Effect of Stimulus Position and Velocity Upon the Maintenance of Smooth Pursuit Eye Velocity MARK A

Vkon Res. Vol. 34, No. 18, pp. 2477-24X2, 1994 0042-6989(94)EOO25-6 Elsevier Science Ltd. Printed in Great Bntam

Effect of Stimulus Position and Velocity Upon the Maintenance of Smooth Pursuit Eye Velocity MARK A. SEGRAVES,*t MICHAEL E. GOLDBERG*

Received 19 August 1993; in reoised form 28 January 1994

The relative contributions of retinal slip velocity and position errors to the generation of smooth pursuit eye movements were examined in three rhesus monkeys. Recognizing the unlikelihood of producing a pure retinal slip velocity or position error signal, these two stimulus parameters were combined under open-loop conditions. Both slip velocity and position error were used by the monkey to maintain an established eye velocity. Both parameters had the greatest effects upon eye velocity when they were in the same direction, enabling the monkey to maintain an established pursuit velocity. When slip velocity and position error were in the direction opposite to the initial pursuit, eye velocity reversed direction and moved very quickly towards zero. When the two parameters were in opposite directions, their effect upon eye velocity was minimized.

Oculomotor Smooth pursuit Eye movements Macaca mulatta

INTRODUCTION target movement system is never perfect. As a result, target motion during saccades may lag retinal move- Smooth pursuit eye movements minimize visual target ment, resulting in brief movements of the target on the movement on the retina by matching eye movements to retina. This introduction of retinal slip velocities con- target motion in space. Both target motion on the retina founds the interpretation of how the pursuit system (retinal slip) and position offset of the target from the responds to positional offsets. The following experiments fovea might drive smooth pursuit movements, and there were designed to examine the contributions of retinal slip is evidence that the smooth pursuit system responds to and position offset to the generation of pursuit each of these stimulus parameters (Robinson, 1965; Pola movements, not by attempting to produce stimuli with & Wyatt, 1980; Morris & Lisberger, 1987). In the purely motion or positional components, but by combin- laboratory, one can easily produce and monitor changes ing the two stimulus parameters in both agonistic and in retinal slip, demonstrating the pursuit system’s antagonistic ways and examining the pursuit system’s response to motion of targets on the retina. However, it response to targets whose direction of motion implied by has been more difficult to study the effect of position retinal slip was sometimes the same and sometimes offset on pursuit. One common technique is to stabilize opposite to the direction implied by position offset from the location of a visual target on the retina by continu- the fovea. A preliminary report of these experiments has ally adding a measure of eye position to target position been published elsewhere (Segraves & Goldberg, 1988). (Pola & Wyatt, 1980; Morris & Lisberger, 1987; Segraves, Goldberg, Deng, Bruce, Ungerleider & Mishkin, 1987). In this way, when the eye moves, the MATERIALS AND METHODS target moves with it, and its position will, ideally, remain Pre-operative training fixed on the retina. In this experimental situation, the subject frequently makes saccades in an attempt to Three adult rhesus monkeys (Macaca mulatta) were foveate the target. Unfortunately, the response of the trained preoperatively to do a simple visual fixation task using established techniques (Wurtz, 1969). The monkey was seated in a primate chair, and began a trial by pressing a metal bar in front of him. This resulted in the *Laboratory of Sensorimotor Research, National Eye Institute, onset of a target light on a screen in front of the monkey. National Institutes of Health, Bethesda, MD 20892, U.S.A. The monkey was required to detect the dimming of the TDepartment of Neurobiology and Physiology, 0. T. Hogan Hall, Northwestern Univeristy, Evanston, IL 60208-3520, U.S.A. [Email light, and signal this detection by releasing the metal bar M-Segraves(a nwu.edu]. to receive a liquid reward. 2417 2418 MARK A. SEGRAVES and MICHAEL E. GOLDBERG

Surgery, feedback signal of the mirror galvanometer. Both Surgery was performed under aseptic conditions. The horizontal and vertical eye and mirror position were monkey was anesthetized with ketamine hydrochloride sampled at a rate of I kHz. (10 mg/kg i.m.) followed by sodium pentobarbital to Behavioral trials used for this study began with the effect and supplemented through an i.v. catheter as monkey pursuing a target moving horizontally at needed. During the surgical procedure, a subconjuncti- 10 -2Odeg/sec. At an unpredictable time the target val wire coil for the measurement of eye position with the jumped to a position calculated by adding a step ranging magnetic search coil technique was implanted in one eye from - 3 to + 3 deg to eye position. Thereafter, each (Judge, Richmond & Chu, 1980; Robinson, 1963). Two millisecond, target position was calculated by adding an to three trephine holes were made through the skull at amount to eye position sufficient to provide the target sites where recording cylinders would be located. with a retinal slip velocity of - 2 to + 2 deg/sec. The net Recording cylinders were used in neurophysiological effect being that the target was stepped to a location near experiments performed after the behavioral experiments the fovea and then began to move slowly towards or described in this report. Small s inless steel bolts to away from it. Because the monkeys were rewarded for maintaining eye position within a window surrounding strengthen the bond of dental acrP lit to the skull were fastened in slots cut through the skull and extending the target, a criteria that was always met in open-loop away from the edges of the trephine holes. The recording trials, open-loop trials were intermixed as needed with cylinders, a stainless steel receptacle to fix the monkey’s closed-loop trials to maintain the monkeys’ perform- head during recording sessions, and the connector for ance. The initial starting point of the target was adjusted, the eye coil were fixed in place and bonded to the skull so that stabilization would occur at about the time when with dental acrylic. At the completion of surgery, the the eyes were crossing the primary position. Figure 1 monkey was given the analgesic pentazocine (Talwin, illustrates the correspondence between horizontal eye 1.5-3 mg/kg) to relieve pain. Gentamicin sulfate and target position when eye position feedback is used (5 mg/kg i.m.) was given immediately after surgery and to stabilized the target on the retina. For purpose of in daily dosages for 1 week post-operatively as a prophy- illustration, a 2deg rightward position offset was lactic measure against infection. Post-operative training subtracted from the target trace so that it could be was begun between If and 2 weeks after surgery. superimposed on the eye trace. No intentional retinal slip velocity was introduced during this trial. Note that during the saccade in the middle of the figure, target Post-operatice rraining position lags behind eye position. This lag in the ability After surgery, each monkey received additional train- of the mirror galvonometer to update target position ing in several visual and eye movement tasks. The produces an initial leftward deceleration of the target as computer hardware and software used to monitor and the eye moves toward the target during the saccade control the monkey’s behaviour has been described in followed by rightward acceleration as the target moves detail elsewhere (Goldberg, 1983). The monkey was further ahead of the eye near the end of the saccade. seated in a primate chair with its head fixed, and centered within horizontal and vertical magnetic field coils. Visual sitmuli presented to the monkey included stationary and b_ moveable light stimuli originating from red light- emitting diodes rear-projected onto a tangent screen 86 cm in front of the monkey. Each projected stimulus was about 0.25 deg in diameter with a brightness 1.4 log units above a background of 0.18 cd/m2. The moveable stimulus was positioned by a pair of servo-controlled mirror galvanometers (General Scanner Inc.) driven by analog signals synthesized by 12 bit digital to analog converters under the control of a PDP 1l/73 computer (Digital Equipment Co.). Stimulus position was updated t I at a rate of 1 kHz. Since, after surgery, it was possible 0 10 20 30 40 50 60 70 mJm Time to accurately measure eye position, the monkey was no longer required to detect the dimming of the stimulus. FIGURE I. Target lag hing saccaaks to stabilized images. To Instead, the monkey had to meet predetermined criteria facilitate the comparison, target position has been superimposed upon for eye position relative to target position, and for eye position by shifting the target’s location 2 deg to the left. Although the eye never catches up to the target, the lag in target position results saccade amplitude and direction in order to receive a in an initial backward movement of the target toward the fovea at the liquid reward. Eye position was measured by the beginning of the saccade followed by a forward movement of the target magnetic search coil system (C.N.C. Engineering) using away from the fovea near the end of the saccade. The lag in target a phase-sensitive detector. Eye position measurement position behind eye position during a rightward saccade results in a brief leftward movement of the target on the retina. This and all was accurate to 15 min arc within a range of 20 deg from subsequent figures use the convention that movement to the right is the center of gaze, and was not corrected for cosine plotted upward and positive, and movement to the left is plotted error. Mirror position was measured from the position downward and negative. SMOOTH PURSUIT EYE VELOCITY 2479

RESULTS

Four examples of single trials with diRerent combinations of position error and retina1 slip velocity are illustrated in Fig. 3. In each of these trials, the monkey began by tracking a target moving to the right at 10 deg/sec. At time zero, the target was stabilized with position error of +2 deg, and a retinal slip velocity of i-2 deg/sec was introduced. The initial rightward track- 1 I I ing velocity was affected least when the position error -200 0 200 400 ms and retina1 slip velocity were also directed to the right [Fig. 3(A)]. The greatest decrement in velocity occurred when both position error and retinal slip velocity were B in the direction opposite to the initial tracking velocity 3 [Fig. 3(D)]. With position error to the right and a c Velocity (‘ls) I I leftward slip velocity [Fig. 3(B)], the initial tracking velocity was maintained for about 300 msec. At this point, the retinal slip velocity appeared to become the more salient stimulus, causing eye velocity to reverse, and begin moving to the left. Note that for the first 1000 msec, the monkey was pursuing a target that was drifting towards the fovea. From approximately the 500msec time-mark onward, the monkey generated leftward pursuit to a target that was actually moving -200 ;, 200 400 ms towards the fovea until about 100 msec after stabiliz- Time ation. With a leftward position error and slip velocity to the right [Fig. 3(C)], eye velocity slowed to near zero and FIGURE 2. Measuring eye a&wit.): ZOOmser affer the start oftarget then began to accelerate towards the right at about stabilization. (A) Using acceleration criteria, data analysis software 500 msec, following the direction of the retinal slip. As placed vertical cursors at the beginning and end of the first saccadic velocity profile occurring after the target was stabilized. The position was the case for Fig. 3(B), the eyes were moving of these cursors could also be adjusted manually by the investigator. rightward before the rightward moving target crossed The saccadic velocity was then deleted by drawing a straight line the fovea. between the two cursors. (B) First vertical cursor on the velocity trace We used both instantaneous velocity 200msec after marks the beginning of target stabilization. Second and third vertical stabilization and mean velocity in the interval from 200 cursors mark points 200 and 225 msec after target stabilization. Pursuit velocity was measured at the 200msec point, and mean to 225 msec after the beginning of stabilization as a pursuit velocity was computed for the interval between 200 and parameter to indicate the effect of target position and 225 msec. For Figs 2 and 3, the y-axis calibration for eye velocity on smooth pursuit. Figure 4 illustrates the effect velocity (degjsec) is identical to the calibration for eye and target of changing position error for three different retinal slip position (deg). velocities. For these trials, the monkey was pursuing to the left at 20 deg/sec. For retinal slip velocities of 0 deg and 2 deg left or right, position error in the on-direction (- 1 to - 3 deg) increases pursuit velocity to as much as DATA ANALYSIS 40 deg/sec for a combination of 2 deg/sec leftward slip velocity with a 2 deg leftward position error. Position Eye velocities were calculated using a 51 component error in the off-direction (+ I to +3 deg) decreased finite impulse response differentiating digital filter with a pursuit velocity. Increasing position error increased the 3 dB roll-off at 9 Hz. The filter did not induce a phase effect upon velocity for both directions, with the lag but broadened velocity peaks. exception that -3 deg was less effective in increasing To assess the effect of different combinations of leftward eye velocity than was -2 deg. position offsets and retinal slip velocities upon pursuit In a similar series of data taken from a different maintenance, pursuit velocities were sampled at monkey, a combination of righward slip velocity and 200 msec after target stabilization. Since saccades often position error enabled the monkey to maintain a occurred during this interval, saccadic velocities were rightward pursuit velocity (top half of Fig. 5). All other removed during the time period following target stabiliz- combinations of slip velocity and position error resulted ation (Fig. 2). Saccades were located by computer using in decreases from the initial rightward velocity. an acceleration criterion, and confirmed by one of the Combining leftward slip velocity with leftward position investigators. Eye velocity attrributable to the saccade error caused eye velocity to approach Odeg/sec. For was then removed from the record by linear extrapol- initial pursuit towards the left (bottom half of Fig. 5), ation between points on the velocity trace before and leftward position error combined with leftward slip after the saccade. velocity evoked pursuit velocities that were greater than 2480 MARK A. SEGRAVES and MICHAEL E. GOLDBERG

A Position ermr 2’ light B Position error 2’ right Retinal slipvelocity 2+/s ri,@ward Retinalslip velocity 2’/s lefnvard

k3 0 400 800 12OOms 0 400 800 12OOms :g

D PcmitionemrZ’kft Retinal slip velocity 2-h kfhwd

0400800 12OOmS 0 400 800 12OOms Tune

FIGURE 3. Examples of single trials where position errors and slip velocities were inrroduced while rhe monkey was (racking IO the righf ar fO&g/sec. Target stabilization and retinal slip velocities were introduced at time 0. When initial position error and slip velocity were in the same direction (A, D), the position error increased. When initial position error and slip velocity were in opposite directions (B, C), position error decreased, with the target moving towards and eventually crossing the fovea.

the initial velocity. Rightward slip velocities in DIXXSSION combination with leftward position error enabled the In these experiments we sought to estabiish the contri- monkey to maintain velocity near the initial level. A bution of position error to the monkey smooth pursuit combination of rightward slip velocity with rightward system. Because humans can generate smooth pursuit position error brought eye velocity to a level near eye movements in response to an extrafoveal afterimage, 0 deg/sec. We noted the same effects when we examined target position error itself must be able to sustain and the instantaneous velocity 200 msec after image initiate pursuit (Heywood & Churcher, 197 1). Monkeys, stabilization. however, do not initiate pursuit to an extrafoveally stabilized image (Morris & Lisberger, 1987). We have established that the velocity of maintained smooth pursuit can be affected by a stabilized position error. Recognizing the technical problems encountered in producing a purely position error stimulus, we have incorporated both position errors and retinal slip velocities into our stimuli. This enabled us to compare the effects of different combinations of position error and slip velocity upon the maintenance of smooth pursuit velocity. It should be noted that both stimulus -__.-.- .-._-- ..--.----._ . .._.- .._._._.._-..- parameters were present in every trial using image stabilization, including trials when the nominal values for position error and retinal slip velocity were zero. When position error was zero at the start of image stabilization, retinal slip produced its own position offset from the fovea. When retinal slip velocity was zero at the start of image stabilization, lag of the stimuius movement system during saccades resulted in transient retinal slip velocities (Fig. 1). By comparing the effects of 1 I -3 -2 -1 0 1 2 3’ different combinations of position error and slip vel- Position Error ocity, it is clear that the monkey smooth pursuit system uses both parameters for the generation of smooth FIGURE 4. The effect of target position on eye velocily. Position error pursuit eye veIocity. These two parameters make inde- was varied in 1 deg intervals from 3 deg left to 3 deg right for slip velocities of 2 deg left, 0, or 2 deg right. At the time that the target was pendent contributions to the maintenance of smooth stabilized, the monkey was tracking to the left at 20 dcg/scc (horizontal pursuit velocity. Combinations of slip velocity and pos- dotted line). Vertical bars indicate the SEM. ition error mitigated each other’s effect when they were SMOOTH PURSUIT EYE VELOCITY ‘48 1

Initial Target Velocity Position Error Initial Target Velocity Slip Velocity lo-/S lightward IO-/s rightward _..= . 2’ right ?!h right

103 leftward 2’ left - ,“.. 0 ,“,X ....(.Y,, ...... ((,,..,M

I I I I I I -2 2”lS -2 2’ Slip Vtdocity Position Error

FIGURE 5. Mean pursuit l~el[/~jf~ 20&225msec qfier ~e~i~~in~ of tarp-t slffb~li~~tjo}z. (A) Effect of changing slip velocity between 2 deg left, 0, or 2 deg right with initial position error held constant at 2 deg left or right. Changes in slip velocity towards the right cause increases in pursuit velocity towards the right. (B) Effect of changing position error from 2 deg left to 2 deg right with slip velocity held constant. Position errors towards the right move velocity towards the right. For both (A) and (B), uppertraces are with initial tracking direction to the right and lower traces with initial tracking direction to the left at IO degisec (horizontal dotted lines). Vertical bars indicate the SEM. of opposite sign, and produced the most substantial the presence of saccades had little influence upon the effects upon velocity when they were of the same sign. pursuit eye movements the monkeys made in our exper- Background movement during pursuit is an additional iments. Trial to trial variation in the pattern of saccades signal that has been identified as contributing to the generated did not appear to affect pursuit eye move- maintenance of pursuit (Pola & Wyatt, 1989). However, ments, and very different pursuit movements were made our ability to reverse the direction of pursuit velocity by in the presence of nearly identicat sequences of saccades changing the sign of position error and slip velocity [cf. Fig. 3(A) and (B)]. indicates that these parameters can overcome the influ- Our findings concerning the importance of position ence of background motion. One possible confounding error in the generation of pursuit velocity are in agree- issue is that the act of stabilization at a given position ment with previous reports for both humans (Pola & error involves a target step. Robinson, Gordon and Wyatt. 1980: Carl & Gellman. 1987) and monkeys Gordon (1986) have proposed that the initial step in (Morris & Lisberger, 1987). The present results demon- position of the stimulus when it is stabilized produces a strate that position errors twice the size of those em- signal that is interpreted to be a velocity signal, as in the ployed by Morris and Lisberger (1987) can be effective phi phenomenon. This target step might be construed by in maintaining pursuit velocityr. It should be emphasized the cortical motion detection system as a velocity pulse that our findings pertain to the maintenance of an (Mikami, Newsome & Wurtz, 1986). However, if this existing smooth pursuit velocity. The present findings were the only effect of the position error we would expect are also in agreement with models of the smooth pursuit the effect to be transient, but instead it was quite system that include retinal slip velocity and position sustained. In fact, it has been shown that the human error as inputs used for the maintenance of pursuit response to a target step is very brief, beginning about velocity (Lisberger, Morris & Tychsen, 1987). Future 100 msec after the step and ending about 100 msec later experimental studies and models of the smooth pursuit (Carl & Gellman, 1987). Another potential flaw is the system must account both for retinal slip velocity and presence of saccades during the period of image stabiliz- position error as the visual inputs to the smooth pursuit ation. This also could only have a transient influence. As system. illustrated in Fig. 1, target movement lags that of the eye during saccades producing retinal slip, however the resultant signal is ambiguous since equivalent REFERENCES movements both toward and away from the fovea are fari. J. R. & Geilman. R. S. (1987). Human smooth pursuit: Stimuius- produced. Several additionai observations suggest that dependent responses. J~urnuf of Nuurc~phvsir,lo~~,,57. 1446 1463. 24x2 MARK A. SEGRAVES and MICHAEL E. GOLDBERG

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