0042-6989/92 $5.00 + 0.00
Copyright © 1992 Pergamon Press pIc
Vision Res. Vol. 32, No.1, pp. 167-171, 1992
Printed in Great Britain. All rights reserved
Research Note
Eye Movements During Motion After-effect
s.
H. SEIDMAN,* R. J. LEIGH,*tt
c.
W. THOMAS*
Received 6 February 1991; in revised form 23 May 1991
Using the magnetic search coil technique, we measured torsional eye movements in four male subjects
during and after rotation of a visual display around the line of sight. During rotation of the display,
subjects developed a torsional nystagmus with slow-phases in the direction of target rotation that had
a typical gain of < 0.01. Upon cessation of display motion, subjects experienced a motion after-effect
(MAE) in the direction opposite prior target rotation, which persisted for > 15 sec. During this MAE,
slow-phase eye movements of low velocity were in the same direction as the MAE, but did not persist
as long as perceptual effects. In separate experiments, horizontal eye movements were recorded during
horizontal stimulus motion; during MAE, no eye movements occurred due to stronger fixation
mechanisms. We conclude that MAE is not caused by retinal slip of images, but MAE and the
accompanying eye movements might be produced by shared or similar mechanisms.
Motion after-effect
Human ocular torsion
Magnetic search coil
INTRODUCTION
The motion after-effect (MAE) is an illusory motion
perception which follows the viewing of a moving target.
After the target stops moving, it appears to move in the
opposite direction (Holland, 1965; Wohlgemuth, 1911).
This phenomenon, for historical reasons, is also known
as the waterfall effect. Eye movements during MAE have
not been measured, although there has been speculation
as to their presence and effects (Masland, 1969).
A popular stimulus for the study of MAE has been a
rotating spiral. According to Cavanagh and Favreau
(1980), one justification for this particular stimulus has
been that rotation of a target around the line of sight
involves stimulation of all directions equally, giving rise
to the assumption that the eyes do not move during
stimulation. This is thought to rule out eye movements
as an artifactual cause of the MAE. The eyes, however,
are perfectly able to move about the line of sight during
this type of stimulation (i.e. torsional, or cyclorotatory
eye movements), and therefore the veracity of this
assumption requires investigation.
It has been shown by Collewijn, Van der Steen,
Ferman and Jansen (1985) and by Morrow and Sharpe
*Department of Biomedical Engineering, University Hospitals, Case
Western Reserve University and Cleveland Veteran Affairs Medical
Center, Cleveland, OH 44106, U.S.A.
tDepartments of Neurology, Neuroscience and Otolaryngology, University Hospitals, Case Western Reserve University and Cleveland
Veterans Affairs Medical Center, Cleveland, OH 44106, U.S.A.
tTo whom all correspondence should be addressed at the Department
of Neurology, University Hospitals, 2074 Abington Road, Cleveland, OH 44106, U.S.A.
167
Eye movement
Optokinetic nystagmus
(1989) that torsional optokinetic nystagmus (OKN) and
optokinetic after-nystagmus (OKAN), although low in
gain, do occur when a subject is exposed to a full-field
visual stimulus rotating around the line of sight. If
OKAN occurs when the target stops, then the retinal slip
caused by the OKAN would be in the appropriate
direction to cause an apparent reversal of target motion.
This would suggest that MAE is, at least in part, due to
drift of images on the retina, i.e. "retinal slip".
MAE can also be induced by sustained visual motion
in the horizontal plane, but the properties of horizontal
fixation and pursuit differ greatly from the torsional
case.
Our goals, therefore, were to (1) observe eye movements during torsional and horizontal MAE and (2) to
determine if MAE was caused by retinal slip following
the motion of the target. Some of these findings have
been presented in abstract form (Seidman, Thomas,
Huebner, Billian & Leigh, 1990).
METHODS
Four male human subjects, ages 24-43, were studied.
All gave informed consent. Two subjects were myopes,
one of whom habitually wore contact lenses; none wore
corrections during the experiments.
Torsional and horizontal rotations of one eye were
recorded using a "double-loop" silastic search coil
(Skalar, Delft, the Netherlands) and 6 ft field coils (CNC
Engineering, Seattle, W A) that employed a rotating field
in the horizontal plane and an alternating field in the
torsional plane (Seidman & Leigh, 1989). The search coil
RESEARCH NOTE
168
was precalibrated on a protractor device prior to placement on the subject's eye. The measurements of eye
position were 98.5% linear over an operating range of
± 20°. The SD of the noise of our coil system was
< 1 min arc. The crosstalk artifact on the torsional
channel produced by horizontal or vertical rotations was
セ@ 0.025° torsion per deg of horizontal or vertical movement. Crosstalk of this magnitude did not effect our
results. Data were filtered (0-40 Hz) using 4-pole maximally flat filters (Krohn-Hite Corporation, Avon, MA)
and digitized at 100 Hz using a 16-bit data acquisition
board (Data Translation, Marlborough, MA) installed
in an IBM PC-AT computer.
Because the torsional eye movements produced by
our stimuli were small in magnitude, instantaneous eye
velocity was estimated at approx. 75 instances during
each trial using an interactive program. This provided a
convenient method to view slow-phase direction.
Visual targets were generated using an IBM PC-AT
with a dedicated board used to create the images. These
images were recorded directly on to videotape. A 19"
monitor was used to present the stimuli to the subjects.
The monitor was placed outside of the magnetic field,
and was thus approx. 3 ft from the subject. At this
distance, the monitor sub tended > 30° of the visual field
of the subject, who viewed the display binocularly.
Two different groups of stimuli were generated. The
first group consisted of circular targets which incorporated 8 or 16 alternating light and dark sectors with a
fixation spot in the center, and rotated around the
line of sight with angular velocities of 60 or 90 degjsec
[Fig. 1(A)]. Although this stimulus is not a spiral, MAE
is still elicited, and the torsional optokinetic system is
stimulated without the presence of complicating linear
components. Subjects were requested to fixate upon the
center of the rotating display. The second group consisted of 8 or 16 alternating vertical light and dark bars,
with a central fixation spot [Fig. 1(B)]. These targets
moved to the right, and, at the viewing distance of 3 ft,
had linear velocities of 6 or 9 degjsec. Neither the
torsional or the horizontal stimuli elicited circularvection (CV) in any subjects.
Subjects reported perceptions of motion through use
of a continuous potentiometer, which they were asked to
rotate at a velocity matching the apparent velocity of the
display stimulus. This signal was filtered and digitized in
the same manner as the eye position signal.
The stationary target was presented on the monitor
for a period of 20 sec. At the end of this time period,
the target started to move, and continued to do so for
20 sec. The target then stopped moving, but remained
visible for a further 60 sec. Data collection began
approx. 10 sec prior to target movement, and continued
for 60 sec.
RESULTS
Typical responses are shown in Fig. 2, while the
responses of all subjects are summarized in Table 1.
During rotation of the circular targets, all subjects
TABLE 1
Post-movement
duration (sec)
Target
Subject
Mode
Sectors
Velocity
e/sec)
Perception
Eye
movement
Peak/
steady state
T
16
16
8
16
16
8
16
16
8
16
16
8
16
16
8
16
16
8
16
16
8
16
16
8
60
90
60
6
9
6
60
90
60
6
9
6
60
90
60
6
9
6
60
90
60
6
9
6
21.0
24.6
>33.9
12.6
23.7
27.6
23.3
17.7
18.0
5.9
6.9
6.8
18.7
20.8
16.0
t
11.8
17.1
24.9
t
t
5.4
5.0
15.0
17.2
19.6
26.9
*
*
*
17.5
12.1
5.6
*
*
*
6.9
13.2
7.5
t
*
*
10.0
20.8
11.3
*
*
*
0.01/ <0.01
<0.01/ <0.01
0.01/<0.01
0.72/0.20
0.87/0.08
0.57/0.15
0.04/<0.01
0.06/ <0.01
0.04/<0.01
0.70/0.11
0.55/0.11
0.70/0.15
0.04/0.02
0.03/ <0.01
0.03/<0.01
t
0.79/0.33
0.62/0.13
0.03/0.01
0.02/<0.01
0.03/ <0.01
0.05/0.03
0.04/<0.01
0.08/0.07
H
2
T
H
3
T
H
4
Gain
T
H
T, torsional; H, horizontal; Gain, optokinetic gain during target motion.
*Not applicable (suppressed by fixation, see text).
tNot measured.
RESEARCH NOTE
FIGURE 1. Typical stimuli: (A) torsional and (B) horizontal. See text for details.
169
170
RESEARCH NOTE
(A)
TARGET MOTION
セ@
"0
<V
"2
:e
"0
()
c
2......
0...
<V
セ@
<V
CL
4.0
3.0
+ velocity
3.0
+
2.0
,..-..,
0'
1.0
<V
3
c
0
:;:;
-position
+
+
0.0
-1.0
<V
0'
II>
+
N[Kセ@
GZNMKセ@
+ +
·w -2.0
0
o
QNPセ@
+
+
+ + +++ +
................... +-
2.0
0.0 3
セGK@
1::-
+
'g
-1.0
CL
q;
-3.0
-2.0 >
-4.0
-5.0
'---'---'--.L.----L_'---'---'---'---1_'---'---'---'----'-_'---'---'---'--'-_L..-.J.-o-'---'---'
0
20
10
30
40
50
-3.0
60
Time (sec)
(B)
TARGET MOTION
......
"0
セ@
.!
2
'5
()
c
20セ@
III
III
CL
3.0
4.0
2.0
.......
0'1
III
+ velocity
-position
+
2.0
QNPセ@
0.0
--..
U
II>
0'
II>
3
-2.0
0.0
3
'w0 -4.0
-1.0
'g
c
:3
1::-
CL
Gi
-2.0 >
-6.0
-8.0
0
10
20
40
30
50
Time (sec)
FIGURE 2. Typical responses to torsional and horizontal motion stimuli. Lower traces show eye position (line) and
instantaneous estimates of eye velocity (crosses). Upper trace shows perception, as reported by subjects with a continuous
potentiometer. (A) Torsional motion stimulus of 180 deg/sec and (B) horizontal motion stimulus of 9 deg/sec, followed by
fixation on center of still target. Note reversal of slow phase direction following cessation of target movement in (A) and the
lack of a reversal in (B).
signaled stimulus motion and developed a torsional
nystagmus with slow-phase eye movements going in the
same direction as the target. The gain of the slow-phases
of this nystagmus was low, with a steady state value
usually < 0.01. Peak slow-phase velocity, occurring near
the onset of target motion, tended to be slightly higher
in gain.
Upon motion cessation of the circular target, all
subjects reported an illusory reversal in the direction of
target motion, or MAE. This illusory motion persisted
for a median time of 20.9 sec (range 16.0->33.9 sec).
During this period slow-phase eye movements also reversed direction, with one subject actually developing
torsional nystagmus. This reversed nystagmus was
usually of lower velocity than that developed during
target rotation, and declined to zero in a median time of
12.6 sec [range 5.6-26.9 sec, Fig. 2(A)].
Horizontal eye movements were monitored during
torsional trials, and were found to deviate < 2° from the
center of the target with velocities < 2 deg/sec. These
movements would be expected to produce < 0.05 deg
and < 0.05 deg/sec of crosstalk artifact on the torsional
channel, which is too small to bias our results.
During horizontal target motion, subjects developed
a small horizontal nystagmus, once again with slowphases in the same direction as the target. The
171
RESEARCH NOTE
steady-state gain of the slow-phases of this nystagmus
was low (mean = 0.125) presumably because of the
suppression of OKN by fixation mechanisms.
Following horizontal target movement, subjects experienced a small, short-lived MAE which was reported
to be less compelling than torsional MAE. The MAE
lasted for a median time of 11.5 sec (range 5.0-27.6 sec).
Reversal of horizontal nystagmus did not occur following cessation of target motion [Fig. 2(B)].
DISCUSSION
activity of secondary visual areas in cerebral cortex
that encode both torsional visual stimuli and eye movement signals (Graziano, Andersen & Snowden, 1990;
Newsome, Wurtz & Komatsu, 1988).
REFERENCES
Brandt, T., Dichgans, J. & Biichele, W. (1974). Motion habituation:
Inverted self-motion perception and optokinetic after-nystagmus.
Experimental Brain Research, 21, 337-352.
Cavanagh, P. & Favreau, O. E. (1980). Motion aftereffect: Global
mechanism for the perception of rotation. Perception, 9, 175-182.
Collewijn, H., Van der Steen, J., Ferman, L. & Jansen, T. C. (1985).
Human ocular counterroll: Assessment of static and dynamic properties from electromagnetic scleral coil recordings. Experimental
Brain Research, 59, 185-196.
Ferman, L., Collewijn, H., Jansen, T. C. & Van den Berg, A. V. (1987).
Human gaze stability in the horizontal, vertical, and torsional
direction during voluntary head movements, evaluated with a three
dimensional scleral induction coil technique. Vision Research, 27,
811-828.
Graziano, M., Andersen, R. & Snowden, R. (1990). Stimulus selectivity of neurons in Macaque MST. Society for Neuroscience Abstracts,
16,6.
Holland, H. C. (1965). The spiral after-effect. Oxford: Pergamon Press.
Masland, R. H. (1969). Visual motion perception: Experimental
modification. Science, 165, 819-821.
Morrow, M. J. & Sharpe, J. A. (1989). Effects of head and body
position on torsional optokinetic and vestibular eye movements in
humans. Society for Neuroscience Abstracts, 15, 514.
Newsome, W. T., Wurtz, R. H. & Komatsu, H. (1988). Relation
of cortical areas MT and MST to pursuit eye movements. II.
Differentiation of retinal from extraretinal inputs. Journal of Neurophysiology, 60, 604-620.
Seidman, S. H. & Leigh, R. J. (1989). The human torsional vestibuloocular reflex during rotation about an earth-vertical axis. Brain
Research, 504, 264-268.
Seidman, S. H., Thomas, C. W., Huebner, W. P., Billian, C. & Leigh,
R. J. (1990). Eye movements during motion aftereffect. Society for
Neuroscience Abstracts, 16, 902.
Wohlgemuth, A. (1911). In the after-effect of seen movement. British
Journal of Psychology, Monograph Supplement 1.
We have shown that there are eye movements associated with torsional MAE. These eye movements are
present both during and after the motion stimulation.
During stimulation, torsional eye movements were in
the same direction as the motion stimulus. Following
stimulation, the eye movements reversed direction. The
torsional eye movements during the perception of
illusory motion were not in the direction which would
have produced the retinal slip necessary to cause the
perception. Therefore, we conclude that retinal slip is not
responsible for MAE. Although there are small eye
movements during horizontal motion stimulation, there
are no horizontal eye movements during the MAE. This
difference between torsional and horizontal MAE may
be due to the strength of the horizontal fixation system:
gaze stability during fixation of a stationary target is
much less precise torsionally than horizontally (Ferman,
Collewijn, Jansen & Van den Berg, 1987).
The reversal of eye movements during torsional MAE
may be linked to the illusory reversal of the direction of
the visual stimulus. Similar observations have been made
by Brandt, Dichgans and Biichele (1974) for horizontal
eye movement during CV, in which a reversal in the
direction of CV is accompanied by a reversal in slowphase eye movement. However, since "velocity storage"
in the human torsional optokinetic-vestibular system is
weak or absent (Morrow & Sharpe, 1989; Seidman &
Leigh, 1989), this mechanism is unlikely to contribute to
eye movements during MAE.
Acknowledgements-This work was supported by NIH grant EY06717
Another possibility is that the reversal of torsional eye (to Dr Leigh), the Department of Veterans Affairs, and the Evenor
movements that occurs during MAE may reflect the Armington Fund.