Pilot study of version movements of eyes in cerebral palsied and other children

VisiwtrrRex. Vol. 3, pp. 135-153.

PILOT

Pcrgamon Press 1963. Printed in Great Britain

STUDY

IN CEREBRAL M.

OF VERSION PALSIED

MOVEMENTS AND

OTHER

L. J. ABERCROMBIE, J. R. DAVIS and

OF EYES CHILDREN

B. SHACKEL

Paediatric Research Unit, Guy’s Hospital Medical School, London, S.E. 1 and Psychological Research Laboratory, E.M.I. Electronics Ltd., Feltham, Middlesex (Received 3 I July 1962) eye movements were recorded during simple saccadic and pursuit movement tasks. The success in avowing the ocular tasks was scored objectively and the cerebral palsied children were at least 50 per cent worse than the “normals”. Performance level tended to be related to chronological age, and was strongly correlated with mental age. Performance on the saccadic task was well correlated with that on the pursuit task among the normal children, but the cerebral palsied children were less consistent and four were very discrepant. Some implications of the findings are discussed.

Abstract-The

RCum&-On a enregistm les mouvements oculaires durant des taches simples saccaddes et des mouvements de poursuite. La reussite de ces tlches oculaires Ctait mesuree objectivement et les enfants atteints de paralysie cerebrate Ctaient au moms 50 pour cent plus mauvais que les “normaux”. Le niveau de performance tendait ii. ttre relic a l’age reel, et presentait une forte correlation avec l’age mental. La performance de la t&he saccadte avait une bonne correlation avec celle de la t&he de poursuite parmi les enfants normaux, mais la coherence Ctait moindre chez les enfants paralyses et quatre d’entre eux Ctaient tms discordants. On discute certaines donnees qui sont impliqdes par ces resultats. Zusammenfassung-WLhrend der Darbietung von sprungartigen und gleitenden Bewegungsaufgaben wurden die Augenbewegungen aufgezeichnet. Der Erfolg bei der Durchfiihrung der Sehaufgabe wurde durch Auszlhlen objektiv festgehalten; die Kinder nut Hirnllhmung erwiesen sich als urn mindestens 50 Prozent schlechter als die normalen. Das Erftiliungsniveau neigtedahin, mit demchronologischen Alter zu korrelieren, und es war streng korreliert mit dem biologischen Alter. Bei den normalen Kindem war die Erfiillung der sprun~artigen Bewegungsaufgaben gut mit der der gleitenden ~wegungsaufgaben korreliert; die hirngel~hmten Kinder verheilten sich weniger gleichmassig und vier von ihnen verhielten sich sehr unterschiedlich. Einige Anwendungen der Entdeckungen werden diskutiert. INTRODUCTJON THIS exploratory study of version movements in children is part of an investigation of the relationship of ocular and perceptual disorders in cerebral palsy (ABERCROMBIE et al., 1962). It is well known that the incidence of disorder of eye movements, both of version and of vergence, is more frequent in cerebral palsied than in normal children, and it has been suggested (ABERCROMB’IE, 1960) that this may contribute to some of the disorders of perception known to occur in cerebral palsy. It was thought that, just as cerebral palsied children tend to be retarded in walking and other motor skills, they might also be retarded in attaining full development of control of version movements (even when there is no clinically obvious disorder such as paresis of upward gaze) and that such retardation might be related to the delayed development of perceptual skills. The aim of this study therefore was to explore the possibilities of recording version movements in cerebral palsied children (this as far as we know has not been reported hitherto), and to compare their performance in simple tasks with that of non-cerebral palsied children. 135

I36

M. L. J.

A~~~cR~MBI~, 1.

R.

DAVIS AND B. SHACKEL

Electra-oculography (MARC, 1951; SHACKEL, 1960. 1961) was chosen as the simplest method of recording to apply in a clinical situation while, at the same time, providing immediately available records of acceptable accuracy. Of particular importance was the fact that electro-oculography (EOG) only requires a flexible lead connecting the subject to the apparatus and does not necessarily require the subject’s head or body to stay rigidly still for long. With cerebral palsied children, and particularly the athetoid cases. rigid constraint for any length of time would be impossible: by using EOG, recordings with the head stationary, which are of course the easiest to analyse and interpret subsequently, can be made in short bursts when the child stays still, while leaving him completely free to move when he must do so. The work was done in a school for physically handicapped children. Records were taken of eye movements of 65 children between the ages of 6 and 16 years; of these 36 were braindamaged, 17 physically handicapped but not brain-damaged, and 12 were children from adjoining ordinary schools. The tasks were designed to give records of the primary types of horizontal version movements (saccadic and pursuit) and to minimize, as far as possible, the perceptual and intellectual content of the tasks. The tasks were given in ordinary lighting conditions (with white background for saccadic targets at an apparent luminance of 5 ft L., black background for pursuit target at 0.32 ft L., and targets at 0.5 and 2 ft L. respectively) and with lighted targets in darkness (target background at 0.02 ft L. and target lights at 500 ft L.), to see if eye movements are more precise in the latter conditions; if they were, methods for training eye movements might be indicated. Methods were devised for scoring quantitatively the performance in these simple tasks. A record was only scored if the movements and fixations shown on it could easily and clearly be related to the task done; if such self-consistency was absent, because of excessive random eye or body movement, the record was deemed unscoreable, although in fact it could often be interpreted with fair certainty. After analysing the results for the primary enquiry into differences between the subject groups, the relationships of the scores with chronologicai age, mental age, reading age and binocular efficiency were investigated. EXPERIMENTAL METHOD The aim of the project and the nature of the tasks was explained to the children with the co-operation of the teaching staff. The response of the children was excellent: only three of those invited to participate were too timid to do so. Several of the children said that they had enjoyed themselves and requests to be done again have been embarrassingly frequent. The main difficulty was in reducing head and body movements during the task. in almost all of the children the head was kept satisfactorily still by the child biting on a wooden tongue depressor, supported on a burette stand. In a few cases of children with excessive head movement (e.g. athetoids) the head was held by an adult. The younger children tended to move the whole head when following the target in saccadic and pursuit tasks, They also tended to vocalize assent to instructions and grunted as their eyes moved from dot to dot. In a few very zealous children the request to “stare at the light” resulted in their biting so vigorously on the bar or gripping the edge of the table so hard, in their attempts to co-operate, that the record was interfered with by movements other than those of the eyes. The time taken for recording, including the fixing of electrodes, was about half an hour. The experimental work in the school was completed in less than one month.

Pilot Study of Version Movements of Eyes

137

in Cerebral Palsiedand Other Children

Subjects

Records were taken from three main groups of children, cerebral palsied, physically handicapped controls and normal controls. The criteria used for classification of the physically handicapped children are given by ABERCROMBIE et af. (1962). Cerebral palsied children, Records were taken from 30 cerebral palsied children; there were nine others at the school, but no attempt was made to take records from them because of their excessive distractibility or body movements. The records of only 15 cerebral palsied children were scoreable, and of these the Saccades of one were not scoreable. The chronological age of the scoreable group was from 6.6 to 15.8 years (Fig. 1a) ; it included three athetoids, four spastic diplegics, one case of hydrocephalus with diplegia, five right hemiplegics and two left hemiplegics. Among the 15 unscoreable records, the chronotogi~l age range was 6.3 to 14-Oyears; there were three athetoids, seven spastic diplegics, three right hemiplegics, one case of hydrocephalus with diplegia, and one of hyperkinetic ataxia. These records were spoiled by head movements, by squint or by inattentiveness of the child, Six other brain-damaged, but not cerebral palsied, children were tested; three records were unscoreable and three were scored.

i

4

5

t&on

. . c.

,

6

7

. N, . . , . .,.

, 8

9

IO

Chronological

II

ogc - 8.4

,

,

,

,

,

,

12

I3

14

15

16

17

age,

Y-

vo

(a) FIG. 1 (a). Chronological

age distribution of the subjects. the subjects.

(b). Mental age distribution

of

Physically handicapped but not brain-damaged children (control group). These twelve children attended the same school as the cerebral palsied children, and they were selected as the “control” group on the grounds of having had the same kinds of limitatjon of bodily movement starting from birth or before the age of three years, as various kinds of cerebral palsied children are likely to have had (ABERCRONBIE et al., 1962). The age range was 6.2 to 16.2 years (Fig. I a), and the group included five cases of spinal muscular atrophy, five of post-poliomyelitis paralysis, one of talipes with rudimen~ry lower limbs and one of congenital lymphodoema in lower limb. All of these gave scoreable records, but in one case the Saccades score was lost by instrument fault. Five other non-brain-damaged physically handicapped, but not strictly controlled, children were tested; one record was rejected and four were scored.

138

M. L. J. ABE~cR~~~I~, J. R. DAVIS AND B.

SHACWL

Non-pi~~Vsically handicapped cizildren (normal group). These were chiidren from neighbouring primary and junior schools. Six were of chronological age between 6.2 and 6.3 and six between 10.3 and 11.1 years (see Fig. 1a). All of these gave scoreable records. Recording

A portable version was used of the apparatus which had been designed previously for laboratory work (SHACKEL et al.,1958). The rubber suction electrodes which had been previously developed (SHACKEL, 1958) were used throughout with their standard procedure; their performance was entirely satisfactory, despite the constant usage, and only two sets were expended on the whole study. Electrical contact was satisfactory despite the considerable movement and jerking imposed by some of the more handicapped cases. The skin drill (SHACKEL, 1959) was not used, in order to make the procedure as simple as possible; however, significant zero drifts did not occur in many cases, and re-tests were made when necessary. A~tllough an ordinary room was used at the school, no difficulties from electrical interference were experienced despite the presence of mains lighting. Tasks

The child sat at a table on which the targets were displayed at eye level. The tasks which lent themselves to quantitative scoring involved saccadic and pursuit movements. Saccudic movements. The eye movements involved in this task are analogous to those involved in reading. The task required the child to move its eyes from one point to another when the experimenter said “now the next one” at approximately 2 set intervals and moved her finger to point down the board directly to the next target spot. The target consisted of seven points in a horizontal row 72 in. long, exposed at 15 in. from the subject’s eyes, the interval (1.3 in.) between adjacent points subtending an angle of 5”, and the whole line an angle of 30”, to the eyes. The child was asked to fix on each point in turn to the end of the line, and then to go back to the beginning and repeat three times. This was done both from Ieft to right, (i.e. normal reading direction), and from right to left, in the three ways: {a) The target was a white card with a horizontal row of seven black dots, 0.1 in. diameter. The experimenter pointed to each dot in turn, asking the child to look at the dot indicated. (b) The target was a black board with seven holes O-3 in. diameter each containing a small electric light bulb. The lights were switched on in sequence by the experimenter, the room being lit in the normal way. The child was asked to look at each light as it appeared. (c) As (b), but with the room darkened. F~~~~~tmovements. This task requires the child to follow a moving target with the eyes and to hold fixation at a point when the moving target is hidden. The target was a toy electric train which moved out of a “tunnel” in a straight line into another “tunnel”, and travelled backwards and forwards. The distance between the tunnels was 25 in. and was traversed in 4 sec. The target was exposed at 34 in. distance from the subject’s eyes, the interval travelled subtending an angle of 40”. After the subject had been shown the engine doing several trips, a screen was raised in front so that only the fixation part at the funnel was visible; this was to minimize distraction and the possibility of the child changing his fixation to different parts of the engine. A white fixation mark was placed, at funnel height, on the edge of two side screens forming the “tunnel” at each end. Again three ways were used: (a) The child was asked to follow the “smoke” (white cotton wool on the funnel) with the eyes waiting at the entrance to the tunnel while the train was hidden.

FIG. 2 (a). A normal saccadic performance showing two runs from left to right, each with seven clearly defined fixations between the six progressive movements and the move back to the beginning of the line; very little movement on the vertical channel. Normal child C.A. 10.3, M.A. 12.4, mean score on saccadic task 8-8.

FIG. 2 (b). A poor saccadic performance showing one run from left to right and one from right to ieft. Fixation is not steady, and (as shown by the dot numbers) does not proceed regularly from one dot to the next. Normal child C.A. 10.8. M.A. 11%. mean score on saccadic task 15.7.

Frc. 3 (a>. A good pursuit performance showing smooth runs from one side to the other with steady fixation at the “tunnel” entrances: little movement on the vertical channel. Normal child C.A. JO-$, M.A. 1J-6, mean scores: Pursuit tsaccades) 0; Pursuit t”, T.0.T,) 451 per cent.

j; I

.:,,a,,

j ~ .i

FIG. 3 tb). A poor pursuit performance with irregular runs and unsteady fixation on the tunnels; large vertical movements shown on the vertical channel. Cerebral palsied child. C.A. 7.3, M.A. 5~4, mean scores: Pursuit (saccades) l-72, Pursuit (Y;,T.O.T.) 42.1 per cent.

Pilot Study of Version Movements of Eyes in Cerebral Palsied and Other Children

139

(b) The “smoke” was replaced by a small electric light carried on the funnel of the train, the room being normally lit. (c) As (b), but with room darkened. Other movements. Three other tasks involving compensatory movements and scanning and tracing lines were administered but did not give easily analysable results. (a) Compensatory movements. The target was a small electric lamp at a distance of 30 in. from the subject’s eyes. The child was asked to fix the target with his eyes while the head was turned from side to side on the neck, first by the examiner and then by the subject. Performance on this task was not analysed because it was impossible to interpret the records unless the head movements were made exactly as requested. There was great variation within individual records, because some children resisted the experimenter’s moving of the head or moved the head themselves erratically. (b) Scanning and tracing lines. Because some cerebral palsied children are known to have special difficulties in dealing with oblique lines, as in drawing a diamond, an attempt was made to study eye movements when looking at, and then tracing over, horizontal, vertical and oblique lines. The lines were about 5 in. long, and were presented as though the child was working at a desk. The request to “look at the line” was not well understood, and it was difficult to arrange for the child to draw comfortably with the head fixed. The task proved too difficult to standardize in the time available and was abandoned.

scoring

Scores were made from the record of the horizontal movements of the eyes, the vertical channel being used only to help to interpret the horizontal record. Records of good and bad performances on the two tasks are shown in Figs. 2 and 3. Succadic movements. A perfect saccadic pattern would consist of a step-like record, steady fixations being shown as horizontal lines, and horizontal movements of the eyes to a new fixation point being shown as vertical lines on the ink record. It was decided to use the number of movements as a performance score for the saccadic task, the minimum per run and back to starting point being 7. I-Iowever, due to physiologically-generated electrical “noise” and differences between individuals in their eyeball voltage, all vertical lines seen on the ink record may not be due to eye movements. Because such noise seldom exceeds the equivalent of one degree of eye movement, it was decided to score all movements of one degree or more, i.e. all vertical lines one-fifth or more of the height of the normal “steps” were counted. The record was checked and every movement from the first fixation on the first run to the zero point on the last run was counted. To obtain a score for the sub-test the total number of movements was divided by the number of runs. To obtain the final saccadic score used in the analysis, the sums of all the sub-test scores were summed and divided by the number of sub-tests. The perfect Saccades score would be seven.

Two scores were computed for the pursuit task: (a) “Pursuit (saccades)” was similar to that of saccadic ~rfo~an~ in being a measure of the number of movements away from the normal smooth pursuit curve (but not from fixation at the “tunnel”). This was calculated in exactly the same way as the saccadic score for both sub-test scores and final mean performance score. Pursuit movements.

M. L. J.

140

J. R.

ABERCROMBIE.

DAVIS

AND B. SHACKEL

(b) “Pursuit ( y. T .0 .T .)” was a measure of total time spent off the target (i.e. off both train and tunnel). As the chart recording speed was + in.,kec it was simple to measure this score on the record. The time away from target was expressed as a percentage of the total time spent on the sub-test. The final percentage time off target score for a subject was the mean sum of his scores for all sub-tests. With both pursuit scores the perfect score would be 0. RESULTS It should be noted that with all three scores measured, “Saccades”, “Pursuit (saccades)“, and “Pursuit (7; T.O.T.)“, the higher the score the worse is the performance. Group Diferences

From the plot of the individual scores for all subjects in Fig. 4 it is clear that the cerebral palsied group differs from the other two groups in all three measures. The differences between the mean values are shown in Table 1, and it will be noted that in every case the cerebral palsied group is si~ifi~ntly different from both other groups. It is also evident that the scores of the younger sub-group (N2) of six normal subjects tend to be worse than those of the older six (Nl); the difference is significant in the Pursuit (9, T.O.T.) measure. (These differences were examined for significance by the Mann-Whitney U test because the distributions were not all normal, and because some of the variance ratios were significant, a fact which may invalidate the customary I test.) The significant differences between the means are also shown in Table 1 as percentages of the smaller mean. The size of these differences between the cerebral palsied and the other groups is considerable, varying between 20 and 70 per cent; moreover, it should be remembered that the scores of the cerebral palsied group are probably curtailed in size because of the number of subjects whose records were unscoreabie and some of whose scores would have been very high. It is also noticeable in Fig. 4 that the scatter of the cerebral palsied group is greater, but the variance ratio (Table 1) is only significant with respect to the normal group in the Pursuit (% T.O.T.) case. The variance of the control group is also somewhat higher than the normal group, and significantly different from it in the latter case also. One might expect the greater variance in the two physically handicapped groups to be a result merely of the greater age range of our sample, but this can be seen not to be the chief explanation by inspecting Fig. 5 and considering only those plots from the other two groups which fall within the age limits of the normal group. TABLE

1.

GROUP

DIFFERENCES-MEANS,

Saccades K Diff. % Diff. 4*5t 40

C.P. minus Control C.P. minus Normal Normal minus Control Na minus NI Variance Ratios

2.0: 20 1.5 1.6 Not significant

PERCENTAGES,

VARIANCES

AND

SIGNIFICANCE

Pursuit t “, T.O.T.)

Pursuit (saccades)

K Diff. 0.4s*

% Diff. 60

x Diff. 8.9*

0.52* 70 0.04 0.26 Not significant

t P-O.01 :: P=O*ool * P=@O5 (Mean differences were. examined by the Mann-Whitney

7, DilT. 50

10.4’ 60 1.5 12.8t 120 C.P.>N* t. >.Nt

U test)

141

Pilot Study of Version Movements of Eyes in Cerebral Palsied and Other Children Chronological

Age

The distribution of the subjects with respect to chronological age is shown in Fig. 1 (a). The grouping of the normal subjects into two narrow bands, and the tendency for a bias towards the older end in the cerebral palsied group, should be noted. Pursuit

Saccodes ? number / line 0 IO 1

I

C

:: : .*. A

Pursuit %Time

2 number /run I 1

0

20 i

: .** . . . . . . l. . A

CP

(saccodes)

CP

l

: I.

l

CP

..:

NI

:.*

c ::

.*

.. .

l

. c .*..

:,

..

. : :

N

wt.

l

N2

N, A

. :

;

. . .. A Meon Mean

N2

.. score score

l

II Combined groups

III Verbal Mental Age Performance

Mental Age

::*

NI for each for each

. A

Individual subjecl subject group

(PRODWXW~~UEW) OF EYE MOVEMENT READING AGE (R.A.)AND WITH VERBAL

-0.38 -0.25 - 0.46

-0*06 -063t

-0*14 -0.51*

-0.34 - 0.873

-0.22 -044t

-0.20 -0*53t

-0.35* -0.63t

-040 -O-92$ -0.31 -O-83?

-0.32 -0m89t

-0.37 - 0,922 -_0.!9 -o”i9t

-0.32 -0.11 io.01

Control

CA. M.A. R.A.

Normal

C.A. M.A. R.A.

-O-77? -0*87$ - 0*69* -0.37 -044 - 0.43

Control -t Normal

C.A. M.A.

Cerebral palsied i- Control + Normal Cerebral palsied Control Cerebral palsied Control

C.A. M.A.

$ P=O*ool

Pursuit (saccades) -044 -0.36 O%IO - 0.57* -0.67* -0.26

Pursuit (% T.O.T.) -0.58* -0.46 + O-08 -0.70* - 0.84t - 0.30 -0.75t -@73? -0.67’

C.A. M.A. R.A.

t P=O*Ol

scores.

SCORES WITH CHRONOLOGICAL AND PERFORMANCE MENTAL AGE

Cerebral palsied

* P=O.O5

l

*A*:-

Saccades I Separate groups

.

l

:.

4. Individual and group average eye movement performance

TABLE 2. CORRELATIONS (c.A.),MENTAL (MA.) AND

.

A

A

t....

.

: .:.

l

A

:.

:

I

N . . . ..

A

.:

60 1

4

A

.:

FIG.

l

A

: .A:: A

N2

40 i

20 I

l

N’

off target/run

0

2 1

. .. . : .

(‘7~ T.O.T.)

-0.50 -0.76

142

M. L. J. ABERCROMBII’,

J. R. DAVIS

AND B. SHACKEI.

The correlations between eye nlovetl~ent scores and cIlronologica1 age for each group of subjects are given in the first part of Table 2. It should be mentioned that with these small groups of subjects the data, although a sample from a normal distribution. of course depart somewhat from normality of distribution when divided into the separate groups. The nonparametric Kendall T correlation method gives substantially the same results, in statistical significance, as the correlations given in Table 2. The product-moment correlation values are therefore given, as using more of the information in the data. but the conclusions drawn in this pilot study do not rely on the absolute size of these correlation coefficients. There is a tendency throughout for a relationship with age. and it is thought that the lack of statistical significance in four of the nine correlations results mainly from the small number of subjects tested. To illustrate this relationship, the plot of Pursuit ( Ot, T.O.T.) scores against chronologica1 age is shown in Fig. 5 with the regression lines of score upon age added for the three groups of subjects. Mental Age The cerebral palsied and control groups were tested with the WISC (Wechsler Intelligence Scale for Children) within six months of the eye movement testing, with the exception of three for whom data by the Stanford Binet Test, taken two years previously. were used. The &year-old normal children had been tested on the Moray House Picture intelligence Test and the 10-year-old ones on the Schondl Essential Intelligence Test. The mental ages were expressed as at the time of eye movement testing and are shown in Fig. I (b). The correlations of the eye movement scores with mental age for all three subject groups are shown in the first part of Table 2. Again there is a tendency for a relationship with age, which is illustrated also in Fig. 5 by the plots of Pursuit (‘1; T.O.T.) scores against mental age with regression lines added. The WISC test has two sections, one of which (the Verbal Scale) samples mainly comprehension and manipulation of words, i.e. language or verbal ability, and the other (the Performance Scale) tests logical manipulation of visual symbols and more general sensorimotor skill. It was thought that the latter section might show a closer relationship with eye movement performance than the Verbal Scale. But if anything, as is seen in the third part of Table 2. the Verbal Mental Age may show higher values, although the differences between the correlations on the two Scales are not here significant. Comparison of Relut~oi?s~li~swith Clrronoiogical and Mental Age It is interesting to compare the correlations of the eye movement scores with chronological and with mental age; these correlations were of course calculated on exactly the same groups of subjects in each case. It should first be noted from Fig. I (a) and (b) that, although the average chronological ages of the three groups ascend normals-colltrols-cerebrai palsied with nearly two years between each, the average mental ages of the groups run in the reverse order with less than a year successively between each. From the first part of Table 2 there appears to be little difference between the correlations of eye movement scores with chronological and mental age. Iiowever, when the control and normal groups are combined, there being no significant difference between them in their average eye movement scores, the correlations with chronological age are reduced and not significant. whereas the correlations with mental age are all significant and in one case slightly higher than before (Table 2, second part). Moreover, even when the widely scattered

143

Pilot Study of Version Movements of Eyes in Cerebral Palsied and Other Children

results of the cerebral palsied subjects are combined with the other two groups, the relationship between eye movement scores and mental age is stilt substantial, whereas the relationship with chronoiogical age remains a tendency. It therefore seems reasonable to conclude from the results of this pilot study, even though the number of subjects is small, that there may well be a relationship between the eye movement scores and chronological age and that there is a definite relationship between such scores and mental age. 7OP

50.

70

control

c’

T

Normal

r=-0.75’

60

60.

.\”

r

70

Cerebral P olS!Cd , = 0.5a*

.

40. :

30 -

b20.

0

l”,““~““J 4 6

B

MA,

IO

12

YlS

14

16

0

-(

4

6

8

M.A.,

10

YrS

I2

14

0

4

6

M.A.,

8

10

12

14

YfS

FIG. 5. Distribution of Pursuit (7: T.O.T.) scores by chronological age and by mental age separately for all three subject groups, with regression lines of eye movement score upon age.

Retzding Age As the saccadic task involves eye movements analogous to those used in reading, the relation of the scores to performance on the Schonell Graded Word Reading Test, which had been administered by the teachers at the schools, was examined. An interesting difference between the cerebral palsied and the other groups appeared from the correlation of eye movement scores against reading age. These correlations are shown in the first part of Table 2. Although only two of the six correlations for the control and normal groups are significant, there is nevertheless a general tendency in both these groups which might become significant in all correlations with a larger number of subjects. By contrast, the correlations in the cerebral palsied group are almost precisely 0, although the group was a little larger (fifteen instead of twelve subjects).

M.

144

I_.

J.

ABERCROMBIE,

J. R. DAVIS

AND B. SHACKEL

It might well be expected that any correlation with reading age would more likely imply or depend on a correlation with chronological or mental age. rather than a specific correlation between eye movement performance in the experimental tasks and eye movement performance in reading. However, the apparent difference between the subject groups, in the size of the correlations with chronological and mental age compared to those with reading age, does at least suggest that it might be worth exploring the matter further. Direction of movement

The Saccades and Pursuit (saccades) scores were analysed separately for the sections of the tasks when the subject’s eyes moved from left to right and from right to left (Fig. 6). No differences in performance were found among the normal children, but ten of the 15 3.0

7

9

II 13 i5

I7

I9

I-

21 23

R. to L. FIG. 5. Separate graphs of Saccades and Pursuit fsaccades), plotting scores from left to right direction of task against right to left direction for same subject.

R.

to L.

cerebral palsied children and seven of the 12 control children were better in the left to right direction on the pursuit task. This directional bias is statistically significant in the cerebra1 palsied group. Eight of the cerebral palsied, one of the control and four of the normal children wrote with the left hand ; there was no significant correlation with bias. It is also evident from Fig. 6 that the scatter of the data from the cerebral palsied group is greater than that of the other two groups in both tasks. This difference in variance is statistically significant but depends primarily upon four subjects, thus apparently indicating not a general trend but rather the need for further study of such individual cases. Of these four, three showed a strong bias on the Saccades task (Fig. 6a). The first (No. I), worse in right to left performance on both tasks, had a C.A. 7.3, M.A. 5.4, and was a case of hydrocephalus with diplegia. The second (No. 2), also worse in right to left on Saccades but with no bias on Pursuit, was C.A. 158, M.A. 15.2, athetoid. The third (No. 3) worse left to right on Saccades but worse right to left on Pursuit, was C.A. 9.3, M.A. 5.2, right hemiplegic possibly with field defect. The fourth (No. 4), unscoreable on Saccades but markedly worse right to left on Pursuit, was C.A. 9.2, M.A. 5.8, and right hemiplegic with left hemianopia. Light and Dark Conditions

Both the Saccades and the Pursuit tasks were in addition presented, with light sources as fixation points, in normal room lighting and in near darkness. Only a glimmer of fight was allowed to shine on to the pen recorder, for the experimenter’s convenience: for the subject, the fixation lights became by far the brightest part of the visual field. The aim was to examine

Pilot Study of Version Movements of Eyes in Cerebral Palsiedand Other Children

145

whether a phototropic reflex could thus be elicited and might serve to improve the eye movement performance of at least some subjects. If so, an hypothesis might be proposed that such a phototropic guide to assist eye fixation patterns might be a useful training method for infants and young children. Although it is well known that changing from light to near darkness will cause a marked change in the EOG potential level during the subsequent 5 to 20 min (e.g. MILES, 1940; ARDEN and KELSEY, 1962), our results here are not influenced by this fact. All the scores used in this study depend upon frequency and number of Saccades or upon smooth, conststent pursuit movements, not upon the absolute amplitude of such movements. The self-consistency of each record in relation to the task given to the subject was an added confirmation of the reliability of the technique and the scoring. It was when such consistency was absent that a subject’s record was classified unscoreable. The results from this part of the pilot study do not warrant any final conclusions, despite two individual cases which gave unscoreable records in light but tolerable records in dark. On the Saccades task, the combined control and normal groups show equal numbers of subjects doing the task better in the light and better in the dark respectively; in the cerebral palsied group nine did it better in the dark, five did it better in the light, and one gave the same performance in both conditions. However, this tendency toward better performance in the dark by the cerebral palsied group is not significant statistically. On the pursuit task the Pursuit ( 7; T.O.T.) score shows a tendency in favour of light in the control-normal group (eleven better in light, six no difference, seven better in dark), and significantly better performance in light by the cerebral palsied group (twelve better in light, no equals, two better in dark, one subject no dark scores available). It was thought that this difference might be related to whether the train target was visible or in the tunnel, and the Pursuit (saccades) scores, which had been taken separately from the original records for these two parts of the task, were examined. But there were no significant differences, and indeed the numbers giving better performance in light or dark were almost equal, except in the case of the combined control-normal group when the train was in the tunnel; in this part, fourteen were better in light, six no difference and four better in dark. Only tentative conclusions can be made. It would seem that the control and normal groups find little or no difference between light and dark conditions (except possibly for some slight difficulty in the dark when the train was in the tunnel during the pursuit task). It would seem that the cerebral palsied subjects may find some real differences between light and dark conditions, but the effects cannot be clearly resolved; on the Saccades task there was a tendency for better performance in the dark, but on the pursuit task the time off target performance was significantly worse in the dark. Thus it would appear that the form of the task and dark conditions which we arranged may possibly have caused some disorientation, at least initially, and did not elicit phototropic reflex fixations and an immediate improvement among the cerebral palsied subjects as a whole; on the other hand some improvement appears in individual cases, and the idea and method should perhaps not be regarded yet as entirely disproved. Performance

Consisteq

Our expectation was that the subjects’ performance would be consistent and of equivalent goodness on the two types of eye movement, Saccades and Pursuit, but that the performance of the cerebral palsied subjects might be more variable. To examine this, the scores on the Saccades task were tested for correlation with the Pursuit (saccades) and

M.

‘144 TABLE

L. J. ABERCROMBIE,J. R. DAW

3. CORRELATIONS(PR~D~cT-MoMENT)BETWEEN

AND B. SHACKEL

SACCAIXSANII P~~JJIT EYEMOVEMENTSCORES Saccades : Pursuit (s.)

A. Separate groups

Cerebral palsied Control Normal

-0.07 -0*73* 10.15

Saccades : Pursuit (:a, + 0.07 - 0.78.t - 0.39

3. Combined groups

Control +- Normal Cerebral palsied d- Control f Normal

:,0,53f

i- 0.63t

-1 @46t

t 0.50+

* P=O.OS

t P=O*Ol

Pursuit (s.): Pursuit ( :,;I ---0.86: t 0.92: i0.73t -- 0.88: O+!S:

: P-O.001

(7; T.O.T.) scores; the two Pursuit scores were also tested, and the results are shown in Table 3. As would be expected, the two Pursuit scores correlate highly. Also the Saccades scores for the control subjects and for the combined control and normal groups are clearly correlated with both of their Pursuit scores. But for the normal group by itself there appears to be only a non-significant tendency for a relationship, and for the cerebral palsied subjects the correlations are almost zero. Pursuit

I

I

I

#

G

iG

20

30

Pursuit

Time

1

I

40 aff

lorget.

50

1

J

60

70

%

FIG. 7. Plot of Saccades against Pursuit (“i, T.O.T.) scores for all subjects, with regression lines and +2 S.E. of Fit limits added from correlation using combined control and normal scores.

Pilot Study of Version Movements of Eyes in Cerebral Palsied and Other Children

147

The situation is made clearer by reference to Fig. 7. in which the Saccades scores are plotted against Pursuit (% T.O.T.) scores for all subjects, together with the two regression lines, from the correlation of the scores of the control and normal groups combined, and with the area contained by 32 Standard Errors of Fit of the regression lines to the data. The limit lines of this area indicate the limits of normal scatter; any scores lying outside these limits may be taken to indicate subjects with significant discrepancies between their performance on the two tasks. It thus becomes evident that the low correlation in the normal group is caused, not by any lack of consistency in the group as a whole (indeed the scatter is low), but by one significantly discrepant subject. Moreover his discrepancy consists mainly of a very poor Saccades score, which of course also causes the low Saccades: Pursuit (saccades) correlation of the group (as is confirmed by inspection of that correlogram). It is also evident, on the other hand, that the zero correlation in the cerebral palsied group is caused by a somewhat wider scatter of the scores together with two subjects being significantly discrepant in performance and two more on the borderline. Further it should be emphasized that these statistical limit lines are set by the correlation of the scores of the combined normal and controt groups, including the significantly discrepant normal subject. Had his score been omitted, the correlation would have been higher, the limits somewhat narrower, and more cerebral palsied scores would probably have been shown to be significantly discrepant together possibly with one control subject as well (the extra statistical work was not thought justified in a pilot study, since the essence of the situation is already established). In general, then, our expectation was confirmed, but we have also particularly learned that, while noting the significant tendency to inconsistency in the cerebral palsied group, we should direct attention to individual cases which show significantly large discrepancies and which may apparently occur in “normal” groups as well (cf. SHACKEL, 1960, p. 105).

Visual Acuity and Binocdar Funcfion A full ophthalmological examination had been made (ABERCR~MB~E etaf., 1962) of the eyes of the children at the physically handicapped school. Among the 12 physically handicapped controls, visual acuity (with glasses where used) was normal for near and distance in all except one whose acuity for distance was reduced to 6/18; this child achieved a very good performance in the saccadic task and perfect performance in the pursuit tasks. Binocular function was good with the exception of two children who had some convergence weakness; their EOG scores were within the normal range, after allowing for mental age. Among the 15 cerebral palsied children, visual acuity and binocular function were normal in nine; in the remaining six the following disorders occurred. (a) Afhefoid. Visual acuity for near reduced in right eye (Binocular N5; Right eye NS; Left eye N6; B.619, R.6/9, L.6/9); convergence weakness, paralysis of upward gaze. EOG performance in saccadic task fair, pursuit poor. (b) Left hemiplegic. Visual acuity for distance reduced (B.6/18, R.6/24, L.6/18); intermittent squint; difficulty in maintaining fixation; possibly field defect. EOG-very poor Pursuit (saccades) score, but normal in Saccades and Pursuit (% T.O.T.) scores. (c) Afhetoid. Visual acuity for distance reduced in left eye (B.6/5, R.616, L-6/18); left convergent squint; paralysis of upward gaze; slight bilateral restriction of abduction. EOG-very poor saccadic score, fair pursuit scores.

148

M. L. J. ABERCROMBIE, J. R. DAVIS

AND B. SHACK;CL

(d) Right hemiplegic. Visual acuity for distance reduced in right eye (B.616; R.6/ 13; L.6/9); intermittent squint; left hemianopia; difficulty in maintaining fixation. EOGsaccadic record unscoreable except when fixation targets were lights in darkened room. pursuit much better from left to right than right to left. (e) Right hemiplegic. Visual acuity and binocular function normal ; does not follow fixation towards left as easily as towards right; possibly field defect. EOG-all three mean scores within normal range, but the saccadic performance was considerably worse. and the pursuit performance considerably better, in left to right than in right to left direction. (f) Right ~ernjp~egjc. Moderate exophoria, saccadic score poor, pursuit scores good.

apparently

well compensated.

EOG-

Examination of the conditions of all the physically handicapped children whose records were scored (a total of 34, comprising, in addition to the main groups of 15 cerebral palsied and 12 physically handicapped controls, 3 brain-damaged but not cerebral palsied, and 4 physically handicapped but not in the strict control group), show that the relation between the efficiency of vergence and of version movements is not very close in this scoreable group. Binocular movements were normal in 21; convergence weakness was present in 7, heterophoria in 1, intermittent squint in 3 and constant squint in 2. Of the 5 children whose saccadic scores were notably poor, 1 had normal binocular movements, 1 heterophoria, 1 intermjttent squint and 2 constant squint. Of the 7 children whose pursuit score was poor, 2 had normal binocular movements, 3 some convergence weakness, 1 intermittent and 1 constant squint. None of the 5 squinting children made notably good EOG scores, though 2 with convergence weakness did. The relationship between the efficiency of version and vergence movements may bc closer than appears from this group, however, for among the 19 children who gave unscoreable records only 2 had good binocular function; 2 had convergence weakness, 2 heterophoria, 4 intermittent squint, and 9 constant squint. Uniocular Recording

The method of recording described above, in which one pair of elcctrodcs records the horizontal movements of both eyes, is unsuitable for cases in which normal fusion and binocular co-ordination are not maintained. From the point of view of learning to perceive it is possible that squint, and especially perhaps variable squint, is a considerable handicap for infants and young children, so preliminary studies were made of the movements of each eye separately. Smaller electrodes were made by having a +$-mm diameter, 3+-mm high, hollow cone with a hole at the peak turned out of nylon-loaded bakelite. A pure silver, mushroomheaded, relay contact (Johnson, Matthey and Co., type H2/212) with suitable lead wire attached was fastened inside the cone with Araldite adhesive, leaving only the mushrooill face exposed for cleaning and silver chloriding. About one-third of these electrodes had to be rejected after completion, for various faults, but enough remained with the necessary electrical stability and lack of drift voltage. They were attached, either with surgical adhesive tape or with balsa cement as was convenient, near the external canthi, as previously, and on the sides of the nose near the internal canthi, in all four positions as nearly as could be judged on the horizontal plane through the eyeball centres. Thus, the two pairs, one about each eye, conducted to the recording apparatus the horizontal component of movements of the left and right eye separately. Ideally a third recording channel at least is

FIG. 8. Uniocular recording of the horizontal movements of each eye separately during attempted Saccades task by subject with congenital heart disease, C.A. 10.5, M,A. 7.7 (normal record shows parallel traces from the two eyes). (a) Both eyes open, (b) left eye covered, (c)right eye covered.

[ fm-ingjmge148j

Pilot Study of Version Movements

of Eyes in Cerebral Palsied and Other Children

149

needed, to record vertical movements and check on eye closure, and would have been particularly helpful when studying in detail the records of Subject 14 (of which some examples are given in Fig. 8); but unfortunately a third channel was not available for these experiments. Recordings were taken from 11 children with intermittent or constant squint. Two of the recordings were too poor to be analysed; one showed good movement patterns in the right eye only (the left eye showed perception of light but no pattern vision) and three showed fairly good movement patterns with the eyes together most of the time; the remaining five showed poor or variable patterns, the eyes often diverging. For illustration, records from a child with congenital heart disease (C.A. 10.5, M.A. 7.7) are shown in Figs. 8a, b, c. On the Saccades task, with both eyes open there is little sign of effective performance (8a); the eyes drift apart, make parallel saccades for a time, suddenly appear to converge, probably when they are closed for about 3 set, and drift apart again (with lighted targets in the dark, there was better control of saccadic movements and better co-ordination). With one eye covered the eyes move parallel (8 b, c), and there appears a more consistent attempt at the Saccades task, but a marked nystagmus is manifest; where the left eye is covered, the fast phase is from left to right (8b) and when the right eye is covered it reverses (8c), thus illustrating a classic latent nystagmus. In the Pursuit task, there was similarly no clear pattern with both eyes open, though again binocular coordination and task performance was improved in the dark with the lighted target; latent nystagmus was again manifest, but the task was attempted with somewhat better success. DISCUSSION

Saccadic and pursuit version movements of the eyes made by children while doing simple standardized tasks have been satisfactorily recorded in field conditions. The records have been quantitatively scored, and the performance of three groups of children, cerebral palsied, controls (i.e. physically handicapped but not brain-damaged children), and normal children, has been compared on each of three scores. The two most important findings concern the difference between the cerebral palsied and control groups, and the general relation of performance with chronological and mental age. Some interesting points also arose about the relationship between performance on the different tasks. Diferences

between cerebral palsied and other children

The performance of cerebral palsied children was found to be about 50 per cent lower than that of control children and of normal school children. This estimate of proficiency, however, is based on the performance of the more efficient part of the school population of cerebral palsied children. Only half of the cerebral palsied children whose eye movements were recorded gave scoreable records, and there were nine others at the school from whom it was impossible to get records because of body movements or distractibility. It is likely, therefore, that this represents an underestimate of version movement disorder in cerebral palsy. As has been reported in many other respects, the cerebral palsied children were more variable in their performance of version movements than were the controls, both as between members of the group, and as between different aspects of individual performance. The greater scatter of cerebral palsied children’s scores is reflected in the lower correlations with chronological and mental age. A greater number of cerebral palsied children show

150

M. L. J. ABERCROMBIE, J. R. DAVIS AND B. SHACKCL

directional bias in performance, and disparities between performance in the two kinds of task, saccadic and pursuit, are commoner and larger among them. It is to be hoped that this technique. which easily gives precise quantified results of the performance achieved, may be useful for diagnostic and training purposes. Such a possibility is, of course, supported by the widespread use of EOG for routine nystagmography, and also by such findings, for instance, as the increased oculo-motor reaction time in dyslexic children of 7-8 years by comparison with normal children of the same age (LES~VRE et al., 1961). Correlation of performance with age The second interesting finding is that there is a tendency for a relationship of performance with age and particularly with mental age. The suggestion that the development of eye movement skill might be retarded in cerebral palsy, as is the development of other motor skills, such as sitting up or walking, receives support from this finding. That there should also be an improvement in skill in these very simple saccadic and pursuit movement tasks between the ages of 6 and 10 in normal school children is perhaps surprising. It is interesting to note, in this context, that LESBVRE ef al. (1961) have also reported an age correlation in another aspect of oculo-motor performance. In studying by EOG the oculo-motor reaction time to move to left or right or up or down through 20” to a new fixation light when illuminated, they found a similar correlation with chronological age between 6 and 10 years, in a group of 28 children between ages 6 and 15; the 9-to-15year-olds were equivalent to adults in this measure, although somewhat more variable in their scores. The fact that our correlations tend to be higher with mental age than with chronological age is especially interesting. This is consistent with views on the importance of eye movements in perceptual development (HEBB, 1949; PIACET and INHELDER, 1948) and of the reinforcing effect of veridical perception on perceptual learning (SOLLEY and MURPHY, 1960). It is reasonable to suppose that the more accurately a child can direct his eyes to a target, and the longer he can maintain fixation when required, the less will be the proportion of time that irrelevant images occupy the retina and particularly the fovea, and the quicker he will learn to perceive. By contrast, one would expect children with disorderly eye movements to be slowed down in learning. because they are working on “noisy channels”. An unexpected indication, however. was that eye movement performance may possibly be more highly correlated with mental age estimated from the WISC Verbal Scale than with that estimated from the Performance Scale. It had seemed reasonable to suppose that since the Performance Scale tests (among other things) visuomotor skills, it would be more highly correlated with the eye movement scores than would the Verbal Scale, but there is a However, this can only be regarded as tendency for the reverse in the control group. tentative and requiring confirmation, because in the cerebral palsied children the correlations are lower than in the controls, and variable, none reaching significant levels. The normal children had not been tested on the WISC, so they cannot be compared with the physically handicapped children in this respect. Moreover, it is worth noting that in another part of the study to which the current work also belongs, it has been found that disorders of vergence movements are correlated with lowered Performance Scales scores. Brain-damaged children tend to score lower on the Performance than on the Verbal Scales and the disparity is greater in squinting than in non-squinting brain-damaged children (ABERCROMBIE et al., 1962).

Pilot Study of Version Movements of Eyes in Cerebral Palsied and Other Children

151

~e~otions~ip between di~erent kinds of eye mo~~ements It had been expected that there would be consistency of performance in the two types Of version movements, saccadic and pursuit, and, while this was generally true in the control and normal groups, one normal child showed a considerable discrepancy. The lowered consistency that was found in the cerebral palsied children is in line with their general tendency to be variable on almost any parameter; but, in addition, there were two markedly discrepant children and two other borderline cases. This result would seem to suggest that, at least in some subjects of the cerebral palsied group, there may be some impairment which affects performance differently in the two tasks of Saccades and Pursuit. In view of the basic difference between the two types of task, and of the considerable measure of association between the performance level achieved on them by the normal and control groups, we are led to wonder whether these two tasks may be subserved by two, somewhat separate, sections of the oculo-motor system, either of which may be impaired independently in certain cases of cerebral palsy and perhaps occasionally in normal children. This would be consistent with the finding of RASHBASSand WESTHEIMER(1961) that saccadic and pursuit movements appear to be controlled by independent systems in adults. As to the relation of version and vergence movements, there is in the present work some evidence that efficiency in one is only partially related to efficiency in the other, some children whose vergence ‘movements are good having difficulty with version movements. Because a disproportionate number of children with squint gave unscoreable records, this point could not be adequately investigated. In any case the estimates of vergence movement efficiency were based on orthoptic reports, and not amenable to quantifi~tion. However, the indications, such as they are, point in the same direction as the finding of RASHBASSand WESTHEIMER(1961), based on an elegant new technique, that vergence and version movements are independent in adults. Indications for future research This study was prompted by the suggestion that some perceptual disorders of cerebral palsied children might be related to eye movement disorders and that in particular retardation of shape discrimination might be due to delayed acquisition of skill in controlling version movements. It has been shown that cerebral palsied children do indeed have poorer performance in these simple eye movement tasks than do children who are physically handicapped but not brain-damaged, and it remains to see whether these differences are correlated with differences of performance in simple perceptual tasks, holding chronological and mental age constant. Secondly, more intensive study of those children whose quality of ~rformance on different version movement tasks or aspects of them is disparate could be expected to throw light on the neurological basis of eye movement control. A considerable proportion (half in this school) of cerebral palsied children squint, and a more detailed study of their version movements with uniocular recording, on which some promising preliminary work was done, might be fruitful. Such studies must be related on the one hand to neurological and other medical data on individuals and on the other to normative data based on a study of considerable numbers of normal children over a wide age range. SUMMARY

1. Electra-oculographic records have been made of saccadic and pursuit eye movements of children 5 to 16 years old. The records of 12 normal, 15 cerebral palsied, and 12 physi~lly handicapped but not brain-damaged “control” children have been quanti~tively scored.

I52

M. L. J. ABERCROMBIE,J. R. DAVIS ANL) B. SHACKU

2. The performance of the 15 cerebral palsied children whose records were scoreabie was about 50 per cent worse than that of normals and controls; the records of another 15 were unscoreable because of squint, body movements or distractibility. 3. There was a tendency for performance to be related to chronological age, and a greater and more significant correlation with mental age. There was a tendency for a relationship with reading age on the control and normal groups, but not in the cerebral palsied. 4. The normal children showed no difference in performance when moving from left to right or right to left, but 10 of the 15 cerebral palsied children were better in the left to right direction on the pursuit task; in three cerebral palsied children the bias was very marked. Two cerebral palsied children showed strong bias in favour of left to right on the saccades task, and a third strong bias right to left. 5. Performance levels on the two tasks of Saccades and Pursuit were well correlated in the normal and control groups, apart from one exceptional normal and one discrepant control; but the cerebral palsied group was much less consistent and four of the subjects were very discrepant. 6. The significance of these ~ndi~lgs is discussed in relation to retardation of development in the cerebra1 palsied, to perceptuat learning, to the possibitity of separate functional sections of the oculo-motor system, and to indications for future study. Ackffowledge~ents-We are very grateful to the Middlesex County Council, and in particular to Dr. A. C. T. PERKINS, County Medical Officer of Health, Dr. A. ANDERSON, Area Medical Officer, and Mr. W. BENNETT,Borough Education Officer, for making it possible to work with some of their school children, To Dr. R. L. LINDON, Medical Officer, and to the late Mr. W. N. MOXROP, Headmaster, we owe a special debt of gratitude for extending to us the most friendly hospitality of Martindale School for the Physically Handi~p~, and we would like to thank them and the whole staff of the school and the children for their stimulating participation with the project. We are grateful also to Miss J. MANNING and Mr. D. A. SUCH, Heads of the neighbouring Primary and Junior Schools, and the children and their parents for their generous co-operation. The medical classification of the children was done by Dr. R. L. LINDON, M.R.C.S.. D.P.H., D.C.H.; theeyeexa~nationswe~madeby Mr. P. A.GARDINER, M.D..D.O.M.S.,and MissG. SOLOMON, D.B.O.; the WISC testing of four children was done by Mrs. J. M. WILLIAMS, M.A., and of the rest by Mrs. J. JONCKHEERE,B.A. Mr. S. HALLIWELL, B.Sc., helped us with the computing work. Professor 0. L. ZANGWILL, Drs. R. A. WEALE and C. RASHRASS,and Mr. H. NORRIS kindly read the manuscript and made many helpful suggestions. The project was sponsored by the Medical Advisory Committee of the National Spastics Society and WC would like to thankespecially Dr. R. MAC KEITH and Professor P. E. POLANI for their persona1 interest in it. REFERENCES ABERCROMBIE,M. L. J. (1960). Perception and eye movements: some speculations on disorders in cerebral palsy. Cereb. Palsy Bulletin 2, 142-l 48. ABERCROMBIE,M. L. J., GARDINER, P. A., JONCKHEERE, J., LINDOK, R. L. and SOLOMON, G. (1962). In preparation. ARDEN, G. B. and KELSEY,J. H. (1962). Changes produced by light in the standing potential of the human eye. J. Physiof., 161, 189-204. HEBB, D. 0. (1949). The Organisution off?eltacior. John Wiley. New York. LESBVRE, N., GABERSEK, V. and R~MOND, A. (1961). Les temps de r&action oculo-moteurs normaux et leur mesure E.O.G. Rev. neural. 104, 252-257. MARG, E. (1951). Development of El~tro-~ulography. Arch. Op~?thu~.,N. Y. 45, 169-185. MILES, W. R. (1940). M~ification of the human eye potential by dark and light adaptation. Science 91, PI A%: J and JNHELDER B. (1948). La Reprisentation de I’Espace chez I’enfbnt. English ed. 1956. Routledge and ‘K&an Paul, LonAon. RASHBASS,C. (1961). The relationship between sdccadic and smooth tracking eye movements. J. f’hysiol. 159,326-338.

Pilot Study of Version Movements of Eyes in Cerebral Palsied and Other Children

153

RASHBASS, C. and WESTHEIMER,G. (1961). Independence of conjugate and disjunctive eye movements. J. Physiol. 159, 361-364. SHACKEL, B. (1958). A rubber suction cup surface electrode with high electrical stability. J. uppl. Physiol. 13, 153-158. SHACKEL, B. (1959). Skin-drilling; a method of diminishing galvanic skin potentials. Amer. J. Psycho/. 72, 114-121. SHACKEL, B. (1960). Pilot study in Electra-oculography. Brir. J. Opkhal. 44, 89-113. SHACKEL, B. (1961). Electra-oculography: the electrical recording of eye position. Proc. III Intern. ConJ. Med. Electron., Part 3, pp. 323-335; Institution of Electrical Engineers, London. SHACKEL, B., SLOAN, R. C. and WARR, J. J. H. (1958). Detector plots eye movements. Elfctronics 31, No. 5, 3639.

SOLLEY, C. M. and MURPHY, G. (1960). Development of the Perceptual World. Basic Books, New York.