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Development of nystagmus in response to vestibular stimulation in infants.

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ORIGINAL ARTICLES
Development of Nystagmus in
Response to Vestibular Stimulation in Infants
L. Eviatar, M D , S. Miranda, MD, A. Eviatar, M D , K. Freeman, MS, and M. Borkowski, MS
Nystagmus in response to perotatory stimulation by torsion swing or ice-cold caloric (ICC)irrigation of the ear
canals was studied in 276 infants from birth to 12 months of age. T h e percentage of positive responses to perotatory
stimulation correlated with gestational age and weight at birth during the first 3 months of life and became
comparable among groups by 6 months of age. The quality of perotatory nystagmus did not differ among groups.
A direct correlation between the caloric-induced intensity and duration of nystagmus with gestational age and
weight at birth was noted during the first 3 months of life. Premature infants showed the weakest responses, and
term-delivered, large for gestational age children the strongest responses. ICC-induced nystagmus reached comparable levels for all groups by 6 months except for premature infants, in whom comparable responses were attained
by 9 months of age. Vestibular responses mature over time, with patterns that correlate with gestational age and
weight at birth.
Eviatar L, Miranda S, Eviatar A, et al: Development of nystagmus in response to vestibular stimulation in
infants. Ann Neurol 5:508-514, 1979
During the first year of life, the human infant matures
from a state in which motor activity is largely reflex
to one in which motions and postural reactions are
mostly voluntary. T h e development of postural control depends on myelination of the pyramidal tracts,
synaptic organization of the cerebral cortex, and integration of visual, auditory, vestibular, and proprioceptive stimuli with the motor pathways.
Premature babies are initially delayed in acquisition of motor milestones, while those born at term
but below the tenth percentile for gestational weight
display less pronounced motor maturational lags. T h e
observed delay among prematures has traditionally
been ascribed to retardation of myelination and cortical organization [ 11, 121.
Since neurophysiological studies indicate that the
vestibular system is intimately connected with the
proprioceptive, visual, and motor systems in acquisition of developmental reflexes and postural control
[6, lo], vestibular responses may be sensitive indicators of central nervous system maturity. Theoretically, evaluation of vestibular responses should not
be complicated by variations in maturity of the peripheral organ of equilibrium, since it is known to be
anatomically fully differentiated and mature in the
embryo at midterm [3] and the vestibular tract is
completely myelinated at 16 weeks of gestation [S].
Patterns of maturation should therefore be detectable by appropriate vestibular testing methods.
These, in turn, should correlate with gestational age
and weight at birth, and with the timing for disappearance of primitive reflexes and substitution by
more mature equilibrium reactions.
From the DeDartment of Pediatrics (Pediatric Neurolom).
-. The
Accepted for publication Oct 2 4 , 1978.
Departments Of
C o l l e g e Of MedlOtolxYOgOlOgY and Statlstlcs, Albert
cine and Monrefiore Medical Center. Bronx, NY.
Address reprlnt requests to Dr L. Eviatar, The Bronx Lebanon
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center,
1650 Grand Concourse, B
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and
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L. Eviatar
Materials and Methods
Vestibular responses to perotatory and ice-cold caloric
(ICC) stimulation were tested in 276 infants born at the
Bronx-Lebanon Hospital Center between 1970 and 1974.
All babies but 1 were born by spontaneous normal delivery
and had Apgar scores between 7 and 10 at one minute and
9 or 10 at five minutes. One term baby, born by cesarian
section because of fetal distress and amnionitis, had Apgar
scores of 3 at one minute, 6 at eight minutes, and 10 at t e n
minutes.
Gestational age was estimated from the mother’s last
menstrual period, correlated with the clinical signs of
Dubowitz et a1 [5], and the babies were divided into groups
according to the classifications devised by Battaglia and
Lubchenco [4].One hundred eighty-two infants were
deemed to be full term, appropriate for gestational age
(AGA); 35 were full term, small for gestational age (SGA);
32 were full term, large for gestational age (LGA); and 2 7
were premature, appropriate or small for gestational age
(PR). lnformed consent to enroll t h e babies in the study
was obtained from all mothers.
A detailed neurodevelopmental examination adapted
from Saint-Anne Dargassies [161, Andre Thomas et al [2],
Prechtl and Beintema [13], Robinson [IS], and AmielTison [ 11 was performed on each baby. Only babies with a
normal neonatal course were included in the study.
,
slopes of the trends) were calculated and tested for
significance. Deviations from linearity were also evaluated.
Sleep was found to inhibit nystagmus. Children who
could not be aroused were retested at a later date and
showed good responses in most cases when tested during a
state of alertness. Marked irritability and crying produced
numerous muscle artifacts, altering the tracing. In most
cases the use of a pacifier or a bottle with sweetened water
helped soothe the child.
Electronystagmographic recordings of nystagmus induced by perotatory and ICC stimulations [6, 71 were performed o n the babies at the following time periods: between 1 and 90 days of age (Period I), 91 and 180 days
(Period 2). 181 and 270 days (Period 3), and 27 1 and 365
days (Period 4 ) . Selection of these intervals is based on
different described levels of C N S maturation and o n the
time of appearance of the specific righting and equilibrium
responses previously discussed by the authors [6]. Evaluation of postural responses was also performed at the various age intervals and will be the subject of a separate paper.
A one-channel AC dynograph was used for recording from
bitemporally placed Beckman microelectrodes. A neutral
electrode was placed o n the nasion. The test was performed
in a semi-darkened room. Patients were blindfolded to
eliminate fixation and optokinetic nystagmus. Babies were
tested usually two hours after a meal, during a stage of
maximal alertness. Sleepy or irritable babies were retested
at a later date. Only true nystagmus, identified by the presence of a fast and slow component, was considered a positive response and analyzed.
The measurement of nystagmus recorded in response to
perotatory stimulation by torsion swing included: ( 1) the
average number of beats per revolution during 40 second3
of maximal response, (2) the average amplitude of four
maximal beats of nystagmus to the right and to the left, and
(3) the slope of the slow component of nystagmus, measured in degrees of eye movement per second. Averages of
four maximal beats to the right and to the left were calculated separately.
Only 97 of the 276 infants were tested by ICC stimulation at different ages. The method used was previously
described by the authors [6]. Results of right (RICC) and
left (LICC) caloric stimulation were looked at separately
and compared for the four gestational groups within the
first two time periods and for a pool of the last two time
periods; the latter combination of data was intended to
secure a larger sample for statistical analyses. The variables
examined included (1) the number of nystagmus beats per
10 seconds (an average of 40 seconds of tracing) in the first
supine position of the test (SI); (2) the slope of the slow
component of nystagmus, in degrees of eye movement per
second, tested at the culmination of nystagmus (average of
four beats) in S1; (3) amplitude of nystagmus at culmination (average of four beats) in S1; ( 4 ) latency of response;
and ( 5 ) total duration of response in S1.
Results
The n u m b e r s of children tested by perotatory stimulation d u r i n g t h e four t i m e periods are s h o w n in
Table 1. Fewer children were tested d u r i n g Periods 3
a n d 4 because o f poor follow-up. The percentages
of positive nystagmus responses calculated for each
o f t h e four g r o u p s of infants d u r i n g t h e f o u r t i m e
p e r i o d s are shown i n Figure 1. T h e r e was significant
Table I . Number of Infants Tested by Perotatory
Stimulation a t Various Time Periods"
Group
Period 1
Period 2
Period 3
PerioJ
PR
SGA
AGA
LGA
28
35
182
32
21
22
10
13
21
7
11
17
5
69
11
4
4
'Period 1, 1 to 90 days of age; period 2, 91 to 180 days; period 3,
181 to 270 days; period 4 , 271 to 376 days.
PR = premature, appropriate or small for gestational age; SGA =
full term, small for gestational age; AGA = full term, appropriate
for gestational age; LGA = full term, large for gestational age.
':i
70
Statistical Methods
One-way analyses of variance were separately performed
for each variable assessed, on data obtained during each of
the four specified age intervals, for the gestational age
groups (PR, SGA, AGA, and LGA). T h e statistic F was
calculated for each analysis to determine whether stacistically significant differences among groups might exist.
When appropriate, the differences between mean responses were then assessed. In addition, product moment
correlations between right and left responses were calculated for each variable assessed during the four time periods for each gestational group. Trends of responses were
tested for each variable in relation to time and to gestational age and weight at birth. Regression coefficients (i.e.,
l o t
-
0
1 - 90
91-180
181-270
DAY 5
271-365
Fig 1 . Percentage of positive reJponses to per-rotatory stimnlation at various time intervals. (SGA =full term, small for
gestational age; AGA = full term, appropriate for gestationul
age; PR = premature, appropriate or small for gestational age;
LGA =full term, large for gestational age.)
Eviatar et al: Nystagmus after Vestibular Stimulation
509
Table 2 . R e d t s of ICC lwigation at Various Time Periods"
~
~
Period 1
Group
PR
SGA
AGA
LGA
No.
Tested
L 23
R 23
L 24
R 24
L61
R 65
L 29
R 29
No.
Positive
No.
Tested
No.
Positive
26
21.7
20.8
20.8
18
18
93.4
23
24
11
11
8
7
6
5
22
22
96 Positive
6
5
5
5
57
60
22
92.3
75.9
75.9
22
~~
Period 11
9
9
Period 111
% Positive
44.4
38.9
9
66.7
55.6
95.7
91.7
81.8
10
90.9
Abbreviations same as for Table 1.
510 Annals of Neurology
Vol 5 No 6 June 1979
No.
Positive
16
16
20
20
17
15
10
10
15
16
17
14
12
12
9
9
7
aPeriod I, 1 to 90 days of age; period 11, 91 to 180 days; period 111, 181 to 365 days.
ranking by gestational maturity and weight at birth in
the percentage of positive responses ( p < 0.001)
during the first examination period. The PR showed
the lowest percentage of responses, and the LGA the
highest. T h e differences between groups decreased
but remained significant ( p = 0.05) during the second period. There was a significant increase in percentage of positive responses for all groups between
the first and second periods with a slight lag noted for
the prematures, who caught up by the third period.
During the third and fourth time periods, no significant difference among groups and no significant increase or decrease over time were found.
The quality of responses, as measured by numbers
of beats per revolution, by amplitude of nystagmus,
and by slopes of the slow component of nystagmus,
did not differ significantly among the four groups
during the four time intervals. Data from right- and
left-beating nystagmus were virtually identical.
The number of ICC stimulation tests performed
for each group during the three time periods and the
number and percentage of positive responses are
shown in Table 2. Figure 2 shows the percentages of
positive nystagmus responses calculated for the four
groups following RICC stimulation. There was a progressive increase in percentage of positive responses
in the PR and SGA groups over the three time periods, while no significant change over time occurred
for AGA and LGA babies. The percentage of positive responses was comparable among the four
groups in the third and fourth time periods.
During the first and second time periods, there was
a significant increase in the number of beats per 10
seconds according to gestational age and weight at
birth for the RICC (p = 0.01) and LICC (j = 0.03)
stimulations (Fig 3 ) . The lowest values were found in
the PR and SGA groups, and the highest in the AGA
and LGA infants. During the third and fourth time
No.
Tested
% Positive
93.8
100.0
85.0
70.0
70.0
80.0
90.0
90.0
.
loor
c.-...'
...""'.''.'
P SGA
......................................... ...... L'A
AGA
0.-
0
60
/
0
'
7'
X 50
/
/
lot
01
'
1-90
I
91-180
DAY S
I
181-365
F i g 2. Percentage of positive responses to ice-cold caloric
irrigation of the right ear at various time intervals.
(Abbreviations same as for Fig 1 .)
periods there was no difference in frequency among
the various groups.
The mean amplitude of nystagmic beats in the S 1
position varied greatly within each group. The average responses for the four groups were not significantly correlated with gestational maturity o r
weight at birth. An overall increase in mean amplitudes was found for the four groups between the first
and last time periods ( p < 0.01).
An increase in the mean values for the speed of
slow component between the first and last periods
was present in all four groups (Fig 4). This increase
was significant on RICC stimulation for the PR ( p =
0.03), SGA ( p = 0.03), and AGA ( p < 0.01) groups.
PR babies had the smallest mean values of all groups
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F i g 3 . Average number of beats per 10 seconds with ice-cold
caloric irrigation of the left ear (LICC) (left bar of each pair)
and the right ear (RICC) (right bar of each pair)for each
gestational group oiler time. (SEM = standard error of the
mean; other abbreviations same as for F i g 1.)
during the first time period, and LGA the highest. O n
LICC stimulation the level of significance w a s p =
0.03 for PR infants,p < 0.01 for SGA infants,) <
0.01 for AGA infants, andp = 0.05 for LGA infants.
During the first time period, mean latencies were
longer for the PR and SGA groups and shorter for
15 16 I7 14
m
18 12
9 9
AGA and LGA babies. The differences in means
among the four groups were highly significant on
LICC stimulation during the first period (6 < 0.0 1)
and less significant on RICC stimulation ( p = 0.01),
demonstrating inverse correlation with gestational
age and weight at birth.
Significant decreases in mean values over time
were detected on LICC stimulation for PR ( p < 0.01)
and SGA ( p < 0.01) infants, with net decreases in
initial means of 34 and 53 seconds, respectively, from
the first to the third period. Significant negative
linear trends were also detected o n RICC stimulation
for PR ( p = 0.02) and AGA ( p < 0.01) babies, with
Eviatar et al: Nystagmus after Vestibular Stimulation
5 11
I
.
SEM
PR
OSGA
0 AGA
LGA
T
n: 6 5
5 5 64 60 22 22
I
net decreases in initial averages of 3 1 seconds and 2 1
seconds, respectively.
All groups showed an increase over time in the
mean values for total duration of response (Fig 5).
This increase was statistically significant only for the
PR group on LICC stimulation ( p = 0.05) and the
LGA group on both RICC and LICC stimulation ( p
= 0.02).
Discussion
T h e work of Magnus [lo] and d e Klejn [9] in the
early part of the twentieth century initiated our
understanding of the development of balance and
postural control. They demonstrated, via ablation
procedures, that integrity of brainstem structures is
required for preservation of tonic neck responses in
animals, while righting responses are preserved in
decorticate animals in which rostra1 midbrain structures, including the red nucleus, remain intact. Additional anatomical, embryological, and physiological
studies have demonstrated extensive connections
between the vestibular system and the reticular formation of the brainstem, which exert both excitatory
and inhibitory effects on the peripheral vestibular
apparatus, as well as extensive connections of the
vestibular system with the corpus striatum and basal
ganglia. The importance of the integrity of the vestibular apparatus to acquisition of motor milestones
such as sitting, standing, and walking is attested by
the delayed acquisition of these motor milestones
among children with congenital abnormalities of the
vestibular apparatus [14].
512
Annals of Neurology
Vol 5
No 6 June 1979
8 7
6 5
3722
JI
9 10
15 16
I 7 14 18 12
9 9
III
F i g 4. Average speed of the slow component w i t h LICC (left
bar of each pair) and RICC (right bar of each pair) stimulation for each gestationalgroup over time. ( E M = eye movement;
other abbreviations same as for Figs 1 and 3 . )
Although abnormalities of function have been
shown to relate to various components and connections of the vestibular pathways, the influence of delayed vestibular maturation on acquisition of motor
milestones has been hypothesized but never investigated. Vestibuloocular reflexes begin to operate by
the twelfth week of gestation and are fully established by 24 weeks [8]. Premature infants would
therefore be expected to possess fully developed
vestibular responses to perotatory or caloric
labyrinthine stimulation beyond 24 weeks of gestation. T h e present data, however, agree with those of
a previous study [7] and indicate that these vestibular
responses appear much later in premature infants.
Both length of gestation and weight at birth seem
to influence the time of appearance of vestibular responses to perotatory and ICC stimulation. T h e
quality of nystagmus induced by perotatory stimulation does not vary among the four groups or during
the four periods of testing. This is probably due to
the fact that the torsion swing merely produces
physiological threshold stimulation of the labyrinth,
resulting in an “all-or-none’’ response. This stimulation may not be strong enough to elicit qualitative
differences among groups, nor can it test individual
labyrinthine function.
180
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-
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-
6 5
37 22 9 10
II
Fig 5 . Totalduration of response with LlCC (lefi bar of each
pair) and RICC (right bar of each pair) stimulation for
each gestational group over time. (Abbreviationssame as
for Figs 1 and 3 . )
Since ICC irrigation provides supraliminal stimulation individually to each labyrinth, it may demonstrate more clearly than other methods whether each
specific organ can respond appropriately. Indeed, the
correlation between intensity of nystagmus induced
by caloric testing with gestational age and weight at
birth is very striking.
As might be expected, the most reliable variables
for qualitative evaluation of vestibular responses to
ICC irrigation appear to be the frequency of nystagmus and the value of the slope of the slow component. Frequency of nystagmus is a good measure of
the intensity of vestibular response and is a function
of the degree of maturation of the oculomotor system. The slope of the slow component represents
conjugate ocular deviation resulting from stimulation
of vestibular nerve endings by motion of endolymph
15 16
I7 14
m
18 12
9 9
in the semicircular canals, and is therefore considered
the true vestibular component of nystagmus. Both
variables increased significantly in PR and SGA
babies between the first and third testing periods,
indicating progressive maturation of responses during the first year of life. There was a relative lack of
change from the second to the third testing period
among AGA and LGA babies, suggesting the presence of mature responses by 3 to 6 months of age in
those two groups.
While intensity of nystagmus increases with age,
latency decreases with duration of gestation and age.
The shortening of latency concomitant with the increased intensity of vestibular responses suggests a
peripheral, or end-organ, physiological maturation
with time. Indeed, this phenomenon would be
difficult to explain as a result of maturation of supranuclear centers.
The laboratory data presented are in accord with
the clinical findings of developmental lags in muscle
tone, head control, and postural control during the
first 6 months of life among PR and SGA infants. The
Eviatar et al: Nystagmus after Vestibular Stimulation
513
PR babies tested showed the greatest developmental
lags in all areas. Primitive brainstem reflexes tended
to disappear by 4 to 6 months of age in all groups
except among the PR infants, in whom they persisted
into the 6- to 9-month period. Similarly; righting responses in blindfolded infants, which indicate mature
labyrinthine responses, were present in all infants by
6 to 9 months except among PR babies, in whom
these responses could not be detected before 7 to 12
months of age.
Thus, maturation of vestibular responses parallels
acquisition of head and postural control as well as
appearance of righting responses, and correlates well
with birth weight and length of gestation. These data,
together with previous experimental evidence in
animals, support the concept that development of
postural control is dependent in part on information
received from the vestibular system. Whether vestibular maturation can be accelerated, and hence
postural control improved, by any specific treatment
modality still remains to be proved.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
Supported in part by Grant NS 10238 from the National Institute
of Neurological and Communicative Disorders and Stroke.
The authors thank D r M. Davidson and D r E. Weitzman for their
helpful comments during the preparation of this manuscript.
13.
14.
References
I . Amiel-Tison C: Neurological evaluation of the maturity of
newborn infants. Arch Dis Child 43:89-93, 1968
2. Thomas A. Chesni Y , Saint-Anne Dargassies S: The neurological examination of the infant, in MacKeith R C (ed): Little
514 Annals of Neurology
Vol 5
No 6 June 1979
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16.
Club Clinics in Developmental Medicine, N o . 1. London,
Medical Advisory Committee of the Spastics Society, 1960
Bast T H , Anson BJ: T h e Temporal Bone and the Ear.
Springfield, IL. Thomas, 1949
Battaglia FC, Lubchenco LO: A practical classification of newborn infants by weight and gestational age. J Pediatr 7 1 : I 59163, 1967
Dubowitz LM. Dubowitz V, Goldberg C: Clinical assessment
of gestational age in the newborn infant. J Pediatr 77:l-10,
1970
Eviatar L, Eviatar A: Neurovestibular examination of infants
and children. Adv Otorhinolaryngol 23:169-191, 1978
Eviatar L, Eviatar A, Naray I : Maturation of neurovesribular
responses in infants. Dev Med Child Neurol 16:435-446.
1974
Hamilton WJ, Mossman HW: Human Embryology: Prenatal
Development of Form and Function. Fourth edition. Cambridge, England, Heffer, 1972
d e Klejn A: Posture and Reflexes. Quoted by Walsh FMR,
Brain 47:383, 1924
Magnus R: Cameron Prize Lectures on Some results of studies
in the physiology of posture. Lancet 2:531-536, 1926
Moosa A, Dubowitz V: Assessment ofgestational age in newborn infants; nerve conduction velocity versus maturity score.
Dev Med Child Neurol 14:290-295, 1972
Parmelee AH, Wenner W H , Akiyama Y , e t al: Electroencephalography and brain maturation, in Minkowski A (ed):
Regional Development of the Brain in Early Life. Oxford.
England, Blackwell, 1967, p p 459-480
Prechtl H , Beintema D: The Neurological Examination of the
Full Term Newborn Infant (Clinics in Developmental Medicine, No. 12). London, The Spastics Society with Heinemann
Medical, 1964
Rapin I: Hypoactive labyrinths and motor development. Clin
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Robinson RJ: Assessment of gestational age by neurologcal
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Saint-Anne Dargassies S: La maturation neurologique du
prPmature. Etud Neonat 4:71, 1955
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