Eye movements evoked by focal stimulation of the cats superior colliculus

Brain Research, 59 (1973) 211-227 © Elsevier ScientificPublishing Company, Amsterdam - Printed in The Netherlands

211

EYE M O V E M E N T S EVOKED BY FOCAL S T I M U L A T I O N OF T H E CAT'S SUPERIOR COLLICULUS

M A X STRASCHILL AND P E T E R R I E G E R

Max Planck Institut fiir Psychiatrie, 8000 Munich 40 ( G.F.R.) (Accepted February 15th, 1973)

SUMMARY

Focal electrical stimulation through the recording microelectrode was performed in the superior colliculus of spinally anesthetized and of unanesthetized cats. Eye movements were recorded by conventional E O G methods and by a light beam reflected from a corneal mirror. Spontaneous and evoked saccades have a similar amplitudeduration relation, peak velocities of about 300°/sec and maximal amplitudes of 30 °. Amplitude, speed and latency of evoked eye movements depend strongly upon strength of stimulating current. With increasing penetration depth, the threshold intensity of the electrical stimulus decreases abruptly when the electrode approaches the intermediate tectal layer, to decrease only slightly with further downward penetration. Some of the characteristics of oculomotor output of a tectal subarea parallel those of the visual response characteristics of single neurons of the same region. Receptive field position and evoked eye position, preferred direction of single neurons, and direction of saccades are in good agreement when the eyes are in primary position at the onset of stimulation. But direction and amplitude of electrically induced saccades change with changing initial eye position to bring the eyes to a constant position. This indicates that the stimulation point determines eye position with reference to the cat's head or body. In a few instances, electrical stimulation elicited nystagmus or suppressed spontaneous nystagmus.

INTRODUCTION

The results of a number of studies2,4,1°, 12,13,2a have suggested that the superior colliculus of vertebrates is an optomotor integration center, where visual information is processed and transformed into an optomotor response. Several investigations have revealed a retinotopically organized retinal inputl,a, 14, circumscribed receptive fields, and movement and direction selectivity10,17,zs,2L Recent descriptions of tectal neurons

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discharging in synchrony with and prior to eye movements suggest participation in oculomotor function24,29,34, 35. This evidence gains support from observations of conjugate eye movements following electrical stimulation of the optic tectum4,1a,16,z°, ~3. The results of some electrical stimulation studies have given the impression of a correlation between electrically induced position of gaze and the part of visual space represented in the collicular stimulation point4,2°,2a, 2s. The following problems were investigated in the present study. (1) The influence of some parameters of the electrical stimulus, such as stimulus intensity and location of the stimulation electrode, upon the parameters of the resulting eye movements. (2) The relationship between sensory properties of neurons located around the stimulation point and the parameters of electrically induced eye movements. The method of focal stimulation with the recording microelectrode 5 permitted a direct comparison between neuronal response characteristics and parameters of the saccades. Part of the results has been reported elsewhere 80. METHODS

Twenty-two cats were prepared under ether anesthesia and fixed in a stereotactic head holder by skull bolts which were cemented onto the skull. A small metal mirror was inserted into the center of the locally anesthetized cornea of one eye. During the experiment general anesthesia was discontinued and replaced by spinal anesthesia by means of repetitive instillation of Xylocaine (4 ~ , 4 ml) into the lumbar subdural space. This procedure causes a reversible paresis of axial and limb muscles, requires artificial respiration and leaves cranial nerve function intact. The following criteria were taken as indicators of unimpaired supraspinal function: the presence of full range spontaneous and pursuit eye movements, of galvanic nystagmus, of orienting reactions to sound or visual stimuli and of reflex lid closure to threat or corneal touch. Another series of experiments was performed on 3 chronic, non-anesthetized cats with a fixed head, but without further restraint. In these animals, surgery was performed under sodium pentobarbital. An 8 mm trephine hole was made over the occipital cortex and a metal cylinder was fitted onto the hole and embedded in dental cement. Silver-silver chloride electrodes were implanted subcutaneously to record the electrooculogram. Skull bolts were cemented onto the skull to permit fixation of the head during the experiments. This chronic preparation has been described in detail by Noda is. The right or left superior colliculus was stereotactically reached after penetration of the intact dura and the overlying brain structures. The appearance of visually driven activity at the arrival on the collieular surface served during the experiment as a landmark for depth determination during the experiment. Action potentials from single units and background activity were recorded using stainless steel microelectrodes (3-5 #m, 1-2 M~)). Horizontal and vertical eye movements and eye positions were recorded: (a) by electrooculography through amplifiers with DC-coupling; (b) by a light beam, which was reflected from the corneal mirror upon a hemicylindrical

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screen in front of the animal. Eye positions were referred to the intersection line of the animal's midsagittal plane with the hemicylindrical screen and to the connection line of the intersection points of the visual axis with the screen 7. For electrical stimulation, pulse trains of rectangular pulses (0.5 msec), lasting 1-10 sec, were delivered through the recording microelectrode. Current spread to adjacent areas and tissue damage were limited by the low stimulation current intensities of 0.6-5/~A. Current strength was measured by means of a multiflex galvanometer. The method of monopolar focal depth stimulation has been described and discussed in detail by Asanuma and Sakata 5. For their cortical threshold stimulus of 2 #A, these authors calculated an effective current spread of 50/zm, which excited maximally 4-5 cortical cells. Since specific tissue resistance and cell density of the superior colliculus are unknown, we may accept their cortical value as a rough estimate of the number of cells activated in the present experiments. Moving bright spots were projected upon the hemicylindrical screen in front of the cat. Receptive field position was approximately determined during fixation periods with eyes in midposition (primary position), or inferred from the electrode position, using a projection map based upon data from our laboratory 14. Moving bright spots were projected upon a hemicylindrical screen in front of the animal. Differences in strength of response to variation of movement direction, which were recorded by an electronic spike counter, permitted us to determine the preferred direction of single units. At the last recording or stimulation site of the final penetration, a current was passed through the electrode tip. The brain was subsequently perfused with a solution of 10 formaline and 2 ~ potassium ferrocyanide and the midbrain embedded in paraffin. Electrode tip locations were marked as blue spots and could be reconstructed from coronal sections. Only 3 penetrations per animal were made. RESULTS

In order to obtain information about the range of velocities and amplitudes of spontaneous and electrically evoked saccades, the E O G was recorded in a chronic unanesthetized preparation. After spinal and corneal anesthesia of the same animal, the EOG was calibrated by simultaneous registration of spontaneous and electrically induced saccades by means of a refected light beam (see Methods). Electrical stimulation was performed in a rostral (AP 3) and a caudal (AP 1.5) location with currents of 1.6 /~A. The results, as presented in Fig. 1, show: (1) a fairly good agreement between the parameters of spontaneously and electrically induced saccades; (2) an increase of saccade duration with increasing saccade amplitude; (3) a moderate increase of saccade velocities with increasing amplitudes up to 20 °. With 300°/see (spontaneous) v s . 320°/sec (electrically evoked), the peak velocities of eye movements were clearly below those reported for man and monkey. Amplitudes of most spontaneous eye movements ranged from 6 to 20 °. Amplitudes exceeding 35 ° were not observed in spontaneous or electrically induced saccades. The majority of eye movements following suprathreshold electrical stimulation were saccades. Slow eye movements ( < 50°/see), or saccades decelerating into slow

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M. STRASCHILL AND P. RIEGER saccades

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movements were frequently observed, when threshold intensities were used (Figs. 3, 8A). During electrical stimulation, the eye reached its final position either directly by a single saccade (Fig. 8), or by a staircase-like succession of 2 or 3 saccades. In the latter case, the first saccade was always considerably larger than the subsequent ones. There was a tendency for stimuli of low current intensity and for rostral stimulation sites to produce a single saccade, while higher current strengths and caudal electrode positions rather predisposed for staircases of saccades. When the electrical stimulus produced a succession of saccades, the total gaze deviation thus depended to a certain extent upon stimulus duration, but also upon the AP position of the electrode. Stimulations in the posterior half of the colliculus drove the eyes to their mechanical limits and thus gave the impression that prolonged stimulation of the colliculus produced the same maximal excursion irrespective of the site of stimulation. The final position was usually maintained during electrical stimulation (Fig. 8). When threshold currents were applied, spontaneous eye movements could interrupt the stimulation effect. After current termination the animal made a return saccade towards the primary position, whose amplitude usually equalled or exceeded that of the electrically induced saccade. The latency of the saccade following current termination was usually shorter than that after onset of stimulation. The parameters of the saccadic eye movements, such as latency, amplitude and velocity, were largely dependent upon intensity and location of the electrical stimulus.

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(1) The influence of current strength W i t h increasing c u r r e n t strength, the d e v i a t i o n o f gaze f r o m p r i m a r y p o s i t i o n (gaze eccentricity) increased to a m a x i m u m , which was m a i n t a i n e d despite f u r t h e r increase o f c u r r e n t (Fig. 2). This m a x i m a l value o f eccentricity was d e t e r m i n e d b y the surface c o o r d i n a t e s o f the collicular s t i m u l a t i o n site, o r by the m e c h a n i c a l limits o f o c u l a r d e v i a t i o n with p o s t e r i o r l o c a t i o n o f the electrode.

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Fig. 2. Influence of current strength upon amplitude (A) and latency (B) of electrically evoked conjugate eye movements. Each point is the mean of about 15 stimulation effects obtained in 3 cats. Vertical bars represent standard deviation. Stimulation sites: stratum griseum medialis and stratum griseum profundum.

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Fig. 3. Influence of current strength upon velocity of electrically evoked eye movements. Each point is the mean of about 15 stimulation effects obtained in 3 cats. Vertical bars represent standard deviation. Stimulation sites: stratum griseum medium and stratum griseum profundum.

The velocity of electrically evoked eye movements increased with increasing current strength (Fig. 3). This increase is only partially accounted for by the moderate increase of speed, which was found to accompany increases of amplitude. Increase of current strength shortened the saccades latency (Fig. 2B). Latencies at onset of stimulation as well as those at current termination were likewise influenced.

(2) The influence of stimulation depth With increasing distance from the collicular surface the threshold intensity of the electric stimulus decreased only slightly within the stratum griseum superficialis (Fig. 4A). When the electrode approached the stratum griseum intermedialis, the threshold fell abruptly to decrease only moderately with further downward penetration of the electrode (Fig. 4). A corresponding maximal increase of saccade amplitude occurred during the transition into the stratum griseum intermedialis, when a constant suprathreshold stimulus was applied (Fig. 4B). These results suggest that the neuronal elements which provide a direct input to the reticular premotor apparatus of the oculomotor nuclei are the pyramidal cells of the medium and deep tectal layers. The direction of the eye movement did not vary significantly with depth.

(3) The influence of the surface coordinates of the stimulation site Collicular points of the equal depth and of systematically varied surface coordinates were stimulated and the horizontal and vertical eccentricity of gaze was determined. Threshold intensities were determined, and effects following supramaximal stimulation of sites of equal threshold were compared. Thresholds were controlled after several stimulations and were found unchanged, with a few exceptions which were disregarded for further evaluation. Displacement of the electrode in a rostro-

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Fig. 4. Influence of depth of the stimulation site upon amplitude (A) and threshold (B) of electrically evoked conjugate eye deviations. A: each point is the mean of about 15 responses of 3 cats to electrical stimulation with a constant current strength of 1.6 /~A. B: the term threshold as used here means the least current which produced a response in 75 ~ of stimulations.

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caudal direction increased the amount of lateral gaze deviation (increase of horizontal eccentricity). Electrode shifts from the midsagittal division line of the colliculus towards the midline produced increasing elevation of gaze above the horizontal meridian (increasing positive vertical eccentricity). Electrode shifts from the midsagittal division line towards the lateral tectal margin caused increasing depression of gaze below the horizontal meridian (increasing negative vertical eccentricity). This dependence of gaze position upon the surface coordinates of the stimulation site becomes more obvious, when we consider the position of gaze after the first large saccade instead of the final position. During prolonged stimulation, the influence of stimulation time (see above) somewhat obscures the influence of electrode position.

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(4) The relationship between sensory properties of neurons around the stimulation electrode and the parameters of electrically induced eye movements (a) The relationship between receptive field position and position of gaze. The above-described relationship between tectal surface coordinates and eye position closely resembles that of surface coordinates and receptive field position 14. The collicular motor map approximately matches the retinotopic sensory map. This is clearly demonstrated when - - as shown in Fig. 5 - - the electrically induced eye position after the first saccade is related to the position of the receptive area of the stimulation point. When the eyes are in primary position before stimulation, there exists a linear, and for horizontal eccentricites a one-to-one, relationship between eccentricity of the receptive area and the eccentricity of gaze position. The receptive area was directly determined, when background or single unit activity could be recorded by the stimulation electrode during fixation in primary position, or indirectly inferred from the position of the electrode (see Methods). (b ) The relationship between preferred directions of directionally selective neurons at the stimulation site and the direction of electrically induced eye movements. Preferred directions of single neurons were determined by moving visual stimuli and related to the direction of eye movements, which were produced by electrical stimulation through the same recording microelectrode. In case of primary eye position before stimulation, the directions of electrically induced eye movements were found to be well correlated with the preferred directions of single neurons (Fig. 6).

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--45 Fig. 6. Regression o f directional angle o f preferred directions o f single units o n directional angles o f eye m o v e m e n t s d u e to electrical s t i m u l a t i o n o f t h e recording point. Regression line with m e a n s t a n d a r d error o f estimate. N u m b e r o f n e u r o n s tested = 50. Correlation coefficient = 0.82; m e a n s q u a r e deviation o f sample points f r o m the e s t i m a t e d regression line: (syx 2) = 44.4. Regression function: Yx = 0.8 x + 2.4. Directional angles were classified into classes o f a size o f 45 °. 0 °, 45 °, 90 °, a n d 135 ° were c h o s e n as class m e a n s .

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M. STRASCHILL AND P. RIEGER

Since preferred directions of tectal neurons usually point from the center of the visual field towards the neurons's receptive field 2, the results shown in Fig. 6 can be predicted from those shown in Fig. 5. The results, as presented in Figs. 5 and 6, suggest two possible hypotheses: (A) Each tectal subarea determines saccades of a certain constant direction and amplitude. The amplitudes of the horizontal vs. vertical vector of eye movements equal the horizontal vs. vertical eccentricities of the receptive field of the collicular subarea, whose electrical or physiological excitation induces the saccade. The direction of the saccades corresponds to the direction of the receptive field in relation to the fixation point and to the preferred directions of single neurons within the subarea. (B) Each tectal subarea determines a certain position of the eye in the orbit, i . e . , a certain constant orientation of the visual axis in space. The angular deviations of the visual axis from primary position are equal to the horizontal vs. vertical eccentricities of the receptive area of the collicular subunit, whose excitation induces the eye movement. If hypothesis A were true, electric stimulation of a collicular subarea should produce saccades of constant amplitude and direction, irrespective of the eye position at the moment of stimulation. If hypothesis B were correct, the eyes would always reach the same position, the 'goal', during stimulation, irrespective of the prestimulation fixation point. This implies that the direction and amplitude of the saccade change with changing initial eye positions. Stimulation effects of this kind were characterized as 'goal directed '16. Our results show that, irrespective of the eye position at the onset of stimulation, the same final position is reached (Fig. 7) when points below the superficial layer are stimulated. Stimulation effects of the superficial layers are difficult to evaluate because of their considerable variability. The impression we obtained from a few reproducible effects was in favor of hypothesis A. Amplitude and direction of saccades did not depend greatly on initial eye position.

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Fig. 7. Constancy of electrically induced eye position (crosses) with changing initial eye position (filled dots). Cross with inscribed small circle represents center of binocular visual field in case of primary eye position. Stimulation site: AP: l; lm: 2.5; depth: stratum griseum profundum. Current intensity: 1.6/~A (suprathreshold intensity).

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In another series of experiments, two microelectrodes were inserted along the midsagittal line of the colliculus. Despite equal thresholds, prolonged stimulation of the rostral point yielded a considerably smaller horizontal deviation of the eyes than

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d i d s t i m u l a t i o n t h r o u g h the c a u d a l electrode, p r o v i d e d t h a t the r o s t r a l one was p l a c e d in the a n t e r i o r h a l f o f the colliculus at a distance o f at least 2 m m f r o m the c a u d a l electrode. A n e x a m p l e o f d o u b l e s t i m u l a t i o n is illustrated in Fig. 8B. W i t h single stimulation, the rostral electrode yields a less eccentric eye position. A l t e r n a t i n g stimul a t i o n in a r o s t r o - c a u d a l sequence results in t e m p o r a l gaze shifts. Reversal o f the sequence p r o d u c e s nasal gaze shifts. W h e n s t i m u l a t i o n o f the c a u d a l site is superi m p o s e d u p o n a p r o l o n g e d r o s t r a l stimulation, the eyes m o v e further t o w a r d s the

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Fig. 9. Examples of nystagmus (A) and poststimulation nystagmus (B) evoked by electrical stimulation of the stratum griseum intermedialis of the cat's superior colliculus. V: vertical vector; H: horizontal vector of eye movements. Numbers indicate current strength. DC-coupling. Black bar indicates period of stimulation.

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periphery. But addition of a rostral stimulus to an ongoing caudal one does not significantly alter the eye position. The caudal site predominates and no compromise is reached. The observations of stimulation effects during eccentric spontaneous eye positions as well as the results of double electrode experiments stress the importance of the collicular surface coordinates as determinants of eye position in the orbit. The dominance of caudal stimulation effects in the competitive situation of simultaneous stimulation suggests unidirectional inhibitory interactions between caudal and rostral collicular regions.

(5) Production of nystagmus or modulation of spontaneous nystagmus by electrical stimulation of the collieulus superior I n two animals, electrical s t i m u l a t i o n of the colliculus p r o d u c e d nystagmus with

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the fast phase in direction of the contralateral side (Fig. 9A). Frequency and amplitude of the nystagmus increased with increasing current strength. In one animal, nystagmus appeared only after termination of the electrical stimulation. The poststimulatory nystagmus beat in an ipsilateral direction and declined both in frequency and amplitude, to disappear after 8-10 sec (Fig. 9B). In 3 animals, spontaneous nystagmus appeared during the experiment probably in consequence of upward diffusion of Xylocaine which was used for spinal anesthesia. Depending on the stimulation intensity, spontaneous nystagmus was totally suppressed, or diminished in amplitude and frequency (Fig. 10A). In one case, electric stimulation produced phase reversal and marked poststimulation enhancement of spontaneous nystagmus (Fig. 10B). DISCUSSION

The cat has a smaller range of velocities and amplitudes of saccades than the monkey 9 or manlS,19, 35, but it shares their positive correlation between saccade duration and amplitudeg,15,19,3L Saccadic eye movements due to electrical stimulation of the monkey's frontal cortex 21, brain stem s and superior colliculus2°, 23 have been systematically studied. Different parameters of the electrical stimulus proved to be important for different brain sites. When the frontal eye fields or the superior colliculus were stimulated2°, 21, the amplitude, speed and direction of the saccade were independent of the stimulus strength and frequency as long as they were above threshold. It was concluded that the stimulus triggers a train of autonomous events in neural circuits in the brain stem, which produce the burst of activity underlying saccades. With stimulation of the paramedian reticular formation, amplitude and speed of eye movements were linearly related to stimulus frequency and clearly dependent upon stimulus intensity s. In our experiments, current strength proved to be an important parameter in determining amplitude, speed and latency of saccades, while changes of frequency had little effect. Since increase of current strength beyond an upper limit (saturation point) remains ineffective, the higher intensity range of Robinson 2°, which was above our saturation point, may explain the disagreement of experimental data. The ineffectiveness of stimulus frequency variations above 50 Hz suggests a limited transmission capacity of tectal neurons, which is probably due to recurrent inhibitory mechanisms. In the cat, increase of stimulus duration may produce additional smaller saccades, which drive the eyes to their mechanical limits when sites in the posterior half of the colliculus are stimulated. In the monkey, however, prolonged stimulation of any tectal stimulation site evokes a staircase-like series of saccades and short fixation periods, which drive the eyes towards their limits20, z3. The amplitude of the single saccade is dependent, as in the cat, upon surface coordinates of the stimulation site. Amplitude and direction of electrically evoked saccades are independent of initial eye position, and correspond to direction v s . eccentricity of receptive field position of the stimulated subarea. The electric stimulus, simulating photic stimulation in local collicular regions, evokes - - according to the visual grasp reflex2,12 or foveation theory 2°,24 of collicular function - - a saccade, which brings the simulated visual stimulus onto the fovea.

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Continued stimulation will simulate another visual stimulus, removed from the fovea by the same amount as the previous one and will lead to another identical eye movement. In the cat, however, continued stimulation often produced only a single saccade and maintained the eyes in one position during the stimulation period (Fig. 8). Furthermore, evoked saccades were 'goal directed '16. Irrespective of the initial eye position, the eyes reached the same final position in the orbit (the goal) when the deeper layers were stimulated. The motor map of the colliculus seems to determine eye position with reference to the animal's head or body, rather than in relation to retinal coordinates. Only in case of initial primary eye position does the motor output map of eye positions match the sensory map of receptive field positions in the visual field. By its common axis of reference (the head axis), the m o t o r map seems to be particularly related to acoustic space. Acoustic stimuli are quite effective in eliciting the orienting reactions, which are identical with the motor reactions evoked by collicular stimulation. In addition to gaze deviation, rotation of the contralateral pinna was usually observed. Obviously, not only optomotor but also audiomotor integration takes place in the deeper tectal layers. These deeper layers contain neurons with visual and acoustic input28, aa, whose visual and acoustic receptive fields are largely coincident in space a3 and naturally suggest that this mode of convergence would allow either novel sounds or novel optic stimuli to elicit the same exploratory orienting response. But again, as in the case of the sensory and m o t o r map, primary eye position is required to bring visual and auditory sensory space into functional register. This condition is usually fulfilled in the cat's natural life, since changes of gaze are performed by head movements with immobile eyes, or head movements follow initial eye movements, while the eyes move back to restore primary position during fixation periods. In accordance with the close association of eye and head movements in the orienting reaction, electrical stimulation of the colliculus in freely moving cats yields coordinated eye and head movements al. Our results may thus reflect the complex interaction of the tectal eye movement and head movement control systems rather than describe the behavior of the eye movement control system in isolation. This may account for the discrepancies between our findings and the results, which were obtained in the monkey. In the monkey, which does not rely so much upon head movements because of its larger range of eye movements, tectal stimulation may primarily activate the eye movement control system. While tectal stimulation in the monkey did not produce rebound or off response movements, return saccades reliably followed stimulus termination in the cat. I f there are inhibitory connections between neurons related to antagonistic eye muscles, current termination may produce the postinhibitory rebound excitation, which triggers eye movements in the opposite direction. A marked decrease of stimulus threshold with increasing penetration depth was observed in the monkey 2°,23 and in the present experiments. The high threshold of the superficial layer suggests that its relation to the premotor oculomotor apparatus is more indirect than that of the deeper layers. The different properties of the superficial and deeper layers, as revealed by the electric stimulation and by single unit studies, characterize the former as a sensory analyzer

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of the visual environment, the latter as a sensorimotor integration center. Only the deeper layers contain neurons which discharge in response to external stimuli, as well as in synchrony with eye movements, in the absence of external stimulationll,24,29, 34. Bergmann et al. 6 reported that electrical stimulation o f the rabbit's superior colliculus produces nystagmus if the animals are pretreated with drugs affecting the peripheral vestibular system. The effective drugs included local anesthetics. It is therefore possible that the rare instances of electrically evoked or spontaneous nystagmus in our experiments were caused by upward diffusion of the spinal anesthetic, although Syka et al. 81 had occasionally observed nystagmus following stimulation in the deeper tectal layers of freely moving cats. The observation that tectal activation produces or enhances nystagmus in predisposed animals is reminiscent of the beneficial results of stereotactic lesions in the superior colliculi of patients suffering f r o m central nystagmus 32. The electrically induced nystagmus with its fast phase in direction o f the simultaneously evoked conjugate eye deviation bears some resemblance to the gaze direction nystagmus or to fixation nystagmus of clinical neurology. The suppression o f spontaneous nystagmus by electrical stimulation is reminiscent of the well k n o w n suppression of vestibular nystagmus by fixation. ACKNOWLEDGEMENT

This work was supported by the Deutsche Forschungsgemeinschaft.

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