Child's Nerv Syst (1985) 1:115-122
Springer-Verlag 1985
Ocular motility, visual acuity and dysfunction of neuropsychological
impairment in children with shunted uncomplicated hydrocephalus*
Harriet K. Zeiner 1 . . , George P. Prigatano 2, Michael Pollay 2, Charles B. Biscoe 2 and Richard V. Smith 2
1 Section of Neuropsychology, Department of Neurosurgery, Presbyterian Hospital, N.E. 13th at Lincoln Boulevard, Oklahoma City,
OK 73104, USA
2 Department of Ophthalmology, University of Oklahoma Health Sciences Center, Oklahoma, USA
Abstract. Children with shunted, uncomplicated, com-
municating hydrocephalus were tested to determine (1)
the persistence of neuropsychological impairment and (2)
the relationship between neuropsychological functioning,
ocular motility, and acuity abnormalities. Eighteen hydro-
cephalic and 18 individually age- and sex-matched con-
trols were given a neuropsychological battery, repeated
after an interval of 1 year. Hydrocephalic children were
also tested at the beginning of the second year for
strabismus, amblyopia and visual acuity. Their medical
records were reviewed for history of ocular motility and/or
acuity abnormalities. Hydrocephalic children with normal
range IQ were found to have lower verbal IQ, memory,
and fine motor skills compared to controls. A history of
ocular motility and acuity abnormalities was associated
with impaired visuospatial and verbal problem-solving
skills.
Key words: Hydrocephalus - Neuropsychological func-
tioning - Visual acuity - Ocular motility - Cognitive im-
pairment.
Reports in the literature of psychometric and neuro-
psychological assessment of hydrocephalic children have
primarily been cross-sectional in nature [6, 12-15, 21]. Yet
it is clear from the literature on learning-disabled children
that patterns of neuropsychological difficulties may inter-
act with age and change over time as the child proceeds
through various neurodevelopmental stages [4]. These
cross-sectional psychometric and neuropsychological
studies emphasize that hydrocephalic children show a
predominance of failures on visuospatial and visuomotor
tests [12, 13, 15]. Several studies have reported, for exam-
ple, significantly lower performance Intelligence Quotient
* This research was supported by the National March of Dimes
Birth Defects Foundation, Social and Behavioral Sciences Re-
search Grant No. 12-57, and a grant from the Oklahoma Crip-
pled Children's Society
** To whom offprint requests should be addressed
mGN$
(performance IQ) scores in hydrocephalic children com-
pared to normal controls [1, 6, 14, 21]. Performance IQ is
heavily weighted with visuospatial and psychomotor tasks.
Dennis et al. [5] have attempted to explain the pres-
ence of visuospatial and visuomotor deficits in these
children on the basis of ocular abnormalities of acuity and
motility. The incidence of abnormalities of ocular motility
and acuity is known to be high in hydrocephalus [20].
Dennis etal. [5] have correlated a history of ocular
motility and acuity abnormalities in medical histories with
IQ in hydrocephalic children. They found that ocular
abnormalities in medical histories were associated with a
lower absolute level of nonverbal intelligence, i.e., perfor-
mance IQ. However, verbal IQ was not related to oculo-
motor disturbances in a heterogeneous group of hydro-
cephalic children. These authors suggested that ocular
acuity and motility disturbances possibly result in im-
paired development of the visual cortex and, consequently,
influence nonverbal intelligence in hydrocephalus because
of impaired visuospatial and visuomotor performance.
While it is an interesting hypothesis that ocular acuity and
motility abnormalities may underlie visuospatial and
visuomotor impairments in hydrocephalic children, the
evidence is limited to a correlation between performance
IQ and a medical history of ocular acuity abnormalities.
No data have been reported concerning broader neuro-
psychological status, nor have concomitant, or a history
of ocular motility and acuity abnormalities been reported
in these children.
We conducted a longitudinal neuropsychological study
of a homogeneous group of children with shunted, un-
complicated, communicating hydrocephalus. A previous
report of first-year findings disclosed visuospatial, visuo-
motor, verbal intelligence, and memory deficits in hydro-
cephalic children with (estimated) normal range IQ [10].
The hypothesis that ocular acuity and motility abnor-
malities underlay poor visuospatial and visuomotor per-
formance was reported between the first and second year
of our neuropsychological data collection [5]. This report
resulted in the addition of concurrent ocular motility and
acuity testing to the neuropsychological examination
during the second year of our research. Since detailed
116
m e d i c a l records were available o n all h y d r o c e p h a l i c sub-
jects, historical d a t a o n ocular f u n c t i o n i n g could also be
correlated with n e u r o p s y c h o l o g i c a l status. Finally, the
stability o f r e p o r t e d n e u r o p s y c h o l o g i c a l deficits in these
children could be checked since the same clinical group o f
children was serially tested.
The p u r p o s e o f the work p r e s e n t e d in this report was
therefore twofold: (1) to test the stability of previously
reported n e u r o p s y c h o l o g i c a l findings b y a 1-year follow-
up testing a n d (2) to investigate the relationship b e t w e e n
ocular motility a n d acuity d i s t u r b a n c e s a n d n e u r o p s y -
chological i m p a i r m e n t .
Materials and methods
Overview
Eighteen hydrocephalic children with shunted, uncomplicated,
communicating hydrocephalus and 18 age- and sex-matched
normal children were given a series of neuropsychological tests
twice, separated by a period of 1 year. Ocular motility and acuity
functions were also measured via the alternate cover test, the
cover-uncover test, the prism test for strabismus, and a visual
acuity test in the hydrocephalic group. This was at the beginning
of the second year of testing and therefore these tests took place
only on the second occasion. Medical histories of gaze, movement
and/or accommodation abnormalities were also reviewed for
analysis.
Su~ec~
Both an extensive description of the subject population and the
rationale for using homogeneous subgroups of hydrocephalic
children to assess cognitive impairment associated with hydro-
cephalus per se have been described elsewhere [10]. A brief
description of the subjects follows.
Hydrocephalic group
This was a group of 18 children with shunted, uncomplicated,
communicating hydrocephalus, the diagnosis being made by CT.
Ventricular size was essentially normal. The mean age was
6.2 years; standard deviation was 1.5 years, and the range was 4 to
11 years. Eleven were male; 7 female. Eleven were right-handed;
5 left-handed, and 2 were ambidextrous. All had either Block
Design or Vocabulary subtest scale scores of the WISC-R or
WPPSI in the normal or near normal range (i.e., a scale score of 7
or above).
Controls
Control subjects were 18 elementary school children, age- and
sex-matched with the hydrocephalic children. The mean age was
6.3 years; standard deviation 1.3 years (a range of 5 to 11 years).
Eleven were male; 7 female. Sixteen were right-handed; 2 were
ambidextrous. All had either a WISC-R or WPPSI Block Design
or Vocabulary subtest scale score in the normal range.
Neuropsychological assessment
All subjects received a 2-h battery of both verbal and visuospatial
neuropsychologieal tests. These were administered in the same
order, by the same experimenter, to each subject. The tests were
administered twice, with 1 year between the tests. The following
tests were chosen.
The Vocabulary subtest of the WISC-R (age 6.5 and above) or
WPPSI was given to estimate verbal intelligence [17]. The Block
Design subtest of the WISC-R or WPPSI was given to estimate
nonverbal reasoning skills [17, 18]. This was considered to be
representative of performance IQ.
Three tests of memory were given. The Fuld Object-Memory
Test [7] is a verbal recall task and allows initial recall and
consistency of recall over five trials to be assessed independently.
Two Benton Visual Retention tests were administered. The mul-
tiple choice form of the test assesses recognition memory for
visual-spatial material [2].
The Lafayette Grooved Pegboard Test was used as a measure
for both fine motor coordination and speed [9]. All rows were
used.
The Child's Trails Making Test, Parts A and B (intermediate
form), was given to assess more complex forms of visual-spatial
problem solving [11]. The first section of the test gives a baseline
measure of visual scanning and motor speed. Comparison of
Parts A and B were used to measure the individual's speed of in-
formation processing.
Academic reading skill was assessed with the Woodcock
Reading Mastery Test, Forms A and B [19]. The tests selected
sampled verbal reasoning skills, nonverbal reasoning skills, per-
ceptual motor skills, memory, free motor speed and coordination,
speed of information processing, and academic reading perfor-
mance.
Ocular assessment
Concomitant strabismus testing: For the second series, the fol-
lowing tests were used to assess presence or absence of concomi-
tant strabismus, a condition in which there is a deviation of the
eyes.
The cover test for heterotropias. The child was asked to fixate the
eyes on a distant target (6 m). Each eye was then alternately
covered with a visual occluder. If the eyes are straight (ortho-
phoria), the uncovered eye will not move. If strabismus is present
(heterotropia), the uncovered eye will move and will assume
fixation. The alternate cover test was then repeated with a near
target (33 cm).
Cover-uncover testfor heterophorias. The monocular cover-uncover
test detects deviations that are kept under control by fusion
mechanisms, as long as both eyes are open. However, when fusion
is disrupted by covering one eye, a deviation of the covered eye
occurs if a heterophoria is present. As in the cover test, each eye
was covered in turn, but the occluder was quickly removed, and
the examiner noted whether or not the eye under the cover
deviated and performed a fusional movement upon removal of
the cover. The cover-uncover test was performed on both eyes, at
both near and far fixation, with and without corrected vision.
Prism-cover test. The amount of strabismus present was measured
with graduated prisms. The apex of the prism was held towards
the direction of deviation (esotropia or esophoria is an inward
deviation; exotropia or exophoria is an outward deviation).
Successively increasing diopter prisms were applied until the un-
covered eye movement ceased. The amount of strabismus was
then noted, in prism diopters, for each eye. The prism-cover test
was repeated with a near (33 era) and far (6 m) target. Children
were tested with and without glasses [16].
Direction of gaze. Hydrocephalic children were asked to follow a
target and to look left, center, right, upward left, upward center,
upward right, downward left, downward center, downward right
1/m without moving their heads. The presence of strabismus was
then noted in each of these nine positions.

Acuity testing
Visual acuity was checked with a standard Snellen Eye Chart. A
visual acuity discrepancy of two or more lines between the eyes is
the diagnostic test for ambylopia (i.e., the image from one eye is
suppressed by the brain to reduce diplopia). If visual acuity in
one eye is functionally impaired or suppressed, no fixation
deviations will occur during the cover-uncover testing for strabis-
mus.
Past history of ocular abnormality
Medical records (available on all the hydrocephalic children) were
read for a history of ambylopia, esotropia or exotropia, visual
acuity discrepancies between eyes, and corrective lenses or
surgery for strabismus. Three of the children had been referred to
ophthalmologists, who provided medical records for these chil-
dren. Laterality of abnormalities in acuity, accommodation, and
gaze were noted. Excluded from the analyses were references to
the "setting-sun sign." This appearance of the eyes, with impair-
ment of conjugate upward gaze, is believed to be due to in-
creasing pressure on the midbrain or tectum, prior to surgical
shunting for hydrocephalus in infants. This phenomenon is
central in origin, disappears when intracranial pressure is relieved
by surgical treatment, and is not associated with long-standing
defects of gaze, accommodation, or acuity.
Informed consent, prior to participation in the study, was ob-
tained from all parents or legal guardians of the children who
were subjects. The nature of the procedure had been fully ex-
plained; procedures and consent forms were approved by the
Institutional Review Board of the University of Oklahoma Health
Sciences Center.
Results
Since the first-year neuropsychological results have been
described in detail elsewhere [10], a brief review of the
first-year findings will be presented to compare to second-
year results and to relate to ocular motility and acuity
functioning.
First-year neuropsychological results (summary)
Our previous paper documents the initial findings of
neuropsychological test performances in these children.
The basic findings were that hydrocephalic children had
lower Vocabulary scale scores compared to controls. They
did not differ from controls on the Block Design subtest
but did show a trend for poorer performance.
Memory functions, verbal recall, and visuospatial non-
verbal recall were impaired relative to normal controls.
Nonverbal visuospatial recognition m e m o r y was not im-
paired.
Hydrocephalic children suffered impaired speed of fine
motor performance in both right and left hands compared
to controls. This difference in time between dominant and
nondominant hands in the hydrocephalic group was not
significantly different from that between dominant and
nondominant hand times in the controls ( t = 1.37, dr= 18,
P = 0 . 1 9 ) [22]. The difference in pegs dropped (errors) be-
tween hands (dominant hand minus nondominant hand)
117
was not significantly different for hydrocephalic children
compared to controls (t = 0.747, df= 33, P = 0.46) [22].
Speed of information processing in hydrocephalic chil-
dren was impaired only when cognitive elements became
complex. On a task requiring scanning and motor speed
alone (Trails, Part A), no difference between groups was
observed. When a complex cognitive element was added
to the same task (Trails, Part B), hydrocephalic children
were slower and less accurate than controls.
Academic reading performance was in the normal
range - paired t-tests in a "within-group" comparison not
reported in the previous study [10].
Second-year neuropsychological results
Intellectual assessment. Table 1 summarizes the neuro-
psychological test performance of hydrocephalic children
and matched controls for the second assessment. Hydro-
cephalic children demonstrated significantly lower scale
scores on the Vocabulary subtest (t = 2.27, df= 21, P = 0.03)
and the Block Design subtest (t = 3.97, df= 28, P = 0.0005)
than did controls. Thus, there was evidence of impaired
verbal and performance skills in hydrocephalic children in
the 5 to 11 years of age range.
Paired t-tests, in a "within-group" comparison of
Vocabulary subtests and Block Design subtest scale scores,
revealed no significant difference between hydrocephalic
children for the first assessments (t = 1.0, P = 0.33), but sig-
nificantly higher Vocabulary than Block Design scale
scores for the second assessment (t=2.43, P=0.03).
Matched controls demonstrated significantly higher
Vocabulary than Block Design scale scores at the first tests
(t=2.25; P=0.02), but showed no discrepancy between
tests on the second occasion (t = 0.60, P = 0.56).
Memory function. Hydrocephafic children made sig-
nificantly more errors on the Benton Visual Retention Test
(graphomotor form, a measure of nonverbal memory)
than did controls (t = 2.26, df= 28, P = 0.03). Hydrocephalic
performance on the Fuld (verbal memory) and the Benton
Visual Retention Test (multiple choice form) improved to
within normal limits.
Fine motorpeJformance. Hydrocephalic children continued
to demonstrate significantly slower left-hand time on the
Lafayette Grooved Pegboard than did controls. Accuracy
with the left hand improved; there were no significant dif-
ferences in the n u m b e r of left-hand pegs dropped between
groups.
Hydrocephalic children showed a tendency to be
slower with the right hand than did controls, but this was
not significant ( t = 1.97, df= 14, P=0.07). The difference
between right-hand time and left-hand time was not sig-
nificant between groups (t=0.525, df= 15, P=0.61). The
absolute difference in time between hands was not sig-
nificantly different between groups (t=1.51, df=23,
P=0.14), nor was dominant hand minus nondominant
hand time significantly different between groups (t = 1.51,
118

Table 1. Neuropsychological assessment of second-year data

Test Hydrocephalic children First- and Controls First- and Probability

second-year second-year of between
N X SD differences N X SD differences groups t-test
WISC-R or WPPSI
Vocabulary subtest scale score 15 9.1 3.2 -0.2 15 11.2 1.7 - 0.4 0.03
Block Design subtest scale score 15 7.1 2.1 -0.6 15 10.8 3.0 - 1.6 0.0005
Fuld Object-Memory Evaluation
Sum of words recalled, Trial 1 15 7.3 1.4 -1.6 15 7.3 1.2 - 0.4 1.00
Sum of words recalled over 5 trials 15 38.2 5.6 -7.1 15 40.9 3.8 - 1.7 0.12
Benton Visual Retention Test
Multiple choice form: number correct 15 7.3 2.7 -1.9 15 8.0 2.7 - 1.6 0.49
Graphomotor form (D): number correct 15 5.7 13.7 --4.1 15 4.1 2.4 - 1.1 0.66
number errors 15 13.9 6.1 3.9 15 9.5 4.7 2.4 0.03
Lafayette Grooved Pegboard
Right hand
Time (in seconds) 15 133.1 105.0 16.8 15 79.3 11.7 16.1 0.07
Pegs dropped 15 1.3 1.6 -0.6 15 0.6 0.7 - 0.2 0.15
Left hand
Time (in seconds) 15 131.7 50.0 53.3 15 89.8 13.2 20.4 0.006
Pegs dropped 15 0.7 0.9 0.8 15 0.9 1.3 0.3 0.62
Total time (both hands) 15 264.0 145.8 70.9 15 169.1 21.6 36.5 0.02
Child's Trails Making Test
(Intermediate form)
Part A:
Time (in seconds) 15 41.6 20.1 8.7 15 26.1 12.8 12.7 0.02
Errors 15 0.5 0.8 0.4 15 0.1 0.5 0.1 0.19
Part B:
Time (in seconds) 13 100.2 59.4 37.9 15 59.1 29.0 23.5 0.04
Errors 13 2.2 3.6 1.2 15 0.7 1.3 0.4 0.18
Woodcock Reading Mastery Test, Form B
Total reading percentile 12 50.8 27.1 -8.7 14 80.1 22.0 -14.9 0.006

d f = 2 7 , P = 0 . 2 5 ) . The n u m b e r o f errors m a d e between Hydrocephalic scores on all o f the reading subtests

hands (right h a n d minus left hand) was also not sig-
nificantly different between groups ( t = l . 3 1 , d f = 2 7 ,
P = 0 . 2 0 ) . F o r hydrocephalic children, fine m o t o r co-
ordination continued to be i m p a i r e d during the second
year.
Speed of information processing. Hydrocephalic children
were significantly slower than controls on Part A o f the
Trails Test (t=2.52, d f = 2 8 , P = 0 . 0 2 ) . They were also sig-
nificantly slower than controls on Part B ( t = 2.27, df= 16,
P = 0 . 0 4 ) . They did not m a k e more errors than controls.
This appears to represent an i m p r o v e m e n t in the accuracy
o f information processing, but not speed, for hydro-
cephalic children.
Academic reading performance. Hydrocephalie children
significantly differed from controls in total reading
percentile on the Woodcock Reading Test, F o r m B
( t = 3.04, df= 24, P = 0 . 0 0 6 ) . However, this difference was
due to the above-average reading percentile o f the control
children. The hydrocephalic childrens' m e a n was the 50th
percentile, representing average reading skill.
were at the 50th percentile, with the exception of reading
analogies. The hydrocephalic m e a n for the analogies was
32.8 percentile, considerably below average.
One-year, two-year comparisons
A two-way analysis o f variance with r e p e a t e d measures
(group x years x test scores) revealed that both groups im-
proved on the following tests in the second year: F u l d
M e m o r y Test (sum o f words recalled on trial 1, trial 5, over
5 trials and consistency o f recall on trial 1 and over 5
trials); Benton Visual Retention Test, multiple choice form
( n u m b e r correct increased, p e r i p h e r a l errors and m a j o r
distortion errors decreased); Benton Visual Retention Test,
g r a p h o m o t o r form ( n u m b e r correct increased, total num-
ber of errors, ommission errors, perseveration errors and
right side o f design errors decreased). F o r the Benton
Visual Retention Test, g r a p h o m o t o r form, distortion errors,
rotation errors and left side of design errors did not
significantly improve in the second year.
 119

Neuropsychological status and intelligence Table 2. Hydrocephalic neuropsychological impairment

Impairment
Since the groups differed on Vocabulary subtest scale
scores the first year and both Vocabulary and Block Year 1 Year 2
Design scale scores the second year, a multivariant
analysis ofcovariance was applied to partial-out the effects Verbally oriented tests
of IQ, that is, to determine if differences in (estimated) IQ Vocabulary Yes Yes
could account for the differences in neuropsychological Woodcock No No
test performance between groups. Vocabulary scale scores Fuld Yes No
were then used separately as the covariate (groupsx test Visuospatially oriented tests
scores), and then Block Design scale scores were used as Block Design No Yes
the covariate (groups test scores). Benton Visual Retention: graphomotor Yes No
Benton Visual Retention: multiple choice No No
With Vocabulary as the covariate, no neuropsy- Lafayette Grooved Pegboard
chological test revealed significant differences (P--0.05) Right hand Yes No
between groups in either the first or second year. With Left hand Yes Yes
Block Design as the covariate, the following significant Mixed tests
differences between groups were obtained: Trails, Part A
Speed No Yes
Accuracy No No
Firstyear. The Benton Visual Retention Test, graphomotor
Trails, Part B
form number of errors (F=3.87, P=0.05), the Lafayette Speed Yes Yes
Grooved Pegboard combined times (both hands) (F---7.13, Accuracy Yes No
P=0.01) and left-hand time (F=4.75, P=0.03) were sig-
nificantly greater in hydrocephalic children. Nonverbal
recall memory and speed of fine-motor coordination in a
visual-spatial task were poorer for hydrocephalics than
could be accounted for by their lower intellectual abilities
or compared to controls.
Conclusions drawn from neuropsychological data

Second .year. Hydrocephalic children were significantly
slower in left-hand time on the Lafayette Grooved Peg-
board (F=5.67, P=0.02) and on the Trails Test, PartB
(F=5.61, P=0.03) compared to controls. Hydrocephalic
children tended to make more errors on Part B of the
Trails Test, but this failed to reach statistical significance
(F=3.47, P=0.07). Fine motor speed and speed of in-
formation processing on a visuospatial task were slower in
hydrocephalic children than could be accounted for by
their lower intellectual abilities compared to controls.
Neuropsychological analysis by content
To determine if hydrocephalic children demonstrated any
evidence of a material-specific dysfunction, the neuro-
psychological tests were categorized as (1) heavily verbally
oriented (Vocabulary subtest, Woodcock Reading Mastery
Test, Fuld Object Memory Test; (2) heavily performance
(i.e., visuospatially) oriented (Block Design subtest;
Benton Visual Retention Test; graphomotor and multiple
choice forms; the Lafayette Grooved Pegboard); or (3)
mixed i.e., combining both verbal and performance
elements (Trails Making Test, Parts A and B).
Table 2 demonstrates that hydrocephalic children per-
formed equally poorly in all three categories of tests both
years. Their impairments were not limited to visuospatially
oriented material. Verbal performance was equally im-
paired in both years of the study.
Stability of deficits: Hydrocephalic children with normal
range (estimated) IQ, and no other brain anomaly, had
lower (estimated) Verbal IQ scores the first year and lower
Verbal and performance IQ scores the second year, com-
pared to age and sex-matched controls. This is in contrast to
reports in the literature of lowered performance IQ relative
to verbal IQ obtained for populations of hydrocephalic
children with multiple brain problems.
Several subtle neuropsychological deficits occurred in
the presence of normal range (estimated) IQ. Normal IQ
does not equal normal neuropsychological status. Memory
functions, both verbal and nonverbal (visuospatial) recall,
were impaired in these hydrocephalic children when com-
pared with normal controls for the first year. Nonverbal
(visuospatial) recognition memory was not impaired. The
second year nonverbal memory deficits did recur. This
could be accounted for by the lower IQ of the hydrocephalic
children compared to controls. Hydrocephalic children had
impaired speed of fine motor performance in both hands
the first year and only in the left hand the second year (of
testing). At the first assessment, speed of information
processing in hydrocephalic children was impaired only
when cognitive elements became complex (Trails, Part B)
compared to controls. In the second year, the hydro-
cephalic children were slower in motor function than con-
trols in speed of information processing, but did not differ
in accuracy from controls. Academic reading performance
was in the normal range. Hydrocephalus, per se, was not
associated with a reading disability in either year.
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Ocular results
Current strabismus testing. Only 3 of the 18 hydrocephalic
children (16%) had strabismus during the second year of
the study. All ocular-motility abnormalities were right eye
esophorias, that is, the children's eyes appeared straight
when not tested, but the alternate cover-uncover test
revealed a latent inward deviation of the fight eye (12 in
one child, 6 in the second). The third demonstrated an
intermittent esophoria which could not be consistently
measured. Fifteen hydrocephalic children showed no
strabismus with either near or far fixation, with or without
corrective glasses.
Past history. Eight of the 15 children had a history of
strabismus: 53% of the sample. Of these 8, 1 had exotropia
and 7 esotropia. Three underwent corrective surgery. Four
received corrective glasses. None had a record of third or
fourth nerve dysfunction or sixth nerve palsy. Table 3
summarizes the strabismus findings. In addition to strabis-
mus, 2 of the children also had a history of ambylopia, for
which they underwent alternate occlusion therapy. Two of
the children with strabismus also had gaze impairment
(upward) when the eyes were tested jointly (versions), but
no restriction of gaze when the eyes were tested separately
(ductions).
Current acuity testing. None of the 15 children showed a
discrepancy of two or more lines on the Snellen Chart
between right and left eyes. Hence, neither ambylopia nor
functional blindness in one eye could be diagnosed. Six of
the children had corrected vision. When tested for visual
acuity (with corrected vision), all children demonstrated
normal visual acuity.
Direction of gaze. None of the hydrocephalic children
demonstrated current impaired movement of conjugate
gaze (versions or ductions) in any direction. The 3 cases of
current strabismus occurred in the central plane of fixation
only.
Neuropsychological functioning and ocular assessment
To determine the interaction between neuropsychological
functioning and abnormalities of ocular motility and
Table 3. Type of strabismus (N= 15)
Number
Estropia
Right eye 5 which become impaired the second year.
Left eye 1 Impaired functions which remained stable for the year
Both eyes 1 included Verbal (estimated) IQ, nonverbal recall memory,
Exotropia
Right eye 0 plex information processing.
Left eye 1 Impairments which improved during the year to within
Both eyes 0
acuity, two sets of analyses were conducted: (1) current
evidence of strabismus was related to concomitant neuro-
psychological test scores (second year), and (2) past evi-
dence of ocular motility and acuity abnormalities were
related to the earliest neuropsychological test scores (first
year). The hydrocephalic group was divided into two
groups on the basis of the presence or absence of strabis-
mus at the time of neuropsychological testing. Indepen-
dent t-tests on mean test scores for the second year neuro-
psychological tests were then run between strabismus-
present and strabismus-absent groups. Bartletts' correction
was used when applicable. No significant differences were
obtained between evidence of current strabismus and
neuropsychological test scores. This is not surprising, since
only 3 of the 18 children had strabismus at the time of
neuropsychological testing.
The hydrocephalic group was then divided into those
children with a history of strabismus and/or ambylopia
and those with no history of ocular motility or acuity
abnormalities. Independent t-tests were then run between
these groups on the first year's neuropsychological test
scores. Three tests were found to be significantly different
between groups. On Trails Part B, children with a history
of strabismus or ambylopia made significantly more errors
(mean=6.2, SD=2.6, N--6), than did children with no
history of strabismus and/or ambylopia (mean=l.6,
SD= 1.3, N = 8; t=4.26, dr= 12, P=0.001). On the Benton
Visual Retention Test, graphomotor form, children with a
history of strabismus and/or ambylopia made more right-
side-of-design errors (mean = 9.7, SD = 1.7, N = 8) than did
children with a normal visual history (mean = 6.9, SD = 3.5,
N = 12; t=2.09, df= 18, P=0.05). On the Fuld test, chil-
dren with a history of strabismus and/or ambylopia
recalled fewer correct words (mean= 27.4, SD =4.3, N = 8)
than did children with a normal visual history (mean=
35.3, SD=4.0, N = 12; t=2.71, dr= 18, P=0.01). Thus, a
history of strabismus and/or ambylopia was associated
with both increased errors of accuracy in visuospatial tasks
and poorer verbal recall memory. Evidence of ocular
motility and acuity abnormalities appears to be associated
with poor neuropsychological performance and is not
restricted solely to visuospatial and/or visuomotor tasks.
Discussion
When the stability of the neuropsychological impairments
in hydrocephalic children is examined over a 2-year
period, three patterns appear: (1) impairments which
remain unchanged, (2) impairments which improve the
second year, and (3) nonimpaired first-year functions
left-hand fine motor speed, and decreased speed of com-
normal limits include verbal recall memory, fight-hand

fine motor speed and accuracy, left-hand fine motor
accuracy, and accuracy of complex information processing.
First-year functions, which became more impaired the
second year compared to controls, include Block Design (a
measure of performance IQ) and speed of both motor
scanning and simple information processing. In the first-
year tests, hydrocephalic children showed a trend for
poorer performance on Block Design compared to con-
trols. In the second year tests, the trend became statistically
significant. The discrepancy between higher Vocabulary
scores compared to Block Design, a frequently reported
discrepancy in hydrocephalics [4, 8, 9], did not occur the
first year, but did the second. This was primarily due to
the decreasing Block Design score. The decrease in motor
speed of simple information processing in hydrocephalics
compared to controls (on Trails Test, Part A) is an inter-
esting anomaly. Hydrocephalic children actually reduced
their time as a group from a mean of 50.3 s (SD 24.9) to a
mean of 41.6 s (SD20.1), an improvement of 8.7 s (see
Table 1). However, their improvement did not keep up
with controls whose first year mean of 38.8 s (SD 27.0)
decreased to 26.1 s (SD 12.8), an improvement of 12.7 s.
Although hydrocephalic children showed improvement in
their speed of simple information processing, they still did
not catch up with normal controls.
This pattern of improvement in hydrocephalic chil-
dren, not enough to catch up with controls, is further
reflected in the continued poor performance of the left
hand in fine motor speed for the second year. Hydro-
cephalic left-hand performance on the Lafayette Pegboard
showed an absolute magnitude of changes of 53-s im-
provement from the first year to the second. This im-
provement was greater than the absolute magnitude of
change of controls (20.4 s) by 33 s. However, the hydro-
cephalic children were at a level notably lower than
controls, so that showing greater improvement than con-
trols still was not enough to reach normal levels of func-
tion. A general pattern can be abstracted from the results:
although hydrocephalic children improve in their actual
scores, they fail to keep up with the concurrently in-
creasing performance of controls.
The previous report on first-year neuropsychological
deficits in hydrocephalic children showed impairment of a
number of generalized neuropsychological functions:
vocabulary, speed of information processing, hand-eye co-
ordination, and memory (verbal and nonverbal). The
second-year testing revealed the stability of the vocabulary,
speed of information processing, hand-eye coordination,
and nonverbal memory impairment. Improvement oc-
curred in verbal recall memory-. This improvement of
verbal memory may be more apparent than real. While
alternative forms of nonverbal memory tests were used
(and nonverbal recall memory remained impaired both
years), the same tests were administered, both first and
second years, for nonverbal recognition (Benton Visual
Retention, Multiple Choice) and verbal recall (Fuld). The
Fuld test has since been shown to be sensitive to practice
effects.
121
It is interesting to note that when vocabulary was
statistically paralled out of the data analysis for the second
year, no significant neuropsychological deficits were ob-
tained. However, when Block Design was paralled out,
significant deficits still remained between hydrocephalic
children and controls. Vocabulary scores may be more a
reflection of long-term learning capacity, while Block
Design (and performance IQ) may reflect current problem-
solving skill levels. Further investigation into these dif-
ferences may help shed light on the nature of cognitive
disturbances in this group ofhydrocephalic children.
A history of strabismus and/or ambylopia was asso-
ciated with impaired performance on three (out of eight)
neuropsychological tests. Two were visuospatial (Trails
and Benton Visual Retention Test, graphomotor form) and
one was verbal memory (Fuld). A history of ocular-
motility and/or acuity abnormalities appears to be related
to impaired neuropsychological functioning for both
verbal and visuospatial material. That is, a history of
ocular motility and acuity abnormalities appears related to
a broad range of neuropsychological functioning and is
not restricted to visuospatial and visuomotor tests.
This mild relationship between a history of ocular
abnormality and poorer neuropsychological functioning is
in agreement with the clinical impressions of the neuro-
surgical authors. They note that hydrocephalic children
who present with strabismus show a poorer clinical course
neurosurgically than do hydrocephalic children without
strabismus.
A caveat must be made, concerning the relationship
between neuropsychological and ocular motility and
acuity functioning. Dennis et al. [5] have suggested that a
relationship between a history of ocular abnormalities and
intellectual functioning revealed information about cortical
dysfunction, e.g., that the effects of visual disturbances
resulted in disrupted development of visual cortex and im-
paired nonverbal intelligence in hydrocephalic children.
Abnormalities of ocular motility and acuity in hydro-
cephalic children may be due to impairment of any of the
following mechanisms: (1) ocular muscle dysfunction
(concomitant strabismus), (2) cranial nerve dysfunction
(oculomotor, trochlear or abducens nerve palsy), (3) up-
ward gaze paresis (Parinaud's sign) with ventriculomegaly
and pressure on the midbrain tectum (eliminated in the
present population which had functioning shunts and
small ventricles), (4) lesions of the brainstem (MLF,
pontine lateral gaze center and vestibular system), and (5)
frontal or occipital eye fields [3, 8]. The CNS level of dys-
function subsuming the documented abnormalities of
ocular motility and acuity function in hydrocephalics is
not known.
The CNS level of dysfunction underlying poor visuo-
motor and visuospatial performance in hydrocephalics is
also not known. To assume that poor performance on a
test which is visuomotor or visuospatial in nature (and
which purports to measure lateralized cortical dysfunction)
is due primarily to cortical dysfunction is a leap-of-logic
beyond the support provided by the data. Poor perfor-
122
mance on visuospatial or visuomotor tests of higher
cortical function with either a history of current motility or
acuity abnormalities m a y be equally due to (1) eye muscle
dysfunction, (2) brainstem and midbrain tectum (cranial
nerve) dysfunction, (3) increased intracranial pressure on
the tectum, (4) cortical dysfunction in frontal eye fields, or
(5) cortical dysfunction (parietal lobe or frontal lobe im-
pairment). Since other levels of CNS dysfunction cannot
be ruled out, it is not warranted to ascribe poor visuomotor
test performance to cortical dysfunction.
Thus the findings of the current study do not disagree
with the findings of Dennis et al. [5], but suggest a refine-
ment. First, a history of ocular motility or acuity abnor-
mality is associated not only with impairment of perfor-
mance IQ, but also with impairment of other neuro-
psychological functions: both verbal and nonverbal
memory, and complex visuospatial problem solving.
Secondly, these ocular abnormalities m a y disappear with
surgical or prismatic intervention, but the neuropsycho-
logical impairments still remain. The presence or absence
of strabismus a n d / o r ambylopia at the time of neuro-
psychological testing will not imply current cognitive func-
tion. Finally, the ocular and longitudinal neuropsycho-
logical evidence found in this study is in agreement with
previous work by the same authors on visual and tactile
information-processing deficits in hydrocephalic children
[22]. There is mild neurobehavioral evidence of persistent
dysfunction on the right side of the brain with strong
evidence of bilateral dysfunction.
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