209

J. Physiol. (1978), 285, pp. 209-229 With 11 text-figures Printed in Great Britain

SACCADIC, SMOOTH PURSUIT, AND OPTOKINETIC EYE MOVEMENTS OF THE TRAINED CAT

BY C. EVINGER AND A. F. FUCHS From the Department of Physiology and Biophysics, and the Regional Primate Research Center, University of Washington, Seattle, Washington 98195, U.S.A.

(Received 3 January 1978) SUMMARY

1. Cats were trained to track a small target by rewarding them for keeping their eyes on target. Eye movements were measured by the electromagnetic search coil technique. 2. Cat saccades are qualitatively similar to primate saccades, but exhibit more variability in their parameters. However, they have longer durations and lower maximum velocities than primate saccades. As in the monkey, the duration of the horizontal or vertical component of an oblique saccade is lengthened when the orthogonal component has a larger amplitude. Cat saccades can be modified in midflight like human saccades. Opening the visual feed-back loop by controlling target position with eye position causes the cat to execute a staircase of equal amplitude saccades if a retinal error is present. Increasing the amount of visual feed-back induces saccadic oscillations. 3. Horizontal smooth pursuit of a 0 5 deg visual target is limited to velocities of less than 1 deg/sec. However, moving an optokinetic background with the 0 5 deg target enables the cat to achieve higher horizontal smooth eye velocities of up to 8-5 deg/sec. Prolonged (10-20 sec) constant velocity rotation of an optokinetic drum evokes horizontal slow-phase velocities of up to 28 deg/sec. In response to vertical movements of the target and optokinetic background, smooth eye movements reached 6 deg/sec maximum upward velocities but only 2-5 deg/sec maximum downward velocities. Opening the feed-back loop with no retinal error present causes the eye to exhibit a growing smooth trajectory. The response to a Rashbass step-ramp target suggests that the feline smooth response is a function of target movement rather than displacement. 4. These data suggest that cat saccadic eye movements resemble those of primates while the cat smooth pursuit and optokinetically induced eye movements are more similar to those of the rabbit. INTRODUCTION

In the past 5 years there have been significant advances in our understanding of the pathways and connexions of the cat oculomotor system. Physiological studies have described the vestibular inputs to the oculomotor nuclei and cerebellar influences on these pathways. In addition, the connexions from potential premotor

C. EVINGER AND A. F. FUCHS areas including the superior colliculus, the interstitial nucleus of Cajal, the nucleus prepositus hypoglossi, and the pontine reticular formation to the oculomotor nuclei have been explored. Finally, recent studies have demonstrated interneurons connecting the abducens and oculomotor nuclei (for review see Baker & Berthoz, 1977). However, comparatively little is known about the functional role of these pathways in the alert animal. At the same time, investigators using the alert monkey have recorded from neurones whose discharge patterns are correlated with eye movements. These studies have, however, provided little information about the pathways and connexions creating the various discharge patterns. Thus, it is tempting to use the pathway data from the anaesthetized cat to account for the discharge patterns found in the awake monkey. A critical factor in assessing the validity of such a comparison is the similarity of cat and monkey eye movements. Monkey saccadic and smoothpursuit capabilities have been fully documented with trained animals (Fuchs, 1967; Barmack, 1970a, b). However, only data on spontaneous saccades (Stryker & Blakemore, 1972; Crommelinck & Roucoux, 1976) and the response to optokinetic drum rotation (Honrubia, Scott & Ward, 1967; Collins, Schroeder, Rice, Mertens & Kranz, 1970) are available for the cat. Since these data were collected on untrained cats, whose level of altertness and motivation may have played an important role in the results, available data on cat eye movements are difficult to compare with monkey data. In addition, no published data exist on the cat's ability to follow the smooth movement of small targets. Therefore, we have trained cats to track such a target, enabling us to obtain data that are directly comparable with results in monkeys (Fuchs, 1967; Barmack, 1970a, b; Lisberger et al. in preparation). 210

METHODS

Control of 8timulUs movement The visual target was a 0 5 deg circular spot of light projected onto a tangent screen 57 cm from the cat subtending 70 by 50 deg. The target was presented alone or with a background consisting of a 55 deg wide field of vertically oriented black and white stripes (0-6 cycle/deg). The striped background was interrupted by a single horizontal black strip (5 deg wide) on which the visual target was centred to eliminate any confusion concerning target position. The target and background were superimposed by a beam splitter and the combined image was reflected off a pair of galvanometer mirrors (CCX100; General Scanning, Inc.). Movements of the target on the screen were caused by driving the mirrors with a function generator or a computer (Raytheon 704). Horizontal optokinetic nystagmus was induced by rotating a striped drum which surrounded the cat at velocities of 4-5-60 deg/sec. The drum contained eight black stripes (6 deg) evenly spaced on a white background. Two large mirrors, one above and one below the eyes, increased the effective size of the optokinetic nystagmus stimulus to cover the cat's entire visual field. The light level was 260 cd/M2.

Eye movement measurement Eye position was monitored with a scleral search coil technique (Robinson, 1963). Under general anaesthesia, the coil was implanted under the insertions of the four rectus muscles of the left eye of two cats (Fuchs & Robinson, 1966). Placing the animal in two alternating magnetic fields in spatial and temporal quadrature induced a current that could be electronically decomposed into voltages proportional to horizontal and vertical eye position. The system was sensitive to eye movements as small as 15 min arc and had a bandwidth of 330 Hz.

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Eye movements were measured relative to a stationary head, which was fixed in the centre of the magnetic field. The head was held by using three dental acrylic lugs implanted in the skull as the sockets for a three-point ball and socket system (Fuchs & Luschei, 1970). To confine the cat's body movements when his head was stabilized, we placed his body in a closely fitting bag, and then put the bag in a rigid cylinder 15 cm in diameter. After several training sessions the cats participated willingly in this procedure, voluntarily climbing into the bag and waiting for the experimenter to zip it up. The cats exhibited no evidence of discomfort and performed the behavioural task for as long as 3-5 hr without vocalizing or struggling.

Eye movement training An initial calibration of the eye coil (accurate within + 3 deg) was achieved by bringing a spoon with beef baby food into the cat's visual field at different points on a perimeter. Using this initial calibration, we electronically compared voltages corresponding to the eye and target position (Fuchs, 1967). If eye position was held within 2 deg of target position for a fixed period, the cat was rewarded with 2 ml. of a mixture of beef baby food and water. During an average training session, cats earned 200-300 g of food. After the training session, this was supplemented with 60 % (72 g) of the normal dry food ration (Purina Cat Chow) as well as water ad lib. Under this regimen both cats gained weight over the course of the experiments. The cat began the training procedures under conditions that permitted frequent and easily obtained reinforcement and was gradually introduced to more rigid behavioural requirements. Initially the animal was presented with a 10 deg diameter target and was required to fixate for only 0-6 sec before being reinforced. The target was moved frequently to different positions on the screen, so that the cat learned to fixate the target rather than associate reinforcement with a fixed eye position. To aid the cat, two different tones signaled the behavioural contingencies. One sounded continuously when the cat was within 2 deg of the target and the second sounded with the reinforcement. After one or two training sessions lasting 1 hr, the target size was gradually reduced to 0 5 deg and the required fixation time was increased to 3-8 sec, allowing the accuracy of the calibration to be increased to ± 1 deg. To avoid penalizing the cat for his natural reaction time, the timing circuitry was activated only 250 msec after a target step. By the second training session the cats usually tracked targets that moved with a stepwise, ramp, or sinusoidal trajectory. However, the training sessions continued for another 10 days to assure reliable performance over a 2-5 hr period. Data collection and analysis Horizontal and vertical eye position and target position were stored on magnetic tape (Honeywell model 7600, DC -1 kHz, -3 db). For hand analysis, data were written out on a direct writing ultra-violet recorder (Bell and Howell Datagraph model 5-134, DC -1 klz, -3 db). Saccades were usually analysed with the help of the computer. Signals proportional to horizontal eye, vertical eye, and target positions were digitized, each signal being sampled at 830 Hz. The digitized data were scrolled in a continuous sequence on a storage oscilloscope, which cleared after each sweep. Any single sweep could be halted to select a saccade for analysis. The experimenter used a cursor to point out the beginning and end of the horizontal and vertical components of the saccade along with the maximum horizontal and vertical eye velocity from a digital, smoothed derivative of eye position. The computer then calculated and stored on digital tape the horizontal and vertical amplitudes, durations, maximum eye velocities, and eye position components preceding the saccade as well as the saccade's polar amplitude and direction. Eye movements made in response to sinusoidal target motion were also analysed by computer. Horizontal eye and target positions were digitized, with each variable sampled at I kHz. Each cycle was divided into 64 equal time bins and the target and eye positions were displayed on the storage oscilloscope. A joystick-controlled cursor was used to point out the beginning and end of corrective saccades and the computer calculated the cumulative eye position (after Meiry, 1965) by replacing the saccades with smooth eye movements with velocities appropriate to those present just before and immediately after the saccade. After at least 10 cycles were collected, the eye and target positions were averaged and subjected to Fourier analysis. The Fourier analysis of averaged cycles of target and eye position revealed a mean harmonic distortion (to the 10th harmonic) of 1-5 % for target position and 12-7 % for eye position over the

212

C. EVINGER AND A. F. FUCHS

target amplitudes and frequencies tested. Therefore, the fundamental components of eye and target position were used to compute the gain (ratio of eye amplitude to target amplitude) and phase shift of the eye relative to target amplitude. Since hand analysis of the raw data differed by no more than 2 deg in phase and 6 % in gain from the computer analysis of data, the distortion did not contribute a significant error to the computer determination of either gain or phase.

RESULTS

Saccade8 A sudden displacement of the target (a 'target-step') reliably elicited shortlatency saccades (Fig. 1 A-C). When the first saccade failed to reach the target, the cat made a second corrective saccade (Fig. 1A, B). Thp short-latency but accurate eye movements in response to target steps demonstrate that the training generated well controlled behaviour. The mean latency of saccades in response to target steps of randomly varied amplitude presented at random intervals was 256 msec (182 saccades ranging from 2 to 20 deg from both cats, Fig. 2). In cats, most saccades of equal size have similar time courses, although their duration is more variable than in primates. For example, the 20 deg rightward saccade in Fig. 1 A (expanded time scale) had a duration of 140 msec while the 20 deg leftward saccade had a duration of 170 msec. During a primate or cat saccade, the eye accelerates to some maximum velocity and then decelerates until the eye reaches its new fixation point. The duration of a primate saccade is equally divided between the acceleratory and deceleratory phases (Fuchs, 1967). The deceleratory phase of a cat saccade, however, usually constitutes 70 % of its duration (Fig. 1). In some cases, a small eye movement had such a long duration and slow maximum velocity that it no longer resembled a saccade. For example, the first 5 deg target step (not shown) in Fig. 1 D elicited an eye movement lasting 460 msec and achieving a maximum eye velocity of only 25 deg/sec. The 4 deg eye movement, only 540 msec after the slow one, had a more normal velocity of 86 deg/sec. Slow changes in fixation were most frequently observed when the cat tracked target steps of 8 deg or less. Of fifty-seven consecutive eye movements made in response to 4 deg target steps, 10 had maximum eye velocities of less than 25 deg/sec. These slow eye movements were always interspersed with normal velocity saccades, as shown in Fig. I D. Therefore, it is unlikely that the extremely slow eye movements are due to a lack of attention. The mean duration of 8 deg horizontal slow eye movements was 250-7 msec (n = 4, cat 1) while for normal horizontal saccades of 8 deg it was 116*7 (± 31.3, n = 17, cat 1). Thus, slow movements did not fall at one end of the distribution of saccade durations, but rather were a type of eye movement quantitatively different from saccades. Slow eye movements do not have an equivalent in the repertoire of primate eye movements. Saccade duration and maximum velocity increased monotonically as a function of saccade amplitude (Fig. 3). To make these relationships comparable to those determined for primates, the unusually slow changes of fixation described in the preceding paragraph were eliminated by requiring each data point to be the average of at least 10 saccades meeting the following criteria: (1) the maximum eye velocity exceeded 25 deg/sec, and (2) when the saccade amplitude was 10 deg or greater, the maximum eye velocity exceeded 100 deg/sec. In addition, each saccade was either purely

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vertical or horizontal. The slopes of the duration-amplitude relationships for both the horizontal and vertical saccades were steeper for movements of less than about 5 deg. For example, the average slope for horizontal saccades of 1-5 deg was 16 msec/deg whereas for saccades of greater than 5 deg, the average slope was 3 msec/deg (Fig. 3A, C). Maximum velocity also increased monotonically as a

C. EVINGER AND A. F. FUCHS 214 function of amplitude for both horizontal and vertical saccades but did not show any difference in slope between large and small saccades. Fig. 3 also shows that vertical saccades were slightly faster than horizontal saccades of the same amplitude. For the two cats, the slopes of linear regression lines relating maximum eye velocity to saccade amplitude were 1441 and 17-6 deg/sec 30 r

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per deg for vertical saccades and 9 0 and 13-5 deg/sec per deg for horizontal saccades. Although horizontal saccades showed some evidence of velocity saturation, vertical saccades did not. Conversely, for saccades between 5 and 20 deg in amplitude, the slope of the linear regression lines relating saccade duration to amplitude was less for vertical (2-96 msec/deg, cat 1; 1P57 msec/deg, cat 2) than for horizontal saccades (5.21 msec/deg, cat 1; 2-52 msec/deg, cat 2). Comparing up with down and left with right saccades revealed no consistent difference in maximum eye velocity or saccade duration. Because of the extreme variability, shown by the standard deviations in Fig. 3, small average directional differences such as those seen in monkeys (Fuchs, 1967) and humans (Robinson,

1964) would be difficult to detect. Most primate saccades occur with an average intersaccadic interval of 200 msec.

CAT EYE MOVEMENTS 215 However, for cats a target step far to the periphery occasionally elicited two saccades in such close temporal proximity that the second was initiated just as or before the first had finished (Fig. 1 E). In sixty-two consecutive saccades in response to 15 deg target steps, 11 of the eye movements overlapped or resembled that in Fig. 1 E. Since such responses were randomly interspersed with single saccades of normal velocity, it is doubtful that they were due to fatigue (Bahill & Stark 1975). Horizontal

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Horizontal and vertical saccades use different extraocular muscle pairs and brain stem areas (Baker & Berthoz, 1977). If the horizontal and vertical components of oblique saccades retain this independence, then, the amplitude-duration relationship dictates that components of unequal size have different durations. For example, an oblique saccade directed 10 deg down and 4 deg left would have a horizontal component that would finish 25 msec before the vertical. In fact, the shorter com-

C. EVINGER AND A. F. FUCHS 216 ponent of an actual oblique saccade is often stretched to nearly equal the duration of the larger component (Fig. 1 F). Comparison of the duration of pure horizontal saccades and the horizontal component of oblique saccades provides an estimate of the number of stretched saccades. For example, the duration of 3 deg pure horizontal saccades distributes around a mean of 90*3 msec (± 30*9; n = 15, cat 1). A 3 deg horizontal component of an oblique saccade lasting longer than 141 msec (95 % confidence level for one-tailed test) has less than a 5 % chance of belonging to the population of pure horizontal saccades, suggesting that such an abnormally long saccade has been stretched. Using the 95 % confidence level criterion, 25 % (cat 2) and 40 % (cat 1) of the 1, 2, 3 and 4 deg horizontal components of oblique saccades were stretched when the amplitude of the vertical component exceeded that of the horizontal component.

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10 5 10 0 Component amplitude (deg) Fig. 4. Duration and maximum eye velocity of the horizontal and vertical components of oblique saccades as a function of component amplitude. Each point represents the mean ( ±s.E.) of at least 30 saccades whose direction was within + 30 deg of horizontal (@-*), within ± 30 deg of vertical (A-A) or in between (Q --- Q).

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The amplitude-duration and amplitude-velocity relationships for the horizontal and vertical components of oblique saccades document the interaction between the two components. Since both cats exhibited similar results, data were pooled (total of 4060 saccades) and each saccade was placed into one of three categories depending on its polar direction: (1) saccades within + 30 deg of the vertical; (2) saccades

CAT EYE MOVEMENTS 217 within + 30 deg of the horizontal; and (3) all remaining saccades. Each cat contributed approximately the same amount of data to each category. Not only did saccade duration increase with amplitude, but a horizontal component of a given amplitude exhibited a longer duration when the net saccade was nearly vertical than when it approached horizontal (Fig. 4). The differences in average duration resulted from a general increase in horizontal component duration rather than from a small population of abnormally long saccades. In a complementary fashion, the maximum horizontal component velocity decreased as oblique saccades became more vertical, although the differences were not satistically significant (Fig. 4). Conversely, vertical duration increased as oblique saccades approached horizontal (Fig. 4). Thus, the amplitude of the orthogonal component (as well as the amplitude of the saccade component under examination) contributes to saccade duration and maximum eye velocity. Fig. 1 contains two examples showing that cats can use visual information occurring during a saccade to alter the saccade in midnight. During the primarily vertical saccade of Fig. I0 the target stepped back to the midline (Fig. 10; T2). About 50 msec after the target step, the eye reversed its direction and with a movement having a maximum velocity of 94 deg/sec obtained the new target position (Fig. 1 G; T2). During the 'hooked' saccade of Fig. 1 H, the target stepped back to mid line (Fig. 1 H; T2). In this case, about 50 msec after the target step both the horizontal and vertical components reversed direction to reach the new target position in a single, uninterrupted movement having a maximum velocity of 60 deg/ sec (Fig. IH; T2). Smooth eye movements When the cats were presented with smoothly moving targets subtending 0 5 deg, the velocity of the horizontal smooth eye movements rarely exceeded 0-6 deg/sec. For example, a cat would accurately pursue a target moving 0-25 deg/sec (Fig. 5A) but would never keep pace with a target moving 2-2 deg/sec (Fig. 5B). The mean eye velocity achieved while attempting to track targets moving faster than 0-6 deg/sec was 0-56 (± 0.24) deg/sec. It should be noted that the training procedure did indeed produce a well maintained tracking behaviour since accurate eye tracking in Fig. 5A continued for over 35 sec. When a striped background moved with the target, the cats achieved velocities of up to 8-5 deg/sec. The importance of the optokinetic background is shown in Fig. 5C: briefly switching the background off (black bar) while the cat was accurately tracking a 2-2 deg/sec target spot that moved with the background reduced the eye velocity to 0.63 deg/sec. Turning the moving background back on elicited a prompt increase in eye velocity. Fig. 5F shows typical smooth eye movements during tracking of constant velocity target movements with the background present. When target ramps of random size and direction were presented, smooth eye movements began 50-100 msec after the target movement (Fig. 2; mean = 89 msec, n = 56). Acceleration to a constant velocity required 636 msec (± 167) for a 2-4 deg/sec target movement and 670 msec (± 128) for a 6-0 deg/sec target movement. When target velocity was less than 8-5 deg/sec, eye movements had velocities equal to the target velocity (Fig. 6) and

C. EVINGER AND A. F. FUCHS 218 were rarely interrupted by saccades (Fig. 5F). At higher target velocities, however, eye movements had velocities that never exceeded 8-5 deg/sec (Fig. 6) and were frequently interrupted by saccades (Fig. 5F). Doubling the target excursion and movement duration, thereby maintaining the same velocities but doubling the time the cats had to achieve those velocities, never increased the maximum eye velocity. No significant asymmetry existed between the mean leftward and rightward eye velocities at target velocities less than 8-5 deg/sec. R

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Fig. 5G shows eye movements elicited by sinusoidal movement of the target plus the background. At 0-3 Hz, a target movement of 5 deg peak amplitude elicited a primarily smooth eye movement that was itself almost 5 deg in amplitude and in phase with the target movement (Fig. 5G). As the target frequency increased, the smooth eye movement decreased in amplitude and lagged farther behind the target that frequent saccades were required in order to stay on target. These observations so

CAT EYE MOVEMENTS 219 were quantified by calculating the gain and phase of the smooth eye movement for each target frequency and amplitude. For both cats the gain decreased as the target frequency increased (Fig. 7). The reduction in gain occurred more rapidly for the larger target amplitudes which elicited the highest maximum smooth eye velocities (8.5 deg/sec for cat 1 and 4*5 deg/sec for cat 2). The eyes usually led the target at 0.1 Hz, suggesting that cats use 'predictive' tracking at low frequencies (Stark et al. 1962). As the target frequency increased, the eyes exhibited an increasing phase lag independent of target amplitude.

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Rotating a striped drum around the cats induced nystagmus (Fig. 8A) having slow phases that exhibited different time courses and velocities depending on the cat's level of alertness. Under the usual stimulation conditions, the eye decelerated to a constant velocity during each slow phase (Fig. 8B). When food was introduced into the cat's view (Fig. 8A; black bar), the slow-phase velocity immediately increased and the eye accelerated rather than decelerated to a constant velocity (Fig. 8C). Even after 40-60 sec of drum rotation at any velocity, exciting the cat with food always increased the slow-phase velocity and changed the deceleratory time course to an acceleratory one. The velocity during either acceleratory or deceleratory slow phases was averaged over the 10-20 see during which the eye achieved the highest velocities and was plotted as a function of drum velocity (Fig. 9). The highest velocities during deceleratory slow phases occurred 15-20 see after the onset of rotation, increased as a function of drum velocity, and were always less than drum velocity (Fig. 9A). The

C. EVINGER AND A. F. FUCHS highest velocities during the acceleratory slow phases occurred 5-10 sec after food entered the cat's visual field, equalled drum velocity up to 28 deg/sec, and remained roughly constant at 25 deg/sec for higher drum velocities (Fig. 9B). No significant asymmetry existed between the maximum slow-phase eye velocities obtained with clockwise and counterclockwise drum rotation. The maximum slow-phase eye velocity achieved during optokinetic nystagmus was approximately 3x5 times higher 220

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than that obtained during sinusoidal or constant velocity background-aided ramp target movements. However, it took 15-20 sec for slow phase velocities to build up in response to optokinetic stimulation, so they cannot be compared with velocities obtained during sinusoidal tracking. During the first 3 sec of optokinetic stimulation, maximum slow-phase velocity never exceeded 7 deg/sec, regardless of drum velocity. In the vertical direction, background-aided tracking was best for upward moving targets, which consistently elicited smooth eye movement while downward target movement elicited primarily saccades (Fig. 10). Maximum eye velocities were 6 deg/ sec for upward tracking, rarely exceeded 2-5 deg/sec during downward tracking and were usually less than target velocity in either direction (Fig. 10). To demonstrate that smooth eye movements were elicited by slow target movement rather than target steps, cats were required to track the step-ramp target

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222 C. EVINGER AND A. F. FUCHS trajectory first used by Rashbass (1961). When the target, together with the background, stepped to the right and then moved leftward at a constant velocity (Fig. 5D), the cat first made a smooth leftward eye movement that actually carried the eye away from the target, followed by a pair of rightward saccades to bring the eye VE T

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back on target (Fig. 5D). If the target velocity was increased, so that the target recrossed its zero position before a saccade was initiated, a smooth movement alone placed the eye on target (Fig. SE). The eye accelerated from zero to a constant velocity in 700 msec, a value near that determined for simple ramps. In addition to demonstrating that the adequate stimulus for smooth eye movements is different from that for saccades, this experiment confirms that smooth eye movements have a shorter latency than saccades (Fig. 2).

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Altered visul feed-back An eye movement normally creates an equal and opposite movement of the retinal image. This unity gain feed-back can be altered by controlling target and background positions (OT) with a signal proportional to eye position (0E). If the constant of proportionality is a and the target controller signal is rC then

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a~aK=-48 I-JlwInfa H-I Fig. 11. Instabilities in the horizontal oculomotor control system under conditions of altered visual feedback. Open loop (K = 0) evokes smooth eye movements with no initial target movement (A) and endless saccades (B) after an intial target step (not shown). Increased negative feedback causes saccadic oscillations (C-E). Calibrations for horizontal eye (HE) and target movement (T) represent 10 deg and 1 sec forA and B, and 20 deg and 0.5 sec for C-E.

When a = 1 0 every eye movement is accompanied by a target movement of equal amplitude in the same direction, the retinal error is constant at 0TC and the tracking system is operating in the open loop condition (K = 0). If the cat is fixating the target when cx is made equal to 1 the eye moves smoothly toward the periphery at velocities less than 8 5 deg/sec (Fig. 1 A). This movement is probably an endless smooth pursuit movement induced by the existence even during fixation of some slight retinal error (Fuchs, 1967). If, when the loop is opened, there is a sufficient discrepancy between target and eye position that the cat executes a saccade, the target will move ahead simultaneously by an equal amount. This error induces a

C. EVINGER AND A. F. FUCHS second saccade and so on, causing a staircase of saccades of equal size occurring every 270 msec (Fig. I IB). Increasing the negative feed-back causes the eyes to break into saccadic oscillations (Fig. 11 C-E). An initial target displacement with K = - 2*75 (a = - 1.75) elicited a saccade that immediately drove the target back past its original position. The eye then followed with a series of saccades of decreasing amplitude until the target was acquired (Fig. 10C). Increasing K to - 3-16 (az = - 2-16) induced sustained saccadic oscillation of approximately constant amplitude (Fig. I ID). Negative feed-back in excess of - 3-5 (a = - 2.5) was required to produce saccadic oscillations of increasing amplitude (Fig. l IE). The mean intersaccadic interval was 258 msec ( + 66 msec, n = 25 successive oscillations, cat 1), corresponding to a frequency of oscillation of 1P9 Hz. This value also corresponds closely to the mean saccadic latency to random target steps (Fig. 2A). 224

DISCUSSION

Behavioural control of eye movements Our training procedure has several advantages over other attempts at training cats to make eye movements (Richardson & Davis, 1960; Berkley & Tunkl, 1969; Schlag-Rey & Schlag, 1977). First, the cats are trained rapidly. Second, the procedure is easily automated and provides continuous rather than discrete control of eye movements. Finally, the trained cat exhibits a high and reasonably constant level of performance without the use of amphetamines. This high performance level was manifest in (1) the short reaction times to random target trajectories (Fig. 2); (2) the cats' accurate tracking of slowly moving targets for long periods (up to 40 sec) without lapses into drowsiness (Fig. 5A); and (3) the maximum velocity of saccades (Fig. 3), which were faster than saccades made by cats under amphetamine (Crommelinck & Roucoux, 1976). Thus our training procedure seems to elict the best eye movements possible by cats with fixed heads. Recent studies, however, suggest that saccade velocities are even higher when the head is free (Collewijn, 1977; Donaghy, 1975).

Characteristic of cat saccades The duration and maximum velocity of cat saccades increased as a function of their amplitude (Fig. 3) although at rates different from those determined for other species. For example, maximum saccade velocity increased more slowly in cat (Fig. 3; 9-17-6 deg/sec per deg) than in monkey (Fuchs, 1967; 40 deg/sec per deg), man (Boghen, Troost, Daroff, Dell'Osso & Birkett, 1974; 20 deg/sec per deg for saccades 5-10 deg in amplitude) or goldfish (Easter, 1975; 21 deg/sec per deg), but at approximately the same rate as in the rabbit (Collewijn, 1970a; 13 deg/sec per deg). In the cat the relation between maximum velocity and amplitude was best described by a straight line. Primates, however, exhibit a nonlinear relationship because of a velocity saturation with large saccades (Fuchs, 1967); cats might also show this if larger saccades were examined. The break in the duration-amplitude relationship which occurred in the cat at about 5 deg (Fig. 3) also occurs in the monkey (X. Lisberger et al. in preparation); however, for saccades greater than 5 deg, duration increases

225 CAT EYE MOVEMENTS more rapidly in the cat (1.5-5.2 msec/deg) than in the monkey (1 msec/deg; Fuchs, 1967). The smaller component of an oblique saccade usually exhibited a longer duration and a slightly smaller maximum velocity than a saccade of the same size with no orthogonal component (Figs. 1 F and 4). This behavioural result provides no evidence as to whether the saccade 'stretching' resulted from peripheral causes such as extraocular muscle interactions, or central cause such as the structure of the motor command. In addition, this result does not imply that the trajectory of an oblique saccade is a straight line between two points. The components of an oblique saccade may have an equal duration yet the eyes follow a curved path if one of the two components accelerates faster than the other (Viviani, Berthoz & Tracey, 1977). Indeed, cat saccades commonly exhibited a curved trajectory (Fig. 1 F) since vertical saccades were faster than horizontal saccades (Fig. 3). The present results resemble those found for humans (Bahill & Stark, 1977) and monkeys (King et al. in preparation), suggesting that the cause of the stretching may be common to all three species. Visual signals that occur during saccades can change the direction of an ongoing eye movement in the cat (Fig. 1 G, H). The reversal of direction is accomplished by initiating a second saccade in a direction opposite to the first before the first has been completed. These second movements are considered to be saccades because their maximum velocity is appropriate for single saccades of that amplitude. Since saccades can interrupt each other in midffight, and since the second movement brings the eye on target, the oculomotor system must take into account the change in eye position caused by the first saccade to program the second accurately. Not only is the retinal error immediately following the target step quite different from the retinal error when the second saccade begins, but the retinal error changes continuously from the time of the target movement until the second saccade is initiated. These double saccade trajectories are similar to those elicited in humans with large doublestep stimuli (Becker & JUrgens, 1975), suggesting that the two species process visual information in a similar fashion to create saccades. Altered visual feed-back in the cat induces eye movements that resemble those observed in humans (Robinson, 1965) and monkey (Fuchs, 1967) under similar conditions. Reducing the feed-back gain to zero while a retinal error is present elicits a staircase of saccades (Fig. 1 B). Increasing the gain of visual feed-back from its normal value of -1 to - 3-5 causes the eyes to go into growing saccadic oscillations at 1 9 Hz (Fig. 11 C-E). Humans require a feed-back gain of -5 before breaking into oscillations at 2-2*5 Hz (Robinson, 1965), while monkeys require a feedback gain of only - 2-3 to initiate 1-8-2-3 Hz saccadic oscillations (Fuchs, 1967). Relative to the rather stereotyped saccades of monkeys (Fuchs, 1967), the time course of cat saccades exhibited considerable variability as illustrated by the large standard deviations of the amplitude-duration and maximum velocity relationships (Fig. 3) as well as the occurrence of 'hooked' saccades (Fig. 1 H) and slow eye move-

ments (Fig. 1D). Other authors have attributed this variability in the cat to the experimental conditions (Stryker & Blakemore, 1972) or to changes in the cat's state of alertness (Crommelinck & Roucoux, 1976). The present experiments, however, excluded both these possibilities because (1) the experimental conditions were 8

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C. EVINGER AND A. F. FUCHS 226 comparable with those for the monkey, and (2) the level of attention was not a factor since slow saccades occurred within 500 msec of rapid saccades. The slow eye movements are not conventional smooth pursuit movements since they occur without a moving target (Robinson, 1976b). However, because of their low velocity, slow eye movements observed in an untrained cat could easily be misinterpreted as smooth pursuit movements. In spite of the larger variability of the time course of cat saccades, their latencies, the stretching of their components, the effectiveness of visual information in altering their trajectories, and their behaviour during altered visual feed-back all suggest that cats and primates may process visual information in similar fashion to create saccades.

Properties of cat smooth tracking The maximum velocity of smooth eye movements achieved by cats while attempting to fixate a small moving target spot was 0-6 deg/sec. These data suggest that the smooth tracking of small targets, which has been attributed to foveal smooth pursuit in the monkey (Fuchs, 1967; Barmack, 1970a), is very poor in the cat. While cats do not have a fovea, ganglion cells within the central specialized area of the cat retina (area centralis) respond to slip velocities well in excess of the cat's smooth pursuit capabilities (Cleland, Dubin & Levick, 1971). Thus, it is difficult to ascribe the low pursuit velocities strictly to retinal limitations. Perhaps image slip on the peripheral retina is a more powerful stimulus for eye movement than image slip on the area centralis. Thus, smooth pursuit of a spot over a stationary background might cause a strong optokinetic stimulation for eye movement in the opposite direction. This explanation would also account for the increase in smooth eye velocity occurring with optokinetically aided tracking (Fig. 5C). Addition of an optokinetic background moving with the target spot increased the maximum velocity of smooth eye movements to 8-5 deg/sec (Fig. 5D, E). This value was never exceeded for targets moving either with constant velocity (Fig. 6) or sinusoidally (Fig. 7), even after increasing the amplitude of target movement to be certain adequate time was provided for the eye to accelerate to higher velocities. In similar experiments in the rabbit, Collewijn (1969) demonstrated that only the eye velocities obtained in the initial 3 sec of optokinetic drum rotation were comparable with eye velocities obtained with sinusoidal target motion. In our experiments, velocities achieved in the first 3 sec of optokinetic drum rotation never exceeded 7 deg/sec. As reported by other investigators (Honrubia et al. 1967; Collins et al. 1970), prolonged horizontal optokinetic stimulation elicited slow phase velocities of up to 28 deg/sec in the cat. These higher velocities required 15-20 sec of continuous stimulation and a high level of alertness. Cohen, Matsuo & Raphan (1977) have suggested that the initial slow-phase velocity results from the activity of direct neural pathways involved with optokinetic stimuli and that the recruitment of slower, indirect pathways produces the gradual increase in slow-phase velocity. Our results suggest that recruitment of the putative slower pathways requires a high level of attention, since the slow-phase velocity during the inattentive periods (Fig. 9) only slightly exceeded the eye velocities obtained with ramp and sinusoidally moved stimuli (Figs. 6 and 7).

227 CAT EYE MOVEMENTS When pursuing a target moving vertically with an optokinetic background, the cats attained higher eye velocities for targets moving upward than downward (Fig. 10). In agreement with our results, Collins et al. (1970) showed that vertical optokinetic stimulation evoked only upward but not downward slow phases. Humans also exhibited a directional asymmetry with vertical tracking (Benson & Guedry, 1971). The poor downward pursuit ability may be a mechanism to avoid nystagmus that could be caused by the downward and lateral optokinetic cues induced during forward motion such as walking (Benson & Guedry, 1971). Even upward vertical smooth eye movements reached lower maximum velocities than horizontal smooth eye movements. Some smooth eye movements of cats and monkeys appear to be similar superficially but most are qualitatively as well as quantitatively different. Cats and monkeys respond similarly to the step-ramp stimulus (Fig. 5D, E; Fuchs, 1967) and both exhibit a roughly constant period of acceleration to achieve target velocity (Fuchs, 1967). Cats are incapable of smooth pursuit velocities of 1 deg/sec (Figs. 5A, B) but reach 28 deg/sec during optokinetic stimulation. Primates, however, achieve smooth pursuit velocities in excess of 100 deg/sec (Barmack, 1970a; X. Lisberger et al. in preparation), comparable to the slow-phase velocities elicited by optokinetic stimulation (Cohen et al. 1977). Finally, lesions of the entire monkey cerebellum (Westheimer & Blair, 1974) or just the vestibulocerebellum (Takemori & Cohen, 1974) eliminate or greatly reduce both smooth pursuit and optokinetic nystagmus, while similar lesions in the cat have no effect on the latter (Robinson, 1976a). On the other hand, the results of optokinetic studies on the rabbit seem more similar to those presented here for the cat. Both animals generate visually induced smooth eye movements primarily with the optokinetic system, since neither animal can produce smooth pursuit eye movements of high velocity (Collewijn, 1970a). The latency of smooth eye movements is approximately equal for the two species (89 msec for cat, Fig. 2B; 100 msec for the rabbit, Collewijn, 1972). Rabbits, like cats, exhibit a velocity limit for smooth eye movements that is lower for sinusoidal movement of an optokinetic drum than for prolonged rotation of the drum at constant velocity (Collewijn, 1969). Finally, as in cats, lesions of the rabbit cerebellum have no effect on optokinetic nystagmus (Collewijn, 1970b). This research was supported by grants RR00166, GM00260 and EY00745 from the National Institutes of Health, IJ.S. Public Health Service. C.E. was supported by a National Science Foundation fellowship. We gratefully acknowledge the support of the Bioengineering Division of the Regional Primate Research Center at the University of Washington. We are also indebted to Gene Johanson for his excellent technical assistance, Cindy Chin for illustrations, Dr Stephen Lisberger for his helpful comments during the preparation of the manuscript, and Kate Schmitt for editorial assistance.

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