Full text of DOI:10.1093/gerona/56.6.M386

Journal of Gerontology: MEDICAL SCIENCES
Copyright 2001 by The Gerontological Society of America
2
001, Vol. 56A, No. 6, M386–M390
Effect of Age on Ocular
Microtremor Activity
1
1
2
2
2
Ciaran Bolger, Stana Bojanic, Noirin F. Sheahan, Davis Coakley, and James F. Malone
1Department of Neurosurgery, Frenchay Hospital, Bristol, UK.
2Mercer’s Institute for Research in Ageing, Dublin, Ireland.
Background. Ocular microtremor (OMT) is a high-frequency tremor of the eyes. It is present in all individuals and is
related to brainstem activity. The OMT signal appears as an irregular oscillatory movement with intermittent burst-like
components. The clinical interest in OMT has centered on its use in the assessment of the comatose patient, with broad
agreement among authors of its prognostic value. The purpose of this study was to examine the changes in OMT activity
related to aging.
Methods. OMT was recorded from 72 normal healthy subjects using the piezoelectric strain gauge technique. The
subjects ranged in age from 21 to 88 years (54.22 ꢀ 20.43 years, mean ꢀ SD).
Results. Our results show that the overall frequency and frequency content of the bursts falls with age (p ꢁ .002 and
p ꢁ .001, respectively). There is a highly significant drop in all three frequency parameters of OMT (p ꢁ .0001) in sub-
jects older than 60 years of age.
Conclusions. These results suggest that different values of normality should operate for subjects over 60 years of age
when considering the clinical application of OMT.
ANY physiological processes change with aging.
Changes in physiological parameters of nervous-sys-
tem activity accompanying aging are well documented;
these include slower motor responses (1), sensory responses
sess a packet-like appearance being clearly defined against
the background tremor (11). The period between the bursts
is termed the baseline. The clinical interest in OMT has cen-
tered on its use in the assessment of the comatose patient,
with broad agreement among authors of its prognostic value
(14,15).
Recent research by Bolger and colleagues measured the
OMT activity in 105 normal healthy adults and found the
mean peak frequency to be 83.68 ꢀ 5.78 Hz (mean ꢀ SD)
(16). However, a significant difference was noted when
comparing the mean peak frequency in subjects younger
and older than 70 years of age [i.e., the mean peak fre-
quency fell in the subjects older than 70 (p ꢁ .008)]. A pre-
vious study by Coakley (17) also compared OMT activity in
26 young adults and 15 subjects over 70 years of age. He
could find no significant change in OMT frequency associ-
ated with age.
M
(
2), and cognition (3). Thus, it is not surprising that histo-
logical changes in extra-ocular muscle, such as the altered
staining of mitochondria, disruption of fibers, and an in-
creased collagen content, also occur with age (4). Age-
related changes in eye movements have been documented.
These include prolonged horizontal latency (3), decreased
amplitude of saccades (5), slower saccades (6), reduced
accuracy of perceptual motor performance (7), and eye–
hand coordination (8). Thus, normal accepted values for
commonly applied physiological measurements of visual
and ocular function, such as the visual evoked response and
vestibulocular reflex, are different for young and older
subjects (9).
Ocular microtremor is a small, high-frequency tremor of
the eyes that is present even when the eyes are at rest. It was
first described fully in 1934 by Alder and Fleigelman (10)
as one of three fixational eye movements—the other two
being drifts and microsaccades. This tremor is caused by
high-frequency extra-ocular muscle stimulation, which
originates in the brainstem from the oculomotor neurones
Many neurological conditions to which the recording of
OMT may be applied are common only to elderly subjects
(e.g., Parkinson’s disease). It could be erroneous to apply
OMT recording and the assessment of normality to these
subjects on the basis of a normal population of young
adults. The purpose of this study was to examine possible
changes in the frequency or pattern of OMT records relating
to age, using the piezoelectric strain gauge transducer tech-
nique, in the normal population.
(
11). The mean extent of the ocular microtremor (OMT)
amplitude is 6 seconds of arc (12), and the peak-to-peak ro-
tation involves a displacement of the surface of the eye of
between approximately 150 and 2000 nm (13). The OMT
signal appears as an irregular oscillatory movement with in-
termittent burst-like components. These bursts have near-
sinusoidal oscillation (range 75–155 Hz), are generally of
greater amplitude than the rest of the microtremor, and pos-
METHODS
Subjects
A total of 72 normal healthy subjects were recruited for
study. Informed consent was obtained from all subjects.
M386

AGE AND OCULAR MICROTREMOR ACTIVITY
M387
Subjects under 21 years of age were not studied because of
concern regarding informed consent as defined by the Hos-
pital Ethics Committee. All subjects underwent a full his-
tory and clinical examination. Exclusion criteria were any
evidence or a history of neurological or ocular disease or
trauma. All subjects were free of medication. The subjects
were 54.22 ꢀ 2.41 years of age (mean ꢀ SD), with a range
of 21 to 88 years. The median was 54.50 years, and the
mode was 23 years. The subjects were divided by age into
seven groups: 21 to 30 years, 31 to 40 years, 41 to 50 years,
This system shows a frequency response between 20 and
150 Hz, which deviates less than 2 dB from peak response.
The system filters out inputs below 20 Hz, in particular any
drift movements. Microsaccades cannot be dealt with as
easily because the frequency content of microsaccades
overlaps that of OMT (12). Microsaccades occur only inter-
mittently. They are excluded by examining the intervening
record during analysis. The system has a signal-to-noise ra-
tio of ꢂ23 dB, and the resolution is less than 1% of the dy-
namic range, or 12 nm.
5
1 to 60 years, 61 to 70 years, 71 to 80 years, and over 80
years. Each group contained 10 subjects except for groups
1 to 40 years and 51 to 60 years, which contained 11 sub-
Record Analysis
3
The peaks occurring per unit time on a printed record are
counted. This provides a good estimate of the high-fre-
quency component of any random signal (20), particularly
OMT (13).
Peak counting is also the method of obtaining frequency
information favored by Coakley (17) who, to date, has pub-
lished the largest series on OMT.
jects each.
OMT was recorded using the piezoelectric transducer
technique. The OMT signal is not a completely determinis-
tic signal but has random elements (18). The piezoelectric
transducer technique is described in detail elsewhere (13)
and provides a reliable estimate of OMT activity (19).
Briefly, the piezoelectric element is mounted in a Perspex
rod and its tip is coated with silicone rubber. The subject
lies supine in a normally lit room looking straight ahead.
The subject is advised to keep their eyes fixating straight
ahead at a point on the ceiling throughout the recording.
Movements of the head can represent a source of noise, and
this problem is overcome by mounting the transducer onto
the head by means of a headset (13). The subject is advised
to keep their head still throughout the recording, but no
means of restraint are used.
The scleral surface is anesthetized with 0.5% proxymetha-
caine hydrochloride solution topically. The eyelids are re-
tracted with adhesive tape. The rubber-tipped piezoelectric
probe is lowered so that the probe is just touching the scleral
surface. Probe placement is judged by visual inspection and
by listening to the signal being recorded, using headphones.
All records were obtained by a single operator, and a re-
cording of between 30 seconds and 1 minute of activity was
taken (16). An example of a normal recording is given in
Figure 1.
The parameters measured were (Figure 1):
1
2
. The overall frequency (Hz)
. The number of bursts occurring per second, calculated
by counting the number of bursts in the record and divid-
ing by the record duration.
3
4
. The duration of bursts (milliseconds), calculated by esti-
mating the total duration of record occupied by bursts
and dividing by the number of bursts.
. The percentage of record occupied by baseline (%), cal-
culated as the total duration of baseline divided by the
record duration ꢃ 100.
5
. The frequency content of bursts (Hz), calculated by peak
counting over the total duration of bursts in a record.
. The duration of baseline (milliseconds), calculated by
taking the total duration of baseline and dividing by the
number of baseline segments in any given record.
. The frequency content of baseline (Hz), calculated by peak
counting over the total duration of baseline segments (16).
6
7
A least-squares linear regression correlation coefficient
The signal from each probe is passed to a conditioning
unit and amplifier with a 40-dB common mode rejection ra-
tio. The signal is then stored on audio tape using an adapted
Sony Walkman without automatic gain control. The tape is
later played back and analyzed on an ECG tape analyzer
was calculated for each parameter. A further comparison
was made between subjects younger than 60 years of age
and those older than 60 years of age.
RESULTS
(
Reynolds Medical Pathfinder 3 and a Reynolds Medical
Thermal Printer).
Linear Regression
The values for linear regression correlation coefficient
and age are given in Table 1, which shows that two parame-
Table 1. Linear Regression Coefficient (r) for 7 Parameters of
Ocular Microtremor Activity and Age in 72 Subjects
Parameter
r Value
t Value
p Value
Frequency, Hz
Baseline, %
Frequency baseline, Hz
Number of bursts
ꢄ.36
ꢄ.087
ꢄ.225
0
ꢄ3.26
ꢄ.728
ꢄ1.934
0
.002
.469
.057
1
Frequency of bursts, Hz
Duration of bursts, ms
Duration of baseline, ms
ꢄ.534
.162
ꢄ.004
ꢄ.528
1.37
ꢄ.365
.00
.17
.72
Figure 1. Example of a normal ocular microtremor record. Bursts,
which are identified visually from the record during analysis, are un-
derlined. The period between the bursts is the baseline.

M388
BOLGER ET AL.
Figure 2. Age versus ocular microtremor frequency (Hz).
ters of OMT activity are significantly correlated with age.
The overall frequency of OMT is negatively correlated with
age, tending to fall in older age groups. Although the corre-
lation coefficient is small at ꢄ0.36, it is highly significant
of r is ꢄ0.53 and is highly significant (p ꢁ .001) (Figure 3).
All of the remaining parameters except duration of bursts
are negatively correlated with age, but not significantly.
None of the mean values for each parameter for each age
group differed significantly from each other (multiple group
comparison and ANOVA). However, there was a tendency
for the overall frequency, baseline frequency, and frequency
content of burst to fall with age.
(
p ꢁ .002) (Figure 2).
The strongest correlation is that between the frequency
content of bursts and age. Once again the correlation is neg-
ative, with the frequency tending to fall with age. The value
Figure 3. Age and frequency content of bursts (Hz).

AGE AND OCULAR MICROTREMOR ACTIVITY
M389
Table 2. Mean Values for 7 Parameters of Ocular Microtremor
Activity in Subjects Younger and Older Than 60 Years of Age
sory input (21). Studies by Shimada and colleagues (22)
looked at age-related changes in brain size in the SAM-R/1
mouse model. They found age-related atrophy only in a re-
stricted part of the cerebral cortex, mainly in the parietal re-
gion. Neural activity from the inferior parietal cortex is
known to impinge on the oculomotor nuclei (23). It may be
that a loss of cells in this area (or decrease in function) with
age could therefore reduce neural activity.
Interestingly, elderly subjects show a decreased fre-
quency of nystagmus as stimulated through the vestibular
system (9). Thus, physiological changes are not confined to
the sensory input level alone. Histological changes in extra-
ocular muscle with age (4) may account for a changing re-
sponse to neuronal input in elderly persons. The disturbance
of orderly fiber alignment and direction of the muscles
themselves would tend to reduce the frequency of move-
ment for any given input. Furthermore, increases in muscle
collagen content would tend to decrease the compliance of
the globe, altering resonance, and could also be responsible
for a reduction in OMT frequency, if the neuromechanical
model of OMT is accepted (18).
ꢂ60 Years
ꢁ60 Years
Parameter
of Age
of Age
t Value
p Value
Frequency, Hz
Baseline, %
Frequency Baseline, Hz
Number of Bursts
Frequency of Bursts, Hz
Duration of Bursts, ms
80.5 ꢀ 4.7
52.3 ꢀ 11.6
85.3 ꢀ 6.8
8 ꢀ 1.4
75.3 ꢀ 4.2
59.1 ꢀ 6.7
86.8 ꢀ 5.5
52.4 ꢀ 11
94.4 ꢀ 10.6
8.2 ꢀ 1.4
80.5 ꢀ 4.1
58.2 ꢀ 7.9
69 ꢀ 28.4
4.7
.0001
.99
.0001
.7
.0001
.64
.76
.012
3.64
.376
4.9
.44
.31
Duration of Baseline, ms 71.3 ꢀ 27.9
Subjects Younger and Older Than 60 Years of Age
Table 2 gives the mean value for each parameter for each
group. There is a highly significant drop in the overall fre-
quency, the frequency content of the baseline, and the fre-
quency content of the bursts in subjects older than 60 years
of age (p ꢁ .0001). There is no significant change in the
other parameters.
In latter years it has been recognized that recording OMT
may be of value in clinical situations, particularly as a
method of assessing brain-stem function (11). Studies have
shown that OMT activity is reduced in comatose patients
and could have prognostic value (14,15). More recently, our
group has shown that OMT activity is absent in subjects
who are clinically diagnosed as being brain-stem dead (24).
Studies have also shown that OMT activity is affected by
anesthetic agents and propose that monitoring OMT may
have a role in assessing the depth of anesthesia (11). In rela-
tion to the clinical application of OMT, these results are im-
portant. They suggest that different values of normality
should operate for subjects older than 60 years of age, at
least for frequency parameters. They also suggest that age
matching of subjects in controlled trials of OMT is essential
if valid conclusions are to be drawn from study results.
DISCUSSION
These results indicate a tendency for two of the three fre-
quency parameters of OMT (i.e., the overall frequency and
the frequency content of the bursts) to fall with advancing
age. Although the strength of the correlation for overall fre-
quency is small (r ꢅ ꢄ0.36), it remains significant (p ꢁ
.
002). The negative correlation between the frequency con-
tent of the burst and age is stronger (r ꢅ ꢄ0.534). In sub-
jects older than 60 years of age there is a significant fall in
all three frequency parameters of OMT activity (i.e., the
overall frequency, the frequency content of the baseline,
and the frequency content of the bursts). In each case the
difference is small, about 5.3 Hz for overall frequency, 9.1
Hz for baseline frequency, and 5.2 Hz for frequency content
of bursts. However, all these differences are significant.
However, a previous study by Coakley (17) compared
OMT in 26 young adults and 15 subjects older than 70 years
of age. He could find no significant change in OMT fre-
quency associated with age. This could be explained by the
small number of subjects studied. The analysis of the mi-
crotremor record in this study was based on velocity rather
than on displacement waveforms, as in our study. Velocity
against time analysis will enhance the contribution of
higher-frequency components to the overall measured fre-
quency.
Acknowledgments
This research was supported by the Health Research Board, Ireland.
Address correspondence to Stana Bojanic, The Department of Neuro-
surgery, The Radcliffe Infirmary, Woodstock Road, Oxford OX2 1HE,
United Kingdom. E-mail: Stana.Bojanic@excite.co.uk
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Received December 1, 2000
Accepted December 5, 2000
Decision Editor: William B. Ershler, MD