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Visual Fixation: a Collicular Reflex?
Visual Fixation: a Collicular Reflex? A. ROUCOUX*, M. CROMMELINCK and M. MEULDERS
Laboratoire de Neurophysiologie, Universitd Catholique a2 Louvain, 1200 Bruxelles (Belgium)
Superior colliculus (SC) is undoubtedly concerned with gaze orientation. Quite demonstrative experiments in the monkey (Robinson, 1972; Schiller and Stryker, 1972) have given a strongsupport to the “foveation hypothesis”. According to this model, when a stimulussuddenly appears within the animal’svisual field or when a particular detail of the visual environment is chosen by the animal as a target, a restricted zone within the sensory upper collicular layers is activated. To the retinotopy of these upper layers corresponds a similar spatial organization in the deep “motor” or efferent layers, a “motor map”. The focal activation of the sensory layers is transmitted to the deep layers which are in register. After an adequate signal processing, a still mysterious spatiotemporal translation (Robinson, 1973), the signal is fed to the ocular motoneurons who manage to bring the image of the stimulusonto the fovea. It is to be noted that, in this model, the collicularsignal merely acts as a trigger of a preprogrammed ballistic saccade. Direction and amplitude of this saccade are spatially or, better, topographically encoded in the SC. The direct transmission of information from upper sensory to lower premotor layers is however questioned bysomeobservations(Moh1erand Wurtz, 1976; WurtzandMohler, 1976). These authors assert that the temporal sequence of neuronal events they record within the collicular layers is in contradiction with this straightforward foveation hypothesis. However, for the monkeys used in these experiments, unavoidably overtrained, stimuli are hardly sudden and unexpected and their behavioral significance is far different from the naturally occurring visual stimulus which is supposed to trigger a fixation reflex in response to a “what is that?”. The contradiction between an attentionshifting and motor command mechanism thus appears rather artificial. It is obvious that the choice of a new target is necessarily correlated with an attention shift. We may admit that the primate SCis involved in reflex orientation of the eyes and operates some sort of sensory-motor point to point translation, be it with the help of a downward, upward flow of information or both. This attractive foveation hypothesis and the fact that monkey’s SC does not seem to directly participate in head orientation (Robinson and Jarvis, 1974; Stryker and Schiller, 1975) maybe has somewhat obscured the implications of old and well established observations in non-primates. The famous “visual grasp reflex” (Hess et al., 1946) is a ~~
*Charge de Recherches, F.N.R.S., Belgium.
746 synchronous movement of eye and head, both cooperating in the achievement of a goal-directed gaze shift. Let us remember that in all species in which SC or tectum has been electrically stimulated, body, head, eye and even pinnae orienting movements have been observed (see bibliography in Roucoux and Crommelinck, 1976).Eye saccade is only one component of a whole sequence of orienting movements. Let us also note that, in the cat, for example, the range of eye movements is only 20"-23" from the primary position (Crommelinck et al., 1977a), and that the retinotopic projection onto the SC covers 70" and more of visual field (Feldon et al., 1970). Thus obviously,the simple and attractive foveation model involving the eye alone does not apply as such to subprimates. The divergence of results of SC stimulation in cats and monkeys constitutes another argument and will be illustrated here. In cats, SC seems to be divided into two distinct regions (Roucoux and Crommelinck, 1976; Crommelinck et al., 1977b). In approximately the anterior half, the organizationofeyesaccadesobtained by electrical stimulation of deep layers is roughly similar to that found in the monkey. A short pulse train (50-100 msec) evokes eye saccades whose amplitude and direction are independent of eye orientation in the orbit (see Figs. 1B and 2B). Direction and amplitude are solely determined by the collicular site being stimulated, according to the retinotopic projection. Increasing the duration of the pulse train evokes a steplike series of identical saccades (Fig. 1A). In the posterior half, evoked saccades are clearly goal-directed. Their direction and amplitude depend on the initial orientation of the eye B.
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Fig. 1. Eyeand headmovementsevokedbystimulatingtheanteriorpartofright SCinalertcat. A)Eyesaccades evokedbya350msecstimulustrain. Headisfixed.Uppertrace: stimulationperiods. EhandEv: horizontaland vertical components of eye movement. Oh and Ov: horizontal and vertical zero position of the eye in the orbit. Upward deflection is right and up. B) Eye saccades evoked by a 50 msec stimulus train. Head is fixed. Saccades wene displayed on the screen of a memory oscilloscope in X-Y mode. Z input was modulated with 1 msec pulses at 400 Hz for the duration of saccades. The dotted contour corresponds to the limits of the oculomotor range. Graduations every So.U, up; D, down; R, right; L, left for the cat. C) Eye and head movements evoked by 1.6 sec stimulation train. Gh and Gv: horizontal and vertical components of eye position in space. Hh and Hv: horizontal and vertical components of head orientation. Eh and Ev: horizontal and vertical components of eye position in the orbit. Oh and Ov: horizontal and vertical zero position of gaze, head and eye.
747
A.
B.
1
D
Fig. 2. Eye and head movements evoked by stimulating anterior part of cat’s right SC. Stimulation site is more caudal than in Fig. 1. Same indications as in Fig. 1.In B, train duration is 100msec. Note that, in the head-fixed condition (A), no “staircase” is evoked, due to the large amplitude of the unitary saccade.
in the orbit so as to bring the line of sight in one particular direction specifiedby the site of stimulation (Fig. 3). The goal, always situated in the visual hemifield contralateral to the stimulated colliculuscan be reached by contraversive or ipsiversivesaccades. In the latter case, latency is longer (80-100 msecvs. 20-30 msec). For long stimulation trains, the eye, once brought on the goal, is kept there for the time of stimulation. The collicularregion in which such saccades can be evoked approximately covers the external 30”-60” of the retinotopically projected visual field. A point worth remembering here is that the oculomotor range of the cat is limited to about 23”from a central position. Goals being situated well within the oculomotor range limits (ipsiversive saccades towards the goal are possible), their position does not correspond to the retinotopic map. Only their direction is specified by the map; their eccentricity does not vary much from rostra1 to more caudal stimulation sites. This obviously raises a crucial question we shall examine later: what is the significance of these goal-directed saccades? Following our idea expressed above that the cat’s SC participates in orienting gaze shifts with the help of coordinated eye and head movements, we stimulated SC of alert cats free to move their heads. Eye and head movements were recorded using the electromagnetic technique. Gaze direction (eye in space) was obtained by electrically subtracting the signalsfrom the eye and head coils.Electromyographic activity (EMG) in the neck muscles contralateral to the SC being stimulated was also monitored. Head movements evoked in the anterior half of the SC (corresponding to the central 20”-30” of retinotopic map) are reminiscent of what has been shown in the monkey by
748
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Fig. 3. Example of goal-directed eye saccades evoked in right posterior SC by a 100 msec stimulus train, with head fixed. Saccades are numbered. Stimulation periods are indicated by black bars in B. Note that the ipsiversive saccades (1, 9, 10 and 11) have longer latencies than contraversive ones.
Stryker and %hiller (1975); though in the cat, it is not required that the eye reaches an extreme orientation in theorbit to start a head movement. For a short stimulation train evoking only one eye samde, the head moves only imperceptibly. If stimulus is long enough to evoke several successive saccades, the head begins to move in the same direction with a rather low velocity. Interestingly, this velocity matches the mean eye velocity in the saccadic step sequence evoked with headxfixed (Figs. lA, C and 2A, C). The head movement appears to start when the eye in the orbit has just crossed its midposition. The latency of the head movement (best illustrated by the latency of the neck EMG discharge) is dependent of the initial eye position in the orbit (Fig. 4). The mean threshold for triggering EMG clearly hes at about 3" contralateral to the midline.
749 B.
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looms Fig. 4. A) Eye saccadesevoked in right Scantenorpart,by 600msecstimulustrain.The latencyof EMG activity recorded from the left biventer cervicis muscle (lower trace) depends on the initial horizontal eye position. Upperexample: theeyestarts from the right sideofits range;lowerexample: initialpositionisslightlytotheleft of the center of the range. B) EMG latency plotted against different initial eye positions. Note the high correlationcoefficient between the twovariables. C) Each dot representsthe position attainedby the eye in the orbit when the EMG begins to burst. The mean position is 3.2"to the left. SD, indicatedby the two dottedlines, is 1.8".
Like in the monkey, where its latency is quite variable and where it only appears for large eye eccentricities, the head movement in this region of the cat's SC seems to be indirectly triggered by the eye movement itself. This will be discussed later on. Another remarkable fact is that, when the head is free, the evoked successivesaccades of gaze have the same amplitude as the staircase of eye saccades with head fixed. This implies that the vestibulo-ocular reflex (VOR) is constantly operating with a gain close to 1 during the whole sequence of evoked movements. Again, this type of eye-head coordination is similar to what has been shown in the monkey (Morass0 et al., 1973). Head movements evbked in the posterior part of cat's SC are another story. Here, stimulation evokes a short latency, rather high velocity head saccade (up to 700 degreessec-') synchronous with an eye saccade in the same direction. Head starts to move slightly after the eye but neck EMG onset just precedes the beginning of the eye movement. Frequently, if stimulation lasts long enough, a second saccade of the head is initiated, accompanied by another eye saccade (Fig. 5 ) . Amplitude and direction of evoked head saccades approximately correspond to the retinotopic map (amplitude of
40"-70").
Considering the high velocity attained by the head during the evoked movements and observing that the eye simultaneously turns in the orbit at a quasi normal velocity in the same direction, and still reaches the goal, we are led to admit that the VOR is cancelled during the evoked eye saccade. Otherwise, supposing a simple addition of VOR slow phase and eye motor command as it is realized in the monkey or by stimulating the anterior part of cat's SC, the eye would at least remain stationary in the orbit or even move
750
B.
A.
Head Fixed
Head Free
C.
Fig. 5. A, B) Eye movementsevoked in right posterior SCby 400 msec stimulustrain with head fixed and free. When the head is free to move, saccades remain goaldirected. C) Eye and head movementsevoked at the same site. Maximum head velocity attains 350 degrees.sec-' and eye in the orbit, 200 degrees.sec-'. Note the beginning of a second evoked head saccade.
in the opposite direction. This type of eye-head coordination has not been described in the monkey. We shall not give here further details on the results of these stimulationsof SC in cats. These elements will enable us to emit some hypotheses on the role of SC in the visual fixation reflex. Several questions may be raised: 1)why would SC organization differ in cat and monkey? 2) is eye-head coordination different in cat and monkey? 3) what is the significance of goal-directed saccades? To try to answerthe first question, let us imaginesome primitive animalwith two lateral eyes, no fovea, and no neck (head immobileon the trunk), maybe some sortof fish. To get a clear view of things, despite the numerous movements of his body, this animal has devised two stabilizing mechanisms: the VORand the optokinetic(OK) system. Both of them workinmperation(Robinson, 1977)andgenerate compensatoryeyemovements (slow phases), aswell asanticompensatorysaccades(quickphases). Slowphases stabilize and quick phases bring the eyes back, keeping it around a central position in the orbit; a most interesting situation because, at this moment, retinal and body coordinatesystems coincide. When this animalorientstowards a prey, he cannot move his eyesor his head, he
75 1 must turn his whole body and the first quick phase helps him to acquire the target. This visual grasp reflex is mediated by the tectum (its stimulation evokes body turning). This way of behaving is however quite time consuming and pretty exhausting. So, more clever animals have decided to move their head independently of their body. Let us consider a rabbit. He still possesses the same basic outfit: VOR and OK system, but he has developed his visual abilities: he has a specialized central region on his retina (though still rather large) and some binocular vision. To take advantage of this, he has learned to pursuit with his head: his two eye stabilizingmechanisms with their quick and slow phases are just good enough to maintain the target’s image within the best zone on his retina. He cannot move his eyes without moving his head. His visual grasp reflex usually consists of a head turning and synchronous eye saccade, itself followed by a compensatory slow phase (Collewijn, 1977). The target is acquired earlier than with a head movement alone and gaze locked on it during the rather long deceleration of head. What is the nature of this synchronous eye saccade: quick phase or voluntary command? God knows. Some evidence in favor of a voluntary movement has been shown (Collewijn, 1977), though, in practice, the distinction might reveal meaningless. Stimulation of rabbit’s SC evokes conjugate head, eye and pinnae movements (Schaefer, 1970). This fixation reflex appears to be organized according to a map in a head coordinate system though no precise recording of eye and head movements have been done. We already know how the monkey manages to acquire visual targets. He executes, like the rabbit, a coordinated eye and head movement (the neck muscles beginning to discharge slightly prior to the onset of the saccade) (Bizzi et al., 1972). But, rather surprisingly,stimulation of his SC only evokes eye saccades. To complete the picture, let us add that the monkey has, over the rabbit, the advantage of possessing a highly specialized fovea, binocular vision, a pursuit mechanism for the eye, and can make saccades whenever he wants without moving his head. From all this, it clearly appears that SC has progressively evolved from a structure governing body orienting reflexes into a head fixation reflex center and, lastly into an eye orienting device, but he has always remained a “ ~ ~ n t r o l l e of r ” gaze orientation. Our results in the cat, placed in this perspective, might appear a little less puzzling. The cat indeed can be safely placed midway between the rabbit and the monkey as far as his visual and oculomotor aptitudes are concerned. His colliculus is composite: half-rabbit, half-monkey . Our second question concerned the differences in eye-head coordination we have evoked between cat and monkey. The cat indeed appears to possess two modes of eye-head coordination. The first one would be similar to that of the monkey. In this mode, only the eye receives the adequate motor command in order to annul a retinal error. This error must be within the reach of the eye alone (within the oculomotor range). As soon as the eye leaves some central zone (whose dimensions may be different in cat and monkey according to the extent of their respective oculomotor range), it triggers a rather slow displacement of the head. This oculocephalic reflex appears quite plausible in the cat. Abrahams and Rose (1975) have indeed discovered an eye muscle proprioceptive input onto collicular cells which are at the origin of the tectospinal tract. This proprioceptive input may be activated by displacements of the eye in the orbit as small as 2” (Abrahams and Anstee, 1977). In this mode, head movement neednot be precisely programmed: the VORis sufficientto keep gaze displacement accurate. This type of eye-head coordination is illustrated by the results of stimulation of the anterior part of cat’s SC and by the observations of Bizzi’s group in the monkey. The other strategy is illustrated by
752 stimulating the posterior part of cat's SC. In this case, the target is too eccentric to be acquired by an eye movement alone. An adequate command is given to the head (in a head coordinate system). The simultaneous eye saccade may have two origins: either it is an anticompensatory eye movement (quick phase) triggered via the labyrinth and then it should at least slightly follow the onset of head movement, or it is a saccade commanded by a copy of the head motor order sent simultaneously to the oculomotor centers. Our data in the cat suggest the second possibility may be plausible. Indeed, the saccade begins slightly before the head movement (excludinga quick phase) and, if the head is prevented from moving, the saccade is still evoked (goal directed saccade with head fixed). As already underlined above, the velocity of the eye saccade remains little affected when the head is allowed to move at high speed. This suggests that the VOR gain is drastically reducedatthismomentthoughcomingbackto1neartheendoftheeyesaccade(Fig.5 ) . To answer our third question, goal-directed movements could be interpreted as the copy of the head motor order sent to the eye, in head coordinates. To be of any value, this copy has to be adapted to the eye movement range. Combination of the head saccade, goal-directed eye movement and brief cancellation of the VOR (via another copy of the head command for example) would result in an adequate target acquisition. The role of the goal-directed saccade would be double: i) to decrease the delay of target acquisition, and ii) to permit a precise foveation even if the eye is not initially centered: the goal, indeed, is in the same direction as the head movement. No overshoot of the target is possible if the eye saccade duration is noticeably shorter than the head movement, what is apparently the case. In the latest accomplishments of evolution, three gaze shifting mechanisms are superimposed. They are designed to cooperate, each in its speciality. This implies that rather complex and multiple coordinations between them exist. No wonder then, that more than one mode of eye-head coordination may exist in the cat as well as in the rabbit (Collewijn, 1977), the monkey (Bizzi et al., 1972) and man (Barnes, 1976). It is not surprisingeither that SC, which has been a center of reflex gaze orientation for millions of years reveals a multiple organization at some levels of its evolution.
SUMMARY Electrical stimulation of superior colliculus (SC) in alert cats with their head free reveals a double organization: 1) The anterior part of the structure, which receives a retinotopic input corresponding to the central 20"-30" of the visual field, is essentially involved in the generation of fixation eye saccades. The data are quite comparable to those obtained in the monkey. 2) The posterior part of the structure, corresponding to the peripheral retina, is, on the other hand, primarily implicated in the control of head fixation movements. This has not been shown in the monkey. These results show that, in the cat, SCconstitutesamajor piece in the mechanismof the visual fixation reflex. It commands gaze shifts by means of two types of eye-head coordination strategies. The presence of this dual operating collicular mechanism in the cat is discussed in the light of evolutionary processes. It is suggested that, from fish to monkey, in parallel with the development of visual performances, tectal structures have evolved from a reflex bod-j-turning device into an eye-orienting machine. The basic function, visual grasping, has been preserved, but the tools have become more and more efficient and precise: movement of the whole body, then of one of its segments, the head, and, finally, of the sensory organ itself, the eye.
753 ACKNOWLEDGEMENTS The authors are grateful to Dr. D. Guitton who devised the eye and head recording apparatus and participated in all the experiments. REFERENCES Abraham, V.C. and Anstee, G . (1977) Units in the superior colliculus and underlying tegmental structures responding to passive eye movement. Neurosci. Abstr., 111: 153, no 467. Abraham, V.C. and Rose, P.K. (1975) Projections of extraocular, neck muscle, and retinal afferents to superiorcolliculusin the cat: their connections tocellsof originof tectospinal tract./. Neurophysiol., 38: 10-18. Barnes, G.R. (1976) The roleof thevestibulo-ocularreflexinvisual target acquisiti0n.J. Physiol. (Lond.),258: 64-65P. Bizzi, E., Kalil, R.E. and Morasso, P. (1972) Two modes of active eye-head coordination in monkeys. Bruin Rex, 40: 45-48. Collewijn, H. (1977) Eye- and head-movements in freely moving rabbits.J. Physiol. (Lond.), 266: 471-498. Crommelinck, M., Guitton, D. and Roucoux, A. (1977a) La position primaire de I’oeil en relation avec le champ oculomoteur chez le chat. J. Physiol. (Paris). 73: 71A. Crommelinck, M., Guitton, D. and Roucoux, A. (1977b) Retinotopic versus spatial coding of saccades: clues obtained by stimulating deep layers of cat’s superior colliculus. In Control of Gate by Bruin Stem Neurons, R. Baker and A. Berthoz, (Eds.), Elsevier, Amsterdam, pp. 425-435. Feldon, S., Feldon, P. and Kruger, L. (1970) Topography of the retinal projection upon the superior colliculus of the cat. Vision Res., 10: 135-143. Hess, W.R., Burgi, S. undBucher, V. (1946) Motorische Funktion desTektal- undTegmentalgebietes. Mschr. Psychiut. Neurol., 112: 1-52. Mohler, C.W. and Wurtz, R.H. (1976) Organization of monkey superior colliculus: intermediate layer cells discharging before eye movements. J. Neurophysiol., 39: 722-744. Morasso, P., Bizzi, E. and Dichgans, J. (1973) Adjustment of saccade characteristicsduring head movements. Exp. Bruin Res., 16: 492-500. Robinson, D.A. (1972) Eye movements evoked by collicularstimulation in the alert monkey. Vision Res., 12: 1795-1808. Robinson, D.A. (1973) Models of the saccadic eye movement control system. Kybernetik, 14: 71-83. Robinson, D.A. (1977) Vestibular and optokinetic symbiosis: an example of explaining by modelling. In Control of Gaze by Bruin Stem Neurons, R. Baker and A. Berthoz (Eds.), Elsevier, Amsterdam, pp. 49-58. Robinson, D.L. and Jarvis, C.D. (1974) Superiorcolliculusneuronsstudiedduringheadandeye movementsof the behaving monkey. J. Neurophysiol., 37: 533-540. Roucoux, A. and Crommelinck, M. (1976) Eye movements evoked by superior colliculus stimulation in the alert cat. Bruin Res., 106: 349-363. Schaefer, K.P. (1970) Unit analysis and electrical stimulation in the optic tectum of rabbits and cats. Bruin Behuv. Evol., 3: 222-240. Schiller, P.H. and Stryker, M. (1972) Single-unit recording and stimulation in superior colliculus of the alert rhesus monkey. J. Neurophysiol., 35: 915-924. Stryker, M.P. and Schiller, P.H. (1975) Eye and head movements evoked by electrical stimulation of monkey superior colliculus. Exp. Bruin Rex, 23: 103-112. Wurtz, R.H. and Mohler, C.W. (1976) Organization of monkey superior colliculus: enhanced visual response of superficial layer cells. J. Neurophysiol., 39: 745-765.
Laboratoire de Neurophysiologie, Universitd Catholique a2 Louvain, 1200 Bruxelles (Belgium)
Superior colliculus (SC) is undoubtedly concerned with gaze orientation. Quite demonstrative experiments in the monkey (Robinson, 1972; Schiller and Stryker, 1972) have given a strongsupport to the “foveation hypothesis”. According to this model, when a stimulussuddenly appears within the animal’svisual field or when a particular detail of the visual environment is chosen by the animal as a target, a restricted zone within the sensory upper collicular layers is activated. To the retinotopy of these upper layers corresponds a similar spatial organization in the deep “motor” or efferent layers, a “motor map”. The focal activation of the sensory layers is transmitted to the deep layers which are in register. After an adequate signal processing, a still mysterious spatiotemporal translation (Robinson, 1973), the signal is fed to the ocular motoneurons who manage to bring the image of the stimulusonto the fovea. It is to be noted that, in this model, the collicularsignal merely acts as a trigger of a preprogrammed ballistic saccade. Direction and amplitude of this saccade are spatially or, better, topographically encoded in the SC. The direct transmission of information from upper sensory to lower premotor layers is however questioned bysomeobservations(Moh1erand Wurtz, 1976; WurtzandMohler, 1976). These authors assert that the temporal sequence of neuronal events they record within the collicular layers is in contradiction with this straightforward foveation hypothesis. However, for the monkeys used in these experiments, unavoidably overtrained, stimuli are hardly sudden and unexpected and their behavioral significance is far different from the naturally occurring visual stimulus which is supposed to trigger a fixation reflex in response to a “what is that?”. The contradiction between an attentionshifting and motor command mechanism thus appears rather artificial. It is obvious that the choice of a new target is necessarily correlated with an attention shift. We may admit that the primate SCis involved in reflex orientation of the eyes and operates some sort of sensory-motor point to point translation, be it with the help of a downward, upward flow of information or both. This attractive foveation hypothesis and the fact that monkey’s SC does not seem to directly participate in head orientation (Robinson and Jarvis, 1974; Stryker and Schiller, 1975) maybe has somewhat obscured the implications of old and well established observations in non-primates. The famous “visual grasp reflex” (Hess et al., 1946) is a ~~
*Charge de Recherches, F.N.R.S., Belgium.
746 synchronous movement of eye and head, both cooperating in the achievement of a goal-directed gaze shift. Let us remember that in all species in which SC or tectum has been electrically stimulated, body, head, eye and even pinnae orienting movements have been observed (see bibliography in Roucoux and Crommelinck, 1976).Eye saccade is only one component of a whole sequence of orienting movements. Let us also note that, in the cat, for example, the range of eye movements is only 20"-23" from the primary position (Crommelinck et al., 1977a), and that the retinotopic projection onto the SC covers 70" and more of visual field (Feldon et al., 1970). Thus obviously,the simple and attractive foveation model involving the eye alone does not apply as such to subprimates. The divergence of results of SC stimulation in cats and monkeys constitutes another argument and will be illustrated here. In cats, SC seems to be divided into two distinct regions (Roucoux and Crommelinck, 1976; Crommelinck et al., 1977b). In approximately the anterior half, the organizationofeyesaccadesobtained by electrical stimulation of deep layers is roughly similar to that found in the monkey. A short pulse train (50-100 msec) evokes eye saccades whose amplitude and direction are independent of eye orientation in the orbit (see Figs. 1B and 2B). Direction and amplitude are solely determined by the collicular site being stimulated, according to the retinotopic projection. Increasing the duration of the pulse train evokes a steplike series of identical saccades (Fig. 1A). In the posterior half, evoked saccades are clearly goal-directed. Their direction and amplitude depend on the initial orientation of the eye B.
A.
_c_
%
-
O-./
-/
4-/ 'O ..
r
R
1
41
r/-
b\
n'
7
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J 1.
Fig. 1. Eyeand headmovementsevokedbystimulatingtheanteriorpartofright SCinalertcat. A)Eyesaccades evokedbya350msecstimulustrain. Headisfixed.Uppertrace: stimulationperiods. EhandEv: horizontaland vertical components of eye movement. Oh and Ov: horizontal and vertical zero position of the eye in the orbit. Upward deflection is right and up. B) Eye saccades evoked by a 50 msec stimulus train. Head is fixed. Saccades wene displayed on the screen of a memory oscilloscope in X-Y mode. Z input was modulated with 1 msec pulses at 400 Hz for the duration of saccades. The dotted contour corresponds to the limits of the oculomotor range. Graduations every So.U, up; D, down; R, right; L, left for the cat. C) Eye and head movements evoked by 1.6 sec stimulation train. Gh and Gv: horizontal and vertical components of eye position in space. Hh and Hv: horizontal and vertical components of head orientation. Eh and Ev: horizontal and vertical components of eye position in the orbit. Oh and Ov: horizontal and vertical zero position of gaze, head and eye.
747
A.
B.
1
D
Fig. 2. Eye and head movements evoked by stimulating anterior part of cat’s right SC. Stimulation site is more caudal than in Fig. 1. Same indications as in Fig. 1.In B, train duration is 100msec. Note that, in the head-fixed condition (A), no “staircase” is evoked, due to the large amplitude of the unitary saccade.
in the orbit so as to bring the line of sight in one particular direction specifiedby the site of stimulation (Fig. 3). The goal, always situated in the visual hemifield contralateral to the stimulated colliculuscan be reached by contraversive or ipsiversivesaccades. In the latter case, latency is longer (80-100 msecvs. 20-30 msec). For long stimulation trains, the eye, once brought on the goal, is kept there for the time of stimulation. The collicularregion in which such saccades can be evoked approximately covers the external 30”-60” of the retinotopically projected visual field. A point worth remembering here is that the oculomotor range of the cat is limited to about 23”from a central position. Goals being situated well within the oculomotor range limits (ipsiversive saccades towards the goal are possible), their position does not correspond to the retinotopic map. Only their direction is specified by the map; their eccentricity does not vary much from rostra1 to more caudal stimulation sites. This obviously raises a crucial question we shall examine later: what is the significance of these goal-directed saccades? Following our idea expressed above that the cat’s SC participates in orienting gaze shifts with the help of coordinated eye and head movements, we stimulated SC of alert cats free to move their heads. Eye and head movements were recorded using the electromagnetic technique. Gaze direction (eye in space) was obtained by electrically subtracting the signalsfrom the eye and head coils.Electromyographic activity (EMG) in the neck muscles contralateral to the SC being stimulated was also monitored. Head movements evoked in the anterior half of the SC (corresponding to the central 20”-30” of retinotopic map) are reminiscent of what has been shown in the monkey by
748
A.
B
204R
7"
11
-
-
mms
Fig. 3. Example of goal-directed eye saccades evoked in right posterior SC by a 100 msec stimulus train, with head fixed. Saccades are numbered. Stimulation periods are indicated by black bars in B. Note that the ipsiversive saccades (1, 9, 10 and 11) have longer latencies than contraversive ones.
Stryker and %hiller (1975); though in the cat, it is not required that the eye reaches an extreme orientation in theorbit to start a head movement. For a short stimulation train evoking only one eye samde, the head moves only imperceptibly. If stimulus is long enough to evoke several successive saccades, the head begins to move in the same direction with a rather low velocity. Interestingly, this velocity matches the mean eye velocity in the saccadic step sequence evoked with headxfixed (Figs. lA, C and 2A, C). The head movement appears to start when the eye in the orbit has just crossed its midposition. The latency of the head movement (best illustrated by the latency of the neck EMG discharge) is dependent of the initial eye position in the orbit (Fig. 4). The mean threshold for triggering EMG clearly hes at about 3" contralateral to the midline.
749 B.
A
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/A 7
200
4O,.-
E"
150
-E : loo ).
0
E
w
M
oh-
/
looms Fig. 4. A) Eye saccadesevoked in right Scantenorpart,by 600msecstimulustrain.The latencyof EMG activity recorded from the left biventer cervicis muscle (lower trace) depends on the initial horizontal eye position. Upperexample: theeyestarts from the right sideofits range;lowerexample: initialpositionisslightlytotheleft of the center of the range. B) EMG latency plotted against different initial eye positions. Note the high correlationcoefficient between the twovariables. C) Each dot representsthe position attainedby the eye in the orbit when the EMG begins to burst. The mean position is 3.2"to the left. SD, indicatedby the two dottedlines, is 1.8".
Like in the monkey, where its latency is quite variable and where it only appears for large eye eccentricities, the head movement in this region of the cat's SC seems to be indirectly triggered by the eye movement itself. This will be discussed later on. Another remarkable fact is that, when the head is free, the evoked successivesaccades of gaze have the same amplitude as the staircase of eye saccades with head fixed. This implies that the vestibulo-ocular reflex (VOR) is constantly operating with a gain close to 1 during the whole sequence of evoked movements. Again, this type of eye-head coordination is similar to what has been shown in the monkey (Morass0 et al., 1973). Head movements evbked in the posterior part of cat's SC are another story. Here, stimulation evokes a short latency, rather high velocity head saccade (up to 700 degreessec-') synchronous with an eye saccade in the same direction. Head starts to move slightly after the eye but neck EMG onset just precedes the beginning of the eye movement. Frequently, if stimulation lasts long enough, a second saccade of the head is initiated, accompanied by another eye saccade (Fig. 5 ) . Amplitude and direction of evoked head saccades approximately correspond to the retinotopic map (amplitude of
40"-70").
Considering the high velocity attained by the head during the evoked movements and observing that the eye simultaneously turns in the orbit at a quasi normal velocity in the same direction, and still reaches the goal, we are led to admit that the VOR is cancelled during the evoked eye saccade. Otherwise, supposing a simple addition of VOR slow phase and eye motor command as it is realized in the monkey or by stimulating the anterior part of cat's SC, the eye would at least remain stationary in the orbit or even move
750
B.
A.
Head Fixed
Head Free
C.
Fig. 5. A, B) Eye movementsevoked in right posterior SCby 400 msec stimulustrain with head fixed and free. When the head is free to move, saccades remain goaldirected. C) Eye and head movementsevoked at the same site. Maximum head velocity attains 350 degrees.sec-' and eye in the orbit, 200 degrees.sec-'. Note the beginning of a second evoked head saccade.
in the opposite direction. This type of eye-head coordination has not been described in the monkey. We shall not give here further details on the results of these stimulationsof SC in cats. These elements will enable us to emit some hypotheses on the role of SC in the visual fixation reflex. Several questions may be raised: 1)why would SC organization differ in cat and monkey? 2) is eye-head coordination different in cat and monkey? 3) what is the significance of goal-directed saccades? To try to answerthe first question, let us imaginesome primitive animalwith two lateral eyes, no fovea, and no neck (head immobileon the trunk), maybe some sortof fish. To get a clear view of things, despite the numerous movements of his body, this animal has devised two stabilizing mechanisms: the VORand the optokinetic(OK) system. Both of them workinmperation(Robinson, 1977)andgenerate compensatoryeyemovements (slow phases), aswell asanticompensatorysaccades(quickphases). Slowphases stabilize and quick phases bring the eyes back, keeping it around a central position in the orbit; a most interesting situation because, at this moment, retinal and body coordinatesystems coincide. When this animalorientstowards a prey, he cannot move his eyesor his head, he
75 1 must turn his whole body and the first quick phase helps him to acquire the target. This visual grasp reflex is mediated by the tectum (its stimulation evokes body turning). This way of behaving is however quite time consuming and pretty exhausting. So, more clever animals have decided to move their head independently of their body. Let us consider a rabbit. He still possesses the same basic outfit: VOR and OK system, but he has developed his visual abilities: he has a specialized central region on his retina (though still rather large) and some binocular vision. To take advantage of this, he has learned to pursuit with his head: his two eye stabilizingmechanisms with their quick and slow phases are just good enough to maintain the target’s image within the best zone on his retina. He cannot move his eyes without moving his head. His visual grasp reflex usually consists of a head turning and synchronous eye saccade, itself followed by a compensatory slow phase (Collewijn, 1977). The target is acquired earlier than with a head movement alone and gaze locked on it during the rather long deceleration of head. What is the nature of this synchronous eye saccade: quick phase or voluntary command? God knows. Some evidence in favor of a voluntary movement has been shown (Collewijn, 1977), though, in practice, the distinction might reveal meaningless. Stimulation of rabbit’s SC evokes conjugate head, eye and pinnae movements (Schaefer, 1970). This fixation reflex appears to be organized according to a map in a head coordinate system though no precise recording of eye and head movements have been done. We already know how the monkey manages to acquire visual targets. He executes, like the rabbit, a coordinated eye and head movement (the neck muscles beginning to discharge slightly prior to the onset of the saccade) (Bizzi et al., 1972). But, rather surprisingly,stimulation of his SC only evokes eye saccades. To complete the picture, let us add that the monkey has, over the rabbit, the advantage of possessing a highly specialized fovea, binocular vision, a pursuit mechanism for the eye, and can make saccades whenever he wants without moving his head. From all this, it clearly appears that SC has progressively evolved from a structure governing body orienting reflexes into a head fixation reflex center and, lastly into an eye orienting device, but he has always remained a “ ~ ~ n t r o l l e of r ” gaze orientation. Our results in the cat, placed in this perspective, might appear a little less puzzling. The cat indeed can be safely placed midway between the rabbit and the monkey as far as his visual and oculomotor aptitudes are concerned. His colliculus is composite: half-rabbit, half-monkey . Our second question concerned the differences in eye-head coordination we have evoked between cat and monkey. The cat indeed appears to possess two modes of eye-head coordination. The first one would be similar to that of the monkey. In this mode, only the eye receives the adequate motor command in order to annul a retinal error. This error must be within the reach of the eye alone (within the oculomotor range). As soon as the eye leaves some central zone (whose dimensions may be different in cat and monkey according to the extent of their respective oculomotor range), it triggers a rather slow displacement of the head. This oculocephalic reflex appears quite plausible in the cat. Abrahams and Rose (1975) have indeed discovered an eye muscle proprioceptive input onto collicular cells which are at the origin of the tectospinal tract. This proprioceptive input may be activated by displacements of the eye in the orbit as small as 2” (Abrahams and Anstee, 1977). In this mode, head movement neednot be precisely programmed: the VORis sufficientto keep gaze displacement accurate. This type of eye-head coordination is illustrated by the results of stimulation of the anterior part of cat’s SC and by the observations of Bizzi’s group in the monkey. The other strategy is illustrated by
752 stimulating the posterior part of cat's SC. In this case, the target is too eccentric to be acquired by an eye movement alone. An adequate command is given to the head (in a head coordinate system). The simultaneous eye saccade may have two origins: either it is an anticompensatory eye movement (quick phase) triggered via the labyrinth and then it should at least slightly follow the onset of head movement, or it is a saccade commanded by a copy of the head motor order sent simultaneously to the oculomotor centers. Our data in the cat suggest the second possibility may be plausible. Indeed, the saccade begins slightly before the head movement (excludinga quick phase) and, if the head is prevented from moving, the saccade is still evoked (goal directed saccade with head fixed). As already underlined above, the velocity of the eye saccade remains little affected when the head is allowed to move at high speed. This suggests that the VOR gain is drastically reducedatthismomentthoughcomingbackto1neartheendoftheeyesaccade(Fig.5 ) . To answer our third question, goal-directed movements could be interpreted as the copy of the head motor order sent to the eye, in head coordinates. To be of any value, this copy has to be adapted to the eye movement range. Combination of the head saccade, goal-directed eye movement and brief cancellation of the VOR (via another copy of the head command for example) would result in an adequate target acquisition. The role of the goal-directed saccade would be double: i) to decrease the delay of target acquisition, and ii) to permit a precise foveation even if the eye is not initially centered: the goal, indeed, is in the same direction as the head movement. No overshoot of the target is possible if the eye saccade duration is noticeably shorter than the head movement, what is apparently the case. In the latest accomplishments of evolution, three gaze shifting mechanisms are superimposed. They are designed to cooperate, each in its speciality. This implies that rather complex and multiple coordinations between them exist. No wonder then, that more than one mode of eye-head coordination may exist in the cat as well as in the rabbit (Collewijn, 1977), the monkey (Bizzi et al., 1972) and man (Barnes, 1976). It is not surprisingeither that SC, which has been a center of reflex gaze orientation for millions of years reveals a multiple organization at some levels of its evolution.
SUMMARY Electrical stimulation of superior colliculus (SC) in alert cats with their head free reveals a double organization: 1) The anterior part of the structure, which receives a retinotopic input corresponding to the central 20"-30" of the visual field, is essentially involved in the generation of fixation eye saccades. The data are quite comparable to those obtained in the monkey. 2) The posterior part of the structure, corresponding to the peripheral retina, is, on the other hand, primarily implicated in the control of head fixation movements. This has not been shown in the monkey. These results show that, in the cat, SCconstitutesamajor piece in the mechanismof the visual fixation reflex. It commands gaze shifts by means of two types of eye-head coordination strategies. The presence of this dual operating collicular mechanism in the cat is discussed in the light of evolutionary processes. It is suggested that, from fish to monkey, in parallel with the development of visual performances, tectal structures have evolved from a reflex bod-j-turning device into an eye-orienting machine. The basic function, visual grasping, has been preserved, but the tools have become more and more efficient and precise: movement of the whole body, then of one of its segments, the head, and, finally, of the sensory organ itself, the eye.
753 ACKNOWLEDGEMENTS The authors are grateful to Dr. D. Guitton who devised the eye and head recording apparatus and participated in all the experiments. REFERENCES Abraham, V.C. and Anstee, G . (1977) Units in the superior colliculus and underlying tegmental structures responding to passive eye movement. Neurosci. Abstr., 111: 153, no 467. Abraham, V.C. and Rose, P.K. (1975) Projections of extraocular, neck muscle, and retinal afferents to superiorcolliculusin the cat: their connections tocellsof originof tectospinal tract./. Neurophysiol., 38: 10-18. Barnes, G.R. (1976) The roleof thevestibulo-ocularreflexinvisual target acquisiti0n.J. Physiol. (Lond.),258: 64-65P. Bizzi, E., Kalil, R.E. and Morasso, P. (1972) Two modes of active eye-head coordination in monkeys. Bruin Rex, 40: 45-48. Collewijn, H. (1977) Eye- and head-movements in freely moving rabbits.J. Physiol. (Lond.), 266: 471-498. Crommelinck, M., Guitton, D. and Roucoux, A. (1977a) La position primaire de I’oeil en relation avec le champ oculomoteur chez le chat. J. Physiol. (Paris). 73: 71A. Crommelinck, M., Guitton, D. and Roucoux, A. (1977b) Retinotopic versus spatial coding of saccades: clues obtained by stimulating deep layers of cat’s superior colliculus. In Control of Gate by Bruin Stem Neurons, R. Baker and A. Berthoz, (Eds.), Elsevier, Amsterdam, pp. 425-435. Feldon, S., Feldon, P. and Kruger, L. (1970) Topography of the retinal projection upon the superior colliculus of the cat. Vision Res., 10: 135-143. Hess, W.R., Burgi, S. undBucher, V. (1946) Motorische Funktion desTektal- undTegmentalgebietes. Mschr. Psychiut. Neurol., 112: 1-52. Mohler, C.W. and Wurtz, R.H. (1976) Organization of monkey superior colliculus: intermediate layer cells discharging before eye movements. J. Neurophysiol., 39: 722-744. Morasso, P., Bizzi, E. and Dichgans, J. (1973) Adjustment of saccade characteristicsduring head movements. Exp. Bruin Res., 16: 492-500. Robinson, D.A. (1972) Eye movements evoked by collicularstimulation in the alert monkey. Vision Res., 12: 1795-1808. Robinson, D.A. (1973) Models of the saccadic eye movement control system. Kybernetik, 14: 71-83. Robinson, D.A. (1977) Vestibular and optokinetic symbiosis: an example of explaining by modelling. In Control of Gaze by Bruin Stem Neurons, R. Baker and A. Berthoz (Eds.), Elsevier, Amsterdam, pp. 49-58. Robinson, D.L. and Jarvis, C.D. (1974) Superiorcolliculusneuronsstudiedduringheadandeye movementsof the behaving monkey. J. Neurophysiol., 37: 533-540. Roucoux, A. and Crommelinck, M. (1976) Eye movements evoked by superior colliculus stimulation in the alert cat. Bruin Res., 106: 349-363. Schaefer, K.P. (1970) Unit analysis and electrical stimulation in the optic tectum of rabbits and cats. Bruin Behuv. Evol., 3: 222-240. Schiller, P.H. and Stryker, M. (1972) Single-unit recording and stimulation in superior colliculus of the alert rhesus monkey. J. Neurophysiol., 35: 915-924. Stryker, M.P. and Schiller, P.H. (1975) Eye and head movements evoked by electrical stimulation of monkey superior colliculus. Exp. Bruin Rex, 23: 103-112. Wurtz, R.H. and Mohler, C.W. (1976) Organization of monkey superior colliculus: enhanced visual response of superficial layer cells. J. Neurophysiol., 39: 745-765.