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Effect of aging on the accuracy of visually guided saccadic eye movement.

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Effect of Aging on the Accuracy
of Visually Guided Saccadic Eye Movement
Tateo Warabi, MD,” Manabu Kase, MD,? and Takamasa Kato, M D t
~~
Changes in oculomotor behaviors with aging were studied in normal young and elderly subjects. Saccadic eye movments induced by presentation of a visual target were analyzed. Elderly subjects commonly showed an elongation of the
time to locate the target, accompanied by an increase in reaction times (mean increase, 100 ms) and a decrease in
saccadic velocities. The decrease in the velocity was particularly notable when a large-amplitude saccade was executed.
In spite of the slowed motor responses, most elderly subjects preserved the function necessary to execute a correct
saccade toward the visual target. The saccadic slowing was accompanied by an increase in saccade duration. Although a
longer time was necessary for elderly subjects to locate the target, the accuracy of the initial saccades was not different
from that of young subjects. One group of elderly subjects showed extremely long reaction times. These subjects,
displaying no abnormal neurological symptoms, were not able to locate the visual target with initial saccades. They had
to execute multistep saccades typically seen in patients with degenerative neurological diseases.
Warabi T, Kase M, Kato T: Effect of aging on the accuracy of visually guided saccadic eye movement.
Ann Neurol 16:449-454, 1984
Visually guided saccades were recorded from 8 young,
healthy subjects whose ages ranged from 19 to 26 years, and
24 elderly subjects whose ages ranged from 59 to 82 years.
The 24 elderly subjects had no history of any neurological
disorders and possessed good visual acuity (better than 0.5)
with or without correction. Subjects had no restriction of
lateral or upward gaze (no Parinaud’s sign).
Four elderly subjects were given either hydrochlorothiatide or furosemide because of moderate hypertension. One
subject had been treated with isoniazid (INH) and rifampin
for inactive pulmonary tuberculosis. Neither sedatives (such
as diazepam) nor anticonvulsants were given to any subjects
during the examination, however.
Eye movements were recorded in a dark room by using a
DC electro-oculograph with an upper frequency limit of 100
Hz after subjects were dark adapted for I 5 to 20 minutes.
Three silver-silver chloride electrodes were attached to the
internal and external canthi of the right eye and the forehead.
Visually guided saccades were induced by five light-emitting
diodes, which were placed at 10-degreeintervals horizontally
from left 20 degrees to right 20 degrees on a tangent screen
1.7 m in front of the subject’s eyes. After head immobilization subjects were instructed to fixate a visual target. The
light-emittingdiode target was presented at varying positions
in irregular sequences at variable frequencies. As an additional paradigm, the visual target was turned off for 500 ms
immediately after a goal-directed saccade had occurred, creating a situation in which the visual feedback signal usable for
correcting the final eye position was eliminated.These examinations were finished within 20 minutes to prevent fatigue in
the subjects.
Signals of eye position, eye velocity, and visual target positions were stored on magnetic tapes. On analysis, the data
signals were played back on a polygraph and a digital memory
From the Departments of *Neurosurgery and Neurology and
Wphthalmology, Hokkaido University School of Medicine, and
SNishimaruyama Hospital, Sapporo, Japan.
Address reprint requests to Dr Warabi, Department of Neurosurgery and Neurology, Hokkaido University School of Medicine,
Kita 15, Nishi 7, Kita-ku, Sapporo, Japan.
Systemic neurological diseases commonly found in
aged patients are frequently accompanied by various
oculomotor disorders. Abnormal ocular movements
have been reported in patients with olivopontocerebellar atrophy, Parkinson’s disease, and progressive supranuclear palsy {6, 8, 12, 15, 23). In evaluating such
patients it is necessary to discriminate abnormal ocular
movements caused by a degenerative brain disease
from those caused by nonpathological changes in brain
tissue associated with aging. Recent studies of the effects of aging on saccadic eye movement have shown a
decrease in saccadic velocities (171 and an increase in
their reaction times [1). These studies were, however,
primarily concerned with limited variables of individual
saccades, and factors such as the accuracy of initial saccades in target location or the effectiveness of corrective saccades have not been evaluated [l, 171. The
present study provides a more detailed description of
nonpathological changes in oculomotor behaviors associated with aging. An effort was made to characterize
not only the motor behavior of saccades, but also the
quality of visually guided saccades, for example, the
effectiveness of the initial saccade in target location.
Methods
Received Nov 17, 1983, and in revised form Feb 15, 1984. Accepted for publication Feb 20, 1984.
449
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C
age 6 7 - 78
m e a n 4 6 8 m s
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4 0 0
600
m s
Fig I Reaction rims of subjects in groups a, b, and c. The mean
reaction times and their standard deviations in individual subjects are represented by dots and horizontal bars, respectively.
Group means of the reaction times for subjects in groups a, b, and
c were 235, 33 7 , and 468 ms, respectively. Note that the reaction
tims and their variations in subjects in group c were particularly large.
~
%
group b
30 .
group c
I
0
11
oscilloscope (Nihonkoden RAT 1loo), and reaction times,
amplitudes, and durations of saccades were measured. The
maximum velocity of a saccade was evaluated from the derivative of the eye position curve by electronic differentiation. The onset and end of the saccade were determined by a
computer from the points of intersections of the regression
lines, derived from the values for periods of presaccadic and
postsaccadic fixation and saccades 171.
Results
Reaction Times
Because reaction times were variable, depending on
the angle of the saccades, reaction times for 20-degree
saccades were used for the standard statistical analysis
(Fig 1).The average reaction time of 8 young subjects
(group a) was 235 ms. The elderly subjects had reaction times significantly longer than those of young subjects. Four of the elderly subjects exhibited large variations in reaction times (standard deviation more than
110 ms), whereas the variations in the 20 other elderly
subjects differed little from those in the young subjects. Therefore, the elderly subjects were classified
into groups b and c.
The average reaction time of the 20 elderly subjects
(group b) was approximately 100 ms longer than that o f
the young subjects (see Fig 1). The other 4 elderly
subjects (group c) had a mean reaction time of 468 ms.
450 Annals of Neurology Vol 16 No 4 October 1984
C
21
Arnpl, tude
of
Ini
31
41 deg
tialsaccade
Fig 2. (A) Accuraq of visually guidedsaccades in subjects in
groups a, 6, and c toward visual target angLes of 10, 20, 30, and
40 degrees. The degree of accuracy is exprersed by metrics, which
are the ratios between the saccrzde amplitude and the target angle.
Note that the metrics values and their standard deviations are almost identical in groups a and 6. The metrics vahes of group c
deciined when a large angle to the target was used. (B,CI Amplitude distributions of the initial saccades in response to 40-degree target displacements in subjects in groups a, 6, and c. The
saccade amplitudes were sampled from ten t o fifeen saccades of all
the subjects of cowesponding groups and are expressed as percentages. Note that there was no significant difference in the amplitude distributions between groups a and 6, whereas group c
subjects showed numerous saccades that werefar smaller than 40
degrees.
The reaction times were significantly different among
the three groups (t test; p < 0.001).
Metrics (Saccade G a i n )
The metrics (saccade gain) were measured by the ratio
of the saccade amplitude to target angle (Fig 2). There
was no significant difference in the metrics between
group a and group b, indicating that in the majority of
the elderly subjects the saccades captured the target as
accurately as in young subjects. In both groups a and b
_'.I
200
A
B
500 ms
l o
1400
Fig 3. (A,Bi Responses ofa group a subject and a group b subject
t o target angles of 10, 20, 30, and 40 degrees. Eye position signals (1) and eye velocity signals (21 are superimposed. Note that
the saccade of the group b subject reached its peak velocity at 20
degrees and did not increase with a larger tdrget angle (b, 2).
(Ci Responses of a group c subject to two 40-degree target displacements. Note the smaller initial saccades of about half the
target angle followed by multiple corrective saccades.
these saccades often fell short of the target by roughly
10% of the target angle. For instance, when the target
jumped 40 degrees, most saccades fell between 35 and
41 degrees in groups a and b (see Fig 2 B,C). The
amplitudes of saccades in group c were smaller than
those of groups a and b, however. This difference was
more prominent when a larger target angle was used.
The average metrics were 0.95 with a 10-degree target
angle but 0.78 with Zo-degree, 0.61 with 30-degree,
and 0.52 with 40-degree target angles. The standard
deviations in group c were always larger than those in
the other groups (see Fig 2). When the target jumped
40 degrees, initial saccades in group c ranged widely,
from 3 to 41 degrees (see Fig 2C). Figure 3C shows
typical examples of saccades of a subject in group c in
response to a 40-degree target angle. The target was
located by two saccades of about half the target angle
followed by two o r three smaller corrective saccades.
Velocities and Durations
Changes in the maximum velocities during saccades of
different amplitudes are shown in Figure 3. In group a
the maximum velocity increased when a larger saccade
was executed (Fig 3A). Interestingly, however, in 8
elderly subjects belonging to group b, a maximum velocity of 400 degrees per second was reached during
20-degree saccades, as shown in Figure 3B, and the
maximum velocity did not increase any further in association with saccades of larger amplitudes. The velocity
during larger-amplitude saccades formed a plateau
rather than a peak, as seen in the example of velocity
curves in Figure 3B, graph 2. Figure 4A shows amplitude/velocity curves in groups a and b. The average
velocities in saccades to 10, 20, and 40 degrees of
target angle and their standard deviations in the two
groups are shown. The means and standard deviations
of the maximum velocities for lo-, 20-, and 40-degree
saccades were 306 2 51, 408 ? 57, and 508 2 76
degrees per second, respectively, in young subjects. In
contrast, those in aged subjects were 300 63, 391 k
65, and 464 2 89 degrees per second. For 10-degree
and 20-degree saccades, there was no significant difference in the maximum velocities of the two groups
(t test; p > 0.05). For 40-degree saccades, however,
the maximum velocities in group b were significantly
smaller than those in group a (p < 0.001). The maximum velocities were significandy smaller in group b
even when smaller saccades (36 to 38 degrees) toward
40-degree target displacements were compared (group
a, 514 2 60 degrees per second; group b, 461 2 89
degrees per second; p < 0.001).This finding is due to
the contribution of a group of subjects whose maximum saccadic velocity reached a plateau during saccades larger than 20 degrees.
The relation between saccade duration and maximum velocity was analyzed for both young and aged
subjects. The inverse relationship between those two
variables was similar in these two groups, and, when
plotted on a scatter diagram, the data points obtained
from the two groups overlapped along a regression line
(Fig 4B). Regression lines for 20-degree saccades and
40-degree saccades were y = - 4 . 1 4 ~ + 686.4 ( r =
-0.94) and y = - 2 . 7 5 ~ + 813.9 ( Y = -0.96), respectively. The elderly subjects of group b were
classified into two age groups, younger than 69 and
older than 69. The mean maximum velocity and saccade duration in response to 40 degrees of target shift
calculated from the 7 subjects less than 69 years of age
were 499 degrees per second and 113 ms, respectively.
They were not significantly different from those of
young subjects Cp > 0.3). The maximum velocity and
duration obtained from the 13 subjects in group b
more than 69 years old were 428 degrees per second
and 141 ms, respectively, They were significantly different from those in the other two groups (p < 0.001),
showing that the saccade velocity was smaller and duration greater in this group.
As already described, the visually guided saccades
were severely impaired in the subjects in group c, indicated by the long reaction times and low metrics values.
The relationship between velocity and duration was
*
Warabi et
al:
Aging and Visually Guided Saccades 451
DEG
/
S
1
DEG
/
S
\
2 0"
A
10
20
40
DEG
within the range of that found in other elderly subjects,
however. In Figure 5 the maximum velocity/amplitude
relationships for subjects in groups b and c are plotted
together. There was no difference in the distributions
of these values in the two elderly groups.
Corrective Saccades and Final Eye Positions
When the initial saccades fell short of the target angle,
corrective saccades followed with latencies of 130 to
230 ms in groups a and b. In group c these intersaccadic intervals between the initial and the corrective
saccades were much more variable, ranging from 60 to
1,200 ms. Half the intervals were longer than 230 ms.
The intervals between saccadic onsets, for both initial
and corrective saccades, were longer than 200 ms in
85% of cases.
In both groups a and b, after a target was attained
with saccades, fixation was steadily maintained in most
cases regardless of the presence or absence of the visual
target after the saccade (Fig 6A,B). In group c, however, the eye position drifted toward the primary position following the saccades, with constant velocities of
about 6 degrees per second, when the target light was
turned off (Fig 6C,D). Similar drift was sometimes observed in groups a and b; in these cases the eyes drifted
with a variable velocity of less than 2 degrees per second, less than the drift speed of group c. In group c the
continuous eye drift persisted throughout the darkness, although corrective saccades occurred when the
target was turned on again (see Fig 6C).
Discussion
Most'elderly normal subjects (except those in group c)
asked to look at a visual target presented in a dark
room were able by the initial saccades to bring the
452
Annals of Neurology
Vol 16 No 4
October 1984
B
100
4 0"
2 0 0 rns
Fig 4. (A)The maximum velocities ofsaccades in group a and b
subjects in response t o lo-. 20-. and 40-degree target displacements. The data were compiled from ten responses of all the subjects of the corresponding groups. (B) The maximum oelocityl
duration relationshipsfor subjects of group Q (open circles) and
group b (filled circles). The data point.! represent afierage values
of sacwde durations and the maximum veLocities observed in individual subjects in response to 20- and 40-degree target displacements. Note that considerable tiaviations in thew z?ulues ulere due
t o variations among indifiduals. Subjects having a larger maximum velocity bad a shorter duration.
image of the target as close to the fovea as were young
subjects. The metrics IS, 11, 14, 191, the ratio between
saccade amplitude and target angle, were not different
from those of young subjects. It appears, therefore,
that the fundamental functions necessary for programming the appropriate size of a saccade are well preserved in the elderly subjects. There were subjects
(group c), however, who had great difficulty in locating
the target with the initial saccades. Particularly when a
large-angle saccade (for example, 40 degrees) was required, several saccades of about 15 degrees and
smaller corrective saccades were repeated until the
target was located. The metrics were, therefore, extremely small and variable. Even when the target was
successfully located, these subjects showed difficulty in
maintaining the peripheral eye position in the darkness, and the eyes drifted toward the primary position
at a fairly constant velocity, suggesting a lack of absolute target position information in space [lo, 16, 20).
The multistep saccades of these subjects (group c)
were not due to fatigue, because the intervals between
the successive saccades were in most cases longer than
200 ms and the saccades were not the so-called double
TARGET
I
BLACK OUT
--I
I' -
A
1 .: ..
:
500
rnx
I,:
:
i
0
10
20
S a c c a d e
30
40 d e g
A r n p l ~ t u d e
BLACK OUT
F i g 5 . The maximum velocitylsaccade amplitude relationships in
groups b and c. The data points represent indiiidual saccades of
a group b subject (circles) and a group c subject (triangles).
Note that the distributions are almost iahtical in groups b and r.
saccades that are known to appear as a result of fatigue
f2, 31. The results were identical even when tests were
conducted on different days. These subjects were 67
years old or older and showed normal findings, not
only in physical and neurological examinations, but also
on computed tomographic scannings. The multistep
saccades have been seen in patients with Parkinson's
disease, progressive supranuclear palsy, and olivopontocerebellar atrophy [b, 8, 12, 15, 231. The present
study suggests that these abnormal eye movements can
occur in subjects without any signs of neurological disease. It is possible, however, that the oculomotor
symptom may be the first sign of a latent degenerative
neurological disease. In considering nonpathological
changes in oculomotor behaviors in association with
aging, it appears more appropriate to deal only with the
subjects of group b in the following discussion.
The most prominent change in saccades in group b
was elongation of time to acquire target, which resulted
from an increase in reaction times and a decrease in
saccadic velocities. The reaction times of elderly subjects were, on the average, 100 ms longer than those of
younger subjects. This value is larger than that (45 ms)
reported by Abel and colleagues [ 11. We attribute this
discrepancy to the difference in the angles of saccades
tested [9, 181. We sampled the data only from 20degree saccades selected from among those of various
angles tested in random sequences. The data of Abel
and colleagues [ l } are based on all successive saccades
of different angles smaller than or equal to 30 degrees.
The elongation of saccades in group b subjects was
always accompanied by a decrease in the maximum
velocities of saccades. There were, however, young
subjects whose saccadic velocities were slower than
those of group b. There were also subjects 80 years
old or older whose maximum velocity almost corresponded to the fastest speed of the young subjects.
Allowing for all these variations in individual subjects,
Fig 6. The target light was blacked out for 500 msfrom the onset
of the initialsaccades. Five executions of saccades by a group b
subject are superimposed in (A) and (B) (A, eye position; B , eye
velocity). Corrective saccades always occurred follwing the reappearance of the target. Two multistep saccades by a group c subject are superimposed in (C) and ID) (C, eye position; D , eye velocity). Centripetal eye drgts, indicated by straight lines in C ,
took place following saccades. and correctiiie saccades occurred afiev
the reappearance of the target.
the curves of the saccadic velocities of elderly subjects
overlapped those of young subjects (control) whose
values were almost comparable to those reported by
other authors 14, 9, 13, 141.When the target angle was
20 degrees or less, the distribution of the maximum
saccadic velocities of group b did not differ significantly
from those of group a. This finding is in agreement
with the results of Abel and colleagues 111. When the
saccade angle was 40 degrees, however, the velocities
of group b were significantly smaller than those of
group a (p < 0.001). This finding agrees with the data
of Spooner and co-workers 117). A significant difference in the maximum saccade velocity of elderly subjects became prominent only when a large saccade (40
degrees) was induced. Despite the marked decrease in
velocity, the accuracy of the initial saccade, expressed
by the values of metrics, was well preserved in the
elderly subjects. In both young and elderly subjects,
the maximum velocities and the accompanying durations were inversely related, relationships expressed by
fairly straight lines when the saccades were directed to
the same visual target (see Fig 4B). The slowing of
saccades was accompanied by an elongation of the du-
Warabi et al: Aging and Visually Guided Saccades 453
ration, resulting in a normal-size saccade, which was
seen in the young subjects. This finding indicates that
the function of the brain that programs the appropriate
size of the saccade, a function necessary to bring the
target image on the fovea, is relatively well preserved
in the elderly subjects. It indicates also that the central
nervous system, by utilizing internal feedback mechanisms C21, 221, can lengthen the duration of the saccade to bring it on target even though its velocity is
decreased. Changes in the saccade velocityiduration relationship observed in group b are considered to be an
outcome of a distinct age-dependent plastic process,
but one within the realm of physiological saccadic functions.
~
~
The authors thank Hiroharu Noda, MD, and Jun Tanji, MD, for
their constructive critic~smson early drafts of the manuscript
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Correction
Correction
In the letter “AphasiaiApraxia and Familial Aggregation in
Alzheimer’s Disease” published in the June 1984 issue (Ann
Neurol 15:614-615, 1984), two of the three authors’ names
were not given. The authors are John C. s. Breitner, MD,
Diane Powell, MD, and Marshal F. Folstein, MD.
In “Measurements In Vivo of Parameters of the Dopamine
System,” by A. M. Ftiedman et al, which appeared in “Research Issues in Positron Emission Tomography,” a supplement to the April issue (Ann Neurol I 5 (suppi):S66-S76,
1984), an error appears in equation 6, page S67. The equation should read:
1
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454 Annals of Neurology
VoI 16 NO 4 October 1984
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