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The relationship of anticipatory smooth eye movement to smooth pursuit initiation
k5ssh
Vision Res. Vol. 34. No. 22. DD. 3027-3036.
Pergamon
Copyrigh; 0 1994 levier
0042-6989(94)EOO70-2
1994
Science Ltd
Printed in Great Britain. All rights reserved 0042-6989/94 $7.00 + 0.00
The Relationship of Anticipatory Smooth Eye Movement to Smooth Pursuit Initiation GRACE W. KAO*, MARK J. MORROW*? Received 7 October 1993; in revised form 25 February 1994
We measured anticipatory smooth eye movements and smooth pursuit initiation with predictable and unpredictable step-ramp stimuli in normal subjects. Subjects generated anticipatory eye motion before targets moved and during intervals when targets suddenly disappeared. Expectations of target trajectory modified pursuit acceleration and latency, demonstrating that pursuit initiation is not governed by visual inputs alone. Anticipatory smooth eye movements and predictive contributions to smooth pursuit had similar accelerations and velocities. Anticipation and pursuit initiation varied in parallel between subjects; anticipation was stronger in subjects who generated faster smooth pursuit. These findings imply that anticipatory and smooth pursuit eye movements are governed by a common mechanism. Anticipatory smooth eye movement
eye movements
INTRODUCTION
The task of the smooth pursuit system is to track a small, slowly moving object by generating an eye velocity that matches the velocity of the object’s image. About 100-l 50 msec after a visual target begins moving, a smooth pursuit eye acceleration is initiated in the direction of target motion (Rashbass, 1961; Tychsen & Lisberger, 1986; Carl & Gellman, 1987). At first, this pursuit initiation response operates as an open-loop system driven by the preceding target motion. However, updated retinal image motion information soon begins to influence the pursuit response, closing the visual feedback loop after about 125 msec of smooth eye acceleration have occurred (Tychsen & Lisberger, 1986; Carl & Gellman, 1987). The initial pursuit acceleration brings eye velocity close to target velocity, after which smooth pursuit is typically maintained despite relatively little retinal image motion. The steady-state, or maintenance, phase of pursuit may be driven partly by internal feedback of a representation of the smooth pursuit command, called efference copy (Young, 1971). Smooth pursuit eye movements require a visual stimulus. Most normal subjects generate very limited smooth eye movements in complete darkness, even when they imagine slow target motion (Heywood & Churcher, 1971). However, subjects can initiate smooth eye movements before the expected motion of a visible target (Kowler & Steinman, 1979). These anticipatory smooth *Department of Neurology, Room 2B-182, Medical Center, Sylmar, CA 91342, U.S.A. tTo whom reprint requests should be addressed.
Smooth pursuit Pursuit initiation
Eye acceleration
Olive
View/UCLA
occur prior to target steps or ramps, even when stimulus motion is unpredictable (Kowler & Steinman, 1981). Anticipatory eye movements are not driven by concurrent target motion; they often occur while a target is still stationary. Although smooth pursuit eye movements are largely guided by visual inputs, they are influenced by cognitive expectations of target trajectory. The effects of expectation on pursuit maintenance have been studied with regularly oscillating stimuli. After tracking one halfcycle or less of predictable sinusoidal motion, subjects typically pursue a target with phase lags that are far smaller than those expected from the time delays of the smooth pursuit system (Bahill & MacDonald, 1983; van den Berg, 1988). Quantitative analysis suggests that mechanisms that predict target motion may account for over half of the normal smooth pursuit response to regularly oscillating targets (van den Berg, 1988). Once pursuit eye velocity has approximated target velocity, the eyes may continue to move smoothly during gaps in the appearance of the target, or while the target is artificially stabilized upon the fovea (Becker & Fuchs, 1985; van den Berg, 1988). Despite these observations, recent smooth pursuit models (Robinson, Gordon & Gordon, 1986; Lisberger, Morris & Tychsen, 1987) have not included a predictive contribution. Step-ramp stimuli are used to investigate smooth pursuit initiation (Rashbass, 1961). It has been assumed that pursuit initiation is influenced only by concurrent target motion and that this response directly reflects fundamental aspects of visual motion processing (Tychsen & Lisberger, 1986; Carl & Gellman, 1987). However, cognitive processes also appear to influence
3027
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GRACE
W. KAO
and MARK 1
pursuit initiation, since the expected duration of target appearance modifies the initial pursuit velocity profile (Kowler & McKee, 1987). We studied smooth pursuit initiation in normal subjects in response to predictable and unpredictable step-ramp targets in order to assess the contribution of neural prediction. Considerable individual differences have been observed both in pursuit initiation (Morrow & Sharpe, 1993a) and in anticipatory eye movement (Kowler & McKee, 1987). In our study, individual differences in these smooth eye movements were compared in order to clarify the relationship between pursuit and anticipation. These results were contrasted with subjects’ ability to produce volitional smooth eye movements in darkness. We explored the effects of expected target trajectory by blanking targets or changing their velocities at unpredictable intervals. Most studies of anticipatory smooth eye movement have used stimulus velocities of 10 deg/sec or less (Kowler & McKee, 1987; Boman & Hotson, 1988). Clinical tests of smooth pursuit, however, generally employ highervelocity stimuli (Morrow & Sharpe, 1993a, b). We used target speeds of up to 40 deg/sec to extend the range of observations of smooth anticipation.
SUBJECTS
AND METHODS
Horizontal eye movements were measured in five subjects (mean age 31 yr; range 25-37 yr) using a magnetic search-coil technique (CNC Engineering, Seattle, Wash.) (Collewijn, van der Mark & Jansen, 1975). No subject had a history of neurologic or ophthalmologic problems and none took medication known to affect smooth pursuit. Target Position
J. MORROW
All had best corrected visual acuity of 20120 and viewed the target binocularly. Subjects 1 and 5 had each undcrgone eye movement recording for a different study on one occasion. The other subjects were naive to ocular motor testing. All subjects were enthusiastic about the experiment and appeared well motivated. The target was a 0.2 deg diameter laser spot driven by a computer-controlled mirror galvanometer (General Scanning, Watertown, Mass.). The laser spot was projected onto a featureless screen I .4 m from the subject. The test room was dimly illuminated. Under the conditions of target and room illumination we used, visual afterimages were not perceived by subjects during gaps in target appearance or after pursuit testing, in darkness. A target position signal was obtained by feedback output from the galvanometer. Eye and target position signals were sent through identical electronic differentiators (Gould Electronics, Valley View, Ohio) to obtain analog signals of eye and target velocity. Eye and target position and velocity signals were then sent through matching low-pass filters with six-pole Bessel characteristics and cutoff frequency ( - 3 dB) of 80 Hz. All stimuli moved in a horizontal step-ramp pattern in which the target jumped instantaneously away from the center of the screen then moved at a constant velocity back, crossing the center in 200 msec. Subjects were instructed to follow targets as well as possible, but were not specifically asked to anticipate target motion. Between trials, subjects fixated the target in the center of the projection screen. The durations of stimulus ramps and of inter-trial fixation intervals were constant at 625 msec. Ramp velocities were 5 deg/sec (with 1 deg
[“I
Target Velocity [“/set]
A
i---__
2
set
FIGURE 1. Examples of step-ramp stimulus paradigms, showing target position (left) and target velocity (right) versus time. For each step-ramp trial, the ramp moves in the opposite direction of the step and crosses the fixation point 200 msec after step onset. (A) Predictable step-ramp stimulus. (B) Unpredictable step-ramp stimulus. (C) Unpredictable gap stimulus. (D) Velocity-shift stimulus.
ANTICIPATION
AND
PURSUIT
3029
INITIATION
step), 20 deg/sec (with 4 deg step) and 40 deg/sec (with 8 deg step). Step-ramp trials were presented in runs lasting 40 set, each comprising 32 step-ramps. Four step-ramp stimulus paradigms were used (Fig. 1), as well as a test of self-generated smooth eye movement in darkness:
(4
Predictable stimulus: all step-ramps
in a run
were identical. Unpredictable stimulus: step-ramps of 5, 20 and 40 deg/sec in both directions were intermixed in a pseudorandom pattern. Unpredictable gap stimulus: during an otherwise predictable run of 40 deg/sec step-ramps, the target was blanked at pseudorandom intervals for the entire duration of an expected step-ramp movement. (D) Velocity-shift stimulus: after 20 identical trials of 40 deg/sec step-ramps, the stimulus was abruptly switched to 5 deg/sec step-ramps in the same direction for the remainder of the run. This change was not expected by the subject.
(B)
cc>
(El
Volitional smooth eye movements in darkness: l-2 min after the last step-ramp stimulus was
viewed, as the final test of each session, subjects were asked to make smooth eye movements in darkness. They were encouraged to observed target imagine the previously motion. Each subject performed at least two runs of each step-ramp paradigm within a single test session lasting less than 30 min. We provided frequent verbal encouragement and brief rests to optimize subjects’ performance. Eye movements were monitored in real time while eye and target position and velocity were plotted on a thermal paper chart recorder (AstroMed, Inc., West Warwick, R.I.). Data acquisition and analysis
Eye and target position and velocity signals were digitized at a sampling rate of 250 Hz and stored for off-line analysis using an interactive program on an 80486-based personal computer. The acquisition and analysis software utilized the ViewDac program (ASYST Technologies, Rochester, N.Y.). Saccades were identified and removed by a digital algorithm using operatoradjustable velocity and acceleration criteria. Gaps left by saccade removal were fitted by linear interpolation of the eye velocity data. Results of saccade removal were viewed before and during pursuit analysis. Smooth eye movements were not quantified for a given trial if saccades occurred during the desired measurement interval. For each step-ramp trial, we measured the following response variables: anticipatory eye acceleration, pursuit eye acceleration, pursuit latency and peak pursuit velocity (Fig. 2). The results of computerized data analysis of each stepramp trial were assessed for accuracy by the operator, who could change analysis variables to obtain optimal best-fit lines for each response.
FIGURE 2. Ckulographic trace of a response to a single predictable 4O”/sec step-ramp stimulus in subject 1, showing eye velocity (irregular line) and target velocity (solid line) versus time. Figure demonstrates measurements made from each step-ramp response: (1) anticipatory eye acceleration (slope of regression line 1); (2) pursuit eye acceleration (slope of regression line 2); (3) pursuit latency; and (4) peak pursuit velocity.
The acceleration of anticipatory eye movements was computed for individual trials by calculating a regression line from eye velocity data over the period from 100 msec before step onset to 80 msec after onset. The figure of 80 msec was chosen since it is near the minimum reported latency of visually guided responses to small target motion in humans (Tychsen & Lisberger, 1986; Carl & Gellman, 1987). The 180 msec pre-pursuit segment we analyzed could be fit well with a single line in each trial, since anticipatory eye acceleration nearly always began more than 100msec before target motion (Fig. 2). The visually guided response of smooth pursuit was considered to begin when smooth eye acceleration exceeded anticipatory eye acceleration by three standard deviations. Even for trials with large anticipatory responses, there was always a clear inflection point where the pursuit response began. Smooth pursuit acceleration was measured from a regression line of the first 100 msec of eye velocity data following this point. Pursuit latency was identified at the point where the anticipatory and pursuit acceleration regression lines intersected. For unpredictable gap stimuli, smooth eye acceleration was measured during the gap when the target image was blanked. The peak velocity of smooth pursuit during each step-ramp trial was recorded. Data from each of over 400 trials in each subject were analyzed with the SYSTAT statistical program (SYSTAT, Inc., Evanston, Ill.), using paired t-tests and one-way analysis of variance (ANOVA). Responses to each direction of target motion were pooled. RESULTS
Anticipation of predictable stimuli
Anticipatory eye acceleration increased with target velocity in response to predictable step-ramp stimuli (P = 0.01, ANOVA; Fig. 3). For predictable 40 deg/sec ramps, all subjects generated peak anticipatory accelerations of over 35 deg/sec’ and three subjects reached values of over 60 deg/sec’ (Table 1). Mean anticipatory
GRACE
3030
_
W. KAO
and MARK
J. MORROW
were very low ( < I degjsec’ at each However, the mean of the absolute values of anticipatory accelerations to unpredictable targets was about 4deg/sec’ (Fig. 3), indicating that subjects anticipated even these pseudorandom stimuli. to target
25.
target
q
predictable
m
unpredictable
Smooth
2 01, 0
30
20
10
Target
Velocity
40
[“/XC]
FIGURE 3. Anticipatory eye acceleration versus target velocity for predictable and unpredictable step-ramp stimuli. Data points represent group means of eye acceleration values of five subjects. Values relative to target velocity are shown for predictable targets; absolute values are shown for unpredictable targets. Error bars indicate one standard deviation.
and smooth pursuit accelerations varied widely among subjects; those who generated higher anticipatory accelerations also generated higher pursuit accelerations, even to unpredictable targets (Fig. 4). This relationship was most apparent for the fastest, 40 deg/sec targets (Table 1). Anticipatory accelerations had values that averaged about 10% those of pursuit acceleration at each target velocity in each subject (Table 2). Prior experience in eye movement testing showed no clear effect, since the subjects who had previously undergone eye movement testing, subjects 1 and 5, generated respectively the best and the worst smooth eye movement. Anticipation
of unpredictable
stimuli
As expected, there was no relationship between anticipatory acceleration and target velocity for unpredictable stimuli (Fig. 3). In contrast to responses to predictable stimuli, anticipatory eye accelerations to unpredictable targets seldom exceeded 15 deg/sec’ (Fig. 5); since they were in the direction opposite target motion in about half of trials, the mean values of these responses relative
TABLE
1. Anticipatory
and pursuit
responses
Responses to predictable 40 deg/sec step-ramps
Subject Subject
Anticipatory acceleration (deg/sec*)
I
81 (24)
2 3 4 5
71 45 66 38
(16) (11) (10) (5)
Pursuit acceleration (deg/sec*) 356 352 235 190 230
(229) (199) (174) (79) (108)
direction
velocity).
pursuit
before and during unpredictable between 40 deg/sec step-ramps
Initial, pre-gap acceleration (deg/se?) 57 (39) 14 (22) 34 (17) 30 (14) 16 (5)
and unpredictuble
,stimuli
Mean pursuit accelerations and peak velocities were higher for predictable than unpredictable stimuli only at the highest target velocity, 40 deg/sec (P < 0.04, paired t-tests; Fig. 6). For 40 deg/sec ramps, responses to predictable stimuli had pursuit accelerations that averaged 59 deg/sec2 faster than those to unpredictable stimuli; peak velocities averaged 9.7 deg/sec faster. At the lowest target velocity, 5 deg/sec, unpredictable stimuli actually evoked higher pursuit accelerations and velocities than predictable stimuli (P < 0.02). Peak pursuit velocities for unpredictable 5 deg/sec targets usually exceeded target velocity, averaging 7.8 deg/sec. Pursuit velocities and accelerations were similar for predictable and unpredictable 20 deg/sec targets. For predictable targets, initial pursuit acceleration rose nearly in proportion to target velocity; at the mean accelerations we measured [Fig. 6(A)], the eyes would reach target velocity between 172 msec (for 5 degjsec targets) and 253 msec (for 40 deg/sec targets) after pursuit onset. Mean pursuit accelerations varied less with the velocities of unpredictable targets. At the mean pursuit accelerations we measured for unpredictable stimuli, the eyes would reach target velocity in only 106 msec for 5 deg/sec targets, but would require 404 msec for 40 deg/sec targets. Mean pursuit latency was 26 msec shorter for predictable than unpredictable stimuli in the group of five subjects (Table 3). This latency difference was significant in each subject (P < 0.007, paired t-tests) and in the group (P = 0.003). The shorter latency of pursuit initiation to predictable targets was not explained by inclusion of very short latency responses. Pursuit latency values for predictable and unpredictable stimuli approximated normal distributions (Fig. 7) and had similar standard deviations in each subject (Table 3). Pursuit latencies of under 80 msec were uncommon, comprising < 6% of responses to predictable targets in each subject.
to predictable 40 deg/sec step-ramp stimuli to smooth eye movements in darkness Responses
qf predictable
Second, intra-gap acceleration (deg/sec2) 114 103 76 87 42
(76) (53) (61) (37) (3 1)
and unpredictable
gaps
Peak intra-gap velocity (deg/sec )
gaps in each subject,
Volitional smooth eye motion in darkness Peak acceleration in darkness (deg/sec’)
27 (19) 19(11) 13 (10) ‘7(7) 7 (6)
Values shown are peak responses with means for step-ramp and gap responses in parenthesis. Eye accelerations and velocities in darkness represent means of highest observed rightward and ‘eftwdrd
compared
Peak velocity in darkness (deglsec )
2 8 3 II 7
smooth
2 4 5 5 2
eye motion
values.
ANTICIPATION
Compared with individual differences in anticipatory and pursuit acceleration (see Fig. 4), differences in pursuit latency were small.
(A)
*“b/act
10
0
Target
20 Velocity
30
3031
AND PURSUIT INITIATION
I
rub/d
2
subject subject
3 4
subject
5
40
[“/see]
Unpredictable
gap stimuli
Responses in the unpredictable gap experiment often showed two anticipatory acceleration components: an initial acceleration that began before target offset and a second, higher acceleration that followed target offset by about 120 msec (range 76187 msec), a latency similar to that of visually-guided pursuit movements (Fig. 8). This double acceleration gave responses to target gaps an appearance like those of responses to visible step-ramps. The tirst eye acceleration had values comparable to other anticipator eye movements that preceded the expected appearance of a 40 deg/sec ramp, averaging 19 deg/sec’ (Table 1). The second anticipatory eye acceleration, beginning after target disappearance, was higher than the pre-gap anticipatory acceleration by an average of about 270%, reaching over 80 deg/sec’ in three subjects and averaging 52 deg/sec2 in the group (Fig. 9). Peak anticipatory eye velocities during gaps reached over 1.5deg/sec, averaging 10.6 deg/sec (Table 1). All subjects produced peak anticipator velocities of over 6 deg/sec during gaps. Velocity -shift stimuli
0
10 Torget
20 Velocity
30
subiect
1
subject
2
subiect
3
subject
5
subject
4
.,.a
rubiect
3
_ 0
subject subject
2 5
40
[“/see]
(Cl
200
1
,_,,,,,..,,......
*_ .__________._*_-----. . . .Cl-., . . . . . . . . . . . . . . . .._._.................
q
Q *“bjsct
Expectations of target trajectory strongly influenced smooth pursuit that occurred immediately after the reduction in target speed in the velocity-shift experiment (Fig. 10). In response to this paradigm, subjects’ smooth pursuit eye movements reliably overshot the velocity of the first few 5 deg/sec ramps, as they expected to track a 40 deglsec ramp. For the first 5 deg/sec target after the shift, mean pursuit acceleration was 91 deg/sec’ and mean peak pursuit velocity was 15.4 deg/sec in our subject group. These values were almost double those for 5 deg/sec ramps in the unpredictable stimulus paradigm (mean acceleration 46 deg/sec*, mean peak velocity 7.8 deg/sec) and were more than double those for 5 deg/sec ramps in the predictable stimulus paradigm (mean acceleration 29 deg/se$, mean peak velocity 4.7 deg/sec). The initial response to 5 deg/sec targets in the velocity-shift paradigm thus had accelerations and velocities that were respectively about 50 deg/sec* and lOdeg/sec faster than responses to other 5 deg/sec targets. These differences, attributable to target expectation, were similar to the differences in pursuit acceleration and velocity between responses to predictable and unpredictable 40 deg/sec ramps (Fig. 6). Anticipatory accelerations and velocities during gaps between 40 deglsec ramps had comparable values (Table 1).
4
TABLE 2. Ratios of mean anticipatory eye acceleratian to mean pursuit eye acceleration (%) at each target speed in each subject for predictable step-ramp stimuli Subject
00 0
10 Target
20 Velocity
30
40
[“/xc]
FIGURE 4. Mean anticipatory acceferation for predictable stimuli (A) and mean pursuit acceleration for predictable stimuli (B) and unpredictable stimuli (C) in each subject, versus target velocity. Note differing y-axis scales. Each data point represents the mean of at least 58 values.
1 2 3 4 5 Mean
5 deg/sec ramps
20 degjsec ramps
40 deg/sec ramps
7.0 7.8 10.4 19.4 8.4
7.7 6.9 11.2 18.8 5.3
11.3 7.8 6.6 12.9 4.3
10.6 + 5.1
9.9 + 5.4
8.6 + 3.5
Mean data + 1SD noted at bottom.
3032
GRACE
W. KAO and MARK
J. MORROW
n predlcteble H unpredlctabie
-30
-15
0
15
30
45
Anticipatory eye accelertion
50
75
90
[“/e&J
FIGURE 5. Histograms of anticipatory eye acceleration to unpredictable step-ramp stimuli (577 data points) and predictable Wjsec step-ramp stimuli (279 data points) in five subjects. Negative values indicate eye accelerations in the direction opposite target motion.
Volitional smooth eye movements in darkness
In darkness, ail subjects generated smooth eye movements to the right and left at velocities greater than those of their spontaneous eye drift. No subject had spontaneous eye drift of over 1 deg/sec near primary position. Volitional smooth eye movements in darkness were of much lower peak velocities and accelerations than anticipatory responses to step-ramp targets (Table 1). No subject generated smooth eye movement at a velocity of over 5 deg/sec or an acceleration over 11 deg/sec* in darkness. There was no relationship between the ability to generate smooth eye movements in darkness and to produce anticipatory smooth eye movements to visual targets. For instance, subject 1, who generated the highest anticipatory accelerations and velocities, produced smooth eye movements in darkness with lower peak velocity and acceleration than any other subject. In contrast, subject 4, who did not make good anticipatory eye movements to step-ramps, showed the best smooth eye movement responses in darkness. DISCUSSION
Anticipatory smooth eye movements to predictable targets
Our subjects anticipated step-ramp stimuli by smoothly accelerating their eyes before targets moved. These anticipatory eye movements reached accelerations of over 35 deg/sec* in each subject. There was no evidence of a saturating effect of target velocity on anticipation. Anticipatory eye acceleration rose with predictable target velocities from 5 to 40 deg/sec, typically corresponding to about 10% of the ensuing pursuit acceleration. Kowler and McKee (1987) demonstrated a similar relationship for slower targets; over a range of stimulus speeds from about 0.5 to 5 deg/sec, their subjects generated anticipatory smooth eye motion with average velocities of lO-25% of target velocity. In contrast, subjects can maintain smooth eye movements at about 60% of target velocity if a stimulus disappears after the eyes have attained its velocity (Becker & Fuchs, 1985).
The ability to generate anticipatory and pursuit eye accelerations varied in parallel between subjects; those who achieved higher smooth pursuit accelerations also produced brisker anticipatory movements. The individual differences in pursuit acceleration were too large to be explained by differences in anticipatory contributions alone. For example, the difference in mean pursuit acceleration between subjects 1 and 4 was about 150 deg/sec2 for predictable 40 deg/sec ramps (see Table 1). In contrast, the difference in their mean anticipatory accelerations for these targets was only about 15 deg/sec2. Moreover, anticipation would not account for the large differences we observed in pursuit accelerations to unpredictable targets, since the mean relative values of anticipatory acceleration to these targets were near zero. The parallel between individual differences of smooth pursuit and anticipatory smooth eye movement suggests that both may be driven by a common neural mechanism. This hypothesis is reinforced by observations from lesion studies. Unilateral frontal eye field lesions in monkeys impair both smooth pursuit and anticipatory smooth eye movements, especially toward the damaged side (MacAvoy, Gottlieb & Bruce, 1991; Keating, 1993). Discrete unilateral brain lesions in humans have similar effects (Hotson, Braun & Boman, 1990). The functional importance of anticipatory smooth eye movement was not clear in our study. When stimuli move as expected, anticipatory smooth motion accelerates the eyes toward target velocity before visual motion inputs can activate the classic, visually-guided smooth pursuit system. One possible goal of anticipation is to minimize the demands on smooth pursuit by helping to match eye velocity to target velocity as soon as possible. This goal would best be served by a high anticipatory acceleration, which might be expected to accompany high pursuit accelerations and velocities. However, our subjects produced anticipatory eye accelerations that averaged only about 10% of pursuit acceleration. Relative values of anticipatory acceleration were higher for predictable targets than for unpredictable targets at all target speeds. Despite this, predictable targets evoked
ANTICIPATION
250
1
200
-
AND
(4
c e s z
150-
e 2 : 4
loo-
t w t
2
50
-
; a
1 0
0
ij
o
predictable
n
unpredictable
I
I
I
I
10
20
30
40
Target
40
Velocity
[‘/set]
-I
10
c? 5 I
0
10 Target
1
I
I
20
30
40
Velocity
[“/see]
FIGURE 6. Pursuit acceleration (A) and peak pursuit velocity (B) versus target velocity for predictable and unpredictable step-ramp stimuli. Data points represent group mean of five subjects. Error bars indicate one standard deviation. In (B), the standard deviation of pursuit velocity for predictable S”/sec targets is too small to be shown
pursuit accelerations and velocities that were similar to or lower than those evoked by unpredictable targets at 5 and 20 deg/sec. There are disadvantages in generating overly brisk anticipatory smooth eye movements. By initiating smooth eye motion while a stationary target is still present, anticipation creates retinal position and velocity errors that are potentially undesireable. In addition, anticipatory movements may increase the demands upon the pursuit system if the stimulus does not move as expected. TABLE 3. Mean pursuit latency for predictable and unpredictable ramps in each subiect
Subject
Predictable targets
1 2 3 4 5 Mean Group
INITIATION
D@erences stimuli
N
0
PURSUIT
122 * 25 132+36 128 k 28 138+42 143 + 34 133 * 8 meanf
1SD noted
f
1SD step-
Unpredictable targets 160 f 21 162 & 36 142+31 174*44 157+38 159* 11 at bottom.
3033
in responses to predictable and unpredictable
Our subjects produced anticipatory smooth eye motion to unpredictable targets, although these movements were of considerably lower accelerations than responses to predictable targets. The generation of anticipatory eye movement takes into account two components: (1) cognitive expectation of the trajectory of target motion and (2) motor habit based on the previous ocular responses (Kowler, Martin & Pavel, 1984; Kowler, 1989). Of these two mechanisms, cognitive expectation is more powerful, since directional cues can override the effects of prior target motion (Kowler, 1989). Both mechanisms are driven by repetitive stimuli like our predictable targets. For unpredictable targets, motor habit remains active as a driving force for anticipation, while uncertainty regarding target trajectory weakens the contribution of cognitive expectation. Pursuit accelerations and peak velocities were higher for predictable targets than unpredictable targets only at the highest target velocity, 40 deg/sec. These smooth pursuit measures were actually lower for predictable stimuli than for unpredictable stimuli at the lowest target velocity, 5 deg/sec. When targets with speeds covering this eight-fold range were alternated unpredictably, the smooth pursuit system responded precisely only to targets in the middle of the range, matching peak eye velocity to target velocity at 20 deg/sec. Kowler and McKee (1987) reported similar biasing of pursuit responses toward the center velocity when a range of target velocities under 5 deg/sec was presented. These findings indicate that the smooth pursuit system has limited ability to respond accurately when it cannot predict target speed and direction. When stimulus velocity was predictable in our study, the pursuit system adjusted initial eye acceleration to reach target velocity in about 200 msec. This implies a specific strategy for governing pursuit initiation, in which the optimal smooth eye acceleration is not necessarily the fastest one. Initial pursuit acceleration represents a compromise between the need to reach target velocity as soon as possible and the necessity of minimizing velocity overshoot (Carl & Gellman, 1987). When initial eye accelerations were too low, as when our subjects responded to unpredictable 40 deg/sec targets, eye velocity did not rise fast enough to approximate target velocity. On the other hand, when pursuit accelerations were too high, as when subjects responded to unpredictable 5 deg/sec stimuli, the eyes overshot target velocity. We found that initial pursuit responses to predictable targets had latencies that averaged 26 msec shorter than responses to unpredictable targets. This difference was not attributable to short-latency responses which might have been anticipatory. We conclude that neural mechanisms that predict target motion may prepare the smooth pursuit system for rapid action by specifying information about desired eye motion beforehand. The decrease in pursuit latency we observed with predictable
3034
GRACE
W. KAO
and MARK
.I. MORROW
40 1
n predictable q unp‘fedictable
0
20
--P40
60
4
-I,
60
100
li0
140
160
180
200
220
240
Pursuit latency (msec) FIGURE
7. Histograms
of pursuit
latency
for predictable and unpredictable step-ramp represents at least I10 data points.
stimuli may partly account for minimization of phase lags during steady-state pursuit of sinusoidal stimuli (Bahill & McDonald, 1983; van den Berg, 1988). We have shown that the acceleration and latency of smooth pursuit initiation are influenced by the predictability of target direction and speed. Expectations of the duration of stimulus appearance also affect pursuit initiation (Kowler & McKee, 1987). The existence of anticipatory smooth eye movements and of predictive modulation of pursuit initiation belie control systems models of smooth pursuit that take into account only concurrent motion of the retinal image and the eyes (Robinson et al., 1986; Lisberger et al., 1987). Modified control systems models have been used to explain predictive effects on the phase of pursuit maintenance, but they still do not explain anticipatory eye movements that occur prior to stimulus motion (van den Berg, 1988; Pavel, 1990). Effective modeling of smooth ocular track-
stimuli in subject
I. Each histogram
ing may require a combination of classical control systems modeling to explain low-level visuomotor processing and decision theory to account for the effects of anticipation and prediction (Kowler et al.. 1984). Neural network approaches to pattern recognition may meet these requirements (Pavel, 1990). Anticipation during target disappearance
Our subjects generated smooth eye accelerations during gaps in target appearance that corresponded to expected stimulus motion. Two sequential eye accelerations were often made in trials with gaps, the first beginning while a fixation target was still illuminated and the second, higher acceleration beginning after the target disappeared. Becker and Fuchs (1985) also observed the phenomenon of sequential anticipatory accelerations to targets which disappeared at the moment of expected motion. Not surprisingly, the first anticipatory
Tafgst oft
lbrgst on
I1 O*faee
FIGURE 8. Oculographic trace of responses to unpredictable gap stimulus in subject I. Eye velocity (irregular line) and target velocity (solid line) are plotted versus time. Within the third response interval, the target has been blanked during its expected period of step and ramp motion. The first anticipatory eye acceleration begins before target disappearance (line I): a second. higher anticipatory acceleration begins about 80 msec after target offset (line 2). A peak anticipatory smooth eye velocity ol 27 set is attained.
ANTICIPATION
d
2b
4b
Eye
6b
acceleration
50
100
AND PURSUIT
li0
[“/se91
W
OD E g ma z ‘O 206
lo-
!? t! o0
I 5
I 10
I 15
Peak eye velocity
I 20
I 25
30
[“/set]
FIGURE 9. Histograms of eye acceleration (A) and peak eye velocity (B) taking place during gap intervals of unpredictable gap stimulus in five subjects. Each histogram represents 30 data points.
acceleration in gap trials in our study had the same characteristics as other eye accelerations preceding the expectation of 40 deg/sec ramp motion. This acceleration averaged about 20 deg/sec’. The second anticipatory acceleration, occurring while no target was visible, was considerably higher, averaging about 50 deg/sec*. This acceleration increase might be explained by the enhancement of anticipatory smooth eye movement noted to
occur when visual fixation is discontinued (Boman & Hotson, 1988). Prior to target disappearance, anticipatory smooth eye motion caused retinal movement of the image of the fixation target that may have inhibited the response; after target offset, no such retinal slip was present. In addition to disinhibiting anticipation by removing retinal slip, the disappearance of the target could act as an independent sensory trigger. Target offset might be sensed as an event in itself, provoking more vigorous anticipation. The timing of the second anticipatory acceleration to gaps was similar to that of smooth pursuit initiation, with a mean latency of about 120 msec after target offset. This observation provides further support for the hypothesis that a common mechanism drives anticipation and smooth pursuit.
Pursuit eye acceleration and peak ,velocity were markedly altered by incorrect expectations of target trajectory in the velocity-shift paradigm. After presenting many 40 deg/sec stimuli, an unexpected reduction of target speed to 5 deg/sec evoked initial pursuit with accelerations much faster than for 5 deg/sec targets in other experiments. This excessive acceleration caused marked overshoot of eye velocity over target velocity. Responses to this paradigm confirm the dependence of pursuit initiation on non-visual, predictive mechanisms. Predictive contributions to smooth pursuit were similar in different paradigms. The difference between mean pursuit eye acceleration to predictable and unpredictable 40 deg/sec targets was about 50 deg/sec*. Comparable acceleration differences were observed between responses to the first 5 deg/sec target in the velocity-shift paradigm, when 40 deg/sec target motion was expected, and to 5 deg/sec targets in other paradigms. Pursuit velocity differences attributable to target expectation averaged about 10 deg/sec in each of these paradigms. Anticipatory smooth eye motion during gaps in which subjects expected a 40 deg/sec ramp had similar mean accelerations and velocities. This suggests that, in some cases, simple addition of an anticipatory smooth eye movement to visually-guided smooth pursuit explains the predictive contribution to pursuit initiation.
_--lS"/SSC
300 msoc
FIGURE velocities
3035
Predictive contributions to pursuit initiation
40-
5 g
INITIATION
10. Oculographic trace of responses to velocity-shift are plotted versus time. Target velocity is abruptly step-ramps. Eye velocity markedly overshoots
stimulus in subject 2. Eye (irregular line) and target (solid line) shifted between the first two (40Ojsec) and last three (5”/sec) target velocity for the first two S”/sec stimuli.
3036
Volitional
GRACE
smooth
eye movements
W. KAO
and MARK
in darkness
Normal subjects have limited ability to move their eyes smoothly in darkness unless they perceive a visual afterimage or non-visual sensory cue (Heywood & Churcher, 1971; Gauthier & Hofferer, 1976). Our subjects made volitional smooth eye movements in darkness with much lower peak accelerations and velocities than those of eye movements made in anticipation of target motion. The relative abilities of subjects to make smooth eye movements in darkness did not correlate with their abilities to generate anticipatory smooth eye movements. These observations imply that mechanisms that produce anticipatory eye movements, including cognitive expectation and motor habit, are inactive in continuous, complete darkness. Cognitive expectations of target motion could not be consciously controlled in that our subjects did not make robust smooth eye movements simply by imagining target motion viewed in the recent past. Anticipatory smooth eye movements seem to be regulated chiefly by subconscious mechanisms, since they are generated even when subjects try to suppress them or are distracted (Kowler & Steinman, 1979, 1981). Motor habit was ineffective at producing smooth eye motion in darkness, even though our subjects had finished their runs of over 400 step-ramp responses only l-2 min earlier. In order to drive anticipatory smooth eye movement, the motor habit mechanism must require frequent updating of experience. REFERENCES Bahill, A. T. & McDonald, J. D. (1983). Smooth pursuit eye movements in response to predictable target motion. Vision Research, 23, 1537-83. Becker, W. & Fuchs, A. F. (1985). Prediction in the oculomotor system: Smooth pursuit during transient disappearance of a visual target. Experimental Brain Research, 57, 562-575. van den Berg, A. V. (1988). Human smooth pursuit during transient perturbations of predictable and unpredictable target movement. Experimental Brain Research, 72, 95-108. Boman, D. K. & Hotson, J. R. (1988). Stimulus conditions that enhance anticipatory slow eye movements. Vision Research, 28, 115745. Carl, J. R. & Gellman, R. S. (1987). Human smooth pursuit: Stimulusdependent responses. Journal of Neurophysiology, 57, 1446-1463. Collewijn, H., van der Mark, F. & Jansen, T. C. (1975). Precise recording of human eye movements. Vision Research, 15, 447450. Heywood, S. & Churcher, J. (1971). Eye movements and the afterimage. I. Tracking the afterimage. Vision Research, 11, 1163-l 168.
J. MORROW
Hotson. J. R., Braun, D. & Boman. D. (1990). Antrcipatory smooth eye movements after human brain lesions. Int~est~guri~~c,Ophtholmolog? and Visual Science (Suppl. 4), 31. 532. Gauthier, G. M. & Hofferer. J. M. (1976). Eye tracking of self-moved targets in the absence of vision. E.~perimental Brain RaseLJrch, 26. 121-139. Keating, E.G. (1993). Lesions of the frontal eye field impair pursuit eqc movements, but preserve the predictions driving them. Behmioural Brain Research, 53, 91-104. Kowler, E. (1989). Cognitive expectations, not habits, control anticipatory smooth oculomotor pursuit. Visiorr Research. 29. 1049%1057. Kowler, E. & McKee, S. P. (1987). Sensitivity of smooth eye movement to small differences in target velocity. Vision Research, 27,993~-1015. Kowler, E, & Steinman, R. M. (1979). The effect of expectations on slow oculomotor control-I. Periodic target steps. Vision Rcscorch, 19, 619-632. Kowler, E. & Steinman, R. M. (1981). The effect of expectations on slow oculomotor control-III. Guessing unpredictable target displacements. Vision Research, 21, 191L203. Kowler, E., Martin, A. J. & Pavel. M. (1984). The effect ofexpectations on slow oculomotor control-IV. Anticipatory smooth eye movements depend on prior target motions. Vision Research, 24. 197 2 IO. Lisberger, S. G., Morris, E. J. & Tychsen. L. (1987). Visual motion processing and sensory-motor integration for smooth pursuit eye movements. Annual Review’ of’ Neuroscience, 10, 97-129. MacAvoy, M. C., Gottlieb, J. P. &Bruce, C. J. (1991). Smooth-pursuit eye movement representation in the primate frontal eye field. Cerebral Cartes, I, 95-102. Morrow. M. J. & Sharpe J. A. (1993a). Smooth pursuit initiation in young and elderly subjects. Vision Research, 33, 203.-210. Morrow, M. J. & Sharpe, J. A. (1993b). Retinotopic and directional deficits of smooth pursuit initiation after posterior cerebral hemispheric lesions. Neurology, 43, 595-603. Pavel, M. (1990). Predictive control of eye movement. In Kowler. E. (Ed.), Eye movements and their role in visual and co,qnitit:e processe.s (pp. 71- 114). Amsterdam: Elsevier. Rashbass, C. (1961). The relationship between saccadic and smooth tracking eye movements. Journal of Physiology, 159, 326.-338. Robinson, D. A., Gordon, J. L. & Gordon, S. E. (1986). A model of the smooth pursuit eye movement system. Biological Cybernetics, 55. 43-57. Tychsen, L. & Lisberger, S. G. (1986). Visual motion processing for the initiation of smooth-pursuit eye movements in humans. Journal of Neurophysiology, 56, 953-968. Young, L. R. (1971). Pursuit eye tracking movements. In Bach-y-Rita, P. & Collins, C. C. (Eds). The control of’ eye movements (pp. 429443). New York: Academic Press.
Acknowledgements-The authors thank Hieu Le. MSEE for his assistance in programming and data analysis. Research supported by Olive View/UCLA Education and Research Institute grant 545 (Dr Morrow).
Vision Res. Vol. 34. No. 22. DD. 3027-3036.
Pergamon
Copyrigh; 0 1994 levier
0042-6989(94)EOO70-2
1994
Science Ltd
Printed in Great Britain. All rights reserved 0042-6989/94 $7.00 + 0.00
The Relationship of Anticipatory Smooth Eye Movement to Smooth Pursuit Initiation GRACE W. KAO*, MARK J. MORROW*? Received 7 October 1993; in revised form 25 February 1994
We measured anticipatory smooth eye movements and smooth pursuit initiation with predictable and unpredictable step-ramp stimuli in normal subjects. Subjects generated anticipatory eye motion before targets moved and during intervals when targets suddenly disappeared. Expectations of target trajectory modified pursuit acceleration and latency, demonstrating that pursuit initiation is not governed by visual inputs alone. Anticipatory smooth eye movements and predictive contributions to smooth pursuit had similar accelerations and velocities. Anticipation and pursuit initiation varied in parallel between subjects; anticipation was stronger in subjects who generated faster smooth pursuit. These findings imply that anticipatory and smooth pursuit eye movements are governed by a common mechanism. Anticipatory smooth eye movement
eye movements
INTRODUCTION
The task of the smooth pursuit system is to track a small, slowly moving object by generating an eye velocity that matches the velocity of the object’s image. About 100-l 50 msec after a visual target begins moving, a smooth pursuit eye acceleration is initiated in the direction of target motion (Rashbass, 1961; Tychsen & Lisberger, 1986; Carl & Gellman, 1987). At first, this pursuit initiation response operates as an open-loop system driven by the preceding target motion. However, updated retinal image motion information soon begins to influence the pursuit response, closing the visual feedback loop after about 125 msec of smooth eye acceleration have occurred (Tychsen & Lisberger, 1986; Carl & Gellman, 1987). The initial pursuit acceleration brings eye velocity close to target velocity, after which smooth pursuit is typically maintained despite relatively little retinal image motion. The steady-state, or maintenance, phase of pursuit may be driven partly by internal feedback of a representation of the smooth pursuit command, called efference copy (Young, 1971). Smooth pursuit eye movements require a visual stimulus. Most normal subjects generate very limited smooth eye movements in complete darkness, even when they imagine slow target motion (Heywood & Churcher, 1971). However, subjects can initiate smooth eye movements before the expected motion of a visible target (Kowler & Steinman, 1979). These anticipatory smooth *Department of Neurology, Room 2B-182, Medical Center, Sylmar, CA 91342, U.S.A. tTo whom reprint requests should be addressed.
Smooth pursuit Pursuit initiation
Eye acceleration
Olive
View/UCLA
occur prior to target steps or ramps, even when stimulus motion is unpredictable (Kowler & Steinman, 1981). Anticipatory eye movements are not driven by concurrent target motion; they often occur while a target is still stationary. Although smooth pursuit eye movements are largely guided by visual inputs, they are influenced by cognitive expectations of target trajectory. The effects of expectation on pursuit maintenance have been studied with regularly oscillating stimuli. After tracking one halfcycle or less of predictable sinusoidal motion, subjects typically pursue a target with phase lags that are far smaller than those expected from the time delays of the smooth pursuit system (Bahill & MacDonald, 1983; van den Berg, 1988). Quantitative analysis suggests that mechanisms that predict target motion may account for over half of the normal smooth pursuit response to regularly oscillating targets (van den Berg, 1988). Once pursuit eye velocity has approximated target velocity, the eyes may continue to move smoothly during gaps in the appearance of the target, or while the target is artificially stabilized upon the fovea (Becker & Fuchs, 1985; van den Berg, 1988). Despite these observations, recent smooth pursuit models (Robinson, Gordon & Gordon, 1986; Lisberger, Morris & Tychsen, 1987) have not included a predictive contribution. Step-ramp stimuli are used to investigate smooth pursuit initiation (Rashbass, 1961). It has been assumed that pursuit initiation is influenced only by concurrent target motion and that this response directly reflects fundamental aspects of visual motion processing (Tychsen & Lisberger, 1986; Carl & Gellman, 1987). However, cognitive processes also appear to influence
3027
3028
GRACE
W. KAO
and MARK 1
pursuit initiation, since the expected duration of target appearance modifies the initial pursuit velocity profile (Kowler & McKee, 1987). We studied smooth pursuit initiation in normal subjects in response to predictable and unpredictable step-ramp targets in order to assess the contribution of neural prediction. Considerable individual differences have been observed both in pursuit initiation (Morrow & Sharpe, 1993a) and in anticipatory eye movement (Kowler & McKee, 1987). In our study, individual differences in these smooth eye movements were compared in order to clarify the relationship between pursuit and anticipation. These results were contrasted with subjects’ ability to produce volitional smooth eye movements in darkness. We explored the effects of expected target trajectory by blanking targets or changing their velocities at unpredictable intervals. Most studies of anticipatory smooth eye movement have used stimulus velocities of 10 deg/sec or less (Kowler & McKee, 1987; Boman & Hotson, 1988). Clinical tests of smooth pursuit, however, generally employ highervelocity stimuli (Morrow & Sharpe, 1993a, b). We used target speeds of up to 40 deg/sec to extend the range of observations of smooth anticipation.
SUBJECTS
AND METHODS
Horizontal eye movements were measured in five subjects (mean age 31 yr; range 25-37 yr) using a magnetic search-coil technique (CNC Engineering, Seattle, Wash.) (Collewijn, van der Mark & Jansen, 1975). No subject had a history of neurologic or ophthalmologic problems and none took medication known to affect smooth pursuit. Target Position
J. MORROW
All had best corrected visual acuity of 20120 and viewed the target binocularly. Subjects 1 and 5 had each undcrgone eye movement recording for a different study on one occasion. The other subjects were naive to ocular motor testing. All subjects were enthusiastic about the experiment and appeared well motivated. The target was a 0.2 deg diameter laser spot driven by a computer-controlled mirror galvanometer (General Scanning, Watertown, Mass.). The laser spot was projected onto a featureless screen I .4 m from the subject. The test room was dimly illuminated. Under the conditions of target and room illumination we used, visual afterimages were not perceived by subjects during gaps in target appearance or after pursuit testing, in darkness. A target position signal was obtained by feedback output from the galvanometer. Eye and target position signals were sent through identical electronic differentiators (Gould Electronics, Valley View, Ohio) to obtain analog signals of eye and target velocity. Eye and target position and velocity signals were then sent through matching low-pass filters with six-pole Bessel characteristics and cutoff frequency ( - 3 dB) of 80 Hz. All stimuli moved in a horizontal step-ramp pattern in which the target jumped instantaneously away from the center of the screen then moved at a constant velocity back, crossing the center in 200 msec. Subjects were instructed to follow targets as well as possible, but were not specifically asked to anticipate target motion. Between trials, subjects fixated the target in the center of the projection screen. The durations of stimulus ramps and of inter-trial fixation intervals were constant at 625 msec. Ramp velocities were 5 deg/sec (with 1 deg
[“I
Target Velocity [“/set]
A
i---__
2
set
FIGURE 1. Examples of step-ramp stimulus paradigms, showing target position (left) and target velocity (right) versus time. For each step-ramp trial, the ramp moves in the opposite direction of the step and crosses the fixation point 200 msec after step onset. (A) Predictable step-ramp stimulus. (B) Unpredictable step-ramp stimulus. (C) Unpredictable gap stimulus. (D) Velocity-shift stimulus.
ANTICIPATION
AND
PURSUIT
3029
INITIATION
step), 20 deg/sec (with 4 deg step) and 40 deg/sec (with 8 deg step). Step-ramp trials were presented in runs lasting 40 set, each comprising 32 step-ramps. Four step-ramp stimulus paradigms were used (Fig. 1), as well as a test of self-generated smooth eye movement in darkness:
(4
Predictable stimulus: all step-ramps
in a run
were identical. Unpredictable stimulus: step-ramps of 5, 20 and 40 deg/sec in both directions were intermixed in a pseudorandom pattern. Unpredictable gap stimulus: during an otherwise predictable run of 40 deg/sec step-ramps, the target was blanked at pseudorandom intervals for the entire duration of an expected step-ramp movement. (D) Velocity-shift stimulus: after 20 identical trials of 40 deg/sec step-ramps, the stimulus was abruptly switched to 5 deg/sec step-ramps in the same direction for the remainder of the run. This change was not expected by the subject.
(B)
cc>
(El
Volitional smooth eye movements in darkness: l-2 min after the last step-ramp stimulus was
viewed, as the final test of each session, subjects were asked to make smooth eye movements in darkness. They were encouraged to observed target imagine the previously motion. Each subject performed at least two runs of each step-ramp paradigm within a single test session lasting less than 30 min. We provided frequent verbal encouragement and brief rests to optimize subjects’ performance. Eye movements were monitored in real time while eye and target position and velocity were plotted on a thermal paper chart recorder (AstroMed, Inc., West Warwick, R.I.). Data acquisition and analysis
Eye and target position and velocity signals were digitized at a sampling rate of 250 Hz and stored for off-line analysis using an interactive program on an 80486-based personal computer. The acquisition and analysis software utilized the ViewDac program (ASYST Technologies, Rochester, N.Y.). Saccades were identified and removed by a digital algorithm using operatoradjustable velocity and acceleration criteria. Gaps left by saccade removal were fitted by linear interpolation of the eye velocity data. Results of saccade removal were viewed before and during pursuit analysis. Smooth eye movements were not quantified for a given trial if saccades occurred during the desired measurement interval. For each step-ramp trial, we measured the following response variables: anticipatory eye acceleration, pursuit eye acceleration, pursuit latency and peak pursuit velocity (Fig. 2). The results of computerized data analysis of each stepramp trial were assessed for accuracy by the operator, who could change analysis variables to obtain optimal best-fit lines for each response.
FIGURE 2. Ckulographic trace of a response to a single predictable 4O”/sec step-ramp stimulus in subject 1, showing eye velocity (irregular line) and target velocity (solid line) versus time. Figure demonstrates measurements made from each step-ramp response: (1) anticipatory eye acceleration (slope of regression line 1); (2) pursuit eye acceleration (slope of regression line 2); (3) pursuit latency; and (4) peak pursuit velocity.
The acceleration of anticipatory eye movements was computed for individual trials by calculating a regression line from eye velocity data over the period from 100 msec before step onset to 80 msec after onset. The figure of 80 msec was chosen since it is near the minimum reported latency of visually guided responses to small target motion in humans (Tychsen & Lisberger, 1986; Carl & Gellman, 1987). The 180 msec pre-pursuit segment we analyzed could be fit well with a single line in each trial, since anticipatory eye acceleration nearly always began more than 100msec before target motion (Fig. 2). The visually guided response of smooth pursuit was considered to begin when smooth eye acceleration exceeded anticipatory eye acceleration by three standard deviations. Even for trials with large anticipatory responses, there was always a clear inflection point where the pursuit response began. Smooth pursuit acceleration was measured from a regression line of the first 100 msec of eye velocity data following this point. Pursuit latency was identified at the point where the anticipatory and pursuit acceleration regression lines intersected. For unpredictable gap stimuli, smooth eye acceleration was measured during the gap when the target image was blanked. The peak velocity of smooth pursuit during each step-ramp trial was recorded. Data from each of over 400 trials in each subject were analyzed with the SYSTAT statistical program (SYSTAT, Inc., Evanston, Ill.), using paired t-tests and one-way analysis of variance (ANOVA). Responses to each direction of target motion were pooled. RESULTS
Anticipation of predictable stimuli
Anticipatory eye acceleration increased with target velocity in response to predictable step-ramp stimuli (P = 0.01, ANOVA; Fig. 3). For predictable 40 deg/sec ramps, all subjects generated peak anticipatory accelerations of over 35 deg/sec’ and three subjects reached values of over 60 deg/sec’ (Table 1). Mean anticipatory
GRACE
3030
_
W. KAO
and MARK
J. MORROW
were very low ( < I degjsec’ at each However, the mean of the absolute values of anticipatory accelerations to unpredictable targets was about 4deg/sec’ (Fig. 3), indicating that subjects anticipated even these pseudorandom stimuli. to target
25.
target
q
predictable
m
unpredictable
Smooth
2 01, 0
30
20
10
Target
Velocity
40
[“/XC]
FIGURE 3. Anticipatory eye acceleration versus target velocity for predictable and unpredictable step-ramp stimuli. Data points represent group means of eye acceleration values of five subjects. Values relative to target velocity are shown for predictable targets; absolute values are shown for unpredictable targets. Error bars indicate one standard deviation.
and smooth pursuit accelerations varied widely among subjects; those who generated higher anticipatory accelerations also generated higher pursuit accelerations, even to unpredictable targets (Fig. 4). This relationship was most apparent for the fastest, 40 deg/sec targets (Table 1). Anticipatory accelerations had values that averaged about 10% those of pursuit acceleration at each target velocity in each subject (Table 2). Prior experience in eye movement testing showed no clear effect, since the subjects who had previously undergone eye movement testing, subjects 1 and 5, generated respectively the best and the worst smooth eye movement. Anticipation
of unpredictable
stimuli
As expected, there was no relationship between anticipatory acceleration and target velocity for unpredictable stimuli (Fig. 3). In contrast to responses to predictable stimuli, anticipatory eye accelerations to unpredictable targets seldom exceeded 15 deg/sec’ (Fig. 5); since they were in the direction opposite target motion in about half of trials, the mean values of these responses relative
TABLE
1. Anticipatory
and pursuit
responses
Responses to predictable 40 deg/sec step-ramps
Subject Subject
Anticipatory acceleration (deg/sec*)
I
81 (24)
2 3 4 5
71 45 66 38
(16) (11) (10) (5)
Pursuit acceleration (deg/sec*) 356 352 235 190 230
(229) (199) (174) (79) (108)
direction
velocity).
pursuit
before and during unpredictable between 40 deg/sec step-ramps
Initial, pre-gap acceleration (deg/se?) 57 (39) 14 (22) 34 (17) 30 (14) 16 (5)
and unpredictuble
,stimuli
Mean pursuit accelerations and peak velocities were higher for predictable than unpredictable stimuli only at the highest target velocity, 40 deg/sec (P < 0.04, paired t-tests; Fig. 6). For 40 deg/sec ramps, responses to predictable stimuli had pursuit accelerations that averaged 59 deg/sec2 faster than those to unpredictable stimuli; peak velocities averaged 9.7 deg/sec faster. At the lowest target velocity, 5 deg/sec, unpredictable stimuli actually evoked higher pursuit accelerations and velocities than predictable stimuli (P < 0.02). Peak pursuit velocities for unpredictable 5 deg/sec targets usually exceeded target velocity, averaging 7.8 deg/sec. Pursuit velocities and accelerations were similar for predictable and unpredictable 20 deg/sec targets. For predictable targets, initial pursuit acceleration rose nearly in proportion to target velocity; at the mean accelerations we measured [Fig. 6(A)], the eyes would reach target velocity between 172 msec (for 5 degjsec targets) and 253 msec (for 40 deg/sec targets) after pursuit onset. Mean pursuit accelerations varied less with the velocities of unpredictable targets. At the mean pursuit accelerations we measured for unpredictable stimuli, the eyes would reach target velocity in only 106 msec for 5 deg/sec targets, but would require 404 msec for 40 deg/sec targets. Mean pursuit latency was 26 msec shorter for predictable than unpredictable stimuli in the group of five subjects (Table 3). This latency difference was significant in each subject (P < 0.007, paired t-tests) and in the group (P = 0.003). The shorter latency of pursuit initiation to predictable targets was not explained by inclusion of very short latency responses. Pursuit latency values for predictable and unpredictable stimuli approximated normal distributions (Fig. 7) and had similar standard deviations in each subject (Table 3). Pursuit latencies of under 80 msec were uncommon, comprising < 6% of responses to predictable targets in each subject.
to predictable 40 deg/sec step-ramp stimuli to smooth eye movements in darkness Responses
qf predictable
Second, intra-gap acceleration (deg/sec2) 114 103 76 87 42
(76) (53) (61) (37) (3 1)
and unpredictable
gaps
Peak intra-gap velocity (deg/sec )
gaps in each subject,
Volitional smooth eye motion in darkness Peak acceleration in darkness (deg/sec’)
27 (19) 19(11) 13 (10) ‘7(7) 7 (6)
Values shown are peak responses with means for step-ramp and gap responses in parenthesis. Eye accelerations and velocities in darkness represent means of highest observed rightward and ‘eftwdrd
compared
Peak velocity in darkness (deglsec )
2 8 3 II 7
smooth
2 4 5 5 2
eye motion
values.
ANTICIPATION
Compared with individual differences in anticipatory and pursuit acceleration (see Fig. 4), differences in pursuit latency were small.
(A)
*“b/act
10
0
Target
20 Velocity
30
3031
AND PURSUIT INITIATION
I
rub/d
2
subject subject
3 4
subject
5
40
[“/see]
Unpredictable
gap stimuli
Responses in the unpredictable gap experiment often showed two anticipatory acceleration components: an initial acceleration that began before target offset and a second, higher acceleration that followed target offset by about 120 msec (range 76187 msec), a latency similar to that of visually-guided pursuit movements (Fig. 8). This double acceleration gave responses to target gaps an appearance like those of responses to visible step-ramps. The tirst eye acceleration had values comparable to other anticipator eye movements that preceded the expected appearance of a 40 deg/sec ramp, averaging 19 deg/sec’ (Table 1). The second anticipatory eye acceleration, beginning after target disappearance, was higher than the pre-gap anticipatory acceleration by an average of about 270%, reaching over 80 deg/sec’ in three subjects and averaging 52 deg/sec2 in the group (Fig. 9). Peak anticipatory eye velocities during gaps reached over 1.5deg/sec, averaging 10.6 deg/sec (Table 1). All subjects produced peak anticipator velocities of over 6 deg/sec during gaps. Velocity -shift stimuli
0
10 Torget
20 Velocity
30
subiect
1
subject
2
subiect
3
subject
5
subject
4
.,.a
rubiect
3
_ 0
subject subject
2 5
40
[“/see]
(Cl
200
1
,_,,,,,..,,......
*_ .__________._*_-----. . . .Cl-., . . . . . . . . . . . . . . . .._._.................
q
Q *“bjsct
Expectations of target trajectory strongly influenced smooth pursuit that occurred immediately after the reduction in target speed in the velocity-shift experiment (Fig. 10). In response to this paradigm, subjects’ smooth pursuit eye movements reliably overshot the velocity of the first few 5 deg/sec ramps, as they expected to track a 40 deglsec ramp. For the first 5 deg/sec target after the shift, mean pursuit acceleration was 91 deg/sec’ and mean peak pursuit velocity was 15.4 deg/sec in our subject group. These values were almost double those for 5 deg/sec ramps in the unpredictable stimulus paradigm (mean acceleration 46 deg/sec*, mean peak velocity 7.8 deg/sec) and were more than double those for 5 deg/sec ramps in the predictable stimulus paradigm (mean acceleration 29 deg/se$, mean peak velocity 4.7 deg/sec). The initial response to 5 deg/sec targets in the velocity-shift paradigm thus had accelerations and velocities that were respectively about 50 deg/sec* and lOdeg/sec faster than responses to other 5 deg/sec targets. These differences, attributable to target expectation, were similar to the differences in pursuit acceleration and velocity between responses to predictable and unpredictable 40 deg/sec ramps (Fig. 6). Anticipatory accelerations and velocities during gaps between 40 deglsec ramps had comparable values (Table 1).
4
TABLE 2. Ratios of mean anticipatory eye acceleratian to mean pursuit eye acceleration (%) at each target speed in each subject for predictable step-ramp stimuli Subject
00 0
10 Target
20 Velocity
30
40
[“/xc]
FIGURE 4. Mean anticipatory acceferation for predictable stimuli (A) and mean pursuit acceleration for predictable stimuli (B) and unpredictable stimuli (C) in each subject, versus target velocity. Note differing y-axis scales. Each data point represents the mean of at least 58 values.
1 2 3 4 5 Mean
5 deg/sec ramps
20 degjsec ramps
40 deg/sec ramps
7.0 7.8 10.4 19.4 8.4
7.7 6.9 11.2 18.8 5.3
11.3 7.8 6.6 12.9 4.3
10.6 + 5.1
9.9 + 5.4
8.6 + 3.5
Mean data + 1SD noted at bottom.
3032
GRACE
W. KAO and MARK
J. MORROW
n predlcteble H unpredlctabie
-30
-15
0
15
30
45
Anticipatory eye accelertion
50
75
90
[“/e&J
FIGURE 5. Histograms of anticipatory eye acceleration to unpredictable step-ramp stimuli (577 data points) and predictable Wjsec step-ramp stimuli (279 data points) in five subjects. Negative values indicate eye accelerations in the direction opposite target motion.
Volitional smooth eye movements in darkness
In darkness, ail subjects generated smooth eye movements to the right and left at velocities greater than those of their spontaneous eye drift. No subject had spontaneous eye drift of over 1 deg/sec near primary position. Volitional smooth eye movements in darkness were of much lower peak velocities and accelerations than anticipatory responses to step-ramp targets (Table 1). No subject generated smooth eye movement at a velocity of over 5 deg/sec or an acceleration over 11 deg/sec* in darkness. There was no relationship between the ability to generate smooth eye movements in darkness and to produce anticipatory smooth eye movements to visual targets. For instance, subject 1, who generated the highest anticipatory accelerations and velocities, produced smooth eye movements in darkness with lower peak velocity and acceleration than any other subject. In contrast, subject 4, who did not make good anticipatory eye movements to step-ramps, showed the best smooth eye movement responses in darkness. DISCUSSION
Anticipatory smooth eye movements to predictable targets
Our subjects anticipated step-ramp stimuli by smoothly accelerating their eyes before targets moved. These anticipatory eye movements reached accelerations of over 35 deg/sec* in each subject. There was no evidence of a saturating effect of target velocity on anticipation. Anticipatory eye acceleration rose with predictable target velocities from 5 to 40 deg/sec, typically corresponding to about 10% of the ensuing pursuit acceleration. Kowler and McKee (1987) demonstrated a similar relationship for slower targets; over a range of stimulus speeds from about 0.5 to 5 deg/sec, their subjects generated anticipatory smooth eye motion with average velocities of lO-25% of target velocity. In contrast, subjects can maintain smooth eye movements at about 60% of target velocity if a stimulus disappears after the eyes have attained its velocity (Becker & Fuchs, 1985).
The ability to generate anticipatory and pursuit eye accelerations varied in parallel between subjects; those who achieved higher smooth pursuit accelerations also produced brisker anticipatory movements. The individual differences in pursuit acceleration were too large to be explained by differences in anticipatory contributions alone. For example, the difference in mean pursuit acceleration between subjects 1 and 4 was about 150 deg/sec2 for predictable 40 deg/sec ramps (see Table 1). In contrast, the difference in their mean anticipatory accelerations for these targets was only about 15 deg/sec2. Moreover, anticipation would not account for the large differences we observed in pursuit accelerations to unpredictable targets, since the mean relative values of anticipatory acceleration to these targets were near zero. The parallel between individual differences of smooth pursuit and anticipatory smooth eye movement suggests that both may be driven by a common neural mechanism. This hypothesis is reinforced by observations from lesion studies. Unilateral frontal eye field lesions in monkeys impair both smooth pursuit and anticipatory smooth eye movements, especially toward the damaged side (MacAvoy, Gottlieb & Bruce, 1991; Keating, 1993). Discrete unilateral brain lesions in humans have similar effects (Hotson, Braun & Boman, 1990). The functional importance of anticipatory smooth eye movement was not clear in our study. When stimuli move as expected, anticipatory smooth motion accelerates the eyes toward target velocity before visual motion inputs can activate the classic, visually-guided smooth pursuit system. One possible goal of anticipation is to minimize the demands on smooth pursuit by helping to match eye velocity to target velocity as soon as possible. This goal would best be served by a high anticipatory acceleration, which might be expected to accompany high pursuit accelerations and velocities. However, our subjects produced anticipatory eye accelerations that averaged only about 10% of pursuit acceleration. Relative values of anticipatory acceleration were higher for predictable targets than for unpredictable targets at all target speeds. Despite this, predictable targets evoked
ANTICIPATION
250
1
200
-
AND
(4
c e s z
150-
e 2 : 4
loo-
t w t
2
50
-
; a
1 0
0
ij
o
predictable
n
unpredictable
I
I
I
I
10
20
30
40
Target
40
Velocity
[‘/set]
-I
10
c? 5 I
0
10 Target
1
I
I
20
30
40
Velocity
[“/see]
FIGURE 6. Pursuit acceleration (A) and peak pursuit velocity (B) versus target velocity for predictable and unpredictable step-ramp stimuli. Data points represent group mean of five subjects. Error bars indicate one standard deviation. In (B), the standard deviation of pursuit velocity for predictable S”/sec targets is too small to be shown
pursuit accelerations and velocities that were similar to or lower than those evoked by unpredictable targets at 5 and 20 deg/sec. There are disadvantages in generating overly brisk anticipatory smooth eye movements. By initiating smooth eye motion while a stationary target is still present, anticipation creates retinal position and velocity errors that are potentially undesireable. In addition, anticipatory movements may increase the demands upon the pursuit system if the stimulus does not move as expected. TABLE 3. Mean pursuit latency for predictable and unpredictable ramps in each subiect
Subject
Predictable targets
1 2 3 4 5 Mean Group
INITIATION
D@erences stimuli
N
0
PURSUIT
122 * 25 132+36 128 k 28 138+42 143 + 34 133 * 8 meanf
1SD noted
f
1SD step-
Unpredictable targets 160 f 21 162 & 36 142+31 174*44 157+38 159* 11 at bottom.
3033
in responses to predictable and unpredictable
Our subjects produced anticipatory smooth eye motion to unpredictable targets, although these movements were of considerably lower accelerations than responses to predictable targets. The generation of anticipatory eye movement takes into account two components: (1) cognitive expectation of the trajectory of target motion and (2) motor habit based on the previous ocular responses (Kowler, Martin & Pavel, 1984; Kowler, 1989). Of these two mechanisms, cognitive expectation is more powerful, since directional cues can override the effects of prior target motion (Kowler, 1989). Both mechanisms are driven by repetitive stimuli like our predictable targets. For unpredictable targets, motor habit remains active as a driving force for anticipation, while uncertainty regarding target trajectory weakens the contribution of cognitive expectation. Pursuit accelerations and peak velocities were higher for predictable targets than unpredictable targets only at the highest target velocity, 40 deg/sec. These smooth pursuit measures were actually lower for predictable stimuli than for unpredictable stimuli at the lowest target velocity, 5 deg/sec. When targets with speeds covering this eight-fold range were alternated unpredictably, the smooth pursuit system responded precisely only to targets in the middle of the range, matching peak eye velocity to target velocity at 20 deg/sec. Kowler and McKee (1987) reported similar biasing of pursuit responses toward the center velocity when a range of target velocities under 5 deg/sec was presented. These findings indicate that the smooth pursuit system has limited ability to respond accurately when it cannot predict target speed and direction. When stimulus velocity was predictable in our study, the pursuit system adjusted initial eye acceleration to reach target velocity in about 200 msec. This implies a specific strategy for governing pursuit initiation, in which the optimal smooth eye acceleration is not necessarily the fastest one. Initial pursuit acceleration represents a compromise between the need to reach target velocity as soon as possible and the necessity of minimizing velocity overshoot (Carl & Gellman, 1987). When initial eye accelerations were too low, as when our subjects responded to unpredictable 40 deg/sec targets, eye velocity did not rise fast enough to approximate target velocity. On the other hand, when pursuit accelerations were too high, as when subjects responded to unpredictable 5 deg/sec stimuli, the eyes overshot target velocity. We found that initial pursuit responses to predictable targets had latencies that averaged 26 msec shorter than responses to unpredictable targets. This difference was not attributable to short-latency responses which might have been anticipatory. We conclude that neural mechanisms that predict target motion may prepare the smooth pursuit system for rapid action by specifying information about desired eye motion beforehand. The decrease in pursuit latency we observed with predictable
3034
GRACE
W. KAO
and MARK
.I. MORROW
40 1
n predictable q unp‘fedictable
0
20
--P40
60
4
-I,
60
100
li0
140
160
180
200
220
240
Pursuit latency (msec) FIGURE
7. Histograms
of pursuit
latency
for predictable and unpredictable step-ramp represents at least I10 data points.
stimuli may partly account for minimization of phase lags during steady-state pursuit of sinusoidal stimuli (Bahill & McDonald, 1983; van den Berg, 1988). We have shown that the acceleration and latency of smooth pursuit initiation are influenced by the predictability of target direction and speed. Expectations of the duration of stimulus appearance also affect pursuit initiation (Kowler & McKee, 1987). The existence of anticipatory smooth eye movements and of predictive modulation of pursuit initiation belie control systems models of smooth pursuit that take into account only concurrent motion of the retinal image and the eyes (Robinson et al., 1986; Lisberger et al., 1987). Modified control systems models have been used to explain predictive effects on the phase of pursuit maintenance, but they still do not explain anticipatory eye movements that occur prior to stimulus motion (van den Berg, 1988; Pavel, 1990). Effective modeling of smooth ocular track-
stimuli in subject
I. Each histogram
ing may require a combination of classical control systems modeling to explain low-level visuomotor processing and decision theory to account for the effects of anticipation and prediction (Kowler et al.. 1984). Neural network approaches to pattern recognition may meet these requirements (Pavel, 1990). Anticipation during target disappearance
Our subjects generated smooth eye accelerations during gaps in target appearance that corresponded to expected stimulus motion. Two sequential eye accelerations were often made in trials with gaps, the first beginning while a fixation target was still illuminated and the second, higher acceleration beginning after the target disappeared. Becker and Fuchs (1985) also observed the phenomenon of sequential anticipatory accelerations to targets which disappeared at the moment of expected motion. Not surprisingly, the first anticipatory
Tafgst oft
lbrgst on
I1 O*faee
FIGURE 8. Oculographic trace of responses to unpredictable gap stimulus in subject I. Eye velocity (irregular line) and target velocity (solid line) are plotted versus time. Within the third response interval, the target has been blanked during its expected period of step and ramp motion. The first anticipatory eye acceleration begins before target disappearance (line I): a second. higher anticipatory acceleration begins about 80 msec after target offset (line 2). A peak anticipatory smooth eye velocity ol 27 set is attained.
ANTICIPATION
d
2b
4b
Eye
6b
acceleration
50
100
AND PURSUIT
li0
[“/se91
W
OD E g ma z ‘O 206
lo-
!? t! o0
I 5
I 10
I 15
Peak eye velocity
I 20
I 25
30
[“/set]
FIGURE 9. Histograms of eye acceleration (A) and peak eye velocity (B) taking place during gap intervals of unpredictable gap stimulus in five subjects. Each histogram represents 30 data points.
acceleration in gap trials in our study had the same characteristics as other eye accelerations preceding the expectation of 40 deg/sec ramp motion. This acceleration averaged about 20 deg/sec’. The second anticipatory acceleration, occurring while no target was visible, was considerably higher, averaging about 50 deg/sec*. This acceleration increase might be explained by the enhancement of anticipatory smooth eye movement noted to
occur when visual fixation is discontinued (Boman & Hotson, 1988). Prior to target disappearance, anticipatory smooth eye motion caused retinal movement of the image of the fixation target that may have inhibited the response; after target offset, no such retinal slip was present. In addition to disinhibiting anticipation by removing retinal slip, the disappearance of the target could act as an independent sensory trigger. Target offset might be sensed as an event in itself, provoking more vigorous anticipation. The timing of the second anticipatory acceleration to gaps was similar to that of smooth pursuit initiation, with a mean latency of about 120 msec after target offset. This observation provides further support for the hypothesis that a common mechanism drives anticipation and smooth pursuit.
Pursuit eye acceleration and peak ,velocity were markedly altered by incorrect expectations of target trajectory in the velocity-shift paradigm. After presenting many 40 deg/sec stimuli, an unexpected reduction of target speed to 5 deg/sec evoked initial pursuit with accelerations much faster than for 5 deg/sec targets in other experiments. This excessive acceleration caused marked overshoot of eye velocity over target velocity. Responses to this paradigm confirm the dependence of pursuit initiation on non-visual, predictive mechanisms. Predictive contributions to smooth pursuit were similar in different paradigms. The difference between mean pursuit eye acceleration to predictable and unpredictable 40 deg/sec targets was about 50 deg/sec*. Comparable acceleration differences were observed between responses to the first 5 deg/sec target in the velocity-shift paradigm, when 40 deg/sec target motion was expected, and to 5 deg/sec targets in other paradigms. Pursuit velocity differences attributable to target expectation averaged about 10 deg/sec in each of these paradigms. Anticipatory smooth eye motion during gaps in which subjects expected a 40 deg/sec ramp had similar mean accelerations and velocities. This suggests that, in some cases, simple addition of an anticipatory smooth eye movement to visually-guided smooth pursuit explains the predictive contribution to pursuit initiation.
_--lS"/SSC
300 msoc
FIGURE velocities
3035
Predictive contributions to pursuit initiation
40-
5 g
INITIATION
10. Oculographic trace of responses to velocity-shift are plotted versus time. Target velocity is abruptly step-ramps. Eye velocity markedly overshoots
stimulus in subject 2. Eye (irregular line) and target (solid line) shifted between the first two (40Ojsec) and last three (5”/sec) target velocity for the first two S”/sec stimuli.
3036
Volitional
GRACE
smooth
eye movements
W. KAO
and MARK
in darkness
Normal subjects have limited ability to move their eyes smoothly in darkness unless they perceive a visual afterimage or non-visual sensory cue (Heywood & Churcher, 1971; Gauthier & Hofferer, 1976). Our subjects made volitional smooth eye movements in darkness with much lower peak accelerations and velocities than those of eye movements made in anticipation of target motion. The relative abilities of subjects to make smooth eye movements in darkness did not correlate with their abilities to generate anticipatory smooth eye movements. These observations imply that mechanisms that produce anticipatory eye movements, including cognitive expectation and motor habit, are inactive in continuous, complete darkness. Cognitive expectations of target motion could not be consciously controlled in that our subjects did not make robust smooth eye movements simply by imagining target motion viewed in the recent past. Anticipatory smooth eye movements seem to be regulated chiefly by subconscious mechanisms, since they are generated even when subjects try to suppress them or are distracted (Kowler & Steinman, 1979, 1981). Motor habit was ineffective at producing smooth eye motion in darkness, even though our subjects had finished their runs of over 400 step-ramp responses only l-2 min earlier. In order to drive anticipatory smooth eye movement, the motor habit mechanism must require frequent updating of experience. REFERENCES Bahill, A. T. & McDonald, J. D. (1983). Smooth pursuit eye movements in response to predictable target motion. Vision Research, 23, 1537-83. Becker, W. & Fuchs, A. F. (1985). Prediction in the oculomotor system: Smooth pursuit during transient disappearance of a visual target. Experimental Brain Research, 57, 562-575. van den Berg, A. V. (1988). Human smooth pursuit during transient perturbations of predictable and unpredictable target movement. Experimental Brain Research, 72, 95-108. Boman, D. K. & Hotson, J. R. (1988). Stimulus conditions that enhance anticipatory slow eye movements. Vision Research, 28, 115745. Carl, J. R. & Gellman, R. S. (1987). Human smooth pursuit: Stimulusdependent responses. Journal of Neurophysiology, 57, 1446-1463. Collewijn, H., van der Mark, F. & Jansen, T. C. (1975). Precise recording of human eye movements. Vision Research, 15, 447450. Heywood, S. & Churcher, J. (1971). Eye movements and the afterimage. I. Tracking the afterimage. Vision Research, 11, 1163-l 168.
J. MORROW
Hotson. J. R., Braun, D. & Boman. D. (1990). Antrcipatory smooth eye movements after human brain lesions. Int~est~guri~~c,Ophtholmolog? and Visual Science (Suppl. 4), 31. 532. Gauthier, G. M. & Hofferer. J. M. (1976). Eye tracking of self-moved targets in the absence of vision. E.~perimental Brain RaseLJrch, 26. 121-139. Keating, E.G. (1993). Lesions of the frontal eye field impair pursuit eqc movements, but preserve the predictions driving them. Behmioural Brain Research, 53, 91-104. Kowler, E. (1989). Cognitive expectations, not habits, control anticipatory smooth oculomotor pursuit. Visiorr Research. 29. 1049%1057. Kowler, E. & McKee, S. P. (1987). Sensitivity of smooth eye movement to small differences in target velocity. Vision Research, 27,993~-1015. Kowler, E, & Steinman, R. M. (1979). The effect of expectations on slow oculomotor control-I. Periodic target steps. Vision Rcscorch, 19, 619-632. Kowler, E. & Steinman, R. M. (1981). The effect of expectations on slow oculomotor control-III. Guessing unpredictable target displacements. Vision Research, 21, 191L203. Kowler, E., Martin, A. J. & Pavel. M. (1984). The effect ofexpectations on slow oculomotor control-IV. Anticipatory smooth eye movements depend on prior target motions. Vision Research, 24. 197 2 IO. Lisberger, S. G., Morris, E. J. & Tychsen. L. (1987). Visual motion processing and sensory-motor integration for smooth pursuit eye movements. Annual Review’ of’ Neuroscience, 10, 97-129. MacAvoy, M. C., Gottlieb, J. P. &Bruce, C. J. (1991). Smooth-pursuit eye movement representation in the primate frontal eye field. Cerebral Cartes, I, 95-102. Morrow. M. J. & Sharpe J. A. (1993a). Smooth pursuit initiation in young and elderly subjects. Vision Research, 33, 203.-210. Morrow, M. J. & Sharpe, J. A. (1993b). Retinotopic and directional deficits of smooth pursuit initiation after posterior cerebral hemispheric lesions. Neurology, 43, 595-603. Pavel, M. (1990). Predictive control of eye movement. In Kowler. E. (Ed.), Eye movements and their role in visual and co,qnitit:e processe.s (pp. 71- 114). Amsterdam: Elsevier. Rashbass, C. (1961). The relationship between saccadic and smooth tracking eye movements. Journal of Physiology, 159, 326.-338. Robinson, D. A., Gordon, J. L. & Gordon, S. E. (1986). A model of the smooth pursuit eye movement system. Biological Cybernetics, 55. 43-57. Tychsen, L. & Lisberger, S. G. (1986). Visual motion processing for the initiation of smooth-pursuit eye movements in humans. Journal of Neurophysiology, 56, 953-968. Young, L. R. (1971). Pursuit eye tracking movements. In Bach-y-Rita, P. & Collins, C. C. (Eds). The control of’ eye movements (pp. 429443). New York: Academic Press.
Acknowledgements-The authors thank Hieu Le. MSEE for his assistance in programming and data analysis. Research supported by Olive View/UCLA Education and Research Institute grant 545 (Dr Morrow).