1Howard Hughes Medical Institute, Department of Physiology and W. M. Keck Foundation Center for Integrative Neuroscience, University of California, San Francisco, California 94143; and 2Department of Physiology, Hokkaido University School of Medicine, Sapporo 060, Japan
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ABSTRACT |
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Tanaka, Masaki and Stephen G. Lisberger. Context-Dependent Smooth Eye Movements Evoked by Stationary Visual Stimuli in Trained Monkeys. J. Neurophysiol. 84: 1748-1762, 2000. The appearance of a stationary but irrelevant cue triggers a smooth eye movement away from the position of the cue in monkeys that have been trained extensively to smoothly track the motion of moving targets while not making saccades to the stationary cue. We have analyzed the parameters that regulate the size of the cue-evoked smooth eye movement and examined whether presentation of the cue changes the initiation of pursuit for subsequent steps of target velocity. Cues evoked smooth eye movements in blocks of target motions that required smooth pursuit to moving targets, but evoked much smaller smooth eye movements in blocks that required saccades to stationary targets. The direction of the cue-evoked eye movement was always opposite to the position of the cue and did not depend on whether subsequent target motion was toward or away from the position of fixation. The latency of the cue-evoked smooth eye movement was near 100 ms and was slightly longer than the latency of pursuit for target motion away from the position of fixation. The size of the cue-evoked smooth eye movement was as large as 10°/s and decreased as functions of the eccentricity of the cue and the illumination of the experimental room. To study the initiation of pursuit in the wake of the cues, we used bilateral cues at equal eccentricities to the right and left of the position of fixation. These evoked smaller eye velocities that were consistent with vector averaging of the responses to each cue. In the wake of bilateral cues, the initiation of pursuit was enhanced for target motion away from the position of fixation, but not for target motion toward the position of fixation. We suggest that the cue-evoked smooth eye movement is related to a previously postulated on-line gain control for pursuit, and that it is a side-effect of sudden activation of the gain-controlling element.
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INTRODUCTION |
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When a small moving target appears in the peripheral visual field, primates use two classes of voluntary eye movements to stabilize the target images on the fovea. Smooth pursuit is a continuous eye movement that reduces the velocity of the target images, whereas saccades are rapid, transient eye movements that bring target images onto the fovea. Although combinations of saccadic and smooth pursuit eye movements are used to track a moving object in daily life, these eye movement systems have been examined separately, leading to the general rule that position errors and stationary stimuli cause saccades while moving targets are generally required to evoke smooth pursuit.
In a classical experiment, Rashbass (1961) showed that
smooth motion is the main source of visual drive for pursuit
initiation. When a step-ramp target motion is configured with steps and
ramps in opposite directions, pursuit is initiated away from target position but in the direction of target motion. In spite of the general
consensus that visual motion provides the main sensory drive for
pursuit, a variety of papers have also analyzed the effect of target
displacement on smooth eye velocity, and some have demonstrated clear
effects (e.g., Carl and Gellman 1987
; Morris and
Lisberger 1987
; Wyatt et al. 1989
). The
most recent suggestion of a possible effect of target position on
pursuit has come from the finding that electrical stimulation of the
fixation zone of the superior colliculus alters the initiation of
pursuit (Basso et al. 1997
). Thus there is a clear
precedent for pursuit to be affected by visual inputs from stationary targets.
All the experiments mentioned above reported pursuit toward
the real, or electrically stimulated, retinal position error. A recent
study has demonstrated that monkeys can also generate smooth eye
movements away from the position of a stationary visual stimulus, called a "cue," if the experimental conditions are
contrived properly (Tanaka and Fukushima 1997). The goal
of the present study was to define the requisite stimulus conditions
for the cue-evoked smooth eye movement more fully and to try to relate it to properties of pursuit that have been identified in previous studies. We will conclude that the cue-evoked eye movement may be
related to a pursuit gain control element that has been suggested in
previous experiments as a way to explain a number of observations (e.g., Grasse and Lisberger 1992
; Schwartz and
Lisberger 1994
). We devote the remainder of the
INTRODUCTION to a consideration of the evidence regarding
the existence and nature of the on-line gain control.
The best evidence for a pursuit gain control comes from experiments
showing that the smooth eye velocity evoked by a given brief
perturbation of target motion depends on the initial conditions. The
size of the response depends on eye/target speed at the time of the
perturbation: the response is small but present if the perturbation is
delivered during fixation or during the offset of pursuit and large if
the perturbation is delivered during the maintenance of pursuit at
target speeds in excess of 20°/s or during the onset of pursuit
(Goldreich et al. 1992; Krauzlis and Miles
1996a
; Schwartz and Lisberger 1994
). The
presence of on-line gain control was interpreted as evidence that
continuous variation in the gain of visuomotor processing was a
component of the neural mechanisms controlling pursuit. As originally
suggested by Robinson (1965)
, the gain would be very low
and the pursuit system rendered "off" during fixation of a
stationary target and the gain would increase to a varying degree to
render the pursuit system "on" after the decision to track a moving target.
In another relevant paper, Lisberger (1998) demonstrated
that pursuit was automatically enhanced in the immediate wake of a
saccade. Further, even though presaccadic pursuit depended strongly on
the position of the moving target (see also Lisberger and
Westbrook 1985
), enhancement was spatially uniform and caused
postsaccadic eye velocity to be independent of the position of the
pursuit target before the saccade. Lisberger's (1998)
interpretation was that saccades could increase the gain of pursuit and
automatically render the pursuit system "on." In contrast, the
status of the gain control before the saccade depended on the exact
configuration of the step-ramp target motion. If the ramp took the
target away from the position of fixation, then the gain remained low
and pursuit was weak. If the ramp was going to bring the target onto the fovea soon, then the gain was increased and presaccadic pursuit was
excellent. Thus he proposed that the toward/away asymmetry in pursuit
resulted from a toward/away asymmetry in activation of the pursuit gain
control element. We will show a striking parallel between the proposed
toward/away asymmetry in the gain control and the directional bias
reflected in the cue-evoked eye movements analyzed in this paper. Based
on this parallel, and the finding that the cue itself can enhance
presaccadic pursuit for targets moving away from the position of
fixation, we suggest that the cue-evoked smooth eye movements are a
manifestation of sudden changes in the value of the pursuit gain control.
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METHODS |
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Animal preparation
Five male monkeys were used in this study. Experiments with three rhesus monkeys (Macaca mulatta, monkeys KLB, NNK, and PCK) were conducted at the Department of Physiology, University of California, San Francisco. Experiments with two Japanese monkeys (Macaca fuscata, monkeys SSK and KRS) were conducted at the Department of Physiology, Hokkaido University School of Medicine, Sapporo, Japan. All experimental protocols described below were approved in advance by the Institutional Animal Care and Use Committee at the respective universities.
The experimental procedures for the rhesus monkeys were similar to
those described previously (Lisberger and Westbrook
1985). After initial behavioral training, the animals were
sedated with ketamine hydrochloride and anesthetized with isoflurane.
Using sterile procedure, a head holder was installed with dental
acrylic, and a coil of wire was implanted under the conjunctiva to
record eye movements (Fuchs and Robinson 1966
;
Judge et al. 1980
). The surgical methods for the
Japanese monkeys have been described elsewhere in detail (Tanaka
and Fukushima 1998
). Briefly, the animals were anesthetized
with pentobarbital sodium and halothane. A pair of head holders and an
eye coil were implanted with sterile procedure. All animals were
trained to sit in a primate chair. During experiments their heads were
restrained by the implanted head holder.
Visual stimulus and behavioral tasks
For experiments done in San Francisco, visual stimuli were presented on a Pentium PC controlled analog oscilloscope (Hewlett Packard 1321B or 1304A) with a refresh rate of 250 Hz. The oscilloscopes were located either 45 or 28 cm away from the eyes and, because they had different sized screens, subtended similar visual angles of 44.4 × 36.3° or 42 × 36°. The visual stimuli were 0.2 and 0.6° white square spots with luminances of 3.8 and 17.6 cd/m2, respectively. The smaller spot served as both a fixation target and a moving pursuit target. The larger spot was used to provide a salient, stationary stimulus that we refer to as a "cue." For experiments done in Sapporo, a red laser spot (0.25°) projected onto the back of a translucent tangent screen (55 cm from the eyes) was used as both the fixation target and pursuit target. The target position was controlled by a pair of mirror galvanometers. The mirror position was updated every millisecond by a Macintosh computer. An array of green light-emitting diodes (LEDs) was attached on the screen to provide the visual cues (Fig. 1A). The array consisted of nine LEDs placed just above the horizontal meridian at 0, 5, 10, 15, and 25° right and left of the vertical meridian and two LEDs placed on the vertical meridian 10° above and below the central fixation target. We were unable to measure the luminance of the visual stimuli used in Sapporo. However, we can report that they were configured with the cue much brighter than the target spot, and they were consistent in luminance from day-to-day.
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The basic paradigm for target presentation and motion was a modified
step-ramp pursuit task (Rashbass 1961). Each trial began with the appearance of a central fixation spot. After a random fixation
period (1-1.5 s), the target spot jumped to the right or left and
moved smoothly along the horizontal meridian. The monkeys were required
to track the moving spot with their eyes to obtain a liquid reward. In
many trials, we introduced a temporal "gap" between the offset of
the fixation target and the appearance of the moving target, because a
previous study showed that eye movement responses to a peripheral
visual "cue" are enhanced if the cue appears during such a gap
(Tanaka and Fukushima 1997
). The fraction of the gap
trials in a block ranged from 0 to 100%, but usually was more than
80%. For experiments done in Sapporo, a 20-ms gap was always
introduced to avoid any visible streak caused when mirror galvanometers
attempted to execute a step of target position.
Different monkeys received different experience with respect to the direction of target motion relative to the position of fixation. For the two Japanese monkeys (SSK and KRS) the target always moved toward the central fixation target from an eccentric position ("toward" pursuit trials e.g., Fig. 1B). For two of the rhesus monkeys (KLB and NNK), most prior experience was with randomized directions of target motion, so there was approximately equal probability that the target would move toward or away from the position of fixation. Except for one experiment (Fig. 3, B and D), we retained that design in all blocks of trials for the present experiments: the tracking target moved toward or away from the fixation target with equal probability. The remaining rhesus monkey (PCK) had not participated in any experiments prior to these and was trained only with tracking targets that moved away from the fixation target ("away" trials). During the initial pursuit training and data collection, which lasted 6 wk, this monkey never saw target motion toward the position of fixation.
In most trials, a larger square spot (San Francisco) or one of the green LEDs (Sapporo) was presented briefly (25-300 ms, usually 100 ms) during the gap period as a visual cue. The location of the visual cue and the direction of target motion were randomized within each experiment so that the monkey could not predict the direction of pursuit by the location of the cue. Figure 1B illustrates the experimental paradigm we used. In this example, the gap between the offset of the fixation target and the onset of the tracking target was 200 ms, and the cue was visible for the last 100 ms before the appearance of the tracking target. The cue appeared either 5° to the left or right of the central fixation target. The pursuit target also appeared at 5° right or left, moved at 30°/s for 666-1,000 ms, and then stopped and remained visible for an additional 300-500 ms. Intertrial intervals were 500-1,000 ms. Each block of trials consisted of up to 68 different variations of the temporal and spatial parameters of the basic trial configuration described above. For example, data depicted in the bottom of Fig. 7B were obtained from a block of 64 different cued trials (2 pursuit directions × 2 step directions × one gap duration × 8 cue-lead times × 2 cue locations) and 4 no-cue controls (2 pursuit directions × 2 step directions). Data in Fig. 6, A and C, were obtained from a block of 60 different combinations (2 pursuit directions × 2 step directions × 5 gap durations × 3 cue conditions). In one experiment, we presented the visual cue during gap saccade trials (Fig. 3, A and C). The monkeys were rewarded with water or juice when they kept their eye position within 2-5° of the moving target for the duration of the trial. In the initial phase of training for those experiments, monkeys frequently made saccades to the visual cue, especially in trials with a gap. As training progressed, monkeys gradually learned to suppress saccades to the cue, so they could track the moving target adequately. We usually mixed many combinations of trials with different cue location, lead-time, and gap duration to train monkeys to learn not to respond to the cue. Data were collected only after the monkeys were well trained in the cue paradigm. Experiments were carried out in a dark room, except for a subset described in the text or illustrated in Fig. 11. For the experiments with some ambient illumination, we estimated the ambient illumination by covering the dark face of the display oscilloscope with white paper and using a photometer to measure the luminance of the paper from the position of the monkeys' eyes. The ambient luminance level measured in this way was 0.51 cd/m2.
Data acquisition and analysis
Horizontal and vertical eye velocity signals were obtained by
analog differentiation (band-pass DC to 25 Hz, 6 dB/oct or DC to 50 Hz,
12 dB/oct). Data were digitized and sampled at either 1 kHz (San
Francisco) or 500 Hz (Sapporo). Eye movements were analyzed by using
homemade interactive computer programs. We first reviewed both eye
position and velocity traces from each trial on the video monitor. The
programs allowed us to visually detect the onset and the offset of each
saccade and mark them with a mouse-controlled cursor. These saccadic
portions of the eye velocity traces were not used in subsequent
analyses. Unusually noisy trials or trials in which the monkey clearly
did not attempt to track the moving target or made a reflexive saccade
to the visual cue were eliminated from analyses. Horizontal eye
velocity traces were aligned on the onset of target motion for
identical tasks in the same block. We then made averages of eye
velocity as a function of time, or measured eye acceleration and
velocity at selected times in individual trials as described below.
Because the magnitude of eye movement responses varied from day to day, data were compared only within single experimental days.
Quantitative analysis entailed measurement of eye velocity immediately before, and eye acceleration during, the initiation of pursuit. In most of our experiments, the cue appeared 100 ms before the onset of target motion, so that the normal onset of pursuit would coincide with the peak of the smooth eye movement evoked by the cue. Therefore we chose the time of the onset of pursuit for step-ramp target motion without a cue as the time for analysis of the response to the cue. Probably because of differences in the exact visual display used at the two sites, the monkeys used in San Francisco had slightly shorter pursuit latency (~100 ms in the "toward" trials, ~80 ms in the "away" trials) than those used in Sapporo (~120 ms in the toward trials). We estimated the size of the response to the cue by measuring eye velocity at the relevant time from individual trials (80 and 100 ms after target motion onset for the San Francisco and Sapporo experiments).
We measured eye acceleration from averages of eye velocity based on
more than 15 individual desaccaded traces, by fitting a regression line
to the average eye velocity for an 80-ms period starting at the onset
of pursuit. The onset of pursuit was detected using a technique similar
to the one developed by Carl and Gellman (1987).
Briefly, baseline eye velocity was analyzed by computing the mean and
standard deviation (SD) of eye velocity for the interval from 100 ms
before to 50 ms after the onset of target motion. Then a regression
line was fit to the average eye velocity for the period from 10 ms
before to 30 ms after the average eye velocity was more than 2 SD above
the baseline mean. The point where the regression line intersected the
mean baseline eye velocity was taken as the pursuit onset. Because the
monkeys often initiated catch-up saccades during this period, we were
sometimes unable to obtain average traces for 80 ms when the target
moved away from the fixation target. In such cases, eye acceleration
was measured from average eye velocity for a period <80 ms.
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RESULTS |
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Figure 2 shows data from three individual trials that delivered the same rightward target motion at 30°/s with a 200-ms gap period between the offset of the fixation target and the onset of the tracking target. The position and velocity traces in Fig. 2 begin at the time when the fixation target disappeared. If we did not present a cue in the gap period (Fig. 2A), then the gap had no apparent effect on pursuit, and rightward eye velocity was initiated with a normal latency of ~100 ms. If a cue appeared during the gap period, 100 ms before the onset of target motion (arrowheads in Fig. 2, B and C), then eye velocity became nonzero during the normal latency of pursuit. When the cue was presented at 5° right (Fig. 2B), there was a substantial leftward deviation in eye velocity, beginning about the time when the tracking target appeared. When the cue was presented at 5° left (Fig. 2C), rightward eye velocity began at about the time the tracking target appeared. In toward pursuit trials like those shown in Fig. 2, catch-up saccades either did not occur during the initiation of pursuit or were delayed until after the first 100 ms of pursuit. Note that with extensive training the monkeys were able to prevent saccades to the visual cue even though its size (San Francisco) or color (Sapporo) made it seem to us more salient stimulus in the display.
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Context specificity of the smooth eye movements evoked by a visual cue
The occurrence of the cue-evoked smooth eye movements depended on whether the cues were delivered during blocks of saccade or pursuit trials. In Fig. 3, each point plots horizontal eye velocity 80 ms after the onset of target motion, and the points are plotted in the order that the trials were delivered. Since trials that presented cues on the left (open symbols) or right (filled symbols), or no cues (solid trace near zero eye velocity) were randomly interleaved, each of these trial types is well represented at each time point. The experiments analyzed in Fig. 3, A and C, consisted of three successive blocks of trials containing 700 pursuit trials, 600 saccade trials, and then 700 more pursuit trials. Pursuit trials were selected randomly from 12 different combinations of the following: two initial positions for the tracking target (right or left of fixation), two directions of target motion (i.e., away or toward the position of fixation), and three cue conditions (right, left, or without a cue). The initial position of the tracking target was always ±5o, and its velocity was ±30°/s. When it was delivered, the cue appeared either 5° right or left of the fixation target for 100 ms before the onset of motion of the tracking target. Saccade trials were delivered with a similar design, except that the tracking target was supplanted by a stationary target that appeared at 10° right or left after the 200-ms gap period and stayed there for 1,000-1,500 ms.
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Inspection of Fig. 3, A and C, reveals that the direction of the eye movements measured just before the onset of pursuit was consistently away from the position of the cue, even though there were large intertrial variations in the magnitude of eye velocity. In contrast, moving averages of eye velocity for every 15 consecutive trials without a cue showed essentially zero eye velocity (continuous thick line). The running standard deviation of eye velocity for trials without a cue (not shown in Fig. 3) ranged from 0.28 to 1.87°/s (monkey KLB) or from 0.16 to 0.95°/s (monkey NNK), indicating that the average eye velocities near zero reflected a consistent absence of a response in the absence of the cue, and not alternation between large leftward and rightward responses. Comparison of the magnitude of the cue-evoked eye velocity during blocks of pursuit and saccade trials shows a large effect on the responses. The cue-evoked smooth eye velocity was much larger in pursuit blocks than in saccade blocks, but was similar in the pursuit blocks that came before and after the saccade blocks. For the data in Fig. 3, A and C, statistical analysis of successive saccade and pursuit blocks revealed significant differences for all four possible comparisons (unpaired t-test, P < 0.001).
We have not attempted to analyze the time course of the transition quantitatively, but it is clear from Fig. 3, A and C, that it occurs within 100 trials, both at the switch from pursuit to saccade trials and the switch from saccade to pursuit trials. These results suggest that the occurrence of the cue-evoked smooth eye movements is related to the behavioral state of the monkeys, in particular, to the preparation for a target motion that will require smooth pursuit. Note that the direction of the cue-evoked smooth eye velocity is not related to the direction of motion of the tracking target, since rightward and leftward target motion, and toward and away trials, were randomly interleaved in trials that presented cues on the left or right. For example, the open symbols in the first block of Fig. 3A represent measurements made from trials that presented a cue on the left in the temporal gap before leftward or rightward target motion toward or away from the position of fixation. Yet, the cue-evoked eye velocities were all rightward.
Monkeys could change the magnitude of the cue-evoked smooth eye movements within 100 trials. Could they also change the direction of the cue-evoked smooth eye movements if the blend of pursuit trials provided a consistent expectation about target motion? Although the monkeys used in Fig. 3 had received extensive previous experience with an approximate balance of toward and away pursuit trials, it is plausible that they had come to expect target motion toward the fixation target rather than that away from the fixation target. If so, then the monkeys might initiate anticipatory eye movements in the direction opposite to any visual stimulus in the anticipation that the stimulus would shortly move toward the position of fixation. We evaluated this possibility by experiments that delivered blocks of away and toward trials separately, where trials included the same 200-ms gap between the offset of the fixation target and the appearance of the tracking target. Figure 3, B and D, shows data from two such blocks of pursuit trials. In the first block, the pursuit target always moved in the same direction as the preceding target step (i.e., away pursuit trials). The first three hundred trials in the away block did not present a visual cue, and the subsequent 500 trials had an equal probability of no cue, a left cue, or a right cue. This was followed by a similar block of 800 toward trials, again with cues absent from the first 300 trials. Figure 3, B and D, shows that the direction of the cue-evoked smooth eye velocity was not altered when all trials took the tracking target away from the position of fixation. This contrasts with the ability of the same monkeys to change the size of the cue-evoked response within 100 trials when the blocks switched from saccade to pursuit trials (Fig. 3, A and C). The magnitudes of the eye movements away from the cue decreased in the toward pursuit trials in one monkey (KLB, unpaired t-test, P < 0.01), possibly because of fatigue. No statistically significant difference in the size of the cue-evoked smooth eye movement was observed in the comparison of away and toward blocks for the other monkey (NNK).
We next asked whether training a naïve monkey only on away pursuit trials could result in cue-evoked smooth eye movements toward the visual cue. Figure 4A shows the time courses of rightward pursuit obtained from monkey PCK after his initial 6 wk of behavioral training in which he was exposed only to targets that moved away from the position of fixation. It was a challenge to obtain strong cue-evoked smooth eye movements in monkeys that lacked extensive experience in pursuit tasks, so we chose conditions that would optimize the responses in this monkey. In this example, the duration of the gap between fixation target offset and tracking target onset (vertical dashed line) was 300 ms, and the cue appeared at 5° right for the last 150 ms before the tracking target appeared at 5° right and moved away from the position of fixation. The time of appearance of the cue is shown by the arrowhead. Figure 4A shows that this configuration of the gap and cue sometimes evoked tiny eye movements toward the visual cue (rightward in this case) followed by larger smooth eye movements away from the cue. The initiation of rightward pursuit then reversed the cue-evoked smooth eye movement. Since the smooth eye movements away from the cue were observed in trials without the tiny eye movements toward the visual cue (data not shown), the cue-evoked eye movements away from the cue were not due to the retinal slip of a stationary visual cue caused by the tiny eye movements toward the cue observed in this monkey. For comparison, Fig. 4B shows data from a different monkey in similar away pursuit trials, in which the cue appeared at 5° right for the last 100 ms of a 200-ms gap. The cue-evoked smooth eye movements had similar latencies of ~100 ms, similar time courses, and both took the eyes away from the position of the cue. Because the cue-evoked smooth eye movements took the eyes smoothly away from the position of cue even in a monkey that had never received training in the toward pursuit paradigm, we conclude that the direction of the cue-evoked smooth eye movements cannot be attributed entirely to past experience on toward pursuit trials.
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Table 1 summarizes the average sizes (±SD) of the cue-evoked eye velocity examined in this study. The values are averages of the data from two to nine different experiments for each monkey, and the standard deviations indicate variation of the average size across days. These data show that the cue-evoked eye movements in monkey PCK were in the same direction as in the other monkeys but were generally of smaller size. Since the magnitude of the eye movements showed large intersubject as well as interexperiment variability, we have not attempted further comparison between the data from different days or monkeys.
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Latency and time course of cue-evoked smooth eye movements
The gap/cue/pursuit paradigm we have used thus far reveals the existence of cue-evoked smooth eye movements, but the visual targets that appear after the cue prevent analysis of the full time course and amplitude of the cue-evoked eye movements. To address this issue, we conducted experiments in which most of the trials consisted of the same blend of trials used in the pursuit blocks in Fig. 3, A and C, but 10% of the trials served as probes and presented cues without any subsequent visual stimuli. Figure 4, C and D, shows examples of individual (fine traces) and average (bold traces) eye velocity for two monkeys in probe trials that delivered a 100-ms duration cue at 5° left, starting 100 ms after the offset of the fixation target, followed by a 950-ms gap that terminated at the end of the trial. In both monkeys, rightward smooth eye movements were initiated ~100 ms after the cue onset. Eye velocity peaked 80-110 ms later, and the full response lasted ~250 ms.
Figure 5 compares the latency of the cue-evoked smooth eye movements with the latency for the initiation of pursuit toward or away from the position of fixation in two monkeys. The data plotted in Fig. 5, A-D, were obtained from right and left pursuit trials without a cue, and those in E and F were from rightward toward pursuit trials with right or left cue. Because of the difficulty of measuring the latency of a small smooth eye velocity response reliably, we have adopted a somewhat different approach. For each target motion, we have made averages of eye velocity triggered on the onset of the cue (Fig. 5, E and F) or the onset of target motion (Fig. 5, A-D) and defined the latency of the response as the time when the responses to leftward and rightward stimuli diverged. This revealed a progression from the shortest latency for target motion away from the position of fixation (Fig. 5, A and B), longer latencies for target motion toward the position of fixation (Fig. 5, C and D), and the longest latencies by a tiny amount for the cue-evoked smooth eye movements (Fig. 5, E and F). To make these effects more visible, we have drawn vertical dashed lines at the time of the initiation of pursuit for target motion away from the position of fixation for each of the monkeys (75 ms for monkey KLB, 90 ms for monkey NNK). We realize that averages of eye velocity give a better indication of the shortest latency response rather than of the average latency. To illustrate that this potential problem was obviated by the consistency of the latencies within each stimulus condition, we have superimposed on the averages (bold traces) all the individual responses for stimuli that evoked rightward smooth eye velocity (fine traces). For monkey KLB (left column), these individual traces support the progression of latencies from shortest in away trials to longest in cue-evoked eye movements. For monkey NNK (right column), the individual traces endorse the longer latency of the cue-evoked smooth eye movement, but raise questions about whether the difference in latency between toward and away trials is large enough to be functionally or statistically significant.
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Factors that affect the magnitude of the cue-evoked smooth eye movements
GAP DURATION. The magnitude of the cue-evoked smooth eye movements depended on the duration of the gap between the offset of the fixation target and the appearance of the tracking target. For the experiments summarized in Fig. 6, we used gap intervals that varied randomly from 0 to 400 ms in 100-ms increments and, again, measured eye velocity immediately before pursuit initiation. As before, the cue appeared at 5° left or right for the last 100 ms before the onset of the tracking target. In each monkey presented here, the magnitude of the cue-evoked eye velocity was largest when the gap duration was 200 or 300 ms and was smaller when the gap duration was longer or shorter. In all panels in Fig. 6, data obtained from rightward pursuit trials are plotted as open circles and those from leftward pursuit trials as filled triangles. Data for left cue trials are connected by solid lines and those for right cue trials by dashed lines. The average eye velocity in noncue control trials is plotted as symbols without connecting lines. Inspection of Fig. 6 shows that the direction and magnitude of the cue-evoked smooth eye movement depended on the presence and position of the cue (discriminated by solid vs. dashed lines), but not on the direction of subsequent target motion (discriminated by filled vs. open symbols). For monkey KLB (Fig. 6, A and C), studied in San Francisco, essentially the same effects are present for the away and the toward pursuit trials, which have been plotted separately even though they were randomly interleaved during the experiments. Monkeys KRS (Fig. 6B) and SSK (Fig. 6D) were both studied in Sapporo, under conditions in which the tracking target always moved toward the position of fixation.
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CUE TIMING. The response evoked by a given cue depended critically on when the cue was presented relative to the offset of the fixation target. The traces in Fig. 7A show averages of eye velocity for rightward pursuit in trials that had different times of cue appearance (triangles) but the same 200-ms gap between the offset of the fixation target (1st vertical dashed line) and the onset of the tracking target (2nd vertical dashed line). Data were aligned on the target motion onset (time 0) and averaged separately for each value of cue-lead time. The cue appeared 5° to the right (top set of traces) or left (bottom set of traces) of the fixation target. If the cue appeared before the moving target (positive values of cue-lead time), then it was extinguished when the moving target appeared. If the cue appeared at or after the moving target appeared (zero or negative values of cue-lead time), then it persisted for only 50 ms. The example traces show an experiment where the cues evoked smooth eye movements ~120 ms after the cue onset, and the amplitude of the responses was largest if the cue appeared during the gap period (between the 2 vertical dashed lines). In this example, the cue evoked little or no smooth eye movement when it appeared before the gap. It was not possible to separate the cue-evoked eye movement from the initiation of smooth pursuit if the cue appeared just before, near, or after the onset of tracking target motion. The magnitude of the cue-evoked eye movement is quantified in the three graphs of Fig. 7B, which plot average eye velocity 200 ms (monkeys SSK and KRS) or 180 ms (monkey KLB) after the onset of the cue as a function of the cue-lead time. We plot eye velocity only for the trials in which the cue appeared 100-300 ms prior to the onset of the tracking target. In two of the three monkeys (SSK and KRS), the cue caused only a slight smooth eye movement if it appeared while the fixation spot was still present (cue-lead time >200 ms). In the third monkey (KLB), the cue was effective even if presented 100 ms before the fixation target was extinguished. We do not have a ready explanation for this variation among monkeys.
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CUE LOCATION. Figure 8, A and C, plots averages of horizontal eye velocity immediately before pursuit initiation as a function of the location of the cue in standard trials with a cue-lead time of 100 ms and a 200-ms gap between the offset of the fixation target and the onset of target motion. Cues could appear up to 25° eccentric on the horizontal axis or at 5 or 10° vertical. Trials with different cue locations were interleaved randomly. As before, the tracking target always appeared 5° right or left and moved toward (A) or away from (C) the fixation target at 30°/s. The cue-evoked smooth eye movements were not present when the cue appeared at the position of fixation. They were largest when the cue appeared 5° eccentric along the horizontal axis. They decreased as a function of eccentricity but were still observable when the cue appeared 15° eccentric. Statistical comparison of the size of the cue-evoked smooth eye movements for cues at 0 versus 15° revealed statistically significant differences in all four cases (unpaired t-test, P < 0.001). No smooth eye movements were observed when the cue appeared above or below the fixation target or did not appear at all (symbols at right of graph, not connected to other points). The cue-evoked smooth eye movements were the same for trials that presented rightward target motion (open circles) and leftward target motion (filled triangles). Data from two other monkeys were nearly identical and are not shown.
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TARGET VELOCITY.
Since the large cue-evoked smooth eye movements were observed only if
the cue was presented in blocks of pursuit trials (Fig. 3, A
and C), it is plausible that the size of the cue-evoked
smooth eye movement might be related to the speed of target that monkey is preparing to pursue. We therefore asked whether the magnitude of the
cue-evoked responses would change in relation to target velocity if
individual velocities were blocked so that the target velocity was
known ahead of time. We used four (monkey SSK) or eight
(monkey KRS) blocks of trials that consisted of a 200-ms gap, a 100-ms cue-lead time, and subsequent horizontal target motion at
one of 10, 20, 30, or 40°/s. The initial position of the tracking
target was 2, 3, 5, and 6° for 10, 20, 30, and 40°/s target motion,
respectively. As before, cues could appear with equal probability to
the left or right of the fixation position or not at all, and the order
of these trials was randomized within each block. Figure 8,
B and D, plot average eye velocity immediately before pursuit onset. The number of trials for each target velocity ranged from 262 to 326 in monkey KRS, and from 229 to 236 in
monkey SSK. Target velocity had a slight but statistically
significant effect on the size of the cue-evoked smooth eye movements.
Regression slopes were 0.064 and 0.046 in B and 0.11 and
0.12 in D and were statistically different from zero
(P < 0.05 for monkey KRS, P < 0.01 for monkey SSK). As before, the direction of the
cue-evoked smooth eye movement depended only whether the cue appeared
to the right (dashed lines) or left (solid lines) of the fixation target and not on whether the subsequent target motion was rightward (open circles) or leftward (filled triangles).
AMBIENT ILLUMINATION.
Significant cue-evoked smooth eye movements were observed only when
experiments were carried out in the dark. We compared the magnitudes of
the cue-evoked smooth eye movements in alternate blocks of pursuit
trials with ambient illumination (0.51 cd/m2), or
in the dark for two monkeys. The cue appeared for 100 ms during the
200-ms gap interval either 5° right or left of the fixation target.
When the monkeys performed pursuit trials in the dark, the cue-evoked
smooth eye movements away from the cue were quite large. For cues
presented on the right and the left, they averaged 4.26 ± 2.74°/s (mean ± SD, n = 228) and 4.39 ± 2.39°/s (n = 218) in monkey KLB, and
2.77 ± 2.06°/s (n = 261) and 1.60 ± 1.61°/s (n = 270) in monkey NNK. The
cue-evoked smooth eye movements were still present but were attenuated
when the monkey performed same blocks of trials under dimly lighted
condition. They averaged
1.29 ± 1.66°/s (n = 204) and 1.75 ± 1.96°/s (n = 180) in
monkey KLB, and
1.11 ± 0.95°/s (n = 188) and 0.38 ± 0.51°/s (n = 281) in
monkey NNK. The effect of ambient illumination on the
velocity of the cue-evoked eye movements was statistically significant
for both cue positions in both monkeys (unpaired t-test, P < 0.0001).
Enhancement of the initiation of pursuit in the wake of cues
The initial pursuit responses to a step of target velocity have
been examined extensively in previous studies (for reviews, see
Keller and Heinen 1991; Lisberger et al.
1987
). Because the first 100 ms of pursuit initiation is driven
by target motion before the eyes begin to move, eye acceleration during
the "open-loop" interval is a sensitive measurement to examine
visuomotor drive for pursuit. Recent studies have also found that the
gain of visuomotor drive for pursuit is subject to on-line gain control
(e.g., Schwartz and Lisberger 1994
), raising the
possibility that eye acceleration in the open-loop interval might be
influenced by this on-line gain control. For example, Lisberger
(1998)
proposed that weak presaccadic pursuit for target motion
away from the position of fixation might result primarily from a
failure to turn up the gain for visuomotor drive. We now analyze eye
velocity during the open-loop interval for target motion toward and
away from the position of fixation, to ask whether the cues affect the
gain of subsequent pursuit, as well as causing the smooth eye movements we have documented thus far.
Before analyzing the effect of the cue on subsequent pursuit, we developed a cue paradigm that minimized the size of the large cue-evoked smooth eye movements. Figure 9 shows the results of experiments that delivered, with equal probability, no cue, single cues that appeared left or right of the fixation target, or bilateral cues that appeared simultaneously on both sides of the fixation target. As before, each trial had a 200-ms gap between the offset of the fixation target and the appearance of the tracking target. Each graph shows the distribution of eye velocity measured from individual trials just before the normal initiation of pursuit for different cues. Bilateral cues (Fig. 9, A and B) evoked responses with a narrower distribution of eye velocities than would have been predicted by simply summing the distributions of responses to right and left cues (Fig. 9, C and D, filled and open histograms, respectively). However, the responses to bilateral cues remained considerably larger than eye velocity just before the onset of pursuit in trials without a cue (Fig. 9, E and F).
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The wider distribution of eye velocity in the bilateral cue trials than
in noncue trials might occur if separate responses to each cue were
summed or averaged. To test this possibility, we attempted to predict
the distribution of eye velocity in bilateral cue trials based on the
data obtained in unilateral cue trials using the following equations
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We next compared the eye acceleration evoked by target motion toward or away from the position of fixation in bilateral cue trials with that in no-cue trials. Because the cue-evoked smooth eye movements were often minimized in the bilateral cue trials, this comparison was not contaminated by the changes in the retinal image motion of the target that would occur if large cue-evoked smooth eye movements preceded the initiation of pursuit. To further improve the validity of this comparison, we selected for analysis only bilateral cue trials in which eye velocity just before the normal onset of pursuit was less than ±1.5°/s (the central 3 bins of the histograms in Fig. 9, A and B). Figure 10A illustrates average eye velocity for trials that provided rightward target motion in the same experiments used to create Fig. 9. These averages were made by eliminating the parts of the traces that corresponded to saccades and then by averaging eye velocity at each millisecond where data from 15 or more trials were available. Because saccades always occurred with relatively short and consistent latencies for target motion away from the position of fixation, this left a gap in the averages where almost all the saccades occurred. Because saccades were infrequent for target motion toward the position of fixation and had highly variable latencies, the traces lack any interruptions.
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Figure 10A reveals that the presaccadic eye movements of both monkeys KLB and NNK showed markedly higher eye accelerations in the wake of a bilateral cue (solid traces) than in the absence of a cue (dashed traces), when target motion was away from the position of fixation. In contrast, bilateral cues had relatively little effect on the presaccadic eye velocity for target motion toward the position of fixation. We quantified the changes in initial pursuit response by using the approach described in METHODS to measure presaccadic eye acceleration from traces of average eye velocity. Because of the tendency for early saccades in away trials, analysis of these averages were often based on intervals with durations shorter than 80 ms. In the averages of away trials in Fig. 10A, measurements were as follows: KLB bilateral cue 192o/s2 over 80 ms; KLB no cue, 111°/s2 over 80 ms; NNK bilateral cue, 161°/s2 over 42 ms; NNK no cue, 51°/s2 over 76 ms.
Figure 10B summarizes the effect of bilateral cues on the initiation of pursuit for toward and away trials in all the experiments we conducted on two monkeys. In each graph, the connected pairs of points compare the responses in bilateral cue trials with noncue trials for a given experimental session, and the left-hand and right-hand stacks of connected points show the responses to target motion away from and toward the position of fixation, respectively. Most of the pairs of points are connected by solid lines, indicating that at least 40 ms of data were available to measure eye acceleration. When delivered in the wake of a bilateral cue, target motion away from the position of fixation evoked responses that were consistently enhanced by comparison with those evoked by the same stimulus in a gap trial without a cue. This difference was statistically significant in each case (paired t-test, **P < 0.01, *P < 0.05). In contrast, the initiation of pursuit for target motion toward the position of fixation was not consistently affected by the presence or absence of bilateral cues. Note that the enhanced responses to target motion away from the position of fixation in the wake of a bilateral cue remained statistically smaller than the eye acceleration evoked by target motion toward the position of fixation (paired t-test, P < 0.01) except for one case (left pursuit of monkey KLB, P = 0.10).
Since both the initiation of pursuit has shorter latencies and higher
eye accelerations when the tracking target appears several hundred
milliseconds before its motion onset (Krauzlis and Lisberger 1994a), one might assume that the enhancement of pursuit
initiation in away pursuit trials resulted from the fact that one of
the bilateral cues appeared at the location where the tracking target started to move. We next asked whether the bilateral cue enhances the
pursuit initiation when the initial position of the tracking target is
different from the location of either cue. The experiment was carried
out in a dimly lit room, and the tracking target started to move from
the position of fixation without a gap between fixation target offset
and target onset. Figure 11,
A and B, shows the time courses of eye velocity
in those trials, and the inset of each panel shows the
distribution of eye velocity 80 ms after target motion in bilateral cue
trials. Again, only the trials with cue-evoked smooth eye velocity less
than ±1.5°/s (central 3 bins of each histogram) were included when
averaging eye velocity. In both examples illustrated in Fig. 11,
A and B, the initiation of pursuit was enhanced
in the wake of a bilateral cue (bold, solid traces), relative to the
responses in trials without cues (bold, dashed lines). Relative to the
responses to targets moving toward the position of fixation from 5°
eccentric (thin, dotted line), the enhanced responses to target motion
starting from the position of fixation had arguably lower eye
accelerations in this particular experiment.
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Figure 11, C and D, summarizes the data obtained by repeating this experiment four times in monkey KLB (C) and seven times in monkey NNK (D). Each trio of connected points compares the initial eye acceleration in trials that presented target motion starting from the position of fixation with or without bilateral cues, and those that presented target motion toward the position of fixation with no cue. For both monkeys (Fig. 11, C vs. D) and both rightward and leftward target motion (separate graphs in Fig. 11, C and D), the bilateral cues caused statistically significant enhancement of the initiation of pursuit for target motion starting from the position of fixation (paired t-test, P < 0.01). The cue-enhanced eye accelerations evoked by target motion that started from the position of fixation, however, were still smaller than those for target motion toward the position of fixation (paired t-test, P < 0.01 for 3 cases, P < 0.05 for 1 case).
The bilateral cue paradigms allowed us to examine the effects of the visual cue on the initiation of pursuit by minimizing the cue-evoked smooth eye movements. However, we thought it was also important to attempt analysis of the initiation of pursuit in the wake of single cues, in spite of the fact that these cues also evoked large smooth eye movements. Our strategy was to measure the pursuit response to a given combination of cue and target motion and then subtract the response to the cue alone (cf. Fig. 4, C and D) from the response to the same cue followed by target motion. The left columns of Fig. 12, A and B, superimpose average eye velocity for target motion with a cue (bold, solid traces), target motion without a cue (dashed traces), and for a cue without subsequent visual stimuli (fine, solid traces). The right columns of Fig. 12, A and B, superimpose the response to target motion without a cue (dashed trace) and the millisecond-by-millisecond subtraction of the response to the cue only from the response to the cue and the target motion. In the top two conditions for each monkey, which show away trials for monkey KLB (Fig. 12A) or "nonstep" trials for monkey NNK (Fig. 12B), the "difference" responses to target motion in the presence of a unilateral cue were consistently enhanced relative to the responses to target motion without a cue. As shown earlier in this paper for bilateral cues, the enhancement of pursuit initiation was inconsistent and smaller for target motion toward the position of fixation, and the main effect was a slight change in latency in monkey KLB.
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Figure 12 used a subtraction analysis to remove the cue-evoked smooth eye velocity before analyzing the response to the onset of target motion, but it failed to correct for the fact that the cue-evoked smooth eye movement also modifies the image motion that ultimately drives the initiation of pursuit. Examples from Fig. 12 show that the apparent enhancement is not due solely to the change in retinal image motion. For the right cues (2nd row of traces), the enhanced responses could be attributed to the increase in image motion caused by the leftward cue-evoked smooth eye movement during the initial period of rightward target motion. However, the opposite logic must then apply for left cues (1st row of traces); the rightward cue-evoked eye movement should decrease the image motion and decrease the eye acceleration at the initiation of rightward pursuit. Yet, the difference eye velocity responses show enhancement (bold lines in 2nd column of each panel). We therefore conclude that at least the effect of the cue in the first row of traces in Fig. 12, A and B, reflects enhancement of the initiation of pursuit.
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DISCUSSION |
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Novel form of smooth eye movement
It is accepted widely that visual motion is the main sensory
stimulus for the initiation of smooth pursuit. Most studies have found
that changes in target position during fixation do not initiate smooth
eye movements (Morris and Lisberger 1987;
Rashbass 1961
). When we altered the standard step-ramp
paradigm by incorporating a temporal gap between the offset of the
fixation target and the appearance of a moving tracking target, and by
training the monkeys to suppress a reflexive saccade toward an
extraneous visual "cue" during the gap, smooth eye movements away
from the stimulus were consistently evoked by the cue. The cue-evoked
eye movements had a latency comparable to or slightly longer than that
of normal smooth pursuit (~100 ms). The cue-evoked eye movements were
largest when the gap was 200-300 ms, the cue appeared 100-150 ms
before the onset of target motion, the cue was 5° eccentric from the position of fixation along the horizontal meridian, and the
experimental room was otherwise dark. We think that the use of a new
combination of task conditions enabled our discovery of a new form of
smooth eye movement that can be evoked without visual motion.
The cue-evoked smooth eye movements reported by Tanaka and
Fukushima (1997) and studied in detail here seem to be
different from anything reported previously by other authors. Smooth
eye movements without visual motion have been reported mostly in human subjects in situations where the direction of subsequent target motion
is highly predictable (Becker and Fuchs 1985
;
Boman and Hotson 1988
; Carl and Gellman
1987
; Kowler and Steinman 1979
). The
anticipatory eye movements found in previous studies generally preceded
the normal latency of pursuit and consisted of a gradual increase in
eye velocity in the direction of predicted target motion. In contrast,
the cue-evoked smooth eye movements reported in the present paper were
observed when the cue provided no predictable information about the
direction of subsequent target motion. In our experiments, the
cue-evoked smooth eye movements took the eyes in the wrong direction
for half of the subsequent target motions. Although the cue-evoked eye
movements were more compelling when the task involved preparation for
pursuit eye movement (Fig. 3, A and C), their
appearance during training with "away" target motion in
monkey PCK makes it impossible to explain their direction purely as trained anticipation that the target would move toward the
position of fixation (Fig. 4A). Other studies (Carl
and Gellman 1987
; Wyatt et al. 1989
)
have shown that human subjects initiate transient eye movements
toward the target step in step-ramp pursuit paradigms, in
contrast to the cue-evoked eye movements, which take the eyes
away from the position of a stationary cue. Further, the eye
movements evoked in previous step-ramp experiments have been rather
small (~1°/s), in contrast to the cue-evoked smooth eye movements
reported in the present paper, which often had peak velocity >5°/s.
The cue-evoked smooth eye movements also do not seem to form the basis
for two other features of pursuit that our laboratory has reported
previously. 1) Lisberger and Westbrook (1985)
reported an asymmetry in the initiation of pursuit that favored target motion toward the position of fixation. We do not think that the asymmetry can be understood as the addition of the cue-evoked eye
movement away from the position of the target to otherwise symmetrical
initiation of pursuit. The asymmetry of pursuit initiation persisted
even when the tracking target appeared eccentric and was stationary for
300 ms before starting to move, an interval long enough for any
cue-evoked smooth eye movement to die out. 2)
Krauzlis and Lisberger (1994a
,b
) suggested that three
types of visual motion signals contribute to pursuit initiation for a
step of target velocity: image velocity, image acceleration, and a
motion onset transient. The motion onset transient results from the
abrupt onset of image motion and makes a large contribution to the
initial ~40 ms of pursuit initiation. Two observations make it
unlikely that the cue-evoked smooth eye movements are related to the
motion onset transient. First, the direction of the cue-evoked smooth
eye movements was always away from the cue, whereas the direction of
the initial ~40 ms of pursuit initiation was the same as target
motion and was independent of initial target position (Lisberger
and Westbrook 1985
). Second, the latency of the cue-evoked
smooth eye movements (100-130 ms) was slightly longer than that of the
minimal pursuit latency observed in the away pursuit trials (80-90 ms).
Necessary and sufficient stimulus conditions for the cue-evoked smooth eye movement
The presence of a temporal gap between the offset of the fixation
spot and the appearance of the tracking target seems to be one
necessary condition for large cue-evoked smooth eye movements. The
importance of the temporal gap can be appreciated by comparison with
the results of experiments published by Krauzlis and Lisberger (1994a) where the tracking target appeared before its motion
onset, much as our cues do, but did not evoke a smooth eye movement. The gap that is necessary for expression of the cue-evoked smooth eye
movement parallels the necessary conditions for the short latency
"express saccades," which appear when the fixation target is
extinguished before the presentation of an eccentric, stationary target. It is known that a temporal gap releases fixation and/or attention systems that are engaged during fixation (Fischer
1987
). These systems appear to suppress the initiation of both
saccades and pursuit (e.g., Krauzlis and Miles 1996b
;
Morrow and Lamb 1996
), and might also suppress the
cue-evoked smooth eye movements during fixation. We suggest that the
release of fixation during the gap is necessary for the generation of
the cue-evoked smooth eye movement.
Preparation for pursuit eye movements seems to be a second necessary
condition for the cue-evoked smooth eye movements. The cue-evoked
smooth eye movements were attenuated when the animals initiated
saccades to stationary targets in a block of trials. The prior evidence
of the difference between neural substrates for saccades and pursuit
cause us to favor the idea that the preparation for pursuit is
different from the preparation for saccades. Cues might evoke smooth
eye movements through neuronal pathways for pursuit that are
facilitated when the monkey is preparing for pursuit. It would be
possible to develop theories based on a common participation of the
collicular fixation zone in small saccades and pursuit eye movements
(Basso et al. 1997; Krauzlis et al. 1997
), or smooth eye movements designed to counteract those
that might be evoked by the apparent motion at the time of fixation target offset and cue onset. Our data neither support nor refute these
possible explanations, and they will not be considered further.
Our data do not reveal whether the presence of a gap and preparation
for a pursuit movement are sufficient to enable the cue-evoked smooth
eye movement. For example, it may or may not be necessary to provide a
cue that looks different from the tracking target. The visual cue used
in this study was different in size or color from the moving target,
and it appeared at a location selected randomly with respect to the
initial position of the moving target. Unfortunately, it was essential
to make the cue and tracking target appear different so that the
monkeys could be trained not to make a saccade to the cue. In addition,
it may prove critical that the stimulus configuration forced monkeys to
select the visual stimuli and to make much effort not to respond to the
visual cue. We cannot exclude the possibility that our stimulus
configuration requires voluntary processes to suppress a reflexive
saccade toward the cue, and that these processes in the saccadic and/or
fixation systems might be related to the cue-evoked eye movement. It
has been shown recently that the saccade motor commands increase the gain of pursuit initiation for a step of target velocity
(Lisberger 1998; Ogawa and Fujita 1998
;
Yang et al. 1999
). Perhaps the cue evokes covert saccade
commands that are sufficient to activate the pursuit system and cause
both the transient smooth eye movements and the enhancement of pursuit
initiation for targets moving away from the position of fixation. Given
the absence of neural recordings related to the cue, we choose not to
speculate further about the neural substrate of the cue-evoked smooth
eye movement.
Possible relationship of the cue-evoked smooth eye movement to the pursuit gain control
Several of the recent papers from our laboratory have presented
data related to the existence and properties of an on-line gain control
for pursuit. The clearest evidence for on-line gain control comes from
experiments showing that larger smooth eye movements are evoked by a
given brief image motion if the motion occurs during pursuit versus
during fixation (Goldreich et al. 1992; Schwartz
and Lisberger 1994
). A more recent analysis of the postsaccadic
enhancement of visuomotor drive for pursuit (Lisberger 1998
) has revealed a potential toward/away asymmetry in the
gain controller that may be related to the directional bias of the cue-evoked smooth eye movements analyzed in the present paper. We
elaborate below.
Analysis of presaccadic pursuit has revealed that the initial eye
acceleration depends on the eccentricity of the moving target and on
whether it is moving toward or away from the position of fixation
(Lisberger and Westbrook 1985). Initial eye acceleration decreases as a function of increases in target eccentricity, and eye
acceleration is larger for target motion toward than for target motion
away from the position of fixation for targets moving across a given
eccentricity. Analysis of postsaccadic eye velocity yields a completely
different picture. Neither the initial target position nor the
direction of target motion relative to the position of fixation had
strong effects on postsaccadic eye velocity (Lisberger 1998
; Ogawa and Fujita 1998
). Because the eye
movements immediately after saccades are driven by visual inputs
present before the saccades (Newsome et al. 1985
), the
lack of a positional or directional bias in postsaccadic eye velocity
renders it unlikely that visuomotor drive for pursuit is biased for
either target eccentricity or the direction of target motion.
Lisberger (1998) interpreted these data in the context
of the pursuit gain control. He suggested that presaccadic pursuit has
a toward/away asymmetry and positional dependence because the
controller of pursuit gain has these features. The degree of activation
of the gain control, and the "gain" of the presaccadic initiation
of pursuit would then depend on whether the target was moving toward or
away from the position of fixation and on the eccentricity of the
moving target. He accounted for the lack of asymmetry or positional
dependence of postsaccadic eye velocity by the suggestion that
postsaccadic enhancement was implemented by turning up the pursuit gain
control. In accordance with this hypothesis, we propose that the cue
used in the present experiments also turns up the pursuit gain control.
We suggest that sudden changes in the value of the gain control cause,
as a side effect, a command for a blip of eye velocity that is biased
by the inherent toward/away asymmetry of the gain controller. In the
absence of a fixation or tracking target under conditions of
preparation for pursuit, the internal signal causes a cue-evoked blip
of eye velocity away from the cue.
Our explanation for the cue-evoked smooth eye movement is supported by
the finding that the relationship between its size and the eccentricity
of the cue is very similar to the relationship suggested by
Lisberger (1998) between the eccentricity of the pursuit
target and the degree of presaccadic activation of the gain control.
Further, our finding of enhancement of the initiation of pursuit for
target motion away from the position of fixation in the wake of
bilateral cues is entirely consistent with this interpretation. We
suggest that bilateral cues turn up the pursuit gain control, allowing
enhancement of the initiation of pursuit while the two cue-evoked
smooth eye movements in opposite directions average to a mean response
amplitude near zero. The absence of enhancement of the initiation of
pursuit for target motion toward the position of fixation would be
expected if pursuit gain is already maximal for target motion toward
the position of fixation.
Separate control of the pursuit gain and visuomotor drive
Figure 13 shows a conceptual model
of pursuit that includes two separate pathways for controlling
visuomotor drive and pursuit gain. The basic structure of this model is
essentially the same as the ones proposed previously (Grasse and
Lisberger 1992; Krauzlis and Lisberger 1994b
;
Krauzlis and Miles 1996a
). In keeping with the
suggestions of Lisberger (1998)
, we assume that
visuomotor drive processes its inputs in retinal coordinates, in a way
that is independent of target eccentricity. In contrast, the gain of pursuit is controlled by a combination of retinal and extra-retinal signals. To account for the dependence of presaccadic pursuit on target
eccentricity, and for the toward/away asymmetries in the responses to
both moving targets and stationary cues, we suggest that the inputs to
the gain controller are strongly dependent on target eccentricity,
favoring stimuli moving toward the fovea. We also suggest that the gain
controller receives extra-retinal inputs related at least to saccades,
selective attention, and anticipation. We postulate that a sudden
increase in pursuit gain cause a small smooth eye movement in the
direction of the inherent bias of the gain controller, and that this
eye movement is responsible for the cue-evoked smooth eye movements we
have recorded in highly trained monkeys.
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One curious aspect of the proposal outlined above is the fact that the
latency of pursuit is shorter than the latency of the cue-evoked smooth
eye movement, at least for target motion away from the position of
fixation. If the latter response is a side effect of activating the
pursuit gain controller, why does it not have a shorter latency?
Perhaps the earliest part of the initiation of pursuit reflects a
strong visuomotor drive that is attenuated by the fact that pursuit
gain has not yet been increased. This proposal is compatible with the
observation that many neurons in the middle temporal area have
large transients at the onset of motion (Lisberger and Movshon
1999), since we would expect these transients to drive eye
acceleration powerfully if pursuit gain had been increased. It is also
compatible with the finding that eye acceleration in the first ~40 ms
of pursuit is independent of target eccentricity, while eye
acceleration 40-100 ms after the initiation of pursuit assumes the
position dependence (Lisberger and Westbrook 1985
) that
we have tentatively attributed to different levels of the pursuit gain
control. We realize that the scenario outlined in Fig. 13 is highly
speculative. Yet, it is compatible with available data, and we propose
it with the expectation that future physiological experiments will
provide critical tests.
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ACKNOWLEDGMENTS |
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We are grateful to Drs. K. Fukushima and C.R.S. Kaneko for support and helpful discussion during the earlier part of this study. We also thank H. Rambold, I. Chou, and J. Gardner for valuable comments on the manuscript.
This research was supported by the Howard Hughes Medical Institute, of which S. G. Lisberger is an Investigator and M. Tanaka is an Associate.
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FOOTNOTES |
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Address for reprint requests: M. Tanaka, Dept. of Physiology, 513 Parnassus Ave., Rm. S-762, University of California, San Francisco, CA 94143-0444 (E-mail: masaki{at}phy.ucsf.edu).
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Received 6 December 1999; accepted in final form 31 May 2000.
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REFERENCES |
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