.
Relationship with learning disability
Clinically the children with slower
saccadic eye-movements tended to have
poorer reading and writing skills, motor
achievement and visuo-spatial abilities,
and poorer learning capacity in these
spheres. This is our strong clinical
impression, but it is difficult to quantify
the type and extent of such learning
disabilities, particularly in children with
cerebral palsy.

Discussion
Children with cerebral palsy have
complex and multifaceted reading and

37

38

writing problems, even when they have

relatively little motor involvement. In
spite of this (or perhaps because of it),
there have been few investigations in this
field using a quantitative physiological
approach. This has led to difficulty in
establishing a rationale for various
therapeutic strategies. Our approach
therefore was to study a very specific
topic-horizontal saccades-in cerebralpalsied children.
Normal saccades are stereotyped
movements with predictable characteristics (Fuchs 1971). Between 5 " and 15"
saccades the eye accelerates rapidly and
then decelerates onto the target with little
or no error. In response to changes in
target position larger than 15", the eye
generally falls short of the target and
needs a second corrective saccade to
reduce the retinal error to zero. Robinson
(1964) found that it was very unusual for
there to be more than one corrective
saccade to achieve target fixation, while
Warabi et al. (1984) found that such
under-shooting occurred mainly in older
individuals. Five of our 16 children
required two or more eye-movements to
fixate on a target.
Reaction times increase with saccadic
magnitude, the average for 5" and 40"
saccades being 200 and 250ms,
respectively (Fuchs 1971, Morasso et al.
1973, Dell'Osso and Daroff 1974). Only
two children in our study showed
prolonged reaction times, and these
occurred inconsistently, so we may infer
that their reaction times to visual stimuli
probably are normal.
The velocity of saccadic eye-movements
cannot be controlled by voluntary effort,
though drowsiness may have an effect
(Fuchs 1971), so that in a fixed testing
situation, changes in velocity should
largely reflect biological factors. Warabi
et al. (1984) found the mean peak velocity
for 40" saccades in normal young people
to be 508"/second (SD 76), though the
youngest in their series was aged 16. Funk
and Anderson (1977) found a very similar
mean velocity of 535"/second (455 to 667)
in a small group of normal children. Fully
50 per cent of our children had saccade
velocities less than 400"/second, which,
based on the above data. we interpret as
being pathologically slow. Furtheirnore,

three patients in this group had no clinical

evidence of an oculomotor disorder, so
significant but subtle abnormalities may
exist in these children.
Anatomical localization of the lesion(s)
responsible
for these oculomotor
abnormalities is difficult, as shown by the
lack of correlation even between the side
of clinical motor involvement and the
abnormality of gaze. Since almost all
patients with slow saccades showed them
on looking only to one side, a suprabulbar
mechanism is suggested. The tendency to
slowing of eye-movements to the left
rather than to the right is puzzling, and
raises the possibility that the so-called
'associative reactions' ubiquitous to
cerebral-palsied children may play a rdle.
A tendency to move the right arm on
seeing the target could result in more
'associative' interference with movements
of the eyes to the left, though this is highly
speculative.
Abnormal eye-movements may cause
particular problems for these children,
since often their control of head and neck,
as well as other postural muscle groups
contributing to gaze fixation, is also poor.
Festinger (1971) suggested that this may
lead to abnormal visual perception, and
this was demonstrated experimentally by
Cohen (1963), who found that adaptation
to vision through a distorting prism by
normal subjects required full, normal
head- and neck-movements.
'

Conclusions
Children with cerebral palsy have a very
high
prevalence
of
oculomotor
abnormalities, which in some cases are
not detected by simple clinical testing.
These may contribute to learning
disorders, and their recognition may help
to understand better the physiological
basis of these disorders. This may be
particularly useful for those with lesser
degrees of disability, who therefore have
a greater rehabilitation potential, but for
whom there is a greater likelihood of
overlooking or misdiagnosing the deficit.
Accepted for publication 21st March 1986.
Acknowledgements

This study was supported by the Ottawa Crippled

Children's Treatment Center, and by the National
Research Council of Canada.

Authors Appointments
Mitsuko Katayama, B.Sc. (O.T.), Ottawa Crippled
Childrens Treatment Centre, Ottawa, Ontario.
*Laszlo B. Tamas. M.D., C.M., Department of
Neurological Surgery, University of Washington

School of Medicine, Seattle WA 98195.

*Correspondence to second author at present address:
Biomed Inc., Suite 512, Oxford Tower, 10235-101st
Street, Edmonton, Alberta, Canada T6G 2L3.

SUMMARY
Oculomotor disorders are frequently observed in cerebral-palsied children, and are thought t o contribute to
impairment of verbal as well as non-verbal skills. The authors present the first quantitative analysis of
saccadic eye-movements of these children, choosing those with normal verbal IQ but evidence of a learning
disability. A majority showed various abnormalities of saccadic eye-movements and these should be taken
into account when evaluating and treating children with cerebral palsy.
RESUME
Mouvernenls oculaires saccades des jeunes IMC
Les troubles oculo-moteurs sont frequemment observes chez les enfants IMC et sont consideres comme des
causes dalteration des fonctions verbales ou non verbales. Les auteurs presentent la premiere analyse
quantitative de mouvements oculaires saccades de ces enfants, choisissant ceux qui presentaient un QI
verbal normal mais des troubles des apprentissages. Une majorite presentait des anomalies variees des
mouvements oculaires saccades ce qui devrait itre pris en compte dans le diagnostic fonctionnnel et le
traitement des enfants IMC.

ZUSAMMENFASSUNC
Sakkadische Augenbewegungen bei Kindern rnit Cerebralparese
Bei Kindern mit Cerebralparese werden haufig Oculomotoriusstorungen beobachtet und man nimmt an, da8
diese fur die Beeintrachtigung der verbalen und non-verbalen Fahigkeiten mitverantwortlich sind. Die
Autoren stellen die ersten Ergebnisse einer quantitativen Analyse sakkadischer Augenbewegungen bei diesen
Kindern vor. Sie haben dafiir die Kinder mit normalem verbalem IQ aber mit Hinweis auf Lernprobleme
ausgewahlt. Ein GroBteil zeigte verschiedene Veranderungen der sakkadischen Augenbewegungen und diese
sollten bei der Beurteilung und Behandlung der Kinder mit Cerebralparese beriicksichtigt werden.
RESUMEN
Movimientos oculares en sacudidas en nifios con paralisis cerebral
En niflos con paralisis cerebral se observaron a menudo alteraciones oculomotoras y se Cree que
contribuyen a la alteracion de las habilidades verbales y n o verbales. Los autores presentan el primer
analisis cuantitativo de 10s movimientos oculares en sacudidas en estos niflos, escogiento 10s quen tienen un
CI verbal normal, pero con evidencia de transtornos del aprendizaje. Una mayoria mostro diversas
anomalias de este tip0 de sacudidas. las cuales deben ser tenidas en cuenta al evaluar y tratar niflos con
paralisis cerebral.
References
Abercrombie, M . L. J . (1960) Perception and eyemovements: some speculations on disorders in
cerebral palsy. Cerebral Palsy Bulletin, 2,
142-148.
- Davis, J . R., Shackel, B. (1963) Pilot study of
version movements of eyes in cerebral palsied and
other children. Vision Research, 3, 135-153.
Ayres, A. J . (1972) Sensory Integration and
Learning Disorders. Los Angeles: Western
Psychological Services.
- (1976) The Effect of Sensory Integrative
Therapy on Learning Disabled Children.
Pasadena, CA: Center for the Study of Sensory
Integrative Dysfunction.
Buckley, E., Seaber, J . H . (1981) Dyskinetic
strabismus as a sign of cerebral palsy. American
Journal of Ophthalmology, 91, 652-657.
Cohen, M. (1963) Visual curvature and feedback
factors in the production of prismatically induced
curved-line after-effect. Paper presented at the
Eastern Psychological Association Meeting, New
York.
DellOsso, L. F., Daroff, R. B. (1974) Functional
organization of the oculomotor system.
Aerospace Medicine, 45, 873-875.
DeQuiros, J . (1976) Diagnosis of vestibular
disorders in the learning disabled. Journal of
Learning Disabilities, 9, 39-47.
- Schrager, 0. L. (1978) Neuropsychological
Fundamentals in Learning Disabilities. San
Rafael, CA: Academic Therapy Publications.
Duckman, R . (1979) The incidence of visual

anomalies in a population of cerebral palsied

children. Journal of American Optometric
Association, 50, I01 3- 1016.
Festinger, L. (1971) Eye-movements and
perception. In Bach-Y-Rita, P., Collins, C. C .
(Eds.) The Control of Eye-Movements. New
York: Academic Press.
Fuchs, A. F. (1971) The saccadic system. In BachY-Rita, P., Collins, C. C. (Eds.) The Control of
Eye- Movements. New York: Academic Press, pp.
343-362.
Funk, C. J., Anderson, M. E. (1977) Saccadic eyemovements and eye-head coordination in
children. Perceptual and Motor Skills, 44,
5 99-6 I 0.
Miyashita, S. (1970) Studies on eye-movements of
cerebral palsy. Psychiatria et Neurologia
Japonica, 13, 221-240.
Morasso, P., Bizzi, E., Dichgans, J. (1973)
Adjustment of saccade characteristics during
head movements. Experimental Brain Research,
16, 492-500.
Robinson, D. A. (1964) The mechanics of human
saccadic eye-movement. Journal of Physiology,
114, 245-264.
Troost, B. T., Daroff, R. B., DellOsso, L. F. (1986)
Quantitative analysis of the oculomotor deficit in
progressive supranuclear palsy. (Submitted f o r
publication.)
Warabi, T., Kase, M., Kato, T. (1984) Effect of
aging on the accuracy of visually guided saccadic
eye-movement. Annals of Neurology, 16,
449-454.

39