Vision Res. Vol. 32, No. 4, pp. 675689, 1992 Printed in Great Britain. All rights reserved
Copyright
0042-6989/92 $5.00 f 0.00 Q I992 Pergamon Press plc
Predictive Smooth Pursuit Eye Movements Near Abrupt Changes in Motion Direction DUANE K. BOMAN,*t
JOHN R. HOTSON*
Received 3 January 1991; in revised form 14 August 1991
The stimulus-response characteristics of predictive smooth pursuit eye movements near the thue of predictable, abrupt changes in target motion direction were studied. Expectations about the speed and direction of target motion both before and after the direction change affected specific components of the predictive pursuit responses. We propose that, when the direction of target motion is expected to change, the cessation of motion in one direction and the initiation of motion in a new direction are separately anticipate and that predictive pursuit movement are s~rnat~ responses to these two events. Motion
Prediction
Smooth pursuit
Eye movement
INTRODUCTION Prediction is a ubiquitous component of human smooth pursuit eye movements. Even when tracking “unpredictable” moving targets, people produce expectations about the future target path that affect smooth eye movements (Kowler & Steinman, 1979b, 1981; Kowler, Martins & Pavel, 1984). Depending on the situation, however, predictive smooth pursuit can either help minimize retinal velocity errors or cause an increase in velocity errors. When a target is expected to continue moving at a constant velocity or to undergo a gradual velocity change, predictive smooth pursuit helps to maintain foveation on the target, thereby maximizing visual acuity of the moving target. Predictive smooth pursuit can also drive the eye through visual gaps when a target is briefly extinguished (von Noorden & Mackensen, 1962; Eckmiller & Mackeben, 1978; Whittaker & Eaholtz, 1982; Becker & Fuchs, 1985) or continue pursuit during fovea1 stabilization of a target (Morris & Lisberger, 1987; van den Berg, 1988). In contrast, predictive smooth pursuit movements drive the fovea off a moving target when an abrupt change in the direction of target motion is expected (Dodge, Travis & Fox, 1930; Boman & Hotson, 1987; Kowler, 1989). These direction-changing responses transiently increase retinal velocity and position errors during smooth pursuit. However, these predictive responses may quicken the subsequent resynchronization *California Institute for Medical Research, Santa Clara Valley Medical Center, San Jose, Calif., Stanford University Medical Center, Stanford, Calif. and SRI I~te~ational, Menlo Park, Calif., U.S.A. tTo whom all correspondence should be addressed at: Sensory Sciences and Technology Center, SRI International, 333 Ravenswood Avenue, Menlo Park, CA 94025, U.S.A.
Anticipatory
slow eye-movements
of eye and target velocity after the motion direction change. Smooth eye movements also drive the fovea off target when a stationary target is expected to move either smoothly or in a step (Kowler & Steinman, 1979a,b, 1981; Kowler et al., 1984; Boman & Hotson, 1988, 1989). These responses, referred to as anticipatory slow eye movements, usually have velocities of < 1 deg/sec unless active fixation is transiently extinguished prior to the expected target movement (Boman & Hotson, 1988). The utility of these anticipatory movements is unclear, as their low velocity does little to aid eye-target velocity synchronization or speed saccadic shifts. Anticipatory slow eye movements also occur during smooth pursuit when a moving target is expected to stop (Boman & Hotson, 1988; Kowler, Steinman, He & P&lo, 1989). These responses transiently disengage fovea1 fixation by decreasing smooth pursuit velocity prior to the expected termination of target motion. These decelerating anticipatory events halt slow eye movement close to the time that target motion stops. It is unclear how these different predictive smooth eye movements are related; they may result from the operation of a single smooth eye movement mechanism or reflect specialized predictive oculomotor mechanisms. We began examining this question by comparing the predictive responses that move the fovea off target prior to motion initiation, motion termination and abrupt changes in motion direction. To be consistent with previous literature, we will refer to the predictive smooth eye movements produced prior to motion initiation and termination as anticipatory slow eye movements, and the predictive smooth eye movements produced prior to abrupt direction changes as predictive pursuit. In the present experiments, we examine the stimulus-response characteristics of predictive pursuit by
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varying the speed and direction of the target both before and after the motion direction change and by varying the time between the termination of motion in one direction and the initiation of motion in a new direction. Comparisons were then made to the stimulus-response characteristics of anticipatory slow eye movements which have previously been studied in this and other laboratories (Kowler & Steinman. 1979a.b; Boman & Hotson. 1988). Our findings suggest that, when the direction of target motion is expected to abruptly change, the cessation of motion in one direction and the initiation of motion in a new direction are separatefy predicted. Furthermore, predictive pursuit stimulus-response characteristics are similar to those of anticipatory slow eye movements. Closely matching models of the predictive pursuit movements were produced by summing anticipatory slow eye movements produced prior to motion termination and initiation. These findings suggest that anticipatory slow eye movements are active during smooth pursuit and summate to produce predictive pursuit movements. METHODS Right eye position was monitored with an SRI dualPurkinje-image eyetracker (Crane & Steele, 1985). As previously described (Boman & Hotson, 1988), the eye-position signals were low-pass filtered (DC-100 Hz) and eye velocity was obtained by analog differentiation (high cutoff 10 Hz). The peak to peak noise level for the velocity channel was 2 deg/sec. The signals were recorded on magnetic tape and were later digitized and sampled at a rate of 1000 Hz by a 1Zbit A/D converter. In each experiment, slow eye velocities were analyzed from 88 msec before to 1 set after each change in stimulus velocity. Slow eye velocities were isolated from the eye velocity signals by identifying and discarding saccadic velocities. The eye position and velocity traces over the time period of interest were displayed on a computer terminal and the beginning and end of saccade velocities were automatically identified by acceleration criteria. The 1800 msec time period was divided into 25 msec bins. If a time bin did not include a saccadic velocity, the average eye velocity during that bin was computed and stored. The stimulus device was a cathode ray oscilloscope with a Pi phosphor located 57 cm from the subject. The green spot, 2mm in dia, was moved under computer control using a D/A converter. The target could also be extinguished by moving the spot behind an occluding screen. Three male subjects between the ages of 25 and 40 yr participated in the tests. Two subjects were experienced with eye movement studies and were aware of the research ptan. One subject was naive on both accounts. Each had an uncorrected visual acuity of 20/30 or better in each eye and no history of ocular or oculomotor problems. Informed consent was obtained from each subject before participation in any experiment.
In order to make stimulus motion highI> pt‘edictahl~:. blocks of 30 trials were run in which ;(I1 aspects 01. stimulus presentations were constant. in the lirst three experiments, stimulus motion consisted of !HCIct)nstantvelocity ramps. We refer to these stimuli as double-ramp stimuli. In the last experiment, the stimulus underwent repetitive triangle-wave motion. In each experiment, the subject initiated a trial by pressing a button. The computer produced an audible cue I set before the target began moving. The subjects were instructed to keep their eye on the target and follow it as well as possible. In the first experiment, horizontal double-ramp stimuli with 180 deg direction changes were presented. Individual ramps with speeds of 2, 6 and IO degisec were used. Ramp durations were 3000, 2000 and 1500 msec, respectively. All nine combinations of first and second ramp speeds were tested. The target was also extinguished for either 0, 400, or 800 msec prior to the initial ramp motion. Each subject participated in four blocks ol trials with each stimulus condition. two with initial target motion to the left and two with initial target motion to the right. In the second experiment, double-ramp stimuli with 90deg direction changes were used. Each of the eight of horizontal-vertical or verticalcombinations horizontal ramp motion were presented. Horizontal ramp velocity was always 6deg/sec, while vertical ramp velocity was either 6 or 10 deg/sec, thus producing 16 stimulus conditions. Ramp duration was 2000 and 1500 msec for the 6 and IO deg/sec ramps, respectively. The target was extinguished for 6OOmsec prior to the initiation of the first ramp. Each subject participated in one block of trials with each stimulus. Horizontal double-ramp stimuli with 180 deg reversals were again used in the third experiment. However, in these tests, the target was extinguished for either 200, 800, or 2000msec between the time that the first ramp ended and the second ramp began. Ramp velocity was always 10 deg/sec with a duration of 1500 msec. Trials were also run in which the target remained visible and stationary for 800 msec between the time that the first ramp ended and the second ramp began. Each subject participated in four blocks of trials with each stimulus condition, two with initial target motion to the left and two with initial target motion to the right. In the last experiment, the stimulus consisted of 3.5 cycles of horizontal triangle-wave motion. Three target reversals in each direction occurred during a trial and ten trials were run in a block. Each subject participated in a block of trials with initial target motion to the left and a block with initial target motion to the right. Average slow eye velocity curves were produced by combining the data from blocks of 30 trials, from the 120 trials that a subject performed with each stimulus and from the 360 trials that the three subjects performed with each stimulus. In order to compare predictive pursuit
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responses to anticipatory slow eye movements in experiments 1, 2 and 4, model velocity curves were produced by summing averaged anticipatory slow eye accelerations with averaged anticipatory slow eye decelerations, point by point. Comparisons between pairs of averaged velocity curves were made by computing the mean error between the curves and by a nonparametric sign test. Mean errors were computed to compare entire velocity curves, while the nonparamet~c sign tests provided comparisons between events that s~ifi~ally occurred during anticipatory phases of the responses. To determine the mean error, the difference between the curves was calculated point by point and then the average of the absolute values of these differences was calculated. The mean errors that are reported are from comparisons between combined subject averaged velocity curves. In the nonparametric statistical tests, specific events were compared; either the velocities at a specific time or the points of time that a specific velocity was achieved. To minimize effects of intersubject variability and variability due to the direction of movement in this test, comparisons were only made between data from the same observer and movement in the same direction. For each stimulus condition, two blocks of 30 trials in each of two stimulus directions were analyzed from each the three subjects. By averaging the 30 responses in each block of trials, 12 averaged responses were produced that could then be compared. When comparisons were made between modeled and measured responses, 12 model curves were produced using data from blocks of 30 trials. The nonparametric sign test was used to test the probability that the velocity curves were different. The velocities at specified points of time were compared and the curve with the higher velocity was given a plus.
Similarly, the time that the curves reached specified velocities were compared and the first curve to reach that velocity was given a plus. For each comparison, the number of pluses for one of the sets of 12 velocity curves were summed. Ties were excluded from the analyses. P-values were then computed using an exact binomial distribution. In each experiment, slow eye velocities were compared at the time of each stimulus velocity change and 200 msec before each velocity change (see Figs 5,6,7 and 9). In expe~ments 1,3 and 4, the times at which slow eye velocities reversed direction were compared, and the times at which the velocities became less than l/2 the steady-state velocity when pursuing the first ramp were compared (see Figs 5, 7 and 9). In experiment 2, the direction of target motion changed by 90 deg rather than reversing, so, for slow eye decelerations, the times at which slow eye velocity became less than 0.5 deg/sec were compared and the times at which slow eye velocities became less than l/2 the steady state velocity when pursuing the first ramp were compared [see Fig. 5(B)], while for slow eye accelerations, the time at which slow eye velocity became greater than 0.5 deg/sec were compared [see Fig. 5(A)]. Also, for the slow eye accelerations in experiment 2, the velocities 100 msec after the stimulus change were compared in order to have four comparisons between these curves. RESULTS Experiment 1 The double-ramp stimuli used in the first two experiments included three predictable changes in target velocity, namely, the initiation of target motion, the direction change, and the termination of motion (Fig. 1).
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FIGURE I. Individual eye movement to a predictable double-ramp stimulus with a 180deg direction change. Upward deflections of the curves indicate rightward movements or velocities. In this trial, the target spot was extinguished at time = 600 msec. The target (1) reappeared 400 msec later and moved rightward at 10 deg/sec for 1500 msec, (2) reversed direction and moved leftward at 6 degjsec for 2000 msec, and then (3) stopped. Slow eye velocities changed prior to each of these three changes in target motion.
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By the third or fourth trial in a block, the subjects were altering slow eye velocity prior to each of these events, Anticipatory slow eye movements were present prior to the onset and termination of target motion. Similarly, predictive pursuit movements occurred prior to and during the change in the direction of target motion. In the first experiment, the effect of indi~du~1 ramp velocities on predictive pursuit was studied using horizontal doubie-ramp stimuli. Figure 2 shows combined subject averaged responses for al1 nine stimulus conditions. The velocities of both ramps affected predictive pursuit. The average smooth eye velocity curves could be segregated in accord with the velocity of either the first or second ramp of the stimulus. The speed of the first ramp affected the time at which the eye began to decelerate significantly. This initial deceleration began earlier with faster first ramp speeds. The speed of the second ramp affected the rate at which smooth eye velocity changed. Higher accelerations occurred with higher speed second ramps. Therefore, each ramp of the double-ramp stimuli altered specific components of the predictive pursuit responses. These tendencies were apparent in the averaged responses from individual subjects {Fig. 3) as well as in the combined subject averages (Fig. 2). It appeared that, near the time of ramp reversal, two events were anticipated, namely, the termination of the first ramp and the initiation of the second ramp. If so, then the predictive pursuit movements produced near the time of ramp reversal could be a combination of separate, but admixed responses to these two events. The predictive pursuit response characteristics described above are also characteristic of anticipator slow eye movements (Boman & Hotson, 1988). Anticipator slow eye decelerations prior to expected motion termination begin earlier with higher speed targets (see Fig. 2) and anticipatory slow eye accelerations prior to expected motion initiation are greater with higher speed targets. Therefore, we postulated that anticipatory slow eye accelerations and decelerations are active during smooth pursuit and combine to produce predictive pursuit movements to expected motion direction changes. To test this postulate, modeled velocity curves were produced by summing anticipatory slow eye accelerations and decelerations (Boman & Hotson, 1988) For example, the predictive pursuit response to a doubteramp stimulus with a 10degJsec ramp followed by a 6deg/sec ramp was modeled by summing the average anticipatory slow eye decelerations produced prior to the termination of 10 deg/sec ramps with the anticipatory slow eye accelerations produced prior to the initiation of a 6 deg/sec ramps (Fig. 4). In this manner, modeled response curves were produced for each of our nine double-ramp stimuli. The modeled response curves also incorporated the observation that anticipatory slow eye movements begin earlier and reach higher velocities when the fixation target is transiently extinguished prior to ramp motion onset (Boman & Hotson, 1988). Predictive pursuit also disengaged visual fixation by driving the fovea off
target prior to motion reversals (Fig. I t and ihis d~stmgagement began earlier with higher speed first ramps. Therefore, it was likely that ~ntici~t~~r~ slow eye accelerations from trials with transient target extinction would be needed to develop model velocity curves of predictive pursuit. Modeled velocity curves were produced using anticipatory slow eye accelerations from trials with the target extinguished for 0, 400 and 800msec prior to the onset of motion, producing 27 modeled curves. The mean errors between these derived velocity curves and the average. predictive pursuit vetocities measured near the time of ramp reversal were then compared. In most cases, the modeled curves summat~ng anticrpatory slow eye velocities paralIeled the predictive pursuit responses. However, the mean errors were affected by the anticipatory slow eye accelerations used in the model curves. When the first ramp moved at 2 degjsec, the mean error between the modeled and measured eye velocity curves was minimized when anticipatory slow eye accelerations from trials with no target extjnction were used in the models. When the first ramp moved at either 6 or 10 degjsec, the mean errors were usually lowest when anticipatory slow eye accelerations from trials with 400 msec of target extinction were used. The nine modeled response curves that included anticipatory slow eye accelerations from trials with these periods of target extinction were selected for subsequent nonparametric statistical analyses. Figure 5 shows the modeled and measured responses that produced the lowest [0.09 deg/sec, Fig. S(A)] and highest to.55 degjsec, Fig. 5(B)] mean errors from the nine selected curves. With the nonparamet~c statistical test (see Methods), four compa~sons between the modeled and the measured velocity curves were made for each of the nine stimulus conditions, giving 36 comparisons. At the 95% confidence level, two-thirds of these comparisons were not significantly different. At the 99% confidence level, only 5 of the 36 comparisons showed significant differences. None of the curves from the nine stimulus conditions had significant differences in more than two of the four comparisons. Therefore, the modeled response curves were not significantly different from the measured predictive pursuit curves in most of’ the comparisons.
Predictive pursuit of double-ramp stimuli with 90 deg direction changes was studied to determine whether the stimulus-response characteristics found in the first experiments are produced with motion direction changes other than 180 deg. This stimulus also allowed a direct rather than modeled comparison between anticipatory slow eye movements and predictive pursuit. The horizontal anticipatory slow eye velocities produced prior to the onset of horizontal target motion were directly compared to the horizontal predictive pursuit velocities produced near the shift from vertical to horizontal target motion [Fig. 6(A)]. Also, the horizontal anticipatory slow eye velocities produced when a ramp target was
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FIGURE 2. Combined subject average slow eye velocities from responses to doubl~ramp stimuli with ISOdeg direction changes and to ramp motion termination. Averaged velocities when first ramp velocity was; (A) 2 deg/sec, (B) 6 deg/sec, and (C) IO deg/sec. The motion of the second ramp was in the opposite direction at 2 deg/sec (V), 6 degjsec. (O),lO deg/sec (A) or ramp motion ended (0). The change in stimulus motion always occurred at time = 0. A velocity standard deviation is also shown in each graph. The velocity of target motion both before and after the stimulus change affected slow eye velocity.
DUANE K. BOMAN and JOHN R. HOTSON (4
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FIGURE 3. Average slow eye velocities from responses of subjects DB (El), JH (0) and KN (A} to double-ramp stimuli with 18Odeg direction changes. Individual averages when the velocities of both ramps were: (A) 2deg/sec, (B) 6deg/sec, and (C) lOdeg/sec. The three subjects had similar average responses under all stimulus conditions.
expected to stop horizontal motion and become stationary were directly compared to the horizontal predictive pursuit velocities produced when a ramp target was
expected to shift from horizontal to vertical motion [Fig. 6(B)]. Vertical anticipatory slow eye velocities and predictive pursuit velocities were similarly compared.
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FIGURE 4. Construction of modeled responses. (A) Combined subject average slow eye velocities produced near the termination of a lOdeg/sec ramp (V) and near the initiation of a 6deg/sec ramp when the stimulus was extinguished for 400 msec prior to ramp initiation (0). (B) Comparison of the modeled response (A) produced by summing the two curves shown in (A) with the combined subject average slow eye velocities produced near the 180 deg direction change of a predictable double-ramp stimulus (0). (C) Individual averages from subjects DB (O), JH (0) and KN (A) to this stimulus. The latencies and timecourses of the modeled velocity curves closely paralleled the measured responses to predictable changes in the direction of target motion.
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FIGURE 5. Highest and lowest mean errors between modeled (A) and measured (0) combined subject average responses to double-ramp stimuli. (A) Responses with the lowest mean error (0.08 deg/sec). (B) Responses with the highest mean error (0.98 deglsec). In this and the following figures, the open arrows indicate the selected points of time chosen for velocity comparisons using the nonparametric statistical test. The solid arrows indicate selected velocities that were also compared using the nonparametric test. The selection criteria for these times and velocities are presented in the Methods.
As expected, predictive pursuit moved the eye in the expected future target direction before the stimulus direction change. The times at which the fovea began to move off the target was similar to that produced with 180 deg direction changes. Also, with higher speed vertical ramps, the vertical predictive pursuit movements had
higher accelerations and began decelerating sooner. Therefore, the stimulu~respons~ characteristics of predictive pursuit movements to stirnub with 180 and 90 deg direction changes were similar. The time-courses of the anticipatory slow eye velocities and predictive pursuit velocities were also very
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FIGURE 6. Combined subject average slow eye velocities from responses to double-ramp stimuli with 90 deg direction changes and to ramp motion initiation and termination. (A) Average velocities when a target began moving horizontally after being stationary and then extinguished for 600 msec (17) or after terminating vertical motion (A). (B) Average velocities when a horizontally moving target became stationary (0) or changed to vertical motion (A). The inserts give examples of target motion paths. The thick lines within the inserts indicate the portion of the path over which the slow eye velocity curves were obtained. There are very few differences between the responses in each graph.
similar (Fig. 6). The main difference between these velocity curves was a velocity overshoot that occurred with ramp motion onset but not with an orthogonal change in motion direction [Fig. 6(A)]. The mean errors from the comparisons of combined subject average anticipatory slow eye and predictive
pursuit velocity curves were between 0.08 and 0.46 deg/sec. Using the nonparametric sign test, the eight comparisons shown in Fig. 6 were made on each set of horizontal and vertical velocity curves measured at the two stimulus speeds, giving 32 comparisons. Only three of the 32 comparisons were significantly different at the
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95% confidence level, while none were significantly different at the 99% confidence level. This direct comparison between anticipatory slow eye movements and predictive pursuit revealed minimal differences between their velocity curves. Experimm t 3
The stimulu~response characteristics of predictive pursuit were further characterized by varying the time between the termination of motion in one direction and the initiative of motion in a new direction. Tf these two events are separately anticipated, then including a delay or gap between the end of the first ramp and the beginning of the second ramp may separate the predictive pursuit response into two components. When the stimulus included a 200 msec gap between ramps, the smooth pursuit reversals developed a short velocity plateau that bridged separate decelerating and accelerating slow eye movements [cf. Fig. 7(A) to Fig. 5(A)]. Increasing the stimulus gap between doubleramps to 800 msec caused an increase in the duration of the velocity plateau or bridge [Fig. 7(B)]. When the target stopped but remained visible for 800 msec between ramps [Fig. 7(C)], the velocity of the bridging plateau was reduced. The fixation target attentuated the plateau velocity similar to the effect of a fixation target on anticipatory slow eye velocity prior to the initiation of ramp motion (Boman & Hotson, 1988). When the stimulus gap was further increased to 2000 msec, the average slow eye velocity during the gap became quite variable and showed a very slow acceleration prior to the second ramp. These responses were similar to the variable anticipatory slow eye velocities measured with 2 set of target extinction prior to ramp initiation (Boman & Hotson, 1988). Model responses were made for the conditions with 200 and 800 msec gaps {Fig. 7). To make the model response curves, the anticipatory slow eye accelerations were shifted by either 200 or 800 msec before being summed with the anticipatory slow eye decelerations. The endpoints where the curves no longer overlapped were then taken from the individual curves. The mean error between the measured and modeled combined subject average velocity curves were between 0.24 and 0.42 deg/sec. Using the nonparametric sign test, the 17 comparisons shown in Fig. 7 were made between the modeled and measured curves. The comparisons were signi~~antly different at the 95% confidence level, one of which was significant at the 99% confidence level. The timecourse of the summed anticipatory slow eye movements was similar to the separated components of predictive pursuit.
Predictive responses are also prominent when pursuing repetitive stimuli such as triangle waves, even with high frequency oscillations that cannot be accurately tracked. Repetitive stimuti of this type are often used in clinical studies. Therefore, it was potentially useful to know whether the predictive responses to these continu-
and JOHN R HOTSOh
ous stimuli were similar to those produced w1t11~~~~.~hitramp stimuli. Eye movern~~t~ were monitored while the anbjezia pursued horizontal. triangle-wave stimuli Gllaung a: frequencies of 0.33 and I .5 Hz, Stimulus a~nplit~l~l~was adjusted SO that the speed of the illdi~~id~~~~ ri+mps was always lOdcg/sec. thus producing ramp dttrntions ol 1500 and 333 msec, respectively. At the lower frcyucnc~. the smooth pursuit responses were similar 1~1those produced with double-ramp stimuli [cf. Fig. X(A) I(, f-ig. I]. At the higher frequency. smooth pursuit became much less regular and the peak velocities wzrc‘ quite variable. Predictive responses, however. I-emaincd prominent in these trials [Fig. 8(B)]. The combined subject average predictive pursuit vclocities produced with triangle-wave stimuli were compared with modeled velocity curves iF?g. 9). The modeled response was produced by summing anticipatory slow eye accelerations elicited with 4OOmsec oi target extinction prior to 10 degjsec ramp initi~~tion wirh the anticipatory slow eye decelerations prior to 10 deg/sec ramp termination, similar to the first oxperiment. The modeled response closely resembled the measured predictive pursuit response at the lower stimulus frequency [Fig. 9(A)]. At the higher frequency, the measured responses showed higher accelerations and decelerations than the modeled response [Fig. 9(B)]. Eight comparisons were made using the ~lonp~~arnetri~ sign test. None were signifi~~nti~ different at the 95% confidence level. DISCUSSION The present results demonstrate how predictable changes in the direction and speed of target motion affect predictive pursuit eye movements. With the double-ramp stimuli used in this study, the velocities of both ramps affected specific aspects of the predictive responses. The higher the velocity of the first ramp, the earlier the eye began to decelerate significantly. The expected direction of the second ramp determined the direction of the predictive movement. The higher the velocity of the second ramp, the greater the accele~dtion of the predictive movement in the new direction. Therefore, expectations about target motion both before and after the direction change had specific and different effects on the predictive pursuit responses. From these obse~ations we proposed that, when a moving visual target is expected to undergo a change in the direction of motion, two events are anticipated; the termination of motion in the first direction and the initiation of motion in a new direction. Fnrthe~ore, we proposed that the predictive pursuit movements produced near the time of the expected motion change represent the summated output of two, directionsensitive predictive components, the first being associated with the expected te~i~~tion of motion in one direction and the second being associated with the expected initiation of motion in a new direction. Alternative predictive strategies such as dete~ining the re-
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FIGURE 7. Combined subject average slow eye velocities from responses to double-ramp stimuli with delays between the termination of the first ramp and the initiation of the second ramp. The squares indicate measured responses and the triangles indicate modeled responses. In each graph, the first ramp ended at time = 800 msec. Average responses to stimuli with: (A) 200 msec delays with the target extinguished, (B) 800 msec delays with the target extinguished and (C) 800 msec delays with the target visible and stationary. The construction of each modeled response is described in the text.
sponses velocity,
solely on the basis of expected future target future target direction or the absolute value of
the change in target velocity were not consistent observed two component strategy.
with the
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Copyright
0042-6989/92 $5.00 f 0.00 Q I992 Pergamon Press plc
Predictive Smooth Pursuit Eye Movements Near Abrupt Changes in Motion Direction DUANE K. BOMAN,*t
JOHN R. HOTSON*
Received 3 January 1991; in revised form 14 August 1991
The stimulus-response characteristics of predictive smooth pursuit eye movements near the thue of predictable, abrupt changes in target motion direction were studied. Expectations about the speed and direction of target motion both before and after the direction change affected specific components of the predictive pursuit responses. We propose that, when the direction of target motion is expected to change, the cessation of motion in one direction and the initiation of motion in a new direction are separately anticipate and that predictive pursuit movement are s~rnat~ responses to these two events. Motion
Prediction
Smooth pursuit
Eye movement
INTRODUCTION Prediction is a ubiquitous component of human smooth pursuit eye movements. Even when tracking “unpredictable” moving targets, people produce expectations about the future target path that affect smooth eye movements (Kowler & Steinman, 1979b, 1981; Kowler, Martins & Pavel, 1984). Depending on the situation, however, predictive smooth pursuit can either help minimize retinal velocity errors or cause an increase in velocity errors. When a target is expected to continue moving at a constant velocity or to undergo a gradual velocity change, predictive smooth pursuit helps to maintain foveation on the target, thereby maximizing visual acuity of the moving target. Predictive smooth pursuit can also drive the eye through visual gaps when a target is briefly extinguished (von Noorden & Mackensen, 1962; Eckmiller & Mackeben, 1978; Whittaker & Eaholtz, 1982; Becker & Fuchs, 1985) or continue pursuit during fovea1 stabilization of a target (Morris & Lisberger, 1987; van den Berg, 1988). In contrast, predictive smooth pursuit movements drive the fovea off a moving target when an abrupt change in the direction of target motion is expected (Dodge, Travis & Fox, 1930; Boman & Hotson, 1987; Kowler, 1989). These direction-changing responses transiently increase retinal velocity and position errors during smooth pursuit. However, these predictive responses may quicken the subsequent resynchronization *California Institute for Medical Research, Santa Clara Valley Medical Center, San Jose, Calif., Stanford University Medical Center, Stanford, Calif. and SRI I~te~ational, Menlo Park, Calif., U.S.A. tTo whom all correspondence should be addressed at: Sensory Sciences and Technology Center, SRI International, 333 Ravenswood Avenue, Menlo Park, CA 94025, U.S.A.
Anticipatory
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of eye and target velocity after the motion direction change. Smooth eye movements also drive the fovea off target when a stationary target is expected to move either smoothly or in a step (Kowler & Steinman, 1979a,b, 1981; Kowler et al., 1984; Boman & Hotson, 1988, 1989). These responses, referred to as anticipatory slow eye movements, usually have velocities of < 1 deg/sec unless active fixation is transiently extinguished prior to the expected target movement (Boman & Hotson, 1988). The utility of these anticipatory movements is unclear, as their low velocity does little to aid eye-target velocity synchronization or speed saccadic shifts. Anticipatory slow eye movements also occur during smooth pursuit when a moving target is expected to stop (Boman & Hotson, 1988; Kowler, Steinman, He & P&lo, 1989). These responses transiently disengage fovea1 fixation by decreasing smooth pursuit velocity prior to the expected termination of target motion. These decelerating anticipatory events halt slow eye movement close to the time that target motion stops. It is unclear how these different predictive smooth eye movements are related; they may result from the operation of a single smooth eye movement mechanism or reflect specialized predictive oculomotor mechanisms. We began examining this question by comparing the predictive responses that move the fovea off target prior to motion initiation, motion termination and abrupt changes in motion direction. To be consistent with previous literature, we will refer to the predictive smooth eye movements produced prior to motion initiation and termination as anticipatory slow eye movements, and the predictive smooth eye movements produced prior to abrupt direction changes as predictive pursuit. In the present experiments, we examine the stimulus-response characteristics of predictive pursuit by
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varying the speed and direction of the target both before and after the motion direction change and by varying the time between the termination of motion in one direction and the initiation of motion in a new direction. Comparisons were then made to the stimulus-response characteristics of anticipatory slow eye movements which have previously been studied in this and other laboratories (Kowler & Steinman. 1979a.b; Boman & Hotson. 1988). Our findings suggest that, when the direction of target motion is expected to abruptly change, the cessation of motion in one direction and the initiation of motion in a new direction are separatefy predicted. Furthermore, predictive pursuit stimulus-response characteristics are similar to those of anticipatory slow eye movements. Closely matching models of the predictive pursuit movements were produced by summing anticipatory slow eye movements produced prior to motion termination and initiation. These findings suggest that anticipatory slow eye movements are active during smooth pursuit and summate to produce predictive pursuit movements. METHODS Right eye position was monitored with an SRI dualPurkinje-image eyetracker (Crane & Steele, 1985). As previously described (Boman & Hotson, 1988), the eye-position signals were low-pass filtered (DC-100 Hz) and eye velocity was obtained by analog differentiation (high cutoff 10 Hz). The peak to peak noise level for the velocity channel was 2 deg/sec. The signals were recorded on magnetic tape and were later digitized and sampled at a rate of 1000 Hz by a 1Zbit A/D converter. In each experiment, slow eye velocities were analyzed from 88 msec before to 1 set after each change in stimulus velocity. Slow eye velocities were isolated from the eye velocity signals by identifying and discarding saccadic velocities. The eye position and velocity traces over the time period of interest were displayed on a computer terminal and the beginning and end of saccade velocities were automatically identified by acceleration criteria. The 1800 msec time period was divided into 25 msec bins. If a time bin did not include a saccadic velocity, the average eye velocity during that bin was computed and stored. The stimulus device was a cathode ray oscilloscope with a Pi phosphor located 57 cm from the subject. The green spot, 2mm in dia, was moved under computer control using a D/A converter. The target could also be extinguished by moving the spot behind an occluding screen. Three male subjects between the ages of 25 and 40 yr participated in the tests. Two subjects were experienced with eye movement studies and were aware of the research ptan. One subject was naive on both accounts. Each had an uncorrected visual acuity of 20/30 or better in each eye and no history of ocular or oculomotor problems. Informed consent was obtained from each subject before participation in any experiment.
In order to make stimulus motion highI> pt‘edictahl~:. blocks of 30 trials were run in which ;(I1 aspects 01. stimulus presentations were constant. in the lirst three experiments, stimulus motion consisted of !HCIct)nstantvelocity ramps. We refer to these stimuli as double-ramp stimuli. In the last experiment, the stimulus underwent repetitive triangle-wave motion. In each experiment, the subject initiated a trial by pressing a button. The computer produced an audible cue I set before the target began moving. The subjects were instructed to keep their eye on the target and follow it as well as possible. In the first experiment, horizontal double-ramp stimuli with 180 deg direction changes were presented. Individual ramps with speeds of 2, 6 and IO degisec were used. Ramp durations were 3000, 2000 and 1500 msec, respectively. All nine combinations of first and second ramp speeds were tested. The target was also extinguished for either 0, 400, or 800 msec prior to the initial ramp motion. Each subject participated in four blocks ol trials with each stimulus condition. two with initial target motion to the left and two with initial target motion to the right. In the second experiment, double-ramp stimuli with 90deg direction changes were used. Each of the eight of horizontal-vertical or verticalcombinations horizontal ramp motion were presented. Horizontal ramp velocity was always 6deg/sec, while vertical ramp velocity was either 6 or 10 deg/sec, thus producing 16 stimulus conditions. Ramp duration was 2000 and 1500 msec for the 6 and IO deg/sec ramps, respectively. The target was extinguished for 6OOmsec prior to the initiation of the first ramp. Each subject participated in one block of trials with each stimulus. Horizontal double-ramp stimuli with 180 deg reversals were again used in the third experiment. However, in these tests, the target was extinguished for either 200, 800, or 2000msec between the time that the first ramp ended and the second ramp began. Ramp velocity was always 10 deg/sec with a duration of 1500 msec. Trials were also run in which the target remained visible and stationary for 800 msec between the time that the first ramp ended and the second ramp began. Each subject participated in four blocks of trials with each stimulus condition, two with initial target motion to the left and two with initial target motion to the right. In the last experiment, the stimulus consisted of 3.5 cycles of horizontal triangle-wave motion. Three target reversals in each direction occurred during a trial and ten trials were run in a block. Each subject participated in a block of trials with initial target motion to the left and a block with initial target motion to the right. Average slow eye velocity curves were produced by combining the data from blocks of 30 trials, from the 120 trials that a subject performed with each stimulus and from the 360 trials that the three subjects performed with each stimulus. In order to compare predictive pursuit
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responses to anticipatory slow eye movements in experiments 1, 2 and 4, model velocity curves were produced by summing averaged anticipatory slow eye accelerations with averaged anticipatory slow eye decelerations, point by point. Comparisons between pairs of averaged velocity curves were made by computing the mean error between the curves and by a nonparametric sign test. Mean errors were computed to compare entire velocity curves, while the nonparamet~c sign tests provided comparisons between events that s~ifi~ally occurred during anticipatory phases of the responses. To determine the mean error, the difference between the curves was calculated point by point and then the average of the absolute values of these differences was calculated. The mean errors that are reported are from comparisons between combined subject averaged velocity curves. In the nonparametric statistical tests, specific events were compared; either the velocities at a specific time or the points of time that a specific velocity was achieved. To minimize effects of intersubject variability and variability due to the direction of movement in this test, comparisons were only made between data from the same observer and movement in the same direction. For each stimulus condition, two blocks of 30 trials in each of two stimulus directions were analyzed from each the three subjects. By averaging the 30 responses in each block of trials, 12 averaged responses were produced that could then be compared. When comparisons were made between modeled and measured responses, 12 model curves were produced using data from blocks of 30 trials. The nonparametric sign test was used to test the probability that the velocity curves were different. The velocities at specified points of time were compared and the curve with the higher velocity was given a plus.
Similarly, the time that the curves reached specified velocities were compared and the first curve to reach that velocity was given a plus. For each comparison, the number of pluses for one of the sets of 12 velocity curves were summed. Ties were excluded from the analyses. P-values were then computed using an exact binomial distribution. In each experiment, slow eye velocities were compared at the time of each stimulus velocity change and 200 msec before each velocity change (see Figs 5,6,7 and 9). In expe~ments 1,3 and 4, the times at which slow eye velocities reversed direction were compared, and the times at which the velocities became less than l/2 the steady-state velocity when pursuing the first ramp were compared (see Figs 5, 7 and 9). In experiment 2, the direction of target motion changed by 90 deg rather than reversing, so, for slow eye decelerations, the times at which slow eye velocity became less than 0.5 deg/sec were compared and the times at which slow eye velocities became less than l/2 the steady state velocity when pursuing the first ramp were compared [see Fig. 5(B)], while for slow eye accelerations, the time at which slow eye velocity became greater than 0.5 deg/sec were compared [see Fig. 5(A)]. Also, for the slow eye accelerations in experiment 2, the velocities 100 msec after the stimulus change were compared in order to have four comparisons between these curves. RESULTS Experiment 1 The double-ramp stimuli used in the first two experiments included three predictable changes in target velocity, namely, the initiation of target motion, the direction change, and the termination of motion (Fig. 1).
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FIGURE I. Individual eye movement to a predictable double-ramp stimulus with a 180deg direction change. Upward deflections of the curves indicate rightward movements or velocities. In this trial, the target spot was extinguished at time = 600 msec. The target (1) reappeared 400 msec later and moved rightward at 10 deg/sec for 1500 msec, (2) reversed direction and moved leftward at 6 degjsec for 2000 msec, and then (3) stopped. Slow eye velocities changed prior to each of these three changes in target motion.
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By the third or fourth trial in a block, the subjects were altering slow eye velocity prior to each of these events, Anticipatory slow eye movements were present prior to the onset and termination of target motion. Similarly, predictive pursuit movements occurred prior to and during the change in the direction of target motion. In the first experiment, the effect of indi~du~1 ramp velocities on predictive pursuit was studied using horizontal doubie-ramp stimuli. Figure 2 shows combined subject averaged responses for al1 nine stimulus conditions. The velocities of both ramps affected predictive pursuit. The average smooth eye velocity curves could be segregated in accord with the velocity of either the first or second ramp of the stimulus. The speed of the first ramp affected the time at which the eye began to decelerate significantly. This initial deceleration began earlier with faster first ramp speeds. The speed of the second ramp affected the rate at which smooth eye velocity changed. Higher accelerations occurred with higher speed second ramps. Therefore, each ramp of the double-ramp stimuli altered specific components of the predictive pursuit responses. These tendencies were apparent in the averaged responses from individual subjects {Fig. 3) as well as in the combined subject averages (Fig. 2). It appeared that, near the time of ramp reversal, two events were anticipated, namely, the termination of the first ramp and the initiation of the second ramp. If so, then the predictive pursuit movements produced near the time of ramp reversal could be a combination of separate, but admixed responses to these two events. The predictive pursuit response characteristics described above are also characteristic of anticipator slow eye movements (Boman & Hotson, 1988). Anticipator slow eye decelerations prior to expected motion termination begin earlier with higher speed targets (see Fig. 2) and anticipatory slow eye accelerations prior to expected motion initiation are greater with higher speed targets. Therefore, we postulated that anticipatory slow eye accelerations and decelerations are active during smooth pursuit and combine to produce predictive pursuit movements to expected motion direction changes. To test this postulate, modeled velocity curves were produced by summing anticipatory slow eye accelerations and decelerations (Boman & Hotson, 1988) For example, the predictive pursuit response to a doubteramp stimulus with a 10degJsec ramp followed by a 6deg/sec ramp was modeled by summing the average anticipatory slow eye decelerations produced prior to the termination of 10 deg/sec ramps with the anticipatory slow eye accelerations produced prior to the initiation of a 6 deg/sec ramps (Fig. 4). In this manner, modeled response curves were produced for each of our nine double-ramp stimuli. The modeled response curves also incorporated the observation that anticipatory slow eye movements begin earlier and reach higher velocities when the fixation target is transiently extinguished prior to ramp motion onset (Boman & Hotson, 1988). Predictive pursuit also disengaged visual fixation by driving the fovea off
target prior to motion reversals (Fig. I t and ihis d~stmgagement began earlier with higher speed first ramps. Therefore, it was likely that ~ntici~t~~r~ slow eye accelerations from trials with transient target extinction would be needed to develop model velocity curves of predictive pursuit. Modeled velocity curves were produced using anticipatory slow eye accelerations from trials with the target extinguished for 0, 400 and 800msec prior to the onset of motion, producing 27 modeled curves. The mean errors between these derived velocity curves and the average. predictive pursuit vetocities measured near the time of ramp reversal were then compared. In most cases, the modeled curves summat~ng anticrpatory slow eye velocities paralIeled the predictive pursuit responses. However, the mean errors were affected by the anticipatory slow eye accelerations used in the model curves. When the first ramp moved at 2 degjsec, the mean error between the modeled and measured eye velocity curves was minimized when anticipatory slow eye accelerations from trials with no target extjnction were used in the models. When the first ramp moved at either 6 or 10 degjsec, the mean errors were usually lowest when anticipatory slow eye accelerations from trials with 400 msec of target extinction were used. The nine modeled response curves that included anticipatory slow eye accelerations from trials with these periods of target extinction were selected for subsequent nonparametric statistical analyses. Figure 5 shows the modeled and measured responses that produced the lowest [0.09 deg/sec, Fig. S(A)] and highest to.55 degjsec, Fig. 5(B)] mean errors from the nine selected curves. With the nonparamet~c statistical test (see Methods), four compa~sons between the modeled and the measured velocity curves were made for each of the nine stimulus conditions, giving 36 comparisons. At the 95% confidence level, two-thirds of these comparisons were not significantly different. At the 99% confidence level, only 5 of the 36 comparisons showed significant differences. None of the curves from the nine stimulus conditions had significant differences in more than two of the four comparisons. Therefore, the modeled response curves were not significantly different from the measured predictive pursuit curves in most of’ the comparisons.
Predictive pursuit of double-ramp stimuli with 90 deg direction changes was studied to determine whether the stimulus-response characteristics found in the first experiments are produced with motion direction changes other than 180 deg. This stimulus also allowed a direct rather than modeled comparison between anticipatory slow eye movements and predictive pursuit. The horizontal anticipatory slow eye velocities produced prior to the onset of horizontal target motion were directly compared to the horizontal predictive pursuit velocities produced near the shift from vertical to horizontal target motion [Fig. 6(A)]. Also, the horizontal anticipatory slow eye velocities produced when a ramp target was
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FIGURE 2. Combined subject average slow eye velocities from responses to doubl~ramp stimuli with ISOdeg direction changes and to ramp motion termination. Averaged velocities when first ramp velocity was; (A) 2 deg/sec, (B) 6 deg/sec, and (C) IO deg/sec. The motion of the second ramp was in the opposite direction at 2 deg/sec (V), 6 degjsec. (O),lO deg/sec (A) or ramp motion ended (0). The change in stimulus motion always occurred at time = 0. A velocity standard deviation is also shown in each graph. The velocity of target motion both before and after the stimulus change affected slow eye velocity.
DUANE K. BOMAN and JOHN R. HOTSON (4
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FIGURE 3. Average slow eye velocities from responses of subjects DB (El), JH (0) and KN (A} to double-ramp stimuli with 18Odeg direction changes. Individual averages when the velocities of both ramps were: (A) 2deg/sec, (B) 6deg/sec, and (C) lOdeg/sec. The three subjects had similar average responses under all stimulus conditions.
expected to stop horizontal motion and become stationary were directly compared to the horizontal predictive pursuit velocities produced when a ramp target was
expected to shift from horizontal to vertical motion [Fig. 6(B)]. Vertical anticipatory slow eye velocities and predictive pursuit velocities were similarly compared.
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FIGURE 4. Construction of modeled responses. (A) Combined subject average slow eye velocities produced near the termination of a lOdeg/sec ramp (V) and near the initiation of a 6deg/sec ramp when the stimulus was extinguished for 400 msec prior to ramp initiation (0). (B) Comparison of the modeled response (A) produced by summing the two curves shown in (A) with the combined subject average slow eye velocities produced near the 180 deg direction change of a predictable double-ramp stimulus (0). (C) Individual averages from subjects DB (O), JH (0) and KN (A) to this stimulus. The latencies and timecourses of the modeled velocity curves closely paralleled the measured responses to predictable changes in the direction of target motion.
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FIGURE 5. Highest and lowest mean errors between modeled (A) and measured (0) combined subject average responses to double-ramp stimuli. (A) Responses with the lowest mean error (0.08 deg/sec). (B) Responses with the highest mean error (0.98 deglsec). In this and the following figures, the open arrows indicate the selected points of time chosen for velocity comparisons using the nonparametric statistical test. The solid arrows indicate selected velocities that were also compared using the nonparametric test. The selection criteria for these times and velocities are presented in the Methods.
As expected, predictive pursuit moved the eye in the expected future target direction before the stimulus direction change. The times at which the fovea began to move off the target was similar to that produced with 180 deg direction changes. Also, with higher speed vertical ramps, the vertical predictive pursuit movements had
higher accelerations and began decelerating sooner. Therefore, the stimulu~respons~ characteristics of predictive pursuit movements to stirnub with 180 and 90 deg direction changes were similar. The time-courses of the anticipatory slow eye velocities and predictive pursuit velocities were also very
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FIGURE 6. Combined subject average slow eye velocities from responses to double-ramp stimuli with 90 deg direction changes and to ramp motion initiation and termination. (A) Average velocities when a target began moving horizontally after being stationary and then extinguished for 600 msec (17) or after terminating vertical motion (A). (B) Average velocities when a horizontally moving target became stationary (0) or changed to vertical motion (A). The inserts give examples of target motion paths. The thick lines within the inserts indicate the portion of the path over which the slow eye velocity curves were obtained. There are very few differences between the responses in each graph.
similar (Fig. 6). The main difference between these velocity curves was a velocity overshoot that occurred with ramp motion onset but not with an orthogonal change in motion direction [Fig. 6(A)]. The mean errors from the comparisons of combined subject average anticipatory slow eye and predictive
pursuit velocity curves were between 0.08 and 0.46 deg/sec. Using the nonparametric sign test, the eight comparisons shown in Fig. 6 were made on each set of horizontal and vertical velocity curves measured at the two stimulus speeds, giving 32 comparisons. Only three of the 32 comparisons were significantly different at the
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95% confidence level, while none were significantly different at the 99% confidence level. This direct comparison between anticipatory slow eye movements and predictive pursuit revealed minimal differences between their velocity curves. Experimm t 3
The stimulu~response characteristics of predictive pursuit were further characterized by varying the time between the termination of motion in one direction and the initiative of motion in a new direction. Tf these two events are separately anticipated, then including a delay or gap between the end of the first ramp and the beginning of the second ramp may separate the predictive pursuit response into two components. When the stimulus included a 200 msec gap between ramps, the smooth pursuit reversals developed a short velocity plateau that bridged separate decelerating and accelerating slow eye movements [cf. Fig. 7(A) to Fig. 5(A)]. Increasing the stimulus gap between doubleramps to 800 msec caused an increase in the duration of the velocity plateau or bridge [Fig. 7(B)]. When the target stopped but remained visible for 800 msec between ramps [Fig. 7(C)], the velocity of the bridging plateau was reduced. The fixation target attentuated the plateau velocity similar to the effect of a fixation target on anticipatory slow eye velocity prior to the initiation of ramp motion (Boman & Hotson, 1988). When the stimulus gap was further increased to 2000 msec, the average slow eye velocity during the gap became quite variable and showed a very slow acceleration prior to the second ramp. These responses were similar to the variable anticipatory slow eye velocities measured with 2 set of target extinction prior to ramp initiation (Boman & Hotson, 1988). Model responses were made for the conditions with 200 and 800 msec gaps {Fig. 7). To make the model response curves, the anticipatory slow eye accelerations were shifted by either 200 or 800 msec before being summed with the anticipatory slow eye decelerations. The endpoints where the curves no longer overlapped were then taken from the individual curves. The mean error between the measured and modeled combined subject average velocity curves were between 0.24 and 0.42 deg/sec. Using the nonparametric sign test, the 17 comparisons shown in Fig. 7 were made between the modeled and measured curves. The comparisons were signi~~antly different at the 95% confidence level, one of which was significant at the 99% confidence level. The timecourse of the summed anticipatory slow eye movements was similar to the separated components of predictive pursuit.
Predictive responses are also prominent when pursuing repetitive stimuli such as triangle waves, even with high frequency oscillations that cannot be accurately tracked. Repetitive stimuti of this type are often used in clinical studies. Therefore, it was potentially useful to know whether the predictive responses to these continu-
and JOHN R HOTSOh
ous stimuli were similar to those produced w1t11~~~~.~hitramp stimuli. Eye movern~~t~ were monitored while the anbjezia pursued horizontal. triangle-wave stimuli Gllaung a: frequencies of 0.33 and I .5 Hz, Stimulus a~nplit~l~l~was adjusted SO that the speed of the illdi~~id~~~~ ri+mps was always lOdcg/sec. thus producing ramp dttrntions ol 1500 and 333 msec, respectively. At the lower frcyucnc~. the smooth pursuit responses were similar 1~1those produced with double-ramp stimuli [cf. Fig. X(A) I(, f-ig. I]. At the higher frequency. smooth pursuit became much less regular and the peak velocities wzrc‘ quite variable. Predictive responses, however. I-emaincd prominent in these trials [Fig. 8(B)]. The combined subject average predictive pursuit vclocities produced with triangle-wave stimuli were compared with modeled velocity curves iF?g. 9). The modeled response was produced by summing anticipatory slow eye accelerations elicited with 4OOmsec oi target extinction prior to 10 degjsec ramp initi~~tion wirh the anticipatory slow eye decelerations prior to 10 deg/sec ramp termination, similar to the first oxperiment. The modeled response closely resembled the measured predictive pursuit response at the lower stimulus frequency [Fig. 9(A)]. At the higher frequency, the measured responses showed higher accelerations and decelerations than the modeled response [Fig. 9(B)]. Eight comparisons were made using the ~lonp~~arnetri~ sign test. None were signifi~~nti~ different at the 95% confidence level. DISCUSSION The present results demonstrate how predictable changes in the direction and speed of target motion affect predictive pursuit eye movements. With the double-ramp stimuli used in this study, the velocities of both ramps affected specific aspects of the predictive responses. The higher the velocity of the first ramp, the earlier the eye began to decelerate significantly. The expected direction of the second ramp determined the direction of the predictive movement. The higher the velocity of the second ramp, the greater the accele~dtion of the predictive movement in the new direction. Therefore, expectations about target motion both before and after the direction change had specific and different effects on the predictive pursuit responses. From these obse~ations we proposed that, when a moving visual target is expected to undergo a change in the direction of motion, two events are anticipated; the termination of motion in the first direction and the initiation of motion in a new direction. Fnrthe~ore, we proposed that the predictive pursuit movements produced near the time of the expected motion change represent the summated output of two, directionsensitive predictive components, the first being associated with the expected te~i~~tion of motion in one direction and the second being associated with the expected initiation of motion in a new direction. Alternative predictive strategies such as dete~ining the re-
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FIGURE 7. Combined subject average slow eye velocities from responses to double-ramp stimuli with delays between the termination of the first ramp and the initiation of the second ramp. The squares indicate measured responses and the triangles indicate modeled responses. In each graph, the first ramp ended at time = 800 msec. Average responses to stimuli with: (A) 200 msec delays with the target extinguished, (B) 800 msec delays with the target extinguished and (C) 800 msec delays with the target visible and stationary. The construction of each modeled response is described in the text.
sponses velocity,
solely on the basis of expected future target future target direction or the absolute value of
the change in target velocity were not consistent observed two component strategy.
with the
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