Investigative Ophthalmology & Visual Science, Vol. 32, No. 13, December 1991
Copyright © Association for Research in Vision and Ophthalmology
Upper Eyelid Movements Measured With a Search Coil
During Blinks and Vertical Saccades
Daniel Guirron,* Raymond Simard,t and Francois Coderef
Upper eyelid movements were recorded in nine human subjects by mounting a miniature coil of wire
directly on the eyelid and subjecting the search coil to a vertically directed alternating magnetic field.
The metrics of blinks and lid movements accompanying saccades were described by "main sequence"
relationships, linking maximum velocity to amplitude and duration to amplitude. In general, lid movements were faster than those reported previously in the literature, but there was considerable intersubject variability. On average, the main sequence relationships for blinks were independent of either
starting lid position or whether the blinks were generated spontaneously, reflexively, or voluntarily.
For the down phase of the average blink, both the maximum velocity and duration increased almost
linearly with amplitude. The maximum velocity of the down phase was faster than that of the up phase.
For lid movements accompanying vertical saccades, the maximum velocities in the up and down directions were similar and increased nonlinearly with amplitude, saturating at about 120 mm/sec (approximately 450° /sec). Duration increased approximately linearly with amplitude. The down phases of
blinks were much faster than those of saccade-related lid movements. By comparison, the maximum
velocities of the up phase of blinks and of saccade-related lid movements were almost equal. The large
intersubject variability suggests caution when using normative data to interpret abnormal lid motion for
clinical purposes. Invest Ophthalmol Vis Sci 32:3298-3305,1991
Neuro-ophthalmologists and eyelid surgeons analyze lid motility for assessing ptosis, third and seventh
nerve palsy, myasthenia gravis, Graves's disease, and
Parinaud's syndrome. Currently, mainly static measurements of the lidfissureand levator action (amplitude) are done routinely. No clinical tool is widely
available that easily permits the measurement of the
kinematics of eyelid movements.
Many different techniques have been used to measure the time course of blinks. In some, eyelid motion
was transformed into the motion of an external device
by a mechanical attachment (lever arm) between the
eyelid and the device. These methods include the following systems: lever arm to writing pen,1 lever arm
to potentiometer,2 lever arm to moving light-emitting
diode and photosensitive position detector,3 and lever
arm to search coil in magneticfield.4In other studies,
From the *Montreal Neurological Institute, Department of Neurology and Neurosurgery, and the f Department of Ophthalmology,
McGill University, Montreal, Canada.
Supported by the Medical Research Council of Canada.
Submitted for publication: March 13, 1989; accepted June 27,
1991.
Reprint requests: Dr. Daniel Guitton, Montreal Neurological Institute, 3801 University Street, Montreal, Quebec, Canada H3A
2B4.
the eyelid was not attached to an external device.
These methods include high-speed cinephotography,56 interruption of a light beam by an opaque extension of the eyelashes,7-8 reflection of a light beam
from a reflector mounted on the eyelashes,9 and
changes in overall reflected light measured by a photocell.10
These techniques are cumbersome and difficult to
use, particularly in a clinical environment. We employed a much more convenient technique in our
study and in parallel studies recently published.1112
Eyelid motion was measured with a search coil in a
magnetic field technique.13 In this method, a small
light-weight coil of wire is affixed directly to the upper
eyelid. This highly precise method, requiring no mechanical links between the eyelid and an external device, is simple to install, calibrate, and use. Furthermore, the electronic circuitry is simpler than analogous eye movement measuring systems because only
a single-channel magnetic field generator and demodulator is required.
In nine subjects, we used this technique to measure
and compare upper lid motion during spontaneous,
reflexive, and voluntary blinks and during saccades in
the vertical plane. Our study and a previous one12
define a data base of the kinematics of the different
types of eyelid movements in at least 18 subjects. Ad-
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EYELID MOVEMENTS DURING BLINKS AND VERTICAL SACCADES / Guirron er ol
ditional data on lid movements accompanying saccades were provided in another study.11 A summary
of our results was presented earlier.14
Materials and Methods
A small circular coil of wire (with a 5-mm diameter,
15 epoxy-bound turns, single-conductor, unshielded,
six strands of 1-mil stainless-steel wire, Teflon coated
[Cooner Wire Co., Chatsworth, CA]) was attached to
a cardboard base plate. The total weight of the assembly was 0.1 g. The base plate was positioned close to
the eyelid on the eyelashes of the upper lid by means
of double-sided adhesive tape. The angle of the coil
was adjusted for each subject so that, when the subject
looked straight ahead and the eye was approximately
in the primary position, the plane of the coil was tilted
about 20° back with respect to the vertical plane. According to others,6 a spontaneous blink uses a driving
force of about 20 g in the down-acting orbicularis
oculi (00) muscle. Upper lid stiffness in primary gaze
was estimated to be approximately 10 g/mm.3 By comparison, the weight of our device was negligible and
should not have affected eyelid dynamics. Furthermore, the eyelash-lid substrate provided a stable platform, as evidenced by the lack of coil oscillations during lid accelerations and decelerations.
The subject's head was positioned at the center of a
cube-like field coil arrangement, which in our laboratory is used to monitor eye movements.15 Immobility
of the head was ensured by asking each subject to grip
a disposable wooden bite bar between their teeth. The
search coil signal was filtered electronically (-24 dB,
100 Hz).
Recordings were made in nine healthy subjects
(seven women and two men; mean age, 36 yr; age
range, 26-49 yr). Informed consent was obtained
from each subject after the nature of the procedure
had been explained fully.
To calibrate and evaluate the linearity of the coil
signal, lid positions were monitored photographically
with a 35-mm camera in four subjects as they fixated
targets 10° apart, ranging from primary gaze position
to 40° downward gaze. A measuring scale, fixed laterally to the palpebral fissure, was included in each
photograph to assure precise measurement of the lid
position. With the 10X magnification obtained by
projecting slides onto a screen, the lid position could
be evaluated to ± 0.1 mm. Calibration curves were
obtained by plotting the lid position, in millimeters,
against the coil output voltage; the latter was proportional to sin 9 where 0 was the angle between the
coil's plane and the vertical magnetic field. For lid
motions beginning 2-3 mm above the horizontal
3299
plane (approximate lid position when the eye is in
primary position) to approximately 7-8 mm below
the horizontal (when the eye is looking 40° down), the
coil's signal and the lid's linear displacements were
proportional to each other within approximately 5%
(because sin G = 0 for small 0). Given the excellent
linearity of this method, the calibration curves for the
remaining five subjects were obtained by measuring
the total overall lid displacement (for a gaze change,
0-40° down) with the measuring scale, Movements of
the eyelid above primary gaze were not measured because the superior orbital rim impeded search coil
motion.
Others presented eyelid motion in terms of angular
displacements,1112 and all other studies gave linear
displacements. Although our calibration procedure
gave us results in linear motion, we present our data
on eyelid motion as both linear and angular displacements to permit a comparison with data in the literature. To do this, the linear lid displacements we obtained in the calibration were converted to angular
rotations. In the four subjects in whom lid displacements were measured accurately by photography, we
found 10° of eye rotation equaled 2.6 mm (±0.1) of
lid displacement. On the basis of earlier data,11 we
assumed that angular lid displacements equaled 1.1
X angular eye displacements. This identity may not
be true for a particular subject but may hold on
average.11
Three types of blinks were studied: spontaneous
blinks, reflexively driven blinks using a gentle puff of
air applied to the periorbital region, and voluntary
blinks generated in response to a request by the experimenters. Eyelid movements associated with vertir
cally generated saccades also were studied. A total of
420 blinks and 175 saccade-related lid movements
were recorded and sampled at 500 Hz by a computer.
The amplitude, maximum velocity, and duration of
blinks were obtained using software designed to analyze eye movements.15
Results
Blink Characteristics
Figure 1 shows the position and velocity traces for a
large spontaneous blink. The short pause between the
downward and upward lid movements facilitated the
distinction between these two phases. This pause often was present in large blinks, such as the one in this
example (approximately 13.5 mm) because the upper
lid may rest against the lower lid; the width of the
palpebral fissure averaged approximately 11 mm.
As described in other studies,612 the down phase
had a higher maximum velocity than the up phase.
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INVESTIGATIVE OPHTHALMOLOGY & VISUAL SCIENCE / December 1991
Spontaneous Blink
Vol. 32
amplitude range, show that there were no significant
differences in maximum velocity among spontaneous, reflexive, and voluntary blinks. The differences
between spontaneous and voluntary blinks for amplitudes greater than 11.5/mm may not be significant
because few spontaneous blinks were available at
those amplitudes.
Figures 3B and 3D show the duration versus amplitude characteristics of the down and up phases, respectively, of spontaneous blinks. For clarity, the points
Voluntary Blinks
Closing Phase
300
Fig. 1. Position and velocity traces for a typical large amplitude
spontaneous blink. Vertical dashed lines mark the start and end for
each of the down- and up-phases, respectively.
A
(mm/!
200
150
100
•
elocii
Furthermore, the acceleration and deceleration times
in the down phase were similar. For the up phase,
however, maximum velocity was reached earlier in
the movement, and there was a correspondingly
longer deceleration phase. A typical spontaneous
blink of 10-mm amplitude presented, in the closing
and opening phases, maximum velocities of approximately 350 mm/sec and 150 mm/sec, respectively,
and durations of 85 msec and 200 msec, respectively.
To appreciate the high speed of blinks, a linear velocity of 350 mm/sec at the cornea corresponds to
an angular velocity of the eye of approximately
1700°/sec.
Effect of starting lid position: Because we will be
analyzing different lid disorders (eg, ptosis) in future
studies, we determined (for a given amplitude of voluntary blink) the effect of starting position on maximum velocity. These results are shown in Figure 2 for
a subject whose results were typical. The data for the
closing (Fig. 2A) and opening (Fig. 2B) phases indicated that maximum velocity was dependent on blink
amplitude but hot on starting lid position. This observation led us, in the analyses that follow, to group all
blinks of a given amplitude together independent of
each blink's starting lid position.
Main sequence relations: Figures 3A and 3C show
plots of maximum velocity versus amplitude for the
down and up phases, respectively, of spontaneous, reflex, and voluntary blinks. Each point was obtained
by averaging, across all subjects, the maximum velocities of all blinks in each category (amplitude range,
approximately 1 mm). These results, for most of the
250
50
0
10
X
03
Opening Phase
100
B
50
0
10
Amplitude (mm)
Fig. 2. Effect of starting lid position on maximum velocity versus
amplitude relationship of voluntary blinks. (A, B) Closing and
opening phases, respectively. Each point represents a single movement. Starting lid positions are specified for different downward eye
positions relative to straight ahead. Filled circles, straight ahead
(primary position); triangles, 10° down; filled squares, 20° down.
Note that, for different fixation positions in the vertical plane, 10°
of eye rotation corresponds to about 2.6 mm of lid displacement.
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EYELID MOVEMENTS DURING BLINKS AND VERTICAL SACCADES / Guirron er ol
Blink Up Phase
Blink Down Phase
500
^
400
E,
CO
>, 300
300
"o
•+—>
o
%
200
x
100
>, 200
o
•<—»
•§ 100
10
15
I
5
10
15
10
15
B
100
CO
E,
c:
o
CO
300
50
Q
c
o
200
CO
100
Q
5
10
15
5
Amplitude (mm)
Amplitude (mm)
Fig. 3. Metrics of human blinks: the "main sequence" relationships. (A, C) Maximum velocity versus amplitude. (B, D) Duration versus
amplitude. Blink down-phases are shown in left column; blink up-phases on right. Each point is the mean of between six and 32 blinks except
at amplitudes 1.5 mm, 12.5 mm, and 13.5 mm where less than five blinks were available in each case. Each point represents the mean
amplitude of all blinks whose amplitudes lie between +0.4 mm and -0.5 mm of a scale mark on the abscissa: for example, the blinks whose
mean amplitude is close to 5 mm lie between 4.5 and 5.4 mm. Vertical bars on each point show one standard deviation.
Eyelids Movements
with Ocular Saccade
for reflex and voluntary blinks are not shown because
the lines overlapped extensively.
Lid Movements Accompanying Saccades in the
Vertical Plane
Position
90 mm/s
5.5 mm
Velocity
50 ms
Fig. 4. Downward and upward lid movements accompanying
30° downward and upward saccades, respectively. Vertical dashed
lines indicate start of each phase.
Figure 4 shows an example of a lid movement accompanying 30° downward and upward saccades
that began and ended in central gaze position. These
lid movements also were independent of starting lid
position, and consequently, all movements of a given
amplitude were grouped together, independent of
their initial position. In general, the down phase was
slightly faster than the up phase (Fig. 5 A). An extreme
example of this difference is shown in Figure 4. Correspondingly, the up phase had a longer duration (Fig.
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INVESTIGATIVE OPHTHALMOLOGY & VISUAL SCIENCE / December 1991
Lid Motion with Saccades
180
160
Down
140
120
100
Vol. 32
ours analyzed a large number of blinks. The legend to
Figure 6 gives details on each experimental situation.
In addition to the available data on blink characteristics expressed in linear displacements, we included
in Figure 6 these earlier results12 (line E2M, mean
data; line E2R, reflex blink data) where blinks were
measured in terms of angular rotations. To compare
80
60
Blink Up Phase
40
E
20
300-i
0
10
£»
250
•§
200-
300 r
E
150-
250
I
100-
**
50-
-1000
Amplitude (mm)
B
E
200
+2SD
-500
Down
g
150
3
100
(deg)
5
.
10
15 (mm)
Amplitude
B
50
-$
$
Blink Down Phase
/+2SD
E
E.
Amplitude (mm)
Fig. 5. Metrics of lid movements accompanying vertical saccades. (A) Maximum velocity versus amplitude. (B) Duration versus amplitude. Open circles: down-phase. Filled circles: up-phase.
Each point is the mean of between seven and 32 lid movements. See
Figure 4 for additional details.
500- I-2000
450-
, E2R
400350- -1500
300250
1000
200-
5B). When the subject looked down and the fixation
point was extinguished, signifying that the target at 0°
was being lit, the subject frequently (not shown in Fig.
4) made a step-like sequence of two or more saccades
to reach the target. This was caused by the finding
that, in downgaze, the higher visual target was not
visible; it was hidden by the upper lid. Consequently,
fewer points were available to describe large upward
movements of the lid during upward saccades.
Discussion
Comparisons Between Our Data and Those of Others
Blinks: Figures 6A and 6B compare our results, for
the up and down phases, respectively, of blinks, with
other data published within about the last decade.
The two light solid lines span ± two standard deviations around the mean of all our blinks presented in
Figures 3A and 3C. Only two other studies312 and
150100-
-500
50-
60
40
0
5
10
(deg)
15 (mm)
Amplitude
Fig. 6. Blinks: Comparison between our maximum velocity-amplitude relationships and those obtained by others. Heavy solid
lines: mean through the points shown in Figure 3A; number of
subjects = 9, number of blinks = 410. Thin solid lines show the
range of two standard deviations about our mean line. Dotted line
(E1): Evinger et al,3 number of subjects = 3, number of blinks about
150; spontaneous blinks have amplitudes less than about 6 mm,
voluntary blinks, greater than 6 mm. Dashed lines: Evinger et al,12
line E2M, mean through the data for all blinks obtained from nine
subjects, about 400 blinks; line E2R, mean through reflex blink
data only. Open circle: Collewijn et al,4 one subject, mean of four
voluntary blinks. Closed squares: Hung et al,6 each point is a single
blink, three subjects. Closed circles: Doane,5 each point is a single
spontaneous blink from three subjects. Large dashed square:
Doane,6 boundary of four spontaneous blinks in a "typical subject."
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EYELID MOVEMENTS DURING BLINKS AND VERTICAL SACCADES / Guirron er ol
angular and linear measurements, we assumed 10° of
lid rotation equaled 2.4 mm of lid displacement.
Figure 6 A shows that our measurements of the velocity of blink up phases agreed well with those of
Hung et al6 and with the lower range (approximately
< 45°) of Evinger et al.12 Our results differed from
those of other studies.3-5 The difference between the
two studies of Evinger et al,312 the variability in the
results of Hung et al,6 and our large standard deviation emphasize the variability in blink up phase velocity.
The variability in down phase velocity also is important. Figure 6B shows that the maximum velocity
of down phases we measured tend to be higher than
those reported by other experimenters. Are these differences a result of the measuring technique, related
to natural variations between subjects, or caused by
the nature of the experimental paradigm? With regard
to the latter, it is known that important variations in
velocity may be a result of cognitive effects. When
spontaneous blinks were analyzed with a hidden highspeed camera, it was reported that most blinks were
incomplete and did not completely close the eye.5 For
a "typical subject," a blink of 8-9-mm amplitude had
a maximum velocity of about 190 mm/sec. (We
found approximately 300 mm/sec). When subjects
were aware of the recording process and its purpose,
they had larger and faster movements even if instructed to blink naturally. This behavioral observation could explain why we recorded faster movements
and found large-amplitude blinks when gaze was in
central position. Most of our "spontaneous" blinks
with the eye in primary position had amplitudes
greater than 6 mm. To obtain spontaneous blinks of
smaller amplitude, we required the subjects to look
downward, thereby lowering the initial lid position.
Seven of our nine subjects were naive both as experimental subjects and as to the nature of the experiment. These subjects were somewhat apprehensive of
the experimental situation, but this also would be typical of a clinical population. Thus, we believe that few
of our blinks were genuinely spontaneous as found in
the earlier study where the subjects were unaware of
its experimental purpose.5 For clinical purposes, it is
impractical to distinguish between voluntary and
spontaneous blinks.
Our data agree best with those of two previous studies612 (in the latter, the reflexively driven blinks or line
E2R). In the former study, the subjects were aware of
the experimental paradigm and were asked to blink
naturally while their eyes were being filmed. This behavioral context is analogous to ours. In the latter
study, the reflexive movements were triggered by stimulating the supraorbital branch of the trigeminal
3303
nerve. This produced the fastest movements (compare lines E2R and E2M). In another study (line El), 3
the three subjects were among the authors of the
paper, and their movements less than approximately
6 mm were spontaneous blinks. Their voluntary
blinks (amplitudes greater than 6 mm) showed a rapid
increase in velocity with amplitude; for amplitudes
near 10 mm, they were within our range.
Lid movements with saccades: Figure 7 compares
our results to those of others.3'11>12 The long dashes are
revised values12 compared with those published earlier (dotted lines3) which were obtained for one subject considered to be slow. To compare these results
(and others: short dashes11) with ours, we converted
our results to angular rotations. Our results for upward and downward lid movements were in good
agreement only with those in one study for large blink
angles.12 By comparison, the maximum velocities of
our upward lid movements were in excellent agreement with those of others,11 but our downward movement measurements were faster than theirs. These authors report that a lid movement had a similar maximum velocity as a saccade of the same amplitude:
thus, their average 20° downward saccade had a maximum velocity of approximately 220°/sec. This is an
extremely slow saccade and at the borderline of normality.16 As shown by the ± two standard deviation
line, these results emphasize the inherent large variation in lid velocity that can be obtained for any given
amplitude of lid displacement in a specific experimental condition.
Lid Motion with Saccades
140-
+2SD
-600
'5
O 100- -400
p
E
8
60 H
-200
4020-
(deg)
0
1
2
3
4
5
6
7
8
9
1
0
(mm)
Amplitude
Fig. 7. Lid movement accompanying saccades in the vertical
plane: comparison between our results (open and filled circles
linked by solid lines) and those obtained by Evinger et al,12 dashed
lines; Evinger et al,3 dotted line; and Becker and Fuchs," dashspace-dash line. Arrows on right indicate direction of movement.
Upper thin line labeled +2 SD gives two standard deviations above
mean line for down-phases.
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INVESTIGATIVE OPHTHALMOLOGY & VISUAL SCIENCE / December 1991
General Considerations: Electromyographic Activity
The patterns of electromyographic (EMG) activity
in the 0 0 and levator palpebrae (LP) muscles, responsible for actively lowering and raising the upper eyelid, respectively, were reviewed in detail.12'17 We summarize briefly current views on the EMG patterns
during blinks and lid movements with saccades. In
the resting state, looking straight ahead, the LP muscle generates an upward tonic force that counteracts a
passive downward force generated in the OO and tissues.
Downward lid motion: In the blinking process,
EMG recordings show that the closing phase results
from a cessation of activity in the LP combined with a
pulse-step-like (burst-tonic) discharge (as in rapid ocular saccades) in the 0 0 . For lid movements accompanying down saccades, there is cessation of activity
in the LP, and lid motion is thought to result only
from passive forces in the OO and tissues, assisted by
the rotating eye. Gravity is not necessary for downward lid displacement because the lid also closes when
subjects are standing on their heads.18 These arguments can explain why the down phases accompanying saccades are slower than the down phases in blinks
(Figs. 3A, 5A).
There are strong arguments suggesting that only
passive forces drive downward lid motion during saccades. 12 For example, the OO appears to be inactive in
these movements. Furthermore, patients with seventh nerve palsy (paralyzed OO) cannot blink and yet
have normal downward lid movements during downward saccades.19 Suppression of activity in the LP occurs in both conditions, and the disabled down phase
during blinks with steady gaze may be caused by the
restraining action of the fascia that link the superior
rectus and the LP muscles. During down saccades,
there is relaxation of both these muscles. Arguments
against passive forces were reviewed by others.1' They
state that by invoking "only. . .passive elastic forces,
it is difficult to explain the existence of downward lid
movements with saccade trajectories." In our results,
downward lid motion during saccades was generally
faster than upward motion (Fig. 7). However, the latter motion uses burst-tonic EMG activity in LP.
Upward lid motion: Upward lid movements accompanying upward saccades are thought to be generated
by a pulse-step discharge in the LP similar to that seen
in the superior rectus muscle, and the OO is inactive.
By comparison, the opening phase of a blink is believed to result from a cessation of activity in the OO
and either a step or pulse-step upward force in the LP
that returns the upper lid to its resting state.12 What
type of EMG pattern in LP drove the up phase of
Up Phase
200
..• Blink
E 150
With up-going
saccade
o 100
_o
X
CO
50
5
10
15
Amplitude (mm)
Fig. 8. Comparison between the maximum velocities of the upphases of our spontaneous blinks (filled circles, from Fig. 3C) and
lid movements accompanying saccades in the vertical plane (filled
squares, from Fig. 5A).
blinks in our subjects? Figure 8 compares the up
phase of blinks with that of lid motion during saccades for our results (Figs. 3C, 5A). These movements
have indistinguishable maximum velocities, suggesting that a pulse-step of activity in the LP drove the
upward phase of blinks in our subjects. Saccade velocity saturates at greater amplitudes,15'20 and because
the superior rectus and the LP muscles are believed to
receive similar innervation patterns during vertical
saccades, this could explain why upward lid maximum velocity during saccades also saturates. As suggested by Figure 8, the pulse associated with the up
phase of a blink may not be subject to the same saturation.
Key words: blinks, eyelid movements, search coil in magnetic field
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