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
Lisberger
3 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. Deubel
7 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 drum
8 or a target
spot
9 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
Lisberger
3 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 humans
6 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.
The authors thank David S. Zee and Takehiko Bando for critical
review of the manuscript.