(Investigative Ophthalmology and Visual Science. 2001;42:668-674.)
© 2001
by The Association for Research in Vision and Ophthalmology, Inc.
Cross-Axis Adaptation of Pursuit Initiation in Humans
Yuuki Hayakawa1,
Mineo Takagi1,2,
Haruki Abe1,
Shigeru Hasegawa1,
Tomoaki Usui1,
Hiruma Hasebe1 and
Atsushi Miki1
1 From the Department of Ophthalmology, Niigata University School of Medicine, Niigata, Japan; and
2 Core Research for Evolutional Science and Technology, Saitama, Japan.
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Abstract
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PURPOSE. The initial acceleration of pursuit in the open-loop period is under
adaptive control and undergoes motor learning. The current study was
undertaken to examine the hypothesis that the direction of pursuit
initiation can also be adaptively modified.
METHODS. Four neurologically and ophthalmologically normal subjects participated
in the experiment. A modified step-ramp paradigm was used to induce
cross-axis adaptation, in which a ramp target changed its direction
orthogonally just after the target crossed the center. Four direction
changes were tested in separate experiments: left to up, left to down,
down to left, and up to left. During a 30-minute adaptation session,
the target moved in one of two randomly chosen directions (right to
left or up to down) at one of two randomly chosen speeds (15.6 or 22.3
deg/sec), but the target changed orthogonally in only one direction. A
linear regression fit to the initial 100-msec segment of the pursuit
trace was used to determine the direction of pursuit initiation.
RESULTS. In all cases, an adaptive change in pursuit initiation was gradually
induced in the direction called for by the training paradigm.
Adaptation was usually completed (90° shift) within the 30-minute
training session but declined quickly to an approximate 30°-shift
after training. The latency and vectorial amplitude of the initial
acceleration remained unchanged. The adaptation was specific for the
direction but not the velocity of the target.
CONCLUSIONS. This study showed that the direction of pursuit initiation is under
adaptive control, as has been shown for saccadic eye movements and the
vestibulo-ocular reflex.
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Introduction
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Smooth pursuit is a tracking eye movement performed to
retain the image of a moving target on the fovea. The image of a target
that passes across the fovea (retinal slip), triggers the pursuit
system. The pursuit system has been classically argued to be under
closed-loop control—that is, the accuracy of pursuit eye movements is
maintained using a feedback error signal based on the difference
between target and eye motion. The initiation of pursuit eye movement,
however, operates in an open-loop fashion for roughly the first 130
msec after onset of movement, before visual feedback can influence the
motor response.1
It is known that the initial acceleration
of pursuit in the open-loop period is adaptively controlled with motor
error learning.2
3
4
5
6
In the natural environment, a target
often suddenly changes its direction of movement, as is often observed
when a prey is being chased by a predator. This suggests the need for a
mechanism to keep the direction of pursuit initiation accurate. Both
the magnitude of acceleration and the direction of pursuit initiation
may be preprogrammed in the central nervous system and adaptively
controlled to be appropriate for the target speed and direction.
Directional adaptation has already been demonstrated for saccadic eye
movements7
and the vestibulo-ocular
reflex.8
9
In this experiment, we investigated cross-axis adaptation in the
initiation of pursuit eye movements in which an error signal in
direction was introduced artificially.
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Methods
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Subjects
Four human subjects (age range, 29–37 years) participated in
the experiments after providing informed consent and were
neurologically and ophthalmologically normal except for refractive
errors. Their heads were immobilized with a dental bite bar, and they
were asked to follow a target on the video monitor. The procedure of
this study conformed with the Declaration of Helsinki (1964) and was
approved by the Ethics Committee of Niigata University School of
Medicine.
Experimental Paradigm
The experiments were performed in a dark room. The visual target
was a white square measuring 2 x 2 mm (subtending an angle of
0.20 x 0.20 minutes) displayed on a video monitor placed 60 cm
away from the subject. A modified step-ramp paradigm was used to induce
cross-axis adaptation: A target appeared for 1.5 seconds at the center
of the monitor, jumped 3.6° or 5.1° away from center, and then
moved toward the center at a constant velocity of 15.6 (slow target
movement) or 22.3 deg/sec (fast target movement). When the target
crossed the center 230 msec after the onset of the ramp movement, it
changed direction, horizontal to vertical or vertical to horizontal,
with the same speed. Thus, just after pursuit eye movements started
from the center in response to the first target ramp movement, the
target was moving orthogonal to the pursuit response.
We tested four kinds of cross-axis adaptation (Fig. 1)
. In each experiment, the target first moved in one direction, right to
left or up to down, randomly, but the target changed direction
orthogonally in only one direction: from down to left, from left to up,
from up to left, and from left to down (adaptation side). In the
opposite direction (reference side), the direction of the target did
not change throughout the trial. The ramp velocity was also randomized
so that the subject could not predict the direction or velocity of the
target. The four experiments were conducted on different days. Each
experimental run consisted of preadaptation, adaptation, and
postadaptation sessions. In the preadaptation session, control data
were collected before cross-axis adaptation. Thirty-two trials of the
step-ramp paradigm without directional change were tested. In the
adaptation session, the modified step-ramp paradigm was tested for
approximately 30 minutes. One training subsession consisted of 48
trials followed by a brief pause of approximately 1 minute, and six
subsessions were conducted with a total of 144 trials (72 slow and 72
fast targets) for each adaptation and reference side. The
postadaptation session consisted of the same 32 trials used in the
preadaptation session—that is, the direction of the target did not
change throughout the trial.
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Figure 1. Two-dimensional schematic illustration of target movement during an
adaptation session. In each experiment, one of four kinds of training
paradigms was used. The target first appeared in the center and then
jumped away from the center (step) and began moving at constant
velocity (15.6 or 22.3 deg/sec, ramp). On the adaptation side, the
target always changed direction orthogonally when it crossed the center
230 msec after onset of the ramp (solid lines):
(A) down to left, (B) left to up, (C)
up to left, and (D) left to down. On the reference side, the
target did not change direction (dotted lines). These
experiments were performed on different days for each subject.
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Eye Movement Recording and Data Analysis
Horizontal and vertical movements of both eyes were recorded
simultaneously with an infrared system (Ober 2; Iota, Sundsvall,
Sweden) and stored on a hard disk at 600 Hz for off-line analysis. For
calibration, subjects were required to fixate sequentially 17 points
around the center arranged in a grid pattern separated by 2.5°
horizontally and vertically so that a calibration matrix could be
obtained. This brief calibration session was performed every 5 minutes
during the experiment. After two-dimensional interpolation of the
matrix by the inverse distance method,10
calibration was
applied to raw eye movement data to correct for the two-dimensional
distortion of the recording system. Conjugate eye position traces
(average of right and left horizontal traces) were filtered and
differentiated with a single-pole analog filter with a cutoff frequency
of 15 Hz. We defined pursuit onset as the time when the vectorial eye
velocity exceeded 3 deg/sec. Each conjugate trace of pursuit eye
movement was plotted in two dimensions, and linear regression was used
to fit the eye movement traces for the first 100-msec segment after the
pursuit onset using the method of least squares. The angle of this
regression line was used to determine the initiation angle of pursuit
eye movement. The latency of pursuit and average initial acceleration
during the first 100-msec segment after the onset were also calculated.
Trials were rejected if eye traces were disturbed by blinks or if
saccades occurred within 100 msec after pursuit onset (less than 5%).
All the data were processed using data analysis software (Matlab; The
MathWorks, Natick, MA).
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Results
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Figure 2
shows representative pursuit traces for the first 500-msec segment
after the onset of pursuit before, early in, late in, and after the
training session. In this experiment, the target moved first left and
then down on the adaptation side, but moved right throughout on the
reference side. Before training of cross-axis adaptation, eye movements
were induced exactly to the left (184.2° ± 6.5°, eight traces) on
the adaptation side. At the beginning of training, the eye first moved
left (193.6° ± 7.2°, first 12 traces) to follow the initial
leftward target movement but had to catch up with the target moving
down with oblique corrective saccades approximately 200 to 300 msec
after the onset of pursuit. At the end of training, the eye started
moving down from the beginning (286.6° ± 6.7°, last 12 traces)
although the target first moved left. Approximately 30 minutes after
training, the direction of initial pursuit had shifted down (237.4°
± 30.7°, eight traces) in response to the leftward step-ramp target
movement without direction change.
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Figure 2. Two-dimensional pursuit traces before, early in, late in, and after the
training sessions (subject 3; target direction changed from left to
down). Top: Adaptation side; bottom:
reference side. The traces representing the early and late phases of
training, the first and last 12 traces during training sessions are
shown. The ordinates and the abscissas of the graphs represent vertical
and horizontal angles (in degrees) for pursuit traces for the 500-msec
segment after the target onset, respectively. On the adaptation side,
left horizontal eye movements were induced before training. Early in
training, the eye began moving left in response to the initial leftward
target movement. However, because the target changed its direction
orthogonally down, the eye had to catch up with the target using
saccades and thereafter kept moving down. Later in training, pursuit
began moving not left but down from the beginning, even though the
target first moved left. After subjects trained for 30 minutes, pursuit
initiation shifted down in response to the leftward target movement.
Eye movements were not affected on the reference side.
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On the reference side, there was no effect of the training. The
Mann–Whitney rank sum test revealed a significant difference in the
angle of pursuit initiation before and after training on the adaptation
side (P = 0.008), but not on the reference side
(P = 0.64). Figure 3
shows horizontal and vertical components of pursuit traces for the
adaptation side from the data shown in Figure 2
. It is evident that
even in the late phase of the adaptation session and postadaptation
session, directionally adapted pursuit started smoothly with a latency
of approximately 150 msec. In this case, pursuit latencies were
152.6 ± 5.7, 155.4 ± 7.8, 154.6 ± 12.6, 154.1 ±
7.5 msec before adaptation, in the early and late phases of adaptation,
and after adaptation, respectively. Using Kruskal–Wallis one-way
analysis of variance on ranks, no significant difference was found
among them. Similarly, in all cases we tested the differences in
latency among the four conditions (before, in the early and late
phases, and after adaptation) but no significant difference was found,
the latencies always being approximately 150 msec.
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Figure 3. Horizontal (top) and vertical (bottom)
components of pursuit traces on the adaptation side presented in Figure 2
. Similarly, traces of the 500-msec segment after the target onset
before, early in, late in, and after the training sessions from the
left. For the early and late phases of training, the first and last 12
traces during the training sessions are shown. The ordinates and
abscissas represent horizontal or vertical angles (in degrees) and time
after the target onset, respectively. Note that the latencies of
pursuit initiation were almost constant throughout the experiment.
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Figure 4
shows the time course of changes in angle during the training session
in the same subject as is shown in Figure 2
. The angles of pursuit
initiation were plotted for each of 72 trials for slow and fast targets
during the adaptation session. On the adaptation side, the initial
angle direction changed gradually from left (180°) to down (270°);
however, on the reference side the initial angle direction did not
change for either target speed. An exponential curve was fitted to all
data points as a function of trial number in each panel, using the
least-squares method, and then to evaluate changes in the angle of
initial pursuit direction during the training session, the difference
in angle between trials 1 and 72 was calculated using the exponential
curve. In this experiment, changes in the angle on the adaptation side
were 87.9° and 95.4° for slow and fast target movements,
respectively. In contrast, on the reference side, the respective
changes in angle were only 2.6° and 0.7°. On the adaptation side,
the extent and time course of directional change were almost the same
for both target speeds, as seen in panels L1 and L2. The time constants
of the exponential curve were 30.2 trials for L1 and 32.1 trials for L2
in these cases. In general, the time constants of directional
adaptation were very similar among experiments and subjects. They were
32.1 ± 3.0 (average of slow and fast target for four directions,
i.e., eight cases), 32.4 ± 2.9, 30.9 ± 1.9 and 31.4 ±
2.2 trials for subjects 1 through 4, respectively.
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Figure 4. The time course of directional change of pursuit initiation during a
training session (subject 3; change in target direction from left to
down) for the (top) adaptation side and the
(bottom) reference side (change to the right). The
ordinates and the abscissas of the graphs represent pursuit initiation
angle (in degrees) and number of trials in the experiment,
respectively. The target first moved left at 15.6 deg/sec or 22.3
deg/sec (L1, L2, respectively) or right at 15.6 deg/sec or 22.3 deg/sec
(R1, R2, respectively). An exponential curve was fitted as a function
of trial number for each panel. Changes in pursuit initiation angle
were calculated as the difference between the beginning and end of
training trials using the exponential curve.
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Similar results were obtained in all cases (Fig. 5)
. Changes in angle of almost 90° were obtained (85.0 ± 14.9°
for 32 cases) during training sessions on the adaptation side, but
changes were very small on the reference side (7.5 ± 5.2°). The
paired t-test was performed to compare the change between
the slow and fast target movements. No significant difference was found
on either the adaptation side (P = 0.97,
n = 16) or the reference side (P =
0.54, n = 16). Figure 6
shows the changes in angle of pursuit initiation in the posttraining
sessions for all cases. The changes in angle on the adaptation side
were, on average, 34.4° ± 19.0° for the slow target movement and
27.3° ± 20.0° for the fast target movement. Large changes in angle
of approximately 90° disappeared quickly. However, changes in angle
of approximately 30° persisted or declined slowly during the
postadaptation session. On the reference side, the changes after
training were only 1.86° ± 5.87° for the slow and 0.60° ±
4.87° for the fast target movement. The Mann–Whitney rank sum test
revealed a significant difference in initiation angle between
preadaptation and postadaptation sessions in 14 of 16 cases; there was
no significant difference on the reference side.
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Figure 5. Changes in pursuit initiation angle (in degrees) calculated from the
exponential curve are shown for all cases. Solid bars:
adaptation side; clear bars: reference side. L, R, D, U:
Direction in which target first moved (left, right, down, up,
respectively); 1, 2: mean target velocities of 15.6 and 22.3 deg/sec,
respectively. In all subjects, changes in angle of approximately 90°
were found during the training session on the adaptation side. In
contrast, no changes in angle were observed on the reference side.
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Figure 6. Angle shift of pursuit initiation from the horizontal meridian in the
postadaptation session for all cases. Results of eight trials for each
trial type on the adaptation side are shown in the order of trial
progression from the left. S, Trials for the slow target; F, trials for
the fast target. Significant differences between initial angles between
the pre- and postadaptation sessions using the Mann–Whitney rank sum
test (*P < 0.05; **P < 0.01;
N.S., not significant).
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In summary, it was possible to induce directional adaptation of pursuit
initiation without changes in the latency or acceleration by providing
artificial direction error in the open-loop period of the pursuit eye
movement response. Adaptation was specific for the target’s direction
but not for its velocity.
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Discussion
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Recently, considerable evidence has been accumulated for an
adaptive capability for pursuit acceleration in its initial open-loop
segment. Optican et al.2
showed that adaptation of
acceleration in the open-loop period of pursuit eye movement occurred
in response to anisotropic eye movement deficits caused by ocular
muscle weakness in patients with ocular motor nerve palsies. Kahlon and
Lisberger3
observed that the acceleration of initial
pursuit responses in monkeys changed adaptively on repeated
presentation of targets that moved at one speed for 100 msec and then
changed to a second higher or lower speed. Similar adaptive changes
were also reported in humans.4
5
6
Reports of directional
adaptation in saccadic eye movement and vestibulo-ocular reflex (VOR)
demonstrate that adaptation applies to vector as well as scalar (gain)
values. Deubel7
demonstrated that saccadic direction in
primates was equally as adaptable as saccadic gain by using a target
that was displayed orthogonally to the direction of the initial step.
Adaptive changes of direction in VOR after training were found in
animals by using an optokinetic drum8
or a target
spot9
moved horizontally in synchrony with vertical head
oscillations.
The paradigm used in this experiment seems to be appropriate for
providing artificial directional motor error during the open-loop
period, because the latency of pursuit eye movement remained unchanged
at approximately 150 msec after adaptation for all subjects and the
target’s direction changed within the open-loop period, at
approximately 200 to 300 msec after onset of pursuit. We consider our
results to represent adaptation by motor learning for the following
reasons: First, the change in the direction of eye movement was not an
artifact of the recording system. Although the raw eye movement data
recorded by our monitor system were usually affected by two-dimensional
distortion, a two-dimensional calibration was performed every 5 minutes
during the experiment to monitor the exact direction. Second, it was
not a predictive response, because the direction and speed of the
target were randomized to prevent prediction by the subjects.
Furthermore, whenever the subjects made a predictive pursuit response,
an increase of eye acceleration and decrease of the latency in pursuit
initiation could be expected.11
No such changes in
acceleration and latency were found. Rather, constant latencies
throughout the experiment strongly suggested that the response was
driven reflexively by the first retinal slip signal. Third, it is not a
voluntary directional change arising from a cognitive strategy. The
time course of the directional change during training was not abrupt,
as would be expected from a voluntary change, but was exponential, as
is common for motor error learning.
In the present experiment, directional changes did not transfer to the
reference side. No differences in adaptation between the two levels of
target velocity were observed. Similar results for adaptation of
initial acceleration were described by Kahlon and
Lisberger3
and Scheuerer et al.6
What differs
from gain adaptations such as saccade size and pursuit initial
acceleration is the fast induction, the time constant being
approximately 30 trials and orthogonal adaptation being completed
within 72 trials (Fig. 3)
. Similar rapid cross-axis adaptation is known
for VOR. An orthogonal eye movement response to body rotation in
monkeys appeared after approximately 30 minutes of
training.9
In contrast, gain adaptation requires more
training. At least 60 trials were necessary for acquisition of visible
saccadic and pursuit adaptation in humans6
7
and
approximately 200 trials in primates.3
7
In the
postadaptation session, which began 1 to 2 minutes after the end of
training, the large directional shift of 90° disappeared rapidly, but
a 30° shift persisted during the session. There are two possible
explanations for this result. Directional adaptation can consist of an
immediate component and a slower, long-lasting component.
Alternatively, some deadaptation could be caused by normal VOR during
the interval between sessions, because the subject’s head was not
restricted, and it was possible to glance at the dimly illuminated room
during the interval. Also, because the target presented in the
postadaptation did not change its direction, the trials would have
served as deadapting stimuli.
The central nervous system structures related to pursuit eye movements
have been investigated in monkeys. At present, the middle temporal (MT)
area and the medial superior temporal (MST) area in the cerebral
cortex, the ventral paraflocculus, the posterior vermis and underlying
fastigial nucleus in the cerebellum, the dorsolateral pontine nucleus,
and the nucleus reticularis tegmenti pontis in the brain stem are
believed to be the main structures controlling
pursuit.12
13
However, the mechanism for pursuit
adaptation is still unclear. The neuronal activity related to
adaptation of acceleration in pursuit initiation has been found in the
dorsoventral paraflocculus.14
In addition, lesions of the
VII lobule of the cerebellar vermis cause partially impaired adaptation
of initial pursuit acceleration.15
On the basis of these
reports, the current hypothesis is that gain adaptation of pursuit
initiation is controlled by both the posterior vermis and the
dorsoventral paraflocculus. There is also much debate about the
mechanism involved in directional adaptation of eye movements. In cats,
adaptive changes in VOR direction were disturbed after removal of the
paraflocculus and lobule VII and part of VI in the
vermis.8
However, the central nervous structures involved
in directional adaptation in saccade and pursuit eye movements are not
known. Directional adaptation in pursuit may involve a different
mechanism from that in saccades. In oblique saccades, various types of
saccadic pulse generators are associated with different
directions.16
The outputs of vectorial pulse generators
are transmitted to horizontal and vertical output channels by different
synaptic weightings onto motor neurons.17
In contrast, in
directional tuning of pursuit eye movements, the best directions
elicited by microstimulation of PCs and mossy fibers are split into
pure horizontal and vertical components. Directional adaptation in
initial pursuit may not be a simple adaptive change in angle
information but may be processed analogously to adaptation in
acceleration after being segregated into horizontal and vertical
channels in the same way as ordinary pursuit eye
movement.18
Clinical evidence shows that changes in the ocular motor plant, such as
orbital mass lesions or extraocular muscle weakness, can lead to
adaptive increases in motor signals.2
In other words, when
the direction of eye movement is distorted by eye disease or some other
disorder, the central nervous system must correct and maintain eye
movement. Even in the normal eye, differences in the viscous forces on
the eye arising from differences in the stiffness of nasal and temporal
tissue are known to occur.19
In the eccentric gaze,
elastic forces move the eye toward the center of the
orbit.20
Thus, the direction of pursuit initiation could
be distorted by orbital elastic forces, and directional adaptation
mechanisms would be required to maintain accurate pursuit initiation,
regardless of the starting eye position in the orbit. Consequently,
directional adaptation in the central nervous system maintains the
accuracy of the initial pursuit direction during eye movement disorders
as well as in the normal condition.
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Acknowledgements
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The authors thank David S. Zee and Takehiko Bando for critical
review of the manuscript.
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Footnotes
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Supported by Grants-in-Aid for Encouragement of Young Scientists
09771413 (MT) and for Scientific Research 11671727 from The Japan
Ministry of Education, Science, Sports and Culture.
Submitted for publication May 18, 2000; revised September 28, 2000;
accepted October 16, 2000.
Commercial relationships policy: N.
Corresponding author: Yuuki Hayakawa, Department of Ophthalmology,
Niigata University School of Medicine, 1 Asahimachi, Niigata 951-8510,
Japan. yhaya{at}med.niigata-u.ac.jp
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Top
Abstract
Introduction
