Brain Research, 97 (1975) 95-106 (~5 Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands
95
T H E E F F E C T OF PASSIVE EYE M O V E M E N T ON U N I T D I S C H A R G E IN T H E S U P E R I O R C O L L I C U L U S OF T H E CAT
P. K. ROSE* AND V. C. ABRAHAMS Department of Physiology, Queen's University, Kingston, Ont. K7L 3N6 (Canada)
(Accepted April 7th, 1975)
SUMMARY
The effects of passive eye rotation on unit discharge in the superior colliculus has been examined in the chloralose anaesthetized cat. Providing that velocity exceeded 50°/sec, passive eye movement led to brief-burst discharges in the superior colliculus. This discharge occurred as the eye traversed a fixed point. The displacement of this point from the primary position has been defined as the displacement threshold for that unit. Displacement thresholds range from 3 to 30 ° and are consistent over a wide range of velocities but become larger at the velocity threshold for the unit. Conduction times to the superior colliculus ranged from 7 to 108 msec.
1N T R O D U C T I O N
The central connections of extraocular muscle receptors are extensive and project to pontine and mesencephalic sites, the superior colliculus and cerebellum 1,~, v,lo,tl,13,t4,1v. Extraocular muscles are rich in receptors but the nature of the receptors varies from species to species. Muscle spindles are present in ungulates and primates, but in the cat no spindles are present and the receptors include a number of simpler forms of free nerve endings 12. Recordings made from single fibres in cat extraocular muscle nerves show that the receptors function both as length and tension detectors 6, 12. The functional role of the receptors has been a matter of conjecture for many years and is still not understood. We have recently demonstrated that the projection to the superior colliculus from extraocular muscle afferents in the cat is very rich, and that more units may be activated by these receptors than by retinal stimulation 2. The projection in part is concerned with head movements, for many of the cells in the * Present address: Department of Veterinary Physiology, Royal (Dick) Veterinary College, Edinburgh, Scotland.
96 superior colliculus excited by extraocular muscle afferents are cells of origin ~r,' thc tectospinal tract e. The experiments now described were concerned with the nature ol information conveyed in the projection to the superior colliculus l'rom extraocular muscle receptors in the cat. METHODS
Experiments were performed on 15 adult cats, weighing 2.5-3.8 kg, anaesthetized with chloralose (60 mg/kg, i.V.) after the induction of anaesthesia with ethyl chloride and ether. The cats were placed in a stereotaxic machine (La Precision Cinematographique, Asnieres, France), with their visual fields unobstructed. Just prior to electrical recording the animals were paralyzed with gallamine triethiodide (Flaxedil% Poulenc). The animal was then artificially ventilated and a bilateral pneumothorax created. The temperature of the animal was maintained between 37 and 39 ' C using a heated operating table. One eye, contralateral to the superior colliculus from which unit recordings were to be made, was protected from drying with a conventional contact lens. The other eye was prepared for passive movement of extraocular muscles by the technique of Fuchs and Kornhuber 14, and occluded with an opaque black contact lens. After appropriate bone removal a ligature was looped under the insertion of the lateral rectus muscle of the occluded eye, led forward around a pulley located in front of the cat, and attached to a king-Altec Vibrator (model 203) so that movement led to stretch of the lateral rectus. A ramp generator controlled the eye displacement and the eye was allowed to return passively to its rest position. The ramp generator was designed to allow the magnitude and velocity of eye movement to be controlled independently. Magnitude of movement could be varied from 0 to 30 ' and velocity could be varied from 0 to 750 ~'/sec. It was also possible to start the movement up to 30 nasal to the primary position. Movement was monitored with a length transducer (Hewlett-Packard lype 24 DCDT-250) attached to the moving element of the vibrator. The transducer output was displayed on a digital voltmeter and a storage oscilloscope to give a record of bolh initial position and induced deflection. Movements are expressed in degrees. To convert the transducer length to angular rotation, the globe diameter was assumed to be 19 m m when I m m -~: 6 ~' (see ref. 9). Unit activity within the superior colliculus was recorded with tungsten microelectrodes (Haer, type 25-10-3) introduced stereotaxically through a trephine hole over the occipital cortex. Spontaneous activity was rare in the superior colliculus, so, as the microelectrode was slowly advanced into the superior colliculus units were activated by a 2-msec flash of light to the non-occluded eye 2 or by electrical stimulation of one of the nerves to the neck muscles. It proved difficult to isolate single units in the superficial layers of the superior colliculus, and some of the recordings made there were from multi-unit preparations. Each unit or multi-unit preparation encountered was tested for its responsiveness to passive eye rotation. Upon completion of each electrode penetration the deepest position was marked by a small lesion made by passing 50-100/~A through the recording electrode for 1--2 sec. The amplification and display
97 techniques were conventional. In most experiments, unit spikes were converted into standardized pulses using an amplitude analyser (Haer) and successive sweeps were stored in one frame of a storage oscilloscope (Tektronix DI 3) with the aid of a raster generator (W-P Instruments). At the end of each experiment, the brain was perfused in situ with normal saline and then with 25 [}(,formaldehyde in saline. The location of each recording site in the midbrain was established from serial frontal sections, 30 ffm in thickness, stained for fibres and cells TM. Units within the superior colliculus were assigned to either the superficial, intermediate or deep layers of the superior colliculus using the anatomical criteria established by Cajal 8, Gordon t'5 and Szekely 2:~. Since the colliculotegmental border is not clearly defined in the cat 19, units which were ventral to a line extending horizontally from the lateral extent of the central grey were arbitrarily assigned to the tegmentum. Correlation coefficients were calculated by the least squares method. RESULTS
The responses of 57 well isolated single units to passive rotation of the eye have been examined, Forty-five (79 %) of the units were found in the superficial, intermediate and deep layers of the superior colliculus. The remaining 13 units were located in the tegmentum ventral to the superior colliculus. Sixteen multi-unit recordings were also made in the superficial layers of the superior colliculus. Data from a further 7 multi-unit responses in other parts of the superior colliculus have also been used. All movements of the eye were made in a nasal direction. Constant velocity nasal rotation of the eye provoked a brief burst of a few impulses only (Fig. 1), at all collicular and tegmental recording sites. Latencies of response were long and dependent on the velocity of eye rotation. For a 30 ° rotation at the maximum velocity employed (750'3/sec), latencies from the commencement of rotation to the recording of discharge
[11
,
120 l 40 msec Fig. 1. Relationship of eye rotation and unit discharge in the superior colliculus. Top, unit discharge ; bottom, transducer output. Rotation of 24' at 600'/sec completed in 40 msec.
98 ranged from 25 to 170 msec, with 61 of 80 (76'~,i) response latencies greater than 40 msec. A 30 :~ rotation at 750'/sec is complete within 40 msec so that unit discharge within the superior colliculus frequently occurs after eye movement is completed We have previously remarked on the rapid habituation of unit responses in the superior colliculus lollowing electrical excitation of extraocular muscle ncrves:L Habituation was equally pronounced when eye movement was used as a stimulus. A second attempt to elicit unit discharge was often unsuccessful if the interval between the two stimuli was too short. Responses could only be reliably recorded from the superior colliculus if the interval between successive rotations exceeded 10 sec.
Effect o f magnitude o f eye rotation on unit response In a series of experiments the velocity of eye rotation was kept constant at 750'~/sec. The velocity of' 750'/sec was chosen as it is well above the upper limits of saccadic velocity tbr the cat eye 0.21,ee, and thus should excite all movement-sensitive receptors. The eye was then rotated from the primary position to a position 3 0 nasal. In a series of measurements, the movement was reduced by 3' steps to a minimum rotation of 3 '~. Invariably, the discharge pattern was a brief burst and was unaltered as the magnitude of eye rotation decreased until rotation fell below a critical value. At this value, eye rotation no longer led to unit discharge. If the magnitude of eye rotation was now increased unit discharge to movement reappeared as soon as the critical value was exceeded. The minimum eye rotation necessary to elicit response in any given unit was a constant for that unit which we have defined as the displacement threshold. Any eye rotation at 750"/sec, whose magnitude was greater than the displacement threshold, produced the same discharge pattern. A wide range of displacement thresholds was found for units in the superior colliculus ranging from less than 6 ° to more than 24 ~', Fig. 2 shows the distribution of displacement thresholds meaDISPLACEMENT
THRESHOLD
20-
-25 -20
tO
u~ 1 5 Z
O Q,.
-15
oO
%
-, 10-
-10
d 5z
-5
o
0 o
6
12
18
24
30
ROTATION °
Fig. 2. Histogram illustrating the distribution of displacement thresholds of 57 isolated units and 23 multi-unit preparations recorded in the superior colliculus and adjacent tegmentum.
99 30-
-30
24":
O"
0 -r
0~-'-
----0
, 0_24
-18 m O
Z
N ua 12--
-12
¢D
.(
m a
6--
0 0
I 3
I I 6 9 INITIAL POSITION
I 12
I:
15
Fig. 3. The effect of displacing initial eye position in a nasal direction on the amplitude of constant velocity movement producing unit discharge in the superior colliculus. V - - V : actual movement necessary to produce unit discharge from the range of initial nasal displacements indicated on the abscissa. The displacement needed reduces as the initial position is moved nasally. G . . . . Q: displacement from the primary position which initiates unit discharge. This value is obtained by adding the initial displacement to the movement, so that the value given is the actual displacement from the primary position at which unit discharge is initiated in the superior colliculus.
sured at 750°/sec. It can be seen that more than 75 };~ of the units were excited by eye movement smaller than 24 ° . Experiments were performed on l0 units with large displacement thresholds ( > 20 °) to examine the effect of altering initial eye position on the displacement threshold, Displacement threshold was first determined from the primary position at a velocity of 750'~/sec. The eye was then subjected to a series of rotations each of which was initiated from a progressively more nasal position and the displacement necessary to elicit unit discharge established from each new initial position. These experiments established that when a unit has a large displacement threshold, unit discharge is not normally determined by the magnitude of passive rotation but occurs when the eye passes a position that is fixed with respect to the primary position (Fig. 3). The triangles in Fig. 3 show the reduction in actual movement necessary to initiate discharge as the eye is progressively moved closer to the displacement threshold. This may not be a characteristic of units with small displacement thresholds. Because of the design of the experiments just described, units with small displacement thresholds were not normally examined. However, on one occasion the relationship between initial eye position and displacement threshold was determined for a unit with a displacement threshold of only 5 °. This unit did not fire at a fixed position within the orbit, but to any nasal movement from 4.5 ° to 3 ~ depending on initial position. At an initial nasal deviation of 12 °, a further nasal displacement of 3 ° was necessary for excitation. With an initial nasal displacement of 3 °, a further nasal displacement of 4.5 ° was necessary for excitation.
100 VELOCITY
THRESHOLD
20-
-40
---
15-
-30
u... 10-
-20
0
oZ
, 5-
0
50
150
300
t[
-10
~
I
450
600
O
750
( °/see )
VELOCITY
Fig. 4. Velocity thresholds of 50 units in superior colliculus and underlying tegmentum.
Effect of velocity of eye rotation on unit response Velocity of movement itself can affect unit discharge in the superior cotliculus. The nature of this effect was examined in experiments on 50 units. The eye was rotated a constant 30 ° at velocities ranging from 50°/sec to 750°/sec. These experiments showed that a velocity threshold exists, but discharge is independent of the velocity of rotation until velocity falls below a critical value. The lowest velocity of eye movement at which unit response could be recorded we have defined as the velocity threshold for that unit. Velocity thresholds for 50 units are plotted in Fig. 4. Most units (78 ~ ) had velocity thresholds of between 50°/sec and 450°/sec. Two units responded between 450°/sec and 600°/sec and 9 units (I 8 %) required velocities in excess of 600°/sec for their excitation. Experiments were performed on 9 units to see whether displacement 20-
a,
15-
0
-r F-
~lOZ w
co
50/0\0 0
I
200
-O
I
1
400 600 VELOCITY (°/sec)
I
800
Fig. 5. The effect of displacement velocity on displacement threshold of unit in the superior colliculus.
10l 150
50
°~
67
750
"
\ 107
250 mS
Fig. 6. Discharges from unit in the superior colliculus to 8 sequential 30' nasal rotations. Velocities indicated in degrees/sec. Interval between rotations, 10 sec.
threshold is dependent on eye velocity. As can be seen in Fig. 5, except at velocities close to threshold displacement threshold is independent of velocity. In the experiment illustrated the displacement threshold remained relatively constant as velocity decreased from 750 ° to 200°/sec, but as the velocity threshold of the unit of 100~~/sec was approached the displacement threshold increased sharply. The existence of a fixed displacement threshold independent of velocity was 500" o
400"
J
--
o
3oo.w I00" ~ o J 0 o
o
,;o DURATION OF ROTATION(mS)
Fig. 7. D a t a from Fig. 6 r e p l o t t e d to s h o w the r e l a t i o n s h i p of response latency to d u r a t i o n of rotation. The o r d i n a t e intercept gives the central c o n d u c t i o n t i me to the s upe ri or colliculus, r ,- 0.999, latency 7.1 msec.
102 10
~6
5
E t-
O
0
20
40
60
80
100
120
c o n d u c t i o n t i m e (msec)
Fig. 8. Ordinate intercepts (central conduction time) of 27 units tested at a range of displacement velocities. Data from these units where correlation coefficients --_ 0.05.
emphasized in experiments in which the latency of collicular response was measured during fixed displacements at a range of velocities. The overall latency from the onset of movement to the onset of unit discharge determined in these experiments is dependent not only on the central conduction times, but also the displacement velocity (Fig. 6). A slow movement will take longer to arrive at the displacement threshold than a fast movement. The stability of the displacement threshold is reflected in the linearity of the slope when response latency is plotted against the duration of eye rotation (Fig. 7). In 27 of 33 units tested the l inearity of the relationship was such that the correlation coefficient was significant at the 0.05 ~ level. Lines plotted in this way have an ordinate intercept and this is the conduction time to the superior colliculus, for the value of the intercept represents the latency of response to an infinitely fast rotation. The range of central conduction times estimated in this way was from 7 to 108 msec (Fig. 8), values which are essentially the same as the conduction time to the superior colliculus following electrical excitation of extraocular muscle nerves ~, DISCUSSION
In her original experiments on extraocular muscle stretch, Fillenz ~3 described only a few responses in the superior colliculus, and those that were found were confined to the deep layers. From our experiments, it is clear that passive eye movement can lead to a discharge of cells in all layers in the superior colliculus of the cat as well as the underlying tegmentum, providing that both velocity and amplitude of movement are adequate. At no time in our experiments did we observe the sustained discharges that Fillenz a3 saw in the mesencephalic nucleus of the fifth nerve and in the deep collieular layers in barbiturate anaesthetized and decerebrate cats. The pattern of unit discharge that was invariably observed in our experiments was a brief-burst discharge similar to one pattern described by Fillenz 13.
103 The characteristics of passive muscle stretch that excite the receptors of the inferior oblique muscle of cat have been examined by Cooper and Fillenz 12 and by Bach-y-Rita and lto% Both groups of workers report that some receptors fire at rest, but the results of Bach-y-Rita and Ito 6 show that such units constitute a small minority, and that the majority of receptors (48 of 52) are dynamic receptors and only discharge to muscle length changes. The eye movement used in our experiments should mainly excite receptors in the lateral rectus muscle. Assuming that the receptors in the lateral rectus muscle have properties similar to those in the inferior oblique, then the dynamic nature of response in the superior colliculus is largely a reflection of receptor characteristics. When the data contained in Fig. 9 in the article by Bach-y-Rita and Ito 6 is replotted it is apparent then that in their experiments a linear relation exists between the time of onset of receptor discharge and the duration of the pull. Thus, there is a threshold stretch for receptor activation and the displacement threshold that we have observed in the superior colliculus may be a reflection of this receptor property. The relationship between passive eye movement and unit discharge in the superior collicular cells reported are, however, not entirely a replication of the sensory properties of extraocular muscle receptors. Two major differences exist between the responses of superior collicular cells described here and the responses of extraocular muscle stretch receptors described by Bach-y-Rita and Ito% Receptors in the inferior oblique muscle increase their firing frequency as the velocity of stretch increases 6, but, in the superior colliculus, once the critical velocity is exceeded, the pattern of discharge recorded in the superior colliculus is fixed and independent of the velocity of eye movement. Bachy-Rita and Ito 6 also found that the number of impulses and frequency of discharge to a constant stretch increased as initial muscle length was increased. Thus, the firing pattern of the receptor is sensitive to initial position unlike the firing pattern of units in the superior colliculus. It is unfortunate that in our experiments only one unit with a small displacement was tested for initial position effects. Small displacement thresholds of 6 ° or less were found in 18 ~,,, of the units. If the one small displacement threshold unit is typical, then it is possible that while the fixed displacement threshold is a characteristic of almost all collicular units, it is not an invariant pattern. Recently, we showed that almost 60 ~o of cells of origin of the tectospinal tract in the superior colliculus are excited by electrical stimulation of extraocular muscle afferent nerves% It seems reasonable to conclude that a significant percentage of units examined in this study are cells of origin of the tectospinal tract and thus make disynaptic connection with neck muscle motoneurones 4. Output to neck muscle motoneurones is thus likely to be influenced, in part, by movement of the eye in the orbit. The data now obtained shows that little influence is likely to be exerted at low eye velocities, or when the movements are small. It is only when large movements are executed at saccadic ve[ocities that the eye movement is likely to affect neck motoneurones. Then, because of the wide range of conduction times to the superior colliculus, an eye movement can set up a temporally dispersed bombardment of tectospinal cells which will greatly outlast the eye movement. In the cat eye movements from temporal to nasal extreme of 90 ° are possible 9 although 40 ~,, appears to be the
104 normal range"". ['he n l i n l l n u n l execution tinle of a 9 0 movemenl tit zt sacc~ldic velocity of 600/sec is 150 msec, and il is only in these extreme movements thai nicest of the discharge will occur in the superior colliculus during the e~e movement, At more normal levels of saccadic eye velocity of 300'?sec and for more reslricted m~,',ements precise information will be transmitted to the superior colliculus only after lhe eye movement has been completed and perhaps even after a new eye movelnenl has commenced. It should be noted that the effects of velocity are such that while most units are activated at velocities appropriate to saccadic movements in the cat, a proportion only fire at velocities which probably never normally occur. Because extraocular muscle afferents have the most abundant projection to the superior collicultis e, exceeding retinal and other muscle afferent projections ~, it is likely that these units are activated by such extraocular afferents. However, the technique of eye movement chosen, while it avoids the problem of limited receptor viability lhat occurs after enucleation t:~ does mean that other structures might be contributing to responses recorded in the superior collicuhls. An extraordinary habituation has been demonstrated in the alferent system to the superior collicuhis. This is not a receptor property for a similar habituation was observed when the afferent nerves were electrically excited z. The long latency tc,gether with the adaptation phenomena make it very difficult to propose a role for the system taking origin in the extraocular muscles and projecting to neck motoneurones. it is possible that to a degree these characteristics are imposed by the conditions of anaesthesia. However, chloralose does have some advantages as an anaesthetic in lhis situation, lbr it enables the long-latency responses of the superior collicutus to be demonstrated z, and it is known that brain responses to extraocular muscle stretch under chloralose are similar to those observed in the decerebrate cat la. Few data exist on the relationships between eye movement and unit discharge in the superior colticulus of the conscious cat. Relationships between spontaneous eye movement and unit discharge have been examined in the non-anaesthetized encdphale isol# by Straschill and Hoffman "° and by Arduini el al,:'. Straschill and Hoffman ~° reported that 10 I~; of the units that they observed fired in synchrony with spontaneous movement during total darkness. Discharge could occur prior to or during the movement, or 50-100 msec after the onset of movement. Neither the velocity nor lho magnitude of movements was reported in their experiments. Movement was recorded in the experiments of Arduini et a/. a by a modified Robinson Is technique permitting accurate resolution of movement. They report that eye movement in the eric@hale isol~J during 'sleep' has excursions of ti'om 4 to 5 and peak velocities of 1 30' see. During 'arousal' the excursions were reduced below 1, but velocities increased to 3-20°/sec. In this situation Arduini et al. ~ claimed that more than 80',~,,i of units in the superior colliculus had activity correlated with the small eye movements that they observed. Usually unit discharge preceded eye movement from a l?w to 100 msec. It seems unlikely that the firing patterns that were observed in the superior colliculus in either of these reports could be due to activation of extraocular muscle receptors. Our data would suggest that spontaneous eye movement in the encdphate isolO never achieves either sufficient velocity or amplitude to activate units in the superior col li-
105 culus. The movements are also below threshold for extraocular muscle receptors 6. The data so far obtained in the encdphale isold must have sources other than extraocular muscle receptors and may signal events leading up to movement and connected with movement, but not information arising from the extraocular muscle receptors ACKNOWLEDGEMENT
Supported by the M.R.C. of Canada.
REFERENCES 1 ABRAHAMS,V. C., RICHMOND, F., AND ROSE, P. K., Proprioceptive and retinal afferent connections to the superior colliculus of the cat and their connections to the tectospinal tract, J. Physiol. (Lond.), 241 0974) 101-102P. 2 ABRAHAMS,V. C., AND ROSE, P. K., Projections of extraocular, neck muscle and retinal afferents to the superior colliculus in the cat: their connections to the cells of origin of the tectospinal tract, J. Neurophysiol., 38 0975) 10-18. 3 ABRAHAMS,V. C., AND ROSE, P. K., The spinal course and distribution of fore and hind limb muscle afferent projections to the superior colliculus of the cat, J. Physiol. (Lond.), 247 (1975) 117-130. 4 ANDERSON, M., YOSHIDA, M., AND WILSON, V. J., Influence of superior colliculus on cat neck motoneurones, J. Neurophysiol., 34 (1971 ) 898-907. 5 ARDUINI, A., CORAZZA, R., AND MARZOLLO, P., Relationships of the neuronal activity of the superior colliculus to eye movements in the cat, Brain Research, 73 (1974) 473-481. 6 BACH-Y-RrrA, P., AND ITO, F., Properties of stretch receptors in cat extraocular muscles, J. Physiol. (Land.), 186 (1966) 663-688. 7 BAKER,R., PRECHT., AND LLIN,~S, R., Mossy and climbing fiber projections of extraocular muscle afferents to the cerebellum, Brain Research, 38 (1972) 440 445. 8 CAJAL, S. RAM(')N Y, Histologie du SystOme Nerveux de I'Homme et des Vertdbrds, Consejo de Investigaciones Cientificas, Madrid, 1911. 9 COLL1NS, C. C., Orbital mechanics, in P. BACH-Y-RITA, C. C. COLLINS AND J. E. HYDE (Eds.), The Control of Eye Movements, Academic Press, New York, 1971, pp. 283 326. 10 COOPER, S., DANIEL, P. M., AND WHITTERIDGE, D., Nerve impulses in the brainstem of the goat. Responses with long latencies obtained by stretching the extrinsic eye muscles, J. Physiol. (Lond.), 120 (1953) 491-513. 1 1 COOPER, S., DANIEL, P. M., AND WHITTERII)GE, D., Muscle spindles and other sensory endings in the extrinsic eye rnuscles; the physiology and anatomy of these receptors and of their connexions with the brain stem, Brain, 78 (1955) 564 583. 12 COOPER, S., AND FILLENZ, M., Afferent discharges in response to stretch from the extraocular muscles of the cat and monkey and the innervation of these muscles, J. Physiol. (Lond.), 127 (1955) 400-413. 13 FJLLENZ, M., Responses in the brain stem of the cat to stretch of extrinsic ocular muscles, J. Physial. (Lond.), 128 (1955) 182 199. 14 FrotHS, A. F., AND KORNHUBER, H. H., Extraocular muscle afl'erents to the cerebellum of the cat, J. Physiol. (Lond.), 200 (1969) 713-722. 15 GORDON, B., Receptive fields in deep layers of cat superior colliculus, J. Neurophysiol., 36 (1973) 15% 178. 16 KL(~VER, H., AND BARRERA, E., A method for the combined staining of cells and fibres in the nervous system, J. Neuropath. exp. Neurol., 12 (1953) 400-403. 17 MANNI, E., PALMIERI, G., AND MARINI, R., Mesodiencephalic representation of the eye muscle proprioception, Exp. Neurol., 37 (1972) 412-421. 18 ROBINSON, D., A method of measuring eye movement using a scleral search coil in a magnetic field, I.E.E.E. Trans. Bio-Med. Engng., 10 (1963) 137 145. 19 SPRAGUE, J. M., BERLUCCHI, G., AND RIZZOLATTI, G., The role of the superior colliculus and
106
20 21 22 23
pretectum in vision and visually guided behaviour. In R. JtJNG (Ed.l, Handbook o/,he~ts,J~v Physiolog~v, Springer, Berlin, 1973, pp. 27 101. STRAS('HII.L, M., AND HOFI~MAN, K. P., Activity of movement sensitive neurons of the c;~T's tectum opticum during spontaneous eye movements, Exp. Brain Res., I 1 (1970) 318--326. STRASCHILL,M., AND Rt~C;~R, P., Eye movements evoked by local stimulation of the cat's supcrior colliculus, Brain Research, 59 (1973) 211 227. STRYKt~R, M., AND BLAKtMfJRI, C., Saccadic and disjunctive eye movements in cats, l~i.~'hmRes., 12 (1972) 2005 2013. SZEKELY, G., Anatomy and synaptology of the optic rectum. In R. JuN~.i (t~d.), Hamlbo,~ ¢~f Sensory Physiology. Springer, Berlin, 1973, pp. 1 ~26.
95
T H E E F F E C T OF PASSIVE EYE M O V E M E N T ON U N I T D I S C H A R G E IN T H E S U P E R I O R C O L L I C U L U S OF T H E CAT
P. K. ROSE* AND V. C. ABRAHAMS Department of Physiology, Queen's University, Kingston, Ont. K7L 3N6 (Canada)
(Accepted April 7th, 1975)
SUMMARY
The effects of passive eye rotation on unit discharge in the superior colliculus has been examined in the chloralose anaesthetized cat. Providing that velocity exceeded 50°/sec, passive eye movement led to brief-burst discharges in the superior colliculus. This discharge occurred as the eye traversed a fixed point. The displacement of this point from the primary position has been defined as the displacement threshold for that unit. Displacement thresholds range from 3 to 30 ° and are consistent over a wide range of velocities but become larger at the velocity threshold for the unit. Conduction times to the superior colliculus ranged from 7 to 108 msec.
1N T R O D U C T I O N
The central connections of extraocular muscle receptors are extensive and project to pontine and mesencephalic sites, the superior colliculus and cerebellum 1,~, v,lo,tl,13,t4,1v. Extraocular muscles are rich in receptors but the nature of the receptors varies from species to species. Muscle spindles are present in ungulates and primates, but in the cat no spindles are present and the receptors include a number of simpler forms of free nerve endings 12. Recordings made from single fibres in cat extraocular muscle nerves show that the receptors function both as length and tension detectors 6, 12. The functional role of the receptors has been a matter of conjecture for many years and is still not understood. We have recently demonstrated that the projection to the superior colliculus from extraocular muscle afferents in the cat is very rich, and that more units may be activated by these receptors than by retinal stimulation 2. The projection in part is concerned with head movements, for many of the cells in the * Present address: Department of Veterinary Physiology, Royal (Dick) Veterinary College, Edinburgh, Scotland.
96 superior colliculus excited by extraocular muscle afferents are cells of origin ~r,' thc tectospinal tract e. The experiments now described were concerned with the nature ol information conveyed in the projection to the superior colliculus l'rom extraocular muscle receptors in the cat. METHODS
Experiments were performed on 15 adult cats, weighing 2.5-3.8 kg, anaesthetized with chloralose (60 mg/kg, i.V.) after the induction of anaesthesia with ethyl chloride and ether. The cats were placed in a stereotaxic machine (La Precision Cinematographique, Asnieres, France), with their visual fields unobstructed. Just prior to electrical recording the animals were paralyzed with gallamine triethiodide (Flaxedil% Poulenc). The animal was then artificially ventilated and a bilateral pneumothorax created. The temperature of the animal was maintained between 37 and 39 ' C using a heated operating table. One eye, contralateral to the superior colliculus from which unit recordings were to be made, was protected from drying with a conventional contact lens. The other eye was prepared for passive movement of extraocular muscles by the technique of Fuchs and Kornhuber 14, and occluded with an opaque black contact lens. After appropriate bone removal a ligature was looped under the insertion of the lateral rectus muscle of the occluded eye, led forward around a pulley located in front of the cat, and attached to a king-Altec Vibrator (model 203) so that movement led to stretch of the lateral rectus. A ramp generator controlled the eye displacement and the eye was allowed to return passively to its rest position. The ramp generator was designed to allow the magnitude and velocity of eye movement to be controlled independently. Magnitude of movement could be varied from 0 to 30 ' and velocity could be varied from 0 to 750 ~'/sec. It was also possible to start the movement up to 30 nasal to the primary position. Movement was monitored with a length transducer (Hewlett-Packard lype 24 DCDT-250) attached to the moving element of the vibrator. The transducer output was displayed on a digital voltmeter and a storage oscilloscope to give a record of bolh initial position and induced deflection. Movements are expressed in degrees. To convert the transducer length to angular rotation, the globe diameter was assumed to be 19 m m when I m m -~: 6 ~' (see ref. 9). Unit activity within the superior colliculus was recorded with tungsten microelectrodes (Haer, type 25-10-3) introduced stereotaxically through a trephine hole over the occipital cortex. Spontaneous activity was rare in the superior colliculus, so, as the microelectrode was slowly advanced into the superior colliculus units were activated by a 2-msec flash of light to the non-occluded eye 2 or by electrical stimulation of one of the nerves to the neck muscles. It proved difficult to isolate single units in the superficial layers of the superior colliculus, and some of the recordings made there were from multi-unit preparations. Each unit or multi-unit preparation encountered was tested for its responsiveness to passive eye rotation. Upon completion of each electrode penetration the deepest position was marked by a small lesion made by passing 50-100/~A through the recording electrode for 1--2 sec. The amplification and display
97 techniques were conventional. In most experiments, unit spikes were converted into standardized pulses using an amplitude analyser (Haer) and successive sweeps were stored in one frame of a storage oscilloscope (Tektronix DI 3) with the aid of a raster generator (W-P Instruments). At the end of each experiment, the brain was perfused in situ with normal saline and then with 25 [}(,formaldehyde in saline. The location of each recording site in the midbrain was established from serial frontal sections, 30 ffm in thickness, stained for fibres and cells TM. Units within the superior colliculus were assigned to either the superficial, intermediate or deep layers of the superior colliculus using the anatomical criteria established by Cajal 8, Gordon t'5 and Szekely 2:~. Since the colliculotegmental border is not clearly defined in the cat 19, units which were ventral to a line extending horizontally from the lateral extent of the central grey were arbitrarily assigned to the tegmentum. Correlation coefficients were calculated by the least squares method. RESULTS
The responses of 57 well isolated single units to passive rotation of the eye have been examined, Forty-five (79 %) of the units were found in the superficial, intermediate and deep layers of the superior colliculus. The remaining 13 units were located in the tegmentum ventral to the superior colliculus. Sixteen multi-unit recordings were also made in the superficial layers of the superior colliculus. Data from a further 7 multi-unit responses in other parts of the superior colliculus have also been used. All movements of the eye were made in a nasal direction. Constant velocity nasal rotation of the eye provoked a brief burst of a few impulses only (Fig. 1), at all collicular and tegmental recording sites. Latencies of response were long and dependent on the velocity of eye rotation. For a 30 ° rotation at the maximum velocity employed (750'3/sec), latencies from the commencement of rotation to the recording of discharge
[11
,
120 l 40 msec Fig. 1. Relationship of eye rotation and unit discharge in the superior colliculus. Top, unit discharge ; bottom, transducer output. Rotation of 24' at 600'/sec completed in 40 msec.
98 ranged from 25 to 170 msec, with 61 of 80 (76'~,i) response latencies greater than 40 msec. A 30 :~ rotation at 750'/sec is complete within 40 msec so that unit discharge within the superior colliculus frequently occurs after eye movement is completed We have previously remarked on the rapid habituation of unit responses in the superior colliculus lollowing electrical excitation of extraocular muscle ncrves:L Habituation was equally pronounced when eye movement was used as a stimulus. A second attempt to elicit unit discharge was often unsuccessful if the interval between the two stimuli was too short. Responses could only be reliably recorded from the superior colliculus if the interval between successive rotations exceeded 10 sec.
Effect o f magnitude o f eye rotation on unit response In a series of experiments the velocity of eye rotation was kept constant at 750'~/sec. The velocity of' 750'/sec was chosen as it is well above the upper limits of saccadic velocity tbr the cat eye 0.21,ee, and thus should excite all movement-sensitive receptors. The eye was then rotated from the primary position to a position 3 0 nasal. In a series of measurements, the movement was reduced by 3' steps to a minimum rotation of 3 '~. Invariably, the discharge pattern was a brief burst and was unaltered as the magnitude of eye rotation decreased until rotation fell below a critical value. At this value, eye rotation no longer led to unit discharge. If the magnitude of eye rotation was now increased unit discharge to movement reappeared as soon as the critical value was exceeded. The minimum eye rotation necessary to elicit response in any given unit was a constant for that unit which we have defined as the displacement threshold. Any eye rotation at 750"/sec, whose magnitude was greater than the displacement threshold, produced the same discharge pattern. A wide range of displacement thresholds was found for units in the superior colliculus ranging from less than 6 ° to more than 24 ~', Fig. 2 shows the distribution of displacement thresholds meaDISPLACEMENT
THRESHOLD
20-
-25 -20
tO
u~ 1 5 Z
O Q,.
-15
oO
%
-, 10-
-10
d 5z
-5
o
0 o
6
12
18
24
30
ROTATION °
Fig. 2. Histogram illustrating the distribution of displacement thresholds of 57 isolated units and 23 multi-unit preparations recorded in the superior colliculus and adjacent tegmentum.
99 30-
-30
24":
O"
0 -r
0~-'-
----0
, 0_24
-18 m O
Z
N ua 12--
-12
¢D
.(
m a
6--
0 0
I 3
I I 6 9 INITIAL POSITION
I 12
I:
15
Fig. 3. The effect of displacing initial eye position in a nasal direction on the amplitude of constant velocity movement producing unit discharge in the superior colliculus. V - - V : actual movement necessary to produce unit discharge from the range of initial nasal displacements indicated on the abscissa. The displacement needed reduces as the initial position is moved nasally. G . . . . Q: displacement from the primary position which initiates unit discharge. This value is obtained by adding the initial displacement to the movement, so that the value given is the actual displacement from the primary position at which unit discharge is initiated in the superior colliculus.
sured at 750°/sec. It can be seen that more than 75 };~ of the units were excited by eye movement smaller than 24 ° . Experiments were performed on l0 units with large displacement thresholds ( > 20 °) to examine the effect of altering initial eye position on the displacement threshold, Displacement threshold was first determined from the primary position at a velocity of 750'~/sec. The eye was then subjected to a series of rotations each of which was initiated from a progressively more nasal position and the displacement necessary to elicit unit discharge established from each new initial position. These experiments established that when a unit has a large displacement threshold, unit discharge is not normally determined by the magnitude of passive rotation but occurs when the eye passes a position that is fixed with respect to the primary position (Fig. 3). The triangles in Fig. 3 show the reduction in actual movement necessary to initiate discharge as the eye is progressively moved closer to the displacement threshold. This may not be a characteristic of units with small displacement thresholds. Because of the design of the experiments just described, units with small displacement thresholds were not normally examined. However, on one occasion the relationship between initial eye position and displacement threshold was determined for a unit with a displacement threshold of only 5 °. This unit did not fire at a fixed position within the orbit, but to any nasal movement from 4.5 ° to 3 ~ depending on initial position. At an initial nasal deviation of 12 °, a further nasal displacement of 3 ° was necessary for excitation. With an initial nasal displacement of 3 °, a further nasal displacement of 4.5 ° was necessary for excitation.
100 VELOCITY
THRESHOLD
20-
-40
---
15-
-30
u... 10-
-20
0
oZ
, 5-
0
50
150
300
t[
-10
~
I
450
600
O
750
( °/see )
VELOCITY
Fig. 4. Velocity thresholds of 50 units in superior colliculus and underlying tegmentum.
Effect of velocity of eye rotation on unit response Velocity of movement itself can affect unit discharge in the superior cotliculus. The nature of this effect was examined in experiments on 50 units. The eye was rotated a constant 30 ° at velocities ranging from 50°/sec to 750°/sec. These experiments showed that a velocity threshold exists, but discharge is independent of the velocity of rotation until velocity falls below a critical value. The lowest velocity of eye movement at which unit response could be recorded we have defined as the velocity threshold for that unit. Velocity thresholds for 50 units are plotted in Fig. 4. Most units (78 ~ ) had velocity thresholds of between 50°/sec and 450°/sec. Two units responded between 450°/sec and 600°/sec and 9 units (I 8 %) required velocities in excess of 600°/sec for their excitation. Experiments were performed on 9 units to see whether displacement 20-
a,
15-
0
-r F-
~lOZ w
co
50/0\0 0
I
200
-O
I
1
400 600 VELOCITY (°/sec)
I
800
Fig. 5. The effect of displacement velocity on displacement threshold of unit in the superior colliculus.
10l 150
50
°~
67
750
"
\ 107
250 mS
Fig. 6. Discharges from unit in the superior colliculus to 8 sequential 30' nasal rotations. Velocities indicated in degrees/sec. Interval between rotations, 10 sec.
threshold is dependent on eye velocity. As can be seen in Fig. 5, except at velocities close to threshold displacement threshold is independent of velocity. In the experiment illustrated the displacement threshold remained relatively constant as velocity decreased from 750 ° to 200°/sec, but as the velocity threshold of the unit of 100~~/sec was approached the displacement threshold increased sharply. The existence of a fixed displacement threshold independent of velocity was 500" o
400"
J
--
o
3oo.w I00" ~ o J 0 o
o
,;o DURATION OF ROTATION(mS)
Fig. 7. D a t a from Fig. 6 r e p l o t t e d to s h o w the r e l a t i o n s h i p of response latency to d u r a t i o n of rotation. The o r d i n a t e intercept gives the central c o n d u c t i o n t i me to the s upe ri or colliculus, r ,- 0.999, latency 7.1 msec.
102 10
~6
5
E t-
O
0
20
40
60
80
100
120
c o n d u c t i o n t i m e (msec)
Fig. 8. Ordinate intercepts (central conduction time) of 27 units tested at a range of displacement velocities. Data from these units where correlation coefficients --_ 0.05.
emphasized in experiments in which the latency of collicular response was measured during fixed displacements at a range of velocities. The overall latency from the onset of movement to the onset of unit discharge determined in these experiments is dependent not only on the central conduction times, but also the displacement velocity (Fig. 6). A slow movement will take longer to arrive at the displacement threshold than a fast movement. The stability of the displacement threshold is reflected in the linearity of the slope when response latency is plotted against the duration of eye rotation (Fig. 7). In 27 of 33 units tested the l inearity of the relationship was such that the correlation coefficient was significant at the 0.05 ~ level. Lines plotted in this way have an ordinate intercept and this is the conduction time to the superior colliculus, for the value of the intercept represents the latency of response to an infinitely fast rotation. The range of central conduction times estimated in this way was from 7 to 108 msec (Fig. 8), values which are essentially the same as the conduction time to the superior colliculus following electrical excitation of extraocular muscle nerves ~, DISCUSSION
In her original experiments on extraocular muscle stretch, Fillenz ~3 described only a few responses in the superior colliculus, and those that were found were confined to the deep layers. From our experiments, it is clear that passive eye movement can lead to a discharge of cells in all layers in the superior colliculus of the cat as well as the underlying tegmentum, providing that both velocity and amplitude of movement are adequate. At no time in our experiments did we observe the sustained discharges that Fillenz a3 saw in the mesencephalic nucleus of the fifth nerve and in the deep collieular layers in barbiturate anaesthetized and decerebrate cats. The pattern of unit discharge that was invariably observed in our experiments was a brief-burst discharge similar to one pattern described by Fillenz 13.
103 The characteristics of passive muscle stretch that excite the receptors of the inferior oblique muscle of cat have been examined by Cooper and Fillenz 12 and by Bach-y-Rita and lto% Both groups of workers report that some receptors fire at rest, but the results of Bach-y-Rita and Ito 6 show that such units constitute a small minority, and that the majority of receptors (48 of 52) are dynamic receptors and only discharge to muscle length changes. The eye movement used in our experiments should mainly excite receptors in the lateral rectus muscle. Assuming that the receptors in the lateral rectus muscle have properties similar to those in the inferior oblique, then the dynamic nature of response in the superior colliculus is largely a reflection of receptor characteristics. When the data contained in Fig. 9 in the article by Bach-y-Rita and Ito 6 is replotted it is apparent then that in their experiments a linear relation exists between the time of onset of receptor discharge and the duration of the pull. Thus, there is a threshold stretch for receptor activation and the displacement threshold that we have observed in the superior colliculus may be a reflection of this receptor property. The relationship between passive eye movement and unit discharge in the superior collicular cells reported are, however, not entirely a replication of the sensory properties of extraocular muscle receptors. Two major differences exist between the responses of superior collicular cells described here and the responses of extraocular muscle stretch receptors described by Bach-y-Rita and Ito% Receptors in the inferior oblique muscle increase their firing frequency as the velocity of stretch increases 6, but, in the superior colliculus, once the critical velocity is exceeded, the pattern of discharge recorded in the superior colliculus is fixed and independent of the velocity of eye movement. Bachy-Rita and Ito 6 also found that the number of impulses and frequency of discharge to a constant stretch increased as initial muscle length was increased. Thus, the firing pattern of the receptor is sensitive to initial position unlike the firing pattern of units in the superior colliculus. It is unfortunate that in our experiments only one unit with a small displacement was tested for initial position effects. Small displacement thresholds of 6 ° or less were found in 18 ~,,, of the units. If the one small displacement threshold unit is typical, then it is possible that while the fixed displacement threshold is a characteristic of almost all collicular units, it is not an invariant pattern. Recently, we showed that almost 60 ~o of cells of origin of the tectospinal tract in the superior colliculus are excited by electrical stimulation of extraocular muscle afferent nerves% It seems reasonable to conclude that a significant percentage of units examined in this study are cells of origin of the tectospinal tract and thus make disynaptic connection with neck muscle motoneurones 4. Output to neck muscle motoneurones is thus likely to be influenced, in part, by movement of the eye in the orbit. The data now obtained shows that little influence is likely to be exerted at low eye velocities, or when the movements are small. It is only when large movements are executed at saccadic ve[ocities that the eye movement is likely to affect neck motoneurones. Then, because of the wide range of conduction times to the superior colliculus, an eye movement can set up a temporally dispersed bombardment of tectospinal cells which will greatly outlast the eye movement. In the cat eye movements from temporal to nasal extreme of 90 ° are possible 9 although 40 ~,, appears to be the
104 normal range"". ['he n l i n l l n u n l execution tinle of a 9 0 movemenl tit zt sacc~ldic velocity of 600/sec is 150 msec, and il is only in these extreme movements thai nicest of the discharge will occur in the superior colliculus during the e~e movement, At more normal levels of saccadic eye velocity of 300'?sec and for more reslricted m~,',ements precise information will be transmitted to the superior colliculus only after lhe eye movement has been completed and perhaps even after a new eye movelnenl has commenced. It should be noted that the effects of velocity are such that while most units are activated at velocities appropriate to saccadic movements in the cat, a proportion only fire at velocities which probably never normally occur. Because extraocular muscle afferents have the most abundant projection to the superior collicultis e, exceeding retinal and other muscle afferent projections ~, it is likely that these units are activated by such extraocular afferents. However, the technique of eye movement chosen, while it avoids the problem of limited receptor viability lhat occurs after enucleation t:~ does mean that other structures might be contributing to responses recorded in the superior collicuhls. An extraordinary habituation has been demonstrated in the alferent system to the superior collicuhis. This is not a receptor property for a similar habituation was observed when the afferent nerves were electrically excited z. The long latency tc,gether with the adaptation phenomena make it very difficult to propose a role for the system taking origin in the extraocular muscles and projecting to neck motoneurones. it is possible that to a degree these characteristics are imposed by the conditions of anaesthesia. However, chloralose does have some advantages as an anaesthetic in lhis situation, lbr it enables the long-latency responses of the superior collicutus to be demonstrated z, and it is known that brain responses to extraocular muscle stretch under chloralose are similar to those observed in the decerebrate cat la. Few data exist on the relationships between eye movement and unit discharge in the superior colticulus of the conscious cat. Relationships between spontaneous eye movement and unit discharge have been examined in the non-anaesthetized encdphale isol# by Straschill and Hoffman "° and by Arduini el al,:'. Straschill and Hoffman ~° reported that 10 I~; of the units that they observed fired in synchrony with spontaneous movement during total darkness. Discharge could occur prior to or during the movement, or 50-100 msec after the onset of movement. Neither the velocity nor lho magnitude of movements was reported in their experiments. Movement was recorded in the experiments of Arduini et a/. a by a modified Robinson Is technique permitting accurate resolution of movement. They report that eye movement in the eric@hale isol~J during 'sleep' has excursions of ti'om 4 to 5 and peak velocities of 1 30' see. During 'arousal' the excursions were reduced below 1, but velocities increased to 3-20°/sec. In this situation Arduini et al. ~ claimed that more than 80',~,,i of units in the superior colliculus had activity correlated with the small eye movements that they observed. Usually unit discharge preceded eye movement from a l?w to 100 msec. It seems unlikely that the firing patterns that were observed in the superior colliculus in either of these reports could be due to activation of extraocular muscle receptors. Our data would suggest that spontaneous eye movement in the encdphate isolO never achieves either sufficient velocity or amplitude to activate units in the superior col li-
105 culus. The movements are also below threshold for extraocular muscle receptors 6. The data so far obtained in the encdphale isold must have sources other than extraocular muscle receptors and may signal events leading up to movement and connected with movement, but not information arising from the extraocular muscle receptors ACKNOWLEDGEMENT
Supported by the M.R.C. of Canada.
REFERENCES 1 ABRAHAMS,V. C., RICHMOND, F., AND ROSE, P. K., Proprioceptive and retinal afferent connections to the superior colliculus of the cat and their connections to the tectospinal tract, J. Physiol. (Lond.), 241 0974) 101-102P. 2 ABRAHAMS,V. C., AND ROSE, P. K., Projections of extraocular, neck muscle and retinal afferents to the superior colliculus in the cat: their connections to the cells of origin of the tectospinal tract, J. Neurophysiol., 38 0975) 10-18. 3 ABRAHAMS,V. C., AND ROSE, P. K., The spinal course and distribution of fore and hind limb muscle afferent projections to the superior colliculus of the cat, J. Physiol. (Lond.), 247 (1975) 117-130. 4 ANDERSON, M., YOSHIDA, M., AND WILSON, V. J., Influence of superior colliculus on cat neck motoneurones, J. Neurophysiol., 34 (1971 ) 898-907. 5 ARDUINI, A., CORAZZA, R., AND MARZOLLO, P., Relationships of the neuronal activity of the superior colliculus to eye movements in the cat, Brain Research, 73 (1974) 473-481. 6 BACH-Y-RrrA, P., AND ITO, F., Properties of stretch receptors in cat extraocular muscles, J. Physiol. (Land.), 186 (1966) 663-688. 7 BAKER,R., PRECHT., AND LLIN,~S, R., Mossy and climbing fiber projections of extraocular muscle afferents to the cerebellum, Brain Research, 38 (1972) 440 445. 8 CAJAL, S. RAM(')N Y, Histologie du SystOme Nerveux de I'Homme et des Vertdbrds, Consejo de Investigaciones Cientificas, Madrid, 1911. 9 COLL1NS, C. C., Orbital mechanics, in P. BACH-Y-RITA, C. C. COLLINS AND J. E. HYDE (Eds.), The Control of Eye Movements, Academic Press, New York, 1971, pp. 283 326. 10 COOPER, S., DANIEL, P. M., AND WHITTERIDGE, D., Nerve impulses in the brainstem of the goat. Responses with long latencies obtained by stretching the extrinsic eye muscles, J. Physiol. (Lond.), 120 (1953) 491-513. 1 1 COOPER, S., DANIEL, P. M., AND WHITTERII)GE, D., Muscle spindles and other sensory endings in the extrinsic eye rnuscles; the physiology and anatomy of these receptors and of their connexions with the brain stem, Brain, 78 (1955) 564 583. 12 COOPER, S., AND FILLENZ, M., Afferent discharges in response to stretch from the extraocular muscles of the cat and monkey and the innervation of these muscles, J. Physiol. (Lond.), 127 (1955) 400-413. 13 FJLLENZ, M., Responses in the brain stem of the cat to stretch of extrinsic ocular muscles, J. Physial. (Lond.), 128 (1955) 182 199. 14 FrotHS, A. F., AND KORNHUBER, H. H., Extraocular muscle afl'erents to the cerebellum of the cat, J. Physiol. (Lond.), 200 (1969) 713-722. 15 GORDON, B., Receptive fields in deep layers of cat superior colliculus, J. Neurophysiol., 36 (1973) 15% 178. 16 KL(~VER, H., AND BARRERA, E., A method for the combined staining of cells and fibres in the nervous system, J. Neuropath. exp. Neurol., 12 (1953) 400-403. 17 MANNI, E., PALMIERI, G., AND MARINI, R., Mesodiencephalic representation of the eye muscle proprioception, Exp. Neurol., 37 (1972) 412-421. 18 ROBINSON, D., A method of measuring eye movement using a scleral search coil in a magnetic field, I.E.E.E. Trans. Bio-Med. Engng., 10 (1963) 137 145. 19 SPRAGUE, J. M., BERLUCCHI, G., AND RIZZOLATTI, G., The role of the superior colliculus and
106
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pretectum in vision and visually guided behaviour. In R. JtJNG (Ed.l, Handbook o/,he~ts,J~v Physiolog~v, Springer, Berlin, 1973, pp. 27 101. STRAS('HII.L, M., AND HOFI~MAN, K. P., Activity of movement sensitive neurons of the c;~T's tectum opticum during spontaneous eye movements, Exp. Brain Res., I 1 (1970) 318--326. STRASCHILL,M., AND Rt~C;~R, P., Eye movements evoked by local stimulation of the cat's supcrior colliculus, Brain Research, 59 (1973) 211 227. STRYKt~R, M., AND BLAKtMfJRI, C., Saccadic and disjunctive eye movements in cats, l~i.~'hmRes., 12 (1972) 2005 2013. SZEKELY, G., Anatomy and synaptology of the optic rectum. In R. JuN~.i (t~d.), Hamlbo,~ ¢~f Sensory Physiology. Springer, Berlin, 1973, pp. 1 ~26.
