Functional Role of the Prepositus Hypoglossi Nucleus in the Control of Gaze

Functional Role of the Prepositus Hypoglossi Nucleus in the Control of Gaze J. LOPEZ-BARNEO, C. DARLOT and A. BERTHOZ Labotatoire de Physiologie du Travail du CNRS, Dkpartement de Physiologie Neuro-sensorielle, 75005 Paris (France)

INTRODUCTION The first report concerning a possible role of the perihypoglossal area in the control of gaze is due to Hyde and Eliasson (1957) who suggested the existence of a “hind brain center for horizontal gaze” located caudal to abducens nucleus. Further evidence was obtained by lesion experiments in the monkey (Uemura and Cohen, 1973) which induced a deficit in OKN (optokinetic nystagmus) and OKAN (optokinetic after-nystagmus) together with gaze nystagmus. The relation of the nucleus prepositus hypoglossi (Ph) with the oculomotor and vestibular systems was directly evidenced by anatomical (Mabuchi and Kusama, 1970; Graybiel and Hartwieg, 1974), electrophysiological (Baker and Berthoz, 1975), and neurophysiological (Baker et al., 1976) investigations. Since these first studies, extensive information has been obtained concerning both the afferent and efferent connections of this nucleus (McCrea et al., this volume, chapter VA4). Various classes of neurons have been found in Ph in the alert cat (Baker et al., 1976) and rabbit (Schaefer et al., 1977) which are directly related to eye movements irrespective of their origin (optokinetic, vestibular or spontaneous), and justified further studies concerning the information carried by Ph neurons during pure vestibular stimulation. Two studies made in the ketamine anesthetized (Blanks et al., 1977) and decerebrate (Fukushima et al., 1977) cat addressed this question. Only a few years after the discovery of the involvement of the Ph nucleus in the control of gaze a great number of hypotheses have already been made concerning its function. Although some have been reviewed recently (Baker, 1977), it may be useful at this point to summarize them briefly. Two main types of function have been suggested according to the postulated direction of the flow of information in Ph nucleus. They depend upon whether the nucleus is considered as a “premotor center” carrying motor commands, or as a “corollary discharge” type of structure to transfer signals from motor centers to other areas of the brain. When viewed as a premotor structure, the Ph nucleus can be thought to play a role in the integration along the vestibulo-ocular pathway, namely, the mathematical transformation of head velocity input from the labyrinth into an eye position command (see Fig. 5). Taking in consideration the anatomical connections between Ph and sensorimotor cerebral cortex (Sousa-Pinto, 1970) this nucleus could also integrate, in a Sherringtonian sense, vestibular with other sensory inputs. In particular, it was sug-

668 gested that it could be an important station for the transformation of signals coded in retinal coordinates into head coordinates. Along with these ideas, a visuomoror role has been suggested because of the presence of cells with visual receptive fields in or around the nucleus (Gresty and Baker, 1976), and the existence of a powerful tectal projection to the reticular formation underlying Ph (Kawamura et al., 1974). Finally, the demonstration that horizontal and vertical components of eye movements are generated in different areas of brain stem reticular formation, together with the existence of Ph neurons that code saccade parameters and eye position in these two different main directions, has led to the idea that Ph could contribute to the coordination of these two components during oblique gaze. The possibility for Ph to be premotor has been challenged however, by the fact that most Ph neurons activated by horizontal rotation could not be antidromically activated by microstimulation of ipsilateral abducens nucleus in the cat (Hikosaka, personal communication). In fact, no clear-cut conclusion has been reached to date concerning the role of the monosynaptic projection from the Ph zone to trochlear (Baker et al., 1977) and medial rectus (Baker and Delgado-Garcia, unpublished observation) motoneurons. The powerful projections of Ph neurons to various central structures, in particular the cerebellum, has consequently stimulated speculation concerning a possible “corollary discharge” type of function. Considered as a precerebellar nucleus, Ph could provide eye position or eye velocity (Lisberger and Fuchs, 1977) signals to the cerebellar cortex and hence participate in its regulatory function during visual and vestibular control of eye movement. Another possibility is that the eye position signal contained in Ph neurons be the required input to the so-called vestibular plus eye-position neurons in the vestibular nuclei which have now been demonstrated in various species (see review in Pola and Robinson, 1978, for the monkey). This hypothesis would fit with the suggestion made earlier (Berthoz et al., 1974) that the modulation of vestibular nucleus neuron, during vestibular nystagmus, required a feedback from eye position related neurons in reticular structures. At the present stage of prepositus story, we feel that there is some urgent need for further quantitative studies of the behavior of Ph neurons in the alert animal before any emphasis can be put on any of these ideas. The data obtained in our study from about 150 Ph neurons confirms the general pictures reported by us previously (Baker et al., 1976). In the present paper, we will briefly summarize some new findings obtained with a more precise eye movement measurement concerning those Ph neurons very closely related to eye movements. Bursters with/or visual receptive field and those so-called long-lead burst tonic neurons have not been retained in the present study. We have only considered here these neurons (about 70% of the total number of neurons recorded) which discharged with ipsilateral eye movements and showed a type I1 discharge pattern during vestibular stimulation in the dark. In a subsequent paper (Berthoz et al., in preparation) the physiological properties of more than 300 Ph neurons, in relation with eye movements, will be extensively described. METHODS

Recording and stimulation The experiments have been carried out in four alert cats, with heads restrained, in which eye movements were recorded by the search coil technique (Robinson, 1963).

669 Search coils were implanted chronically three weeks to one month previous to the recording sessions. The animals were placed in a magnetic field. The overall precision of the eye movement recording was about 10' of arc and the frequency band-width 400 Hz. Extracellular neuronal activity was recorded by glass micropipettes filled with 2 M sodium acetate saturated with pontamine sky blue. Electrode impedance varied from 1 to 7 m a . Low impedance electrodes were generally preferred in order to reduce the probability of recording from axons. The Ph nucleus was reached through the intact cerebellum via a small opening (3-4 mm diameter) made chronically in the bone above the posterior cerebellar vermis. This opening was covered by inert material and plugged with bone wax between recording sessions. Ph neurons were identified according to: (i) anatomical, (ii) electrophysiological and (iii) functional criteria. (i) Stereotaxic coordinates were used according to the Bergman (1968) atlas and their location and depth were calculated in this frame of reference. For verification by histology, pontamine marks were left at the end of some electrode tracks. (ii) A stimulating electrode was chronically implanted through the cerebral cortex to stimulate abducens nerve at its exits from the brain stem (Delgado-Garcia et al., 1977; Darlot et al., 1977). The depth and extent of the antidromic field potential so obtained in abducens nucleus was studied and the location of Ph nucleus inferred. (iii) Functional identification and selection of Ph neurons was made on the basis of their clear modulation during eye movements. Because of this selection no attempt was made to calculate the proportions of Ph neurons not related with eye movements. These criteria allowed localization of Ph neurons within 200-300 pm; this is not enough to distinguish the fine mediolateral and the superficial depth organization shown by morphology (McCrea et al., chapter VA4). Further experiments will have to refine this identification. Most of the recordings reported here were made in the rostra1 2/3 of Ph which extended from abducens nucleus to 2 mm caudal and occasionally as far as 3.5 mm caudal. The caudal third of the nucleus has been extensively investigated by our previous studies (Baker et al., 1976). Neuronal activity was studied during spontaneous eye movements and when the animal was rotated in the dark. Results of visual-vestibular interaction will be reported elsewhere. Vestibular stimulation consisted of sinusoidal oscillations (0.05-0.5 Hz) by a turntable on which the animal was mounted. In all cases the head of the cat was rotated 21" nose down to stimulate horizontal semi-circular canals (Blanks et al., 1972). Data processing Although to date most of the data have been processed, those reported here were calculated during fixations and saccades. During fixations discharge rate-position plots were made for both horizontal and vertical components of eye movement. Correlation coefficients and regression lines, as well as 95 per cent confidence intervals, were computed by a standard statistical analysis. Because many Ph neurons show a particular direction in which they are activated (see below), an attempt was made to plot this behavior within the oculomotor range as defined by Crommelinck et al., (1977). The oculomotor range in our experimental conditions was obtained from the storage oscilloscope image of about 2000 consecutive spontaneous fixations of each animal. The preferred direction was defined by the two points obtained by plotting the

670 respective values for the horizontal and vertical positions in which the lowest and highest neuronal discharges during fixation were observed. Details will be given in the Results section. RESULTS About 70% of neurons reported in the present work were closely related to eye movements. All these neurons fall into the categories previously called tonic and burst-tonic (Luschei and Fuchs, 1972). Although we are conscious of the fact that this terminology already impliesthat a variable amount of eye velocity information is coded in the discharge frequency of the neurons, we would like to give a different terminology to describe Ph neurons. As we shall see below they all seem to contain some eye velocity information, and thus we shall place them between two extremes: mainly eye position related neurons (position plus velocity) and mainly eye velocity related neurons (velocity plus position). Discharge patterns of Ph neurons during spontaneous fixations During spontaneous eye movements neuronal discharge was correlated to absolute eye position in the orbit during fixation. In about 10% of the neurons, discharge rate was mainly coupled with the vertical, and in 90% with the horizontal components of eye movements, but this percentage will probably turn out to be linked with the areas explored. From our data we can not yet deduce any orderly arrangement of neurons within Ph nucleus, but they clearly appear in clusters of various properties. Our results on this particular point confirm previous results (Delgado-Garcia et al., 1977) concerning the existence of a group of vertical neurons dorsal and caudal to the abducens nucleus. Some PV neurons never became silent and their discharge rate was precisely modulated by eye position. The behavior of such a position-velocity (PV) neuron located 2.5 mm caudal to abducens nucleus and about 900 pm below the surface of brain stem showed neither pause nor threshold and its rate-horizontal and vertical position plots are shown in Fig. 1. The main features of this neuron are: regular discharge, small eye velocity component and absence of any relationship between neuronal discharge and vertical fixations. This type of neuron had firing rates not higher than 100-1 20 imp/sec. Apart from this particular category of neurons, most other PV neurons encountered showed some clear eye velocity component which induced an increase of firing rate for “on” direction and a pause during ‘ ‘ ~ f f direction ’ saccades. Careful examination of the records showed that on many occasions cells which seemed to have good correlation of their discharge rate with horizontal position were also influenced by vertical components. Fig. 2 shows an example of such a neuron recorded in the left Ph 3 mm caudal to abducens nucleus and about 200 pm below the surface of brain stem whose main “on” direction is to the left. The threshold zero frequency was for eccentric eye position in the orbit. Maximum frequency in our sample (133 imp/sec mean value) was reached when the eye was near the primary position. (The actual maximum-was not reached in this sample.) However, the records shown in Fig. 2A indicate that during a vertical down saccade the discharge frequency increased and decreased after upward saccades (filled stars in Figs. 2A and

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Fig. 1. Prepositus hypoglossi neuron mainly coding horizontal eye position. (A) Behavior of a neuron (recorded in left Ph) during fixation and horizontal saccades in the “on” (left) and “off’directions. Note the regular interspike interval during eye fixations and the absence of pauses during saccades in the “off” directions. Horizontal (H) and vertical (V) components of eye movements are shown below the discharge pattern of the neuron. (B) Rate-position plots for this neuron show the relationship between spike frequency and horizontal or vertical eye position. -, regression lines; - - - -, confidence interval (95%); r, correlation coefficient; a mean rate-position slope in imp/sec/degree.

B). Following these observations, the data points in the rate-position plots for horizontal eye movements were divided into classes of vertical eye position. A “preferred direction” was defined by a vector joining two points within the oculomotor range. Vertical and horizontal axes were divided into segments of 2.5 mm. In each particular neuron, the mean frequency corresponding to each class was calculated. The onset and the end of the vector represented plots of the respective values for the horizontal and vertical classes in which the lowest and highest mean neuronal discharges were observed. Fig. 2C shows an example of how the data points separate if only two classes (1”-7” and 7”-13”) of vertical eye positions are considered. This simple separation leads to two distinct regression lines with an improved correlation coefficient. Note that the mean rate-position slope is the same in both cases. In conclusion, the coding of eye position for this neuron was much more precise than when predicted by the simple correlation with horizontal component only. Fig. 2D shows an attempt to describe schematically the relationship of the firing rate of this neuron according to the position of the eye in the oculomotor range (dotted line). When the eye is in the upper-right quadrant the neuron shows a low firing rate. Firing frequency increases when the eye moves downward and to the left from this area. It must be noted that this vector represents only the mean values of the firing rate for a particular sample of eye positions. Using this method we could show that a number of Ph neurons have a preferred oblique direction. The existence of such a variety of specific directions in the discharge rate of Ph neurons precludes any attempt to correlate their activity with vestibular stimulus without first assessing, for each neuron, its “preferred direction”.

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Fig. 2. Behavior of an oblique position-velocity neuron recorded in left prepositus hypoglossi nucleus during spontaneous eye movements. (A) Although the discharge rate of this neuron sems to be related only to horizontal eye positions, in the selected records of this figure changes in eye position occumng only in the vertical direction (black stars) also modified the firing of the neuron. (B) Rate-position curves for the same neuron showing the existence of two separate populations of data points belonging to two different vertical classes of eye position (1"-7" and 7"-13" upwards). The regression lines have been plotted for these two classes. (C) Schematic representation, within the oculomotor range (----), of the preferred direction along which the neuron is activated. 0 imp/sec at the thin end of the arrow indicates area of firing threshold; 133 imp/sec at the thick end indicates the maximum mean firing rate encountered in the most leftward 2.5" class of horizontal position, for this particular sample of eye movements.

Discharge patterns of Ph neurons during spontaneous saccades During spontaneously occumng saccades in the light, the discharge pattern of Ph neurons was studied in relation to several questions. Firstly, we tried to assess the latency of onset and cessation of neuronal discharge in order to evaluate the possibility for Ph neurons to have a premotor role. The calculation of latency for those neurons which showed little influence of eye velocity (position plus velocity) was found to be irrelevant because the onset of activity in such neurons was only related to the eye position threshold irrespective of the velocity at which the eye moved. In other words, irrespective of the eye velocity, the onset of discharge as well as cessation was always correlated (within 3"-5") with the static threshold of firing as evidenced by the rate-position curve. These results will be reported in a subsequent paper. Latency was only calculated for neurons showing a high velocity sensitivity. As previously described (Baker et al., 1976), such neurons fired about 5 msec (mean value) prior to the onset of the "on" direction saccade. The latency for the pause before an "off" direction saccade shows obviously much more variability because, for instance, when the eye was in the "off" direction the corresponding low discharge rate introduced a great error in determination of "off" latency. Secondly, we computed for velocity plus position neurons the relationship of mean intra-burst frequency versus amplitude of the saccade and initial eye position. The

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Fig. 3. Behavior of a vertical velocity plus position neuron during spontaneous saccades in the light. The rate-position regression line for fixations is drawn for reference (-). Each arrow represents one of 33 saccades. Origin and end of arrows show vertical component of initial and final eye position. Each arrow is drawn at a level equal to the mean intraburst firing frequency during the corresponding saccade. Note that the general orientation of this cloud of arrows is parallel to the regression line, which suggests an algebraic summation cf position and velocity discharge components.

main purpose of this study was to test whether the behavior of Ph neurons was in any way similar to either motoneurons or interneurons in the extraocular muscle motor nuclei. Fig. 3 shows an example of a particularly interesting Ph neuron which was recorded 200 p m .above the antidromic field potential of the abducens nucleus. It belongs to the group of “vertical” Ph neurons found above the VIth nucleus which was observed also by Delgado-Garcia et al. (1977). The mean value of burst frequency (intraburst frequency) during 32 saccades in the “on” direction is shown. Intraburst frequency seems to depend upon the intial position of the eye in the orbit, in the sense that the tonic has been introduced by the eye position dependent mean firing rate (see rate position curve, shown as a solid line). This seems to add to the burst characteristics in a manner similar to the interneurons in the VIth nucleus in contrast to the burst reticular neurons studied by Henn and collaborators. Note that intraburst frequency is in general not higher than 350 imp/sec. Response of Ph neurons to vestibular stimulation Before presenting some preliminary findings concerning the behavior of Ph neurons during vestibular stimulation, we shall summarize the main findings of this problem. The simplified but convenient tool of calculating the phase between input head acceleration and output neuronal firing rate gives an indication of the type of mechanical parameters coded in neurons during vestibular stimulation. Fig. 4 summarizes the phase characteristics which have been obtained for vestibular nuclei, prepositus hypoglossi; abducens motoneurons and eye movements in the cat, either in the dark or in preparations without visual input.

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Fig. 4. Summary of previous data on the dynamic characteristics of vestibulo-ocular reflex. The phase of either neuronal discharge rate or eye angular displacement, with respect to head acceleration during vestibular stimulation in the dark is plotted from various authors. Oscillation frequency is indicated in abscissa. From top to bottom: (1) Data from Shinoda and Yoshida (1974) on two different populations (0. short-phase0 , long-phase) of type I neurons recorded in vestibular nuclei (VN). (2) Results of Blanks et al. (1977) for type I ( 0 ) and type I1 (B) Ph neurons, each referred to peak acceleration in its on-direction. (3) Those of Fukushima et al. (1977) which show two populations of type I1 Ph neurons, in phase with either head velocity (v) or abducens nerve activity (v): (4) Data from Shinoda and Yoshida (1974) on abducens motoneurons (Abd Mn) (A). (5) Phase relation to eye movement (EM) (A) after Landers and Taylor (1975). See.text for experimental conditions of each author.

Shinoda and Yoshida (1974) have calculated the phase of short and long phase type I cells in the vestibular nucleus, and of abducens motoneurons, during horizontal sinusoidal rotation of decerebrate cats. For comparison we have drawn the phase of eye angular displacement obtained by Landers and Taylor (1972) in alert cats. In Ph nucleus a surprising phase lag was obtained by Blanks et al. (1977) in Ketamine anesthetized cats and by Fukushima et al. (1977) in decerebrate cats using also sinusoidal oscillation. These authors consequently suggested that the Ph was part of the integrating network in the vestibulo-ocular arc. However Fukushima et al. (1977) concluded that two distinct classes of neurons were present in the Ph, one of them being clearly similar to abducens motoneurons and the other, less numerous, having a phase which fell in the range of the two classes obtained by Blanks et al. (1977). This last group showed only a small phase lag with respect to vestibular nuclei and contained apparently the same head velocity component. In our experiments, using vestibular stimulation in complete darkness, we have found discharge patterns which confirm the findings of Fukushima et al. (1977). The response of Ph neurons to horizontal angular acceleration was only studied in those neurons which had a clear horizontal direction-specific response according to the analysis described in the first part of this paper. No formal analysis was made at this point of the discharge rate because we used amplitudes of vestibular stimulation which induced saccadic activity, and found that the relation of firing rate with the head acceleration (input) varied according to the state of alertness of the animal. This is exemplified by the recordings of Figs. 5 and 6 for two neurons. The Ph neuron shown

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Fig. 5. Behavior of a'horizontal position plus velocity prepositus neuron during vestibular nystagmus in the dark. From top to bottom: Head velocity (maximum indicated by white star), to the ipsilateral (ipsi) and contralateral (contra) side with respect to recording site (right prepositus: RPh). Unit activity, horizontal (H) and vertical (V) eye position. Vestibular stimulation was given by sinusoidal horizontal rotation (0.2 Hz and 50" peak to peak amplitude) in three different states of alertness. In the alert state, vestibular nystagmus is strong and the neuronal discharge is closely related to extreme ipsilateral eye position corresponding to contralateral head position (black star). The neuronal discharge is modulated by nystagmus and the appearance of neural firing depends on a rather precise eye position threshold. In B and C the animal becomes drowsy and the corrective effects of quick phase is lost. The absolute position of eyes in the orbit differs from the one obtained in the alert state. Note that neuronal discharge remains closely coupled with eye position without any influences of head velocity position. White star indicates maximum head velocity. See text for detailed description.

Fig. 6. Behavior of a horizontal velocity plus position prepositus neuron during vestibular nystagmus in the dark. Same recordings as in Fig. 5 . Neuronal discharge during vestibular stimulation (0.2 Hz and 50" peak to peak amplitude and 30 degrees/sec peak velocity) in two different states of alertness. In the alert state (A) the neuronal discharge is modulated by both eye velocity and position. Peak discharge rate is during peak ipsilateral head velocity. In the drowsy state (B) the peak discharge rate is still related to maximum eye velocity in the "on" direction (small star) but to contralateral peak head velocity (big star). See text for detailed description.

676 in Fig. 5 was recorded 1.8 mm caudal to the abducens nucleus and its firing pattern is shown here during three states of alertness. In Fig. 5A the cat was alert, nystagmus brisk. The discharge rate of this neuron during spontaneous eye movements was related to eye position (correlation coefficient with horizontal component 0.85, rateposition). “On” direction is to the right and its threshold was near the primary position. Whatever the state of the cat, the discharge rate, during vestibular nystagmus, is also only correlated with eye position. When saccades disappear due to drowsiness, the phase of the neuron in relation to the vestibular input changes drastically, probably because the amount of head velocity information contained in the discharge rate is minimal compared to the influence of eye position. Quantitative analysis has revealed a small effect of head movement (10% of change of firing rate at primary position for variations of head velocity from 10 to 60 degreedsec). It could be concluded that this class of neurons is very independent from head acceleration although a clear synaptic input may exist from the labyrinth. This fact could of course be interpreted as either proving that these neurons receive only a weak influence from the labyrinth or that the labyrinth input is integrated and does not show, with its initial phase in the output of these neurons, which is the measured parameter. Only further experiments will clarify this question. Fig. 6 shows an example of a very different type of neuron which has a clear eye velocity component in its discharge pattern. This neuron shows also a modulation which is mainly related to eye velocity and not to head velocity as demonstrated by the fact that when the animal becomes drowsy the maximum discharge rate follows the phase of maximum eye velocity. Quantitative analysis of the head velocity and acceleration component in this neuron will be reported in a subsequent paper, but the clear difference of its behavior with the neuron shown in Fig. 5 points to the existence of extreme, if not distinct types of neurons with their behavior relative to head velocity during vestibular stimulation. DISCUSSION By using precise methods of eye movement measurement and relating the firing rate to the direction of gaze during fixations and saccades, we have established that both the tonic discharge frequency during fixations and the burst characteristics during saccades, of eye movement related neurons, are dependent upon absolute eye position in the orbit coded in head coordinates. In many aspects, Ph neurons have discharge chacacteristics close to both motoneurons and internuclear neurons (see review of these properties in Baker and Berthoz, 1977). It is now clear, very much in accordance with the findings of Fukushima et al. (1977), that at least two extreme classes of neurons exist: those coding mainly eye position and exhibiting a very weak eye velocity signal (which during vestibular stimulation show little head velocity influence) and those coding both eye velocity and eye position. But we cannot yet know if the difference between these two classes corresponds to any of the types of neurons found with morphological methods by McCrea et al. (chapter VA4), or if this is a continuously scaled property of one type of neuron. A second main conclusion which can be drawn from this study is that eye movement related Ph neurons show a change of firing rate which is direction-specificwith respect

677 to eye movements. Horizontal, vertical and oblique “preferred directions’’ have been found and can be measured by a vector analysis, placing the vector in the oculomotor range. The details of this quantitative study will be reported in a subsequent paper but we can already state some of the questions which arise from this finding. It may be important to know whether the preferred direction, when oblique, falls either in the main pulling direction of the extraocular muscles as advocated by Henn and Cohen (1976), or in the plane of the semicircular canals as found in the medial terminal nucleus by Simpson et al. (this volume, chapter VB5), or evenly distributed in space. This last hypothesis would be consistent with a role of Ph as one more of a sensorimotor map involved in visuovestibulo motor coordination. Obviously, more work is necessary to answer the basic question put forward in the title of this paper, but the exquisite relation of Ph neurons to eye position, and strong projection to the cerebellum may indeed support the idea that even if this structure plays some integrating or coordinating role in premotor function, it is a very good candidate for providing a corollary discharge type of signal either to the cerebellum or to the vestibular nuclei themselves. Pathways for this last possibility have recently been evidenced (Pompeiano et al., 1978).

SUMMARY

The main hypothesis concerning the functional role of the prepositus hypoglossi (Ph) nucleus are reviewed. Experimental results obtained in the alert cat using eye movement recording by the search coil technique and extracellular neuronal recording during spontaneous eye movements or vestibular stimulation are described. Ph neurons code eye position with various degrees of eye velocity information. They have a preferred direction which is either horizontal, vertical or oblique. During vestibular stimulation those neurons with mainly eye position information show little head velocity component. Both an immediate premotor role and a corollary discharge type of function involving feedforward of eye position information to the cerebellum or feed back to the vestibular nuclei are compatible with the results. ACKNOWLEDGEMENTS This research was supported by CNRS ATP No. 3626. Dr. Lopez Bameo was supported by a ETP BBR training award. Mrs. A. M. Madariaga developed the technique of marking with pontamine and determined, in a separate study, how long the animals could be kept with the marks for chronic recording. We gratefully acknowledge her participation.

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