1Department of Neurology and 2Department of Neurosurgery, The Johns Hopkins Hospital, Baltimore, Maryland 21287; 3Department of Ophthalmology, Niigata University School of Medicine, Niigata 951; and 4Core Research for the Evolutional Science and Technology Program, Japan Science and Technology, Saitama 332-0012, Japan
![]() |
ABSTRACT |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Takagi, Mineo, David S. Zee, and Rafael J. Tamargo. Effects of Lesions of the Oculomotor Cerebellar Vermis on Eye Movements in Primate: Smooth Pursuit. J. Neurophysiol. 83: 2047-2062, 2000. We studied the effects on smooth pursuit eye movements of ablation of the dorsal cerebellar vermis (lesions centered on lobules VI and VII) in three monkeys in which the cerebellar nuclei were spared. Following the lesion the latencies to pursuit initiation were unchanged. Monkeys showed a small decrease (up to 15%) in gain during triangular-wave tracking. More striking were changes in the dynamic properties of pursuit as determined in the open-loop period (the 1st 100 ms) of smooth tracking. Changes included a decrease in peak eye acceleration (e.g., in one monkey from ~650°/s2, prelesion to ~220-380°/s2, postlesion) and a decrease in the velocity at the end of the open-loop period [e.g., in another monkey from a gain (eye velocity/target velocity at 100 ms of tracking) of 0.93, prelesion to 0.53, postlesion]. In individual monkeys, the pattern of deficits in the open-loop period of pursuit was usually comparable to that of saccades, especially when comparing the changes in the acceleration of pursuit to the changes in the velocity of saccades. These findings support the hypothesis that saccades and the open-loop period of pursuit are controlled by the cerebellar vermis in an analogous way. Saccades could be generated by eye velocity commands to bring the eyes to a certain position and pursuit by eye acceleration commands to bring the eyes toward a certain velocity. On the other hand, changes in gain during triangular-wave tracking did not correlate with either the saccade or the open-loop pursuit deficits, implying different contributions of the oculomotor vermis to the open loop and to the sustained portions of pursuit tracking. Finally, in a pursuit adaptation paradigm (×0.5 or ×2, calling for a halving or doubling of eye velocity, respectively) intact animals could adaptively adjust eye acceleration in the open-loop period. The main pattern of change was a decrease in peak acceleration for ×0.5 training and an increase in the duration of peak acceleration for ×2 training. Following the lesion in the oculomotor vermis, this adaptive capability was impaired. In conclusion, as for saccades, the oculomotor vermis plays a critical role both in the immediate on-line and in the short-term adaptive control of pursuit.
![]() |
INTRODUCTION |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
A role for the cerebellum in the control of
pursuit eye movements was first identified in the pioneering
experiments of Westheimer and Blair (1973) and
Burde et al. (1975)
, who described failure of smooth
following in totally cerebellectomized monkeys. Human patients with
lesions of the cerebellum also show defects in the generation of
pursuit eye movements (Büttner and Straube 1995
; Büttner et al. 1994
; Lewis and Zee
1993
; Straube et al. 1997
; Vahedi et al.
1995
). Based on the anatomic projections to the cerebellum from
areas within the pons that are concerned with pursuit
(Glickstein et al. 1994
; Nagao et al.
1997
; Thielert and Thier 1993
; Yamada and
Noda 1987
), and the effects of focal lesions within the
cerebellum of monkeys, two specific regions of the cerebellar cortex
have been implicated in the control of pursuit: the cerebellar
flocculus and paraflocculus (Zee et al. 1981
), and the
dorsal and posterior cerebellar vermis including lobules VI, VII
(Keller 1988
), and the uvula (Heinen and Keller
1996
). Furthermore, lesions within the portion of the fastigial
nucleus that receives projections from Purkinje cells of the dorsal
vermis, the so-called fastigial oculomotor region (FOR), also affect
pursuit (Ohtsuka et al. 1994
; Robinson et al.
1997
). Recently, the ventrolateral portion of the posterior
interposed nucleus (Robinson and Brettler 1998
) and the
lateral cerebellar hemispheres (Straube et al. 1997
) have also been implicated in pursuit. The finding that multiple areas
within the cerebellum are involved in pursuit is unexplained.
In an attempt to unravel the cerebellar contribution to pursuit eye
movements, we studied the effects of lesions of the dorsal vermis on
pursuit in monkeys. We also studied adaptive capability in the pursuit
system, using a short-term learning paradigm analogous to that used for
the adaptive control of the amplitude of saccades. Because the animals
reported here were also used in a study of the effect of dorsal vermis
lesions on saccades (Takagi et al. 1998), we compared
the effects of lesions on pursuit with those on saccades. Preliminary
reports of some of these results were presented at the Association for
Research in Vision and Ophthalmology (Takagi et al.
1996a
) and the Society for Neuroscience (Takagi et al.
1996b
).
![]() |
METHODS |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
General experimental procedures and recording of eye movements
The general experimental procedures and the details of methods
of recording eye movements have been described in the previous report
that was based on the same three monkeys (Takagi et al. 1998). In brief, the magnetic-field search coil technique was used with coils implanted in both eyes. The output signal from the
phase detectors was filtered with a bandwidth of 0-90 Hz, sampled by a
digital computer at 500 Hz with 12-bit resolution, and then stored to
disk for later off-line analysis. System noise limited resolution to
~0.05°. The coil signal was calibrated by requiring the animal to
fix successively on targets at 2.5° intervals over a range of ±25°
horizontal and ±22.5° vertical. All surgical and experimental
protocols were approved by The Johns Hopkins University committee on
animal experimentation, and all aspects of their care complied with the
guidelines for veterinary care of The Johns Hopkins University School
of Medicine and of the National Institutes of Health Guide for the Care
and the Use of Animals including appropriate analgesia after surgical procedures.
Stimulus presentation
Target stimuli were under computer control and displayed on a video monitor located 33 cm in front of the monkey, in an otherwise dark room. To elicit pursuit movements we used a step-ramp stimulus in which the target (a square, 3.2° on a side) was displaced eccentrically (4-12°, depending on target speed and the saccade latency of the monkey) and then moved back at a constant velocity toward and then beyond the initial straight-ahead target position. The ramp target crossed the center at 180 ms (monkey 1), 220 ms (monkey 2), and 200 ms (monkey 3) after the onset of target motion. In this way saccades were eliminated in the initial portion of pursuit tracking. In some blocks of trials, the target continued on until it went off the screen. The direction and timing of the stimulus onset were randomized. The latency of pursuit and the acceleration of the eye in the open-loop period were calculated from these trials. Pursuit adaptation was elicited using a double-step of velocity, analogous to the double step of position used for saccade adaptation. After the initial step-ramp of target motion, the target speed was doubled (×2) or halved (×0.5) in speed as it crossed the straight-ahead position. The initial target velocities were 20 and 40°/s. The adaptation paradigms were run as trials of all increasing or all decreasing stimuli, but the directions and amplitudes of target motion were randomized. One hundred trials of each stimulus were elicited.
Data analysis
Analysis was performed using the interactive marking program
described in the previous publication (Takagi et al.
1998). Velocity was computed with a digital filter with a 3-dB
point at 112 Hz. Pursuit onset was taken when smooth eye velocity
reached 2°/s in the direction of the target ramp. Pursuit latency was
the difference between the time when the target began to move and the
velocity of the eye reached the threshold value. For displaying of
individual traces, eye position data were processed in Matlab in which
eye position traces were successively filtered (3 db, 30 Hz) and
differentiated to produce eye velocity and eye acceleration. Pursuit
gain (eye velocity/target velocity) during triangular-wave tracking was based on the average value of the median eye velocity taken from 10-12
sustained epochs when the animal was tracking the target well, i.e.,
keeping its eye position within a window of ±2-3° around the target.
Cerebellar lesions
The cerebellum was lesioned under pentobarbital sodium
anesthesia using aseptic techniques. The midline of the dorsal
cerebellum was exposed through a suboccipital approach, and a lesion
centering around lobules VI-VII was made by bipolar cauterization and
aspiration. Corticosteroids and antibiotics were administrated for a
week after the surgery. Monkeys showed no defects in their general neurological performance, and recording of eye movements was initiated within the first week after surgery. Details of the techniques for the
histological examination and the reconstruction of the extent of
lesions are described in our previous publication (Takagi et al.
1998).
![]() |
RESULTS |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Extent of lesions
Figure 1, A and B, shows the reconstruction of the lesions based on histological examination, with the sagittal extent of the lesions being referenced to the bottom of Fig. 1B. The black areas reflect either absence of tissue or areas in which neurons appeared destroyed or white matter disrupted. For monkey 1 (Fig. 1A), the lesion was nearly symmetrical, being deepest in the midline where lobules VII and VIII were completely lesioned. Lobules VI and IX were partially involved. The lesion extended laterally to section 3 on both sides, just encroaching on the simple lobule. The lateral component of the lesion on the left side was slightly more extensive (compare left and right sides in sections L3 and R3). For monkey 2 (Fig. 1A), near the midline, lobules VI-VIII were lesioned on both sides, although the lesion was deeper on the right at the R1 level. The lesion, however, extended slightly more laterally on the left side. For monkey 3 (Fig. 1B), on the midline, lobule VII was completely lesioned, but there was mild sparing in lobule VI and moderate sparing in lobule VIII. Both near the midline and more laterally, the lesion was more extensive on the right side and reached the paravermis. In all three monkeys the cerebellar deep nuclei were spared including the posterior portion of the fastigial nucleus. Only in monkey 1 was there some gliosis at the very posterior tip of the fastigial nucleus, although the neurons appeared intact.
|
General pursuit behavior
Both before and after surgery all animals could hold fixation steadily without spontaneous nystagmus and had no difficulties holding eccentric positions of gaze. There was no spontaneous nystagmus in darkness apart from the low-amplitude drift that many intact rhesus monkeys show. Figure 2 shows a typical example, from monkey 2, of horizontal tracking of a target moving at 20°/s in a triangular-wave pattern, pre- and postlesion. Following the lesion (Fig. 2, right), there was a relatively mild deficit in sustained tracking as reflected in the occasional catch-up saccade, but also a tendency to avoid going to the extremes of eccentric gaze, in this case, more so to the right. The pattern of tracking was qualitatively similar in the other two animals.
|
Quantitative data for gain during the sustained portion of triangular-wave horizontal tracking are shown in Fig. 3. Note that deficits in gain were relatively small and bilateral for all animals, but for monkeys 2 and 3 they were slightly greater and more enduring for leftward tracking. The decrease in gain tended to be greater for higher target velocities. The maximum percentage decrease after the lesion was 15%. For vertical tracking, there were no consistent changes in gain in any monkey.
|
Pursuit latencies for horizontal movements in the step-ramp paradigm ranged between 137 and 162 ms and were unchanged following the lesion. For vertical tracking, there were only a few trial types in which there were small (usually a decrease) but significant changes in pursuit latency following the lesion.
Pursuit metrics during the open-loop period
PURSUIT ACCELERATION DURING STEP-RAMP TRACKING. To examine the open-loop, initial period of pursuit, we used the step-ramp stimulus to eliminate any saccades during the early phase of tracking. Figure 4 shows the pre- and postlesion responses for monkey 3 for leftward tracking at 40°/s. Responses were aligned on the target step. Postlesion, there was an inability to sustain eye acceleration during the latter portion of the open-loop period leading to a slower rise toward the final eye velocity. The transient overshoot in eye velocity during the open-loop period that occurred prelesion was absent following the lesion. In this animal, a small initial eye velocity toward the target step appeared postlesion. Finally, eye velocity was not well sustained as the target moved eccentrically.
|
|
|
|
Pursuit adaptation
Short-term adaptation of pursuit was investigated using a paradigm with a double step of velocity to induce a change in eye acceleration during the open-loop period. Figure 8, left column, shows sample traces of responses of monkey 3 to consecutive trials in the gain-increase (×2) paradigm, pre- and postlesion. Prelesion (left panels), there was an increase in the initial pursuit response with training. Figure 9 shows the average velocity trace for 12 trials during the early and during the late phases of the pursuit adaptation paradigm for monkey 3. Prelesion (Fig. 9, left panel), there is a clear adaptive response, although in this case only after the first ~20-30 ms of pursuit tracking, which was not modified. Figure 10 shows the response to the increasing (×2) and decreasing (×0.5) adaptation stimuli at a target speed of 20°/s for leftward (A) and 40°/s for rightward (B) tracking. Velocity and acceleration traces, pre- and posttraining, are shown for monkeys 2 and 3. Note that for the response in the ×2 adaptation paradigm, the major change is an increase in the duration of the acceleration period. For the ×0.5 adaptation paradigm, the major change is a decrease in the amplitude of peak acceleration. Note that for monkey 2 the earliest ~20-30 ms of pursuit tracking was relatively unchanged, but there was a small change for monkey 3.
|
|
|
Following the lesion, the ability to alter eye acceleration adaptively in the open-loop period was severely impaired. For example, monkey 3 could not follow the double step of target velocity without catch-up saccades (Fig. 8, right). This finding is also reflected in the average traces for monkey 3 in Fig. 9, right. Postlesion, training induced little change in eye acceleration during the open-loop period. The traces only separate when information from visual feedback became available (>100 ms after tracking onset) to adjust the ongoing eye tracking movement.
Individual trials throughout the pursuit adaptation paradigm are shown in Fig. 11 for monkey 3 during leftward tracking in the gain-increase paradigm. Note that the adaptive increase in the average value of acceleration in the first 100 ms is diminished after the lesion. A more extensive quantitative analysis of pursuit adaptation is depicted in Fig. 12 for monkeys 2 and 3. There was a decrease but not an absence of a capability for adaptive modulation of eye acceleration in the open-loop period of pursuit. The deficits were to some extent bidirectional. There was a variable, small recovery of adaptive capability, but in general the deficits were enduring.
|
|
For monkey 1, the data before and after each training session were less complete, but this animal also showed deficits in pursuit adaptation. For example, in the ×0.5 paradigm there was a bidirectional decrease in average acceleration in the first 100 ms of tracking at the higher target speed (from a 51% to a 28% change for leftward tracking and from a 62% to a 24% change for rightward tracking).
![]() |
DISCUSSION |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
The main finding of this study is that lesions restricted to the dorsal vermis of the cerebellum ("the oculomotor vermis") impair smooth pursuit performance, with small changes in the steady-state gain triangular-wave tracking and more marked changes in the pattern of eye acceleration during the first 100 ms (the "open-loop" period) of pursuit. We also found that in paradigms calling for adaptive modification of pursuit performance, there was an impaired ability to modify acceleration in the open-loop period of pursuit. These effects on pursuit and pursuit adaptation were independent of any structural damage to the deep cerebellar nuclei, implicating the cerebellar vermis directly both in the immediate, on-line, and in the short-term, adaptive control of pursuit.
Schema for the control of pursuit by the oculomotor vermis
RESULTS OF EXPERIMENTAL STIMULATION AND OF SINGLE-UNIT RECORDINGS
IN THE FASTIGIAL OCULOMOTOR REGION (FOR) AND IN THE OCULOMOTOR VERMIS.
Many Purkinje cells in the oculomotor vermis discharge in relation to
pursuit (Sato and Noda 1992; Suzuki and Keller
1988a
,b
), with a majority having their preferred direction
contralaterally. Some cells in the dorsal vermis carry a signal related
to motion of images on the retina, allowing for reconstruction of the
velocity of the target in space (i.e., relative to the head).
Experimental stimulation in the dorsal vermis usually decelerates or
reverses contraversive pursuit (Krauzlis and Miles
1998
). In humans, transcranial magnetic stimulation over the
posterior cerebellar vermis accelerates ipsiversive pursuit and
decelerates contraversive pursuit (Ohtsuka and Enoki
1998
).
CONCEPTUAL SCHEME FOR INITIATION OF PURSUIT: EFFECT OF LESIONS OF
THE OCULOMOTOR VERMIS.
Fuchs et al. (1994) suggested that the FOR is poised to
help accelerate the eyes during contralateral pursuit and decelerate them during ipsilateral pursuit. More specifically, in the context of
the response to the step-ramp stimulus, activity in the FOR could
influence the open-loop (1st 100 ms) period of pursuit by increasing
the discharge in different sets of neurons at different times in the
open-loop period. Those cells that start discharging during the very
beginning of the open-loop period could facilitate contralateral
pursuit acceleration, and those that increase their discharge toward
the end of the initial period could help stop ipsilateral acceleration.
VARIABILITY IN THE EFFECTS OF VERMAL LESIONS AMONG ANIMALS.
The amplitude of peak acceleration during pursuit was affected by the
lesion of the vermis to varying degrees, depending on the monkey. For
example, during leftward movements, one animal (monkey 2)
had a relatively large value of peak acceleration prelesion (~600-700°/s2); postlesion, it showed a
marked decrease in peak acceleration to values of
~200-375°/s2. Another animal (monkey
3) had a relatively low value of peak acceleration prelesion
(~275-430°/s2) and showed more of a change
(a decrease) in the duration of peak acceleration, postlesion. For
monkey 1, peak acceleration decreased from a maximum value
of ~475°/s2 prelesion to values of
~175-225°/s2 after the lesion. Among all the
animals, the values of peak acceleration and the duration of peak
acceleration were much closer after than before the lesion. Thus,
although the effects of the lesions on individual monkeys were
variable, the final level of performance postlesion was more
consistent. This finding suggests that some of the seemingly variable
effects of the lesions on pursuit in different animals might be due to
variability in the effect of the cerebellum on the dynamic properties
of their intact pursuit, rather than simply due to differences among
animals in the extent of lesions. Robinson et al. (1997)
also found variability in the effects of muscimol injections into the
FOR of different monkeys, which may reflect the same phenomenon.
Common role for the oculomotor vermis in the control of the open-loop characteristics of saccades and pursuit
This schema for pursuit outlined above for the FOR and oculomotor
vermis is analogous to the posited role for the FOR and oculomotor
vermis in the generation of saccades (Fuchs et al. 1993;
Ohtsuka and Noda 1995
; Quaia et al. 1999
;
Takagi et al. 1998
). This similarity between pursuit and
saccades is seen more clearly if one considers that the initial period
of pursuit acceleration is an open-loop eye movement in the same way a
saccade is open-loop. With this hypothesis, for saccades, premotor
networks would be generating an eye velocity command to bring the eye
to a certain position, and for pursuit, an eye acceleration command to
bring the eye toward a certain velocity (Krauzlis and Lisberger
1994
; Robinson 1975
; Robinson et al.
1986
). Taking this analogy further, the FOR and the oculomotor
vermis could control the dynamic properties of the open-loop period of
pursuit (as reflected in eye acceleration) in the same way that it
controls the dynamic properties of saccades (as reflected in eye velocity).
We previously reported that for individual monkeys saccade amplitude
and saccade dynamics could be affected independently by a lesion of the
vermis (Takagi et al. 1998). One might then expect that
pursuit eye velocity at the end of the open-loop period, which would be
analogous to saccade amplitude, might be affected by a lesion of the
oculomotor vermis differently than the dynamic properties of open-loop
pursuit such as peak acceleration. This was largely true, too, in our
animals. For example, looking at the responses to the 20 and 40°/s
target stimuli in Fig. 5, for monkey 1, the changes in
pursuit eye velocity at the end of the open-loop period were relatively
greater than changes in peak eye acceleration, whereas the opposite was
true for monkey 2.
CORRELATION BETWEEN SACCADE AND PURSUIT DEFICITS AMONG ANIMALS. With the idea that the oculomotor vermis controls the characteristics of saccades and of the open-loop components of pursuit in a similar way, we asked whether there were correlations between the saccade and the open-loop pursuit deficits in individual animals. Although the prelesion pursuit data for monkey 1 was not optimal for scrutinizing the fine structure of pursuit acceleration during the open-loop period, there were clear parallels between the changes in peak saccade velocity and peak pursuit acceleration as the animal recovered. First, following the lesion, for both right and leftward tracking, this animal had the lowest values of both peak eye acceleration during open-loop pursuit and peak eye velocity during saccades. Second, comparing early and late postlesion data, e.g., for 40°/s pursuit target stimuli and 20° saccade amplitude, peak saccade velocity increased from 398 to 641°/s for rightward saccades and from 480 to 616°/s for leftward saccades. Similarly peak pursuit acceleration increased from 143 to 334°/s2 for rightward tracking and from 237 to 322°/s2 for leftward tracking.
One other obvious finding postlesion was that the animal developed a plateau in eye velocity well below target velocity (Fig. 4, arrowhead). This finding of "hypometric" pursuit at the end of the open-loop period [average gain (eye velocity/target velocity) at the end of the open-loop period over all 3 target velocities was 0.46 for rightward tracking and 0.47 for leftward tracking] correlated well with the markedly hypometric saccades [average gain (initial saccade amplitude/target displacement) over all 3 stimulus amplitudes was 0.53 for rightward tracking and 0.55 for leftward tracking] shown by this animal. In contrast to the changes in open-loop pursuit and saccade amplitude, the drop in gain during sustained triangular-wave tracking was much less, to values just under 0.9. For monkeys 2 and 3, we were able to compare pursuit and saccade dynamics more closely (Fig. 13). First, prelesion, for both directions of tracking, monkey 2 had higher values both for peak velocity for saccades and peak acceleration for pursuit than did monkey 3. Following the lesion, monkey 2 had a relatively larger change in saccade peak velocity than in saccade accuracy. Analogously, for monkey 2 the peak value of eye acceleration during the open-loop period of pursuit decreased much more than did the value of eye velocity at the end of the open-loop period. Just the opposite was true for monkey 3. Following the lesion, monkey 3 had a relatively large decrease in saccade (rightward) amplitude, but only a small decrease in saccade peak velocity, with an actual increase in peak eye acceleration. Likewise, for rightward pursuit in this animal, there was a decrease in the duration of peak acceleration during pursuit, and hence a decrease in the value of eye velocity at the end of the open-loop period, but with an increase in the value of peak pursuit acceleration. For this animal, for rightward tracking, however, there was an exception to the general finding that the effect of the lesion on saccades and the open-loop portion of pursuit was the same; there was no increase in saccade eye velocity comparable to the increase in peak pursuit acceleration. For leftward saccades and pursuit, however, the deficits were more comparable; there was little change in peak saccade velocity and no change in peak eye acceleration during smooth pursuit. For monkeys 2 and 3, as was the case for monkey 1 described above, there were comparable deficits in saccade amplitude and in pursuit velocity at 100 ms of tracking, except for leftward tracking for monkey 2, in which case there were hypermetric saccades for some target amplitudes but not "hypermetric" pursuit at 100 ms. Nevertheless, considering the arbitrariness of 100 ms as the end of the open-loop period and the relatively (compared with monkey 1), small changes in gain for both saccades and pursuit shown by monkeys 2 and 3, the analogy between saccades and the open-loop portion of pursuit held reasonably well. To epitomize, when comparing the dynamic properties of saccades with the open-loop portion of pursuit, both before and after the lesion of the oculomotor vermis, all three animals largely showed analogous behavior.
|
Pursuit adaptation
Pursuit eye movements, like the vestibuloocular reflex (VOR) and
saccades, can be shown to undergo adaptive changes to ensure proper
calibration of motor responses to the sensory stimuli that drive them.
Even though the pursuit system is under "immediate" visual feedback
control, because of the inherent latency in visual processing it is
burdened with an obligatory, ~100 ms open-loop period of motor
response that must be calibrated to sensory inputs for optimal
visuooculomotor function. Pursuit adaptation has been less studied than
saccade or VOR adaptation, but both humans and monkeys can undergo
adaptive changes both in short-term (minutes to hours) learning
paradigms in which the visual target stimulus is artificially
manipulated (Carl and Gellman 1986; Fukushima et
al. 1996
; Kahlon and Lisberger 1996
) and in
long-term experiments in which, for example, an ocular muscle is
paralyzed and the subject is asked to view habitually with the paretic
eye (Optican et al. 1985
). The ocular following response
(a smooth tracking response elicited by a rapid movement of the entire
visual field) is probably closely related to pursuit in its underlying
physiological substrate, and it too can be shown to undergo adaptive
modification (Miles 1997
; Miles and Kawano
1986
).
As Kahlon and Lisberger (1996) recently reported, our
animals, prelesion, were able to adaptively modify average eye
acceleration in the open-loop period of pursuit in a paradigm using a
double step of velocity. We did notice, however, a seeming difference in the mechanism between adaptive increases and decreases in initial pursuit acceleration. At the relatively high speeds of target motion
that we used, adaptive increases in acceleration were
usually accomplished by an increase in the duration of the
acceleration period, whereas adaptive decreases in
acceleration were accomplished by both a decrease in the
amplitude and in the duration of peak acceleration. The
maximum value of eye acceleration during the open-loop period of
pursuit may be relatively limited, especially for high target speeds,
necessitating an increase in the duration of the period during which
peak eye acceleration is maintained whenever pursuit innervation must
be further increased. An analogous situation occurs with saccades.
Saccade peak velocity approaches a saturation for large amplitude
saccades, and, when adaptation to muscle weakness is required,
increases in the size of large saccades are probably accomplished by an
increase in the duration rather than in the maximum value of the
saccade velocity command (Abel et al. 1978
;
Scudder 1998
).
For both saccades and the VOR there is direct evidence that the
cerebellum participates in the mechanisms by which these ocular motor
subsystem undergo learning (Cohen et al. 1993;
Lisberger et al. 1984
; Optican and Robinson
1980
; Optican et al. 1986
; Raymond et al.
1996
; Scudder 1998
; Takagi et al.
1998
). The evidence for involvement of the cerebellum in
pursuit or ocular-following adaptation, however, has until now only
been hypothetical (Yamamoto et al. 1998
), with no prior
direct demonstration. Here, we have shown directly for pursuit, as we
did for saccades, that lesions of the oculomotor vermis interfere with
ocular motor adaptation. We emphasize again, however, that as for the
pursuit deficits themselves, the adaptation deficits were not total.
Whether this means that other parts of the oculomotor vermis or other
parts of the cerebellar cortex such as the ventral paraflocculus are involved in pursuit adaptation, remains to be shown (Nagao and Kitazawa 1998
).
In sum, the cerebellar vermis plays a role in both saccade and pursuit adaptation. This is not unexpected because the inherent requirements for optimal visual motor function in tracking systems that are encumbered by an obligatory visual delay are the same for saccades and pursuit. The "open-loop period" must be accessible to long-term calibration so that eye movements bring the image of the object of interest to the fovea and keep it there, but without producing any motor instability that would interfere with visual function.
![]() |
ACKNOWLEDGMENTS |
---|
C. Bridges, D. Roberts, R. Lewis, M. Walker, and A. Lasker provided invaluable assistance. D. Ryugo and K. Ohtsuka helped with the preparation and interpretation of the histology. Professor H. Abe provided continuous support.
D. S. Zee was supported by National Eye Institute Grant EY-01849. M. Takagi was supported by the Uehara Memorial Foundation and by Grants-in-Aid for Scientific Research 11671727 from The Ministry of Education, Science, Sports and Culture.
![]() |
FOOTNOTES |
---|
Address for reprint requests: D. S. Zee, Path 2-210, The Johns Hopkins Hospital, Baltimore, MD 21287.
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Received 3 June 1999; accepted in final form 10 November 1999.
![]() |
REFERENCES |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|