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S CC D C EYE-MOVEMENTS OF

CHILDREN

WITH

CEREBRAL

PALSY

Mitsuko

Katayama

Laszlo

B .

Tamas

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 (Duckm an

1979).

Dyskinetic

m strabismus, with fluctuating esotropia

2 and exotropia, may be the first sign of

m-

cerebral palsy, and is present almost

r4

exclusively in this disorder (Buckley and

Seaber

1981).

A variety of other

abnormalities have been described, but

only Miyashita (1970) has attempted to

c

e make a quantitative assessment of

oculomotor function in this population,

though that was only a preliminary

2

communication.

It

has been suggested

that these disorders may retard the

s

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 co-

5

ordination fails a reading disability

E

results, whereas when eye-head-hand co-

z

ordination fails a writing disability

d

occurs.

A number of therapeutic approaches

36

have been used to try to improve these

m

I

2

P

*

skills, often without a precise knowledge

of the degree of integrity of the many co-

ordination 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 ord er to p erform 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.

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Th e children sat in a chair a t 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 th e 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 rando m ord er 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 electro-

oculography, 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), eye-

movements were recorded on magnetic

tap e, 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 qualita tive analysis of typ es 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 (under-

shooting), 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

mor e than one corrective saccade. Under-

shooting could occur on gazing to one or

p j^

both sides, with laterality showing no

clear relationship t o the type or side of th e

5

hildren's predominant motor involve-

ment. It tended to occur when targets s

were at the outer limits

of

the fields of

testing.

z

Reaction times

L

eaction times averaged 241ms over-all,

8

ith 209ms for targets up to 20 and

273ms for those between 20 and 40 .

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

(200

o 300ms) a t least

one-

third of the time, suggesting that poor

compliance or inattention ma y have been

the reason for the prolongation.

r

Again, no relationship emerged between

j

Saccade velocity

The mean over-all saccade velocity was

452 /second. Eight children's velocities

were less th an 400 /second an d 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, t o the right

in

one,

and to either side in only two cases. Fou r

children had saccade velocities under

300 /second. All five ch ildren with

strabismus and four of the five with

significant under-shooting also belonged

to the slow-saccade grou p.

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 qua ntif y

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

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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 cerebral-

palsied children.

Normal saccades are stereotyped

movements with predictable character-

istics (Fuchs

1971).

Between

5

and

15

saccades the eye accelerates rapidly and

then decelerates on to th e 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 t w o

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.

Th e 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) fou nd 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 n ormal children. Fully

50

per cent

of

our children had saccade

velocities less than 4 00 /second, which,

based on the above data. we interpret as

38 being pathologically slow. Furtheirnore,

three patients in this gro up 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

abnorma lities 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 t o on e 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.

tendency to move the right arm on

seeing the target could result in more

'associative' interference with movements

of th e eyes to the left, tho ugh this is highly

speculative.

Abnormal eye-movements may cause

particular problems for these children,

since ofte n their contr ol of head an d neck,

as well as other postural muscle groups

contributing t o gaze fixation,

is

also poor.

Festinger

(1971)

suggested that this may

lead to abn orm al 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

abnorm alities, 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 f o r publicat ion 21st March 1986

Acknowledgements

This study was supported by the Ottawa Crippled

Children s Treatment Center, and by the National

Research Council

of

Canada.

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Authors Appo intments

School of Medicine, Seatt le WA

98195.

Mitsuko Katayama, B.Sc. (O .T.), Ottawa Crippled

Chi ldrens Treatment Cent re, Ot tawa, Ontar io .

*Correspondence to second author at present address:

*Laszlo B. Tamas. M.D. , C.M., Depar tment of Biomed Inc., Suite

512,

Oxford Tower ,

10235-101st

Neurological Surgery, University

of

Washington St reet , Edm onton, Alber ta, Canad a

T6G 2L3.

SUMMARY

Oculomotor disorders are frequently observed in cerebral-palsied children, and are thought to contribute to

impairment of verbal as well as non-verbal skil ls. The authors present the first quanti tat ive analysis of

saccadic eye-movem ents of these children, choosing those with normal verbal

IQ

but evidence of a learning

disabil i ty. A majori ty showed various abnormalit ies of saccadic eye-movements and these should be taken

into account when evaluating and treating children with cerebral palsy.

R E S U M E

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 fo nctions verbales

ou

non verbales. Les auteurs presentent la premiere analyse

quanti tative d e mouvem ents oculaires saccades de ces enfants , choisissant ceux qui presentaient un

QI

verbal normal mais des troubles des apprentissages. Une majori te presentait des anomalies variees des

mouvements oculaires saccades ce qui devrait i t re pris en comp te dan s le diagnostic fonctionnnel et le

trai tement des enfants IMC.

Z U S A M M E N F A S S U N C

Sakkadische Augenbewegungen bei Kindern rnit Cerebralparese

Bei Kindern mit Cerebralparese werden haufig Oculomotoriusstorungen beobachtet und man nimmt an , da 8

diese fur die Beeintrachtigung der verbalen und non-verbalen Fahigkeiten mitverantwortl ich sind. Die

Autoren stellen die ersten Ergebnisse einer quantitativen Analyse sakkadischer Augenbewegungen bei diesen

Kindern vor. Sie haben dafi ir 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

Mo vim iento s oculares en sacudidas en n ifios 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 no verbales.

Los

autores presentan el pr imer

analisis cuantitativo de

10s

movimientos oculares en sacudidas en estos niflos, escogiento

10s

quen t ienen un

CI verbal normal, pero con evidencia de transtornos del aprendizaje. Una mayoria mostro diversas

anomal ias de este tip0 de sacudidas. las cuales deben ser tenidas en cuenta al evaluar

y

t ratar niflos con

paralisis cerebral.

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