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Neuronal activity in the prepositus hypoglossi nucleus correlated with vertical and horizontal eye movement in the cat
366 ,'
E l s e v i e r Scicrltiiic P t l b l i s h i n g ( o m p a n y ,
tCraht R e s e a r H i , liH (1975i ?;{)~ 3 ! A m s t e r d a m - P r i n t e d iP. 1-he Ncrhcrl:~Hd~;
Neuronal activity in the prepositus hypoglossi nucleus correlated with vertical and horizontal eye movement in the cat
R. BAKER, M. GRESTY A N n A. BERTHOZ* Division of Neurobiology, Department o/' Physiology and Biophysics, University o[" Iowa, Iowa ~70', Iowa 52242 (U.S.A.)
(Accepted September 25th, 1975)
Many neurons in the prepositus hypoglossi nucleus 4 are ortho- and antidromically activated by electrical stimulation of either the oculomotor complex or cerebellum and exhibit disynaptic potentials from either ipsi- or contralateral vestibular nerve stimulation 3. In part, this finding had been anticipated from prior anatomical studies employing horseradish peroxidase tracers, which suggested that prepositus neurons send afferents to the oculomotor nuclei and cerebelluml,L Thus, it seems that the prepositus hypoglossi nucleus may be a vestibulo-cerebellar center concerned with the regulation of eye movement 3,1s. To determine whether prepositus neurons might have art oculomotor role, we recorded their activities during eye movement evoked by visual and vestibular stimuli in alert cats. In 4 animals, microelectrode tracks were correlated with subsequent histological sections (Fig. 1) and the results indicate that prepositus neurons may play a significant ro!e in the generation of vertical and horizontal saccades, fixation and vestibular or visually guided pursuit eye movements. One to 2 weeks before the experiments, cats were anesthetized with pentobarbital (30 mg/kg) and chlorided silver ball electrodes were placed in the bony orbit for recording both horizontal and vertical EOGs. Eye movement was calibrated by comparing E O G records with photographs (simultaneously at two angles) of an elongated marking device attached to the eye by a suction contact lens. Both an anterior and posterior set of stabilization bolts were cemented with acrylic cement to the cat's skull for head immobilization. The lamboidal ridge overlying the posterior vermis (Fig. l, left) was removed and a round polyethylene tube (diameter l cm) was cemented snugly in place. A nylon plug was sculptured to fit the underlying cerebellar cortical areas. A few days after recovery from the surgery, each animal was gently, but tightly, wrapped in thin cloth, placed on foam cushions in a wooden box and its head immobilized for unit recordings. Recording sessions usually lasted about 3 h and animal alertness was maintained by adequate investigator activity.
* Laboratoire de Physiologie du Travail, 41 Rue Gay-Lussac, Paris, France.
367
L
J
//
Fig. 1. Schematic diagrams and histological profile showing the microelectrode tracks and their relationship to the prepositus hypoglossi nucleus and other brain stem nuclei. The diagram on the left (a sagittal section at 1.2 mm lateral to the midline) depicts access to the prepositus hypoglossi nucleus and those structures traversed by the microelectrode. The diagram in the upper right shows a coronal section at the level indicated by the microelectrode in the left sketch. The histological inset was stained with cresyl violet and Luxol blue. It corresponds to the area indicated by the box in the above transverse section. Microelectrode tracks 1, 2 and 3 correspond to those shown in the histological inset (see text). Abbreviations: MLF, medial longitudinal fasciculus; N6, N10 and NI2, cranial motor nuclei; 7N, VII nerve; M and D, the medial and descending vestibular nuclei; ph, prepositus hypoglossi nucleus; x, vestibular nuclei subgroup; Ncue, accessory cuneate nucleus; Ncu, cuneate nucleus; Npr, dorsal group of paramedian reticular nucleus; Npc, nucleus pontis caudalis; Nrm, nucleus reticularis magnocellularis; Nrg, nucleus reticularis gigantocellularis; Nrtp, nucleus reticularis tegmenti pontis; Ntg, ventral tegmental nucleus; Nio, inferior olivary nucleus; Nfast, fastigial nucleus; IC, inferior colliculus.
368 The microelectrodes tbr extracellular recording were filled with I AI NaCl saturated with Fast green. As shown in Fig. 1, the microelectrode was lov~ercd to the brain stem through a small opening in the dura overlying the posterior vermis. Systematic recordings were taken throughout the anterior-posterior extent of the prepositus hypoglossi nucleus. At each level, tracks were made across the brain stem from the left to right at 0.5 mm intervals and the glass microelectrodes were left at interesting recording sites. This method permitted wide areas of the medulla to be surveyed and a subsequent correlation of unit records with anatomical location; however, it limited the number of recording sessions for each animal to a b o m 5. Samples of the activities of several units which are representative of the various types so far discovered are illustrated in Fig. 2. All the units were recorded from a single microelectrode track (Fig. I, No. 1) through the right posterior prepositus hypoglossi nucleus. In the next microelectrode track (Fig. I, No. 2) the glass microelectrode was replaced with a steel one and a small electrolytic lesion (10 ~A tk)r 15 sec) was placed at the most dorsal level at which neuronal activity related to eye movement was found. Eye movement related responses were not found in other more lateral microelectrode tracks which passed through the posterior part of medial vestibular nuclei (example No. 3). The activity seen in most prepositus neurons suggests that they might conveniently be divided into two classes. Neurons of the first group (called burst-tonic by Luschei and F u c h ¢ z) produce a burst of activity preceding saccades in a preferred direction and have a steady firing rate more or less linearly related to eye position*. Such activity is shown in Fig. 2A by a neuron in which firing was tightly coupled with horizontal eye movement to the right. The sensitivity of this cell to a high velocity eye movement is shown by its response during the first small saccade (filled circle). At this time, tonic background activity is absent because the position threshold for this neuron (filled triangles) had not been attained15. A comparison of activity during the two saccades of equal amplitude, but different velocity, which are indicated by the upward directed arrows, demonstrates that discharge frequency was proportional to eye movement velocity. About 200/zm below the right burst-tonic neuron an up burst-tonic cell was isolated (Fig. 2B). Its sensitivity to eye movement is indicated by the neuronal discharge during first upward eye saccade. A tonic activity is maintained during fixation once its position threshold has been exceeded as shown during the next two upward saccades (second and third arrows). Both an irregular and regular discharge rate during maintained fixation have been observed in these ceils (compare Fig. 2A and B). In all burst-tonic neurons the duration of the burst was equal to that of the saccade. Onset of the burst could precede the saccade by up to 20 msec. When the unit was near its position threshold the latency was about 5-10 msec. However, any tonic
* Appropriately, Fig. 5 of Luschei and Fuchs a2, depicts the activity of two units which according to their anatomical location are likely to have been recorded from the prepositus hypoglossi nucleus in the monkey. The responses of these cells are representative of the two classes of cells we describe in this study.
369
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Jill ~ I IItL[I'I IlllllltlllllliUI~ll~[~]lll [~ ................... ~u,,,nj,,,,dllllllJllll!ll|lilllJl[llIlllllll~l[~Jlllh~J .......... l,,,u,J,dd ......... El[ T'TI1 I( TIll IIIIIIIIIIIII[IIINTIJTI TI1 ~llll~lmlll mll[rlllllll'll Ill[llll llRIIl|l~lmlillmIRI/lll fl I NIl~ll[ll~lll[rllllllq[I1[~1 IIllllllllltl'~"l'
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Fig. 2. Representative activity from 4 prepositus neurons during voluntary horizontal and vertical eye movement. These neurons were recorded successively from dorsal to ventral in microelectrode track No. 1 shown in Fig. 1. A: a prepositus neuron correlated with rightward eye movement. B: a prepositus neuron correlated with upward eye movement. C: reciprocally related down (large unit) and up (small unit) neurons. Eye movement calibrations shown in A applicable to B and C. Unit activity recorded from 100 to 5,000 Hz and eye movement from DC to 100 Hz. The straight arrows mark on the EOG trace (A-C) the occurrence of a change in neuronal discharge. The curved arrows in C indicate two occasions where the position-threshold for the down and up neurons overlap. Further explanation in text. activity during fixation was nearly always t e r m i n a t e d 10-20 msec before a saccade in the off-direction. In this p o p u l a t i o n o f cells we have f o u n d a c o n t i n u u m o f c o m b i n e d v e l o c i t y p o s i t i o n sensitivities b u t m o s t o f the n e u r o n s showed a high p o s i t i o n threshold. This m e a n s t h a t when the c a t ' s eyes are m o r e o r less centrally situated in orbit, i.e. n o r m a l position, tonic activity is usually absent. The second class o f responses consisted o f n e u r o n a l activity t h a t c o u l d be correlated p r i m a r i l y with changes in eye position. Very near the u p - b u r s t tonic neurons s h o w n in Fig. 2B, we were able to isolate, simultaneously, the activity o f two reciprocally related vertical units. T h e responses o f the d o w n (large) and up (small) unit were clearly d e v o i d o f a burst (or eye m o v e m e n t sensitivity) shown in the previous two units. As i n d i c a t e d by the curved a r r o w s in Fig. 2C there is a n o v e r l a p p i n g ( a b o u t 5°) p o s i t i o n - t h r e s h o l d for the d o w n a n d up unit. I n addition, the discharge rate o f these units was never m o d u l a t e d until after the onset o f the saccades (in b o t h on- a n d off-directions). A few n e u r o n s with eye p o s i t i o n sensitivities a p p e a r e d to pause for saccades in b o t h the on- a n d off-direction; however, they were l o c a t e d lateral in the nucleus a n d thus c o u l d be vestibular in o r i g i n n , la. W e frequently e n c o u n t e r e d clusters o f
370 neurons (mixed horizontal and vertical directions) responding like the lwo ceils shown in Fig. 2C. The activities of all such neurons described in Fig. 2 were modulated during both voluntary and compensatory vestibular evoked eye movement. In addition, a third type of activity (not illustrated in this paper) was found in prepositus neurons and/or axons. I1 consisted of an intense burst or, in cells with a maintained firing rate, a pause of activity during saccades (both uni- and pandirectional). When tonic activity was present in these neurons, it was not a function of eye position l~ ~a. In summary, we have been able to acquire records, typified by those shown in Fig. 2, from microelectrode tracks throughout the prepositus hypoglossi nucleus, extending from its posterior border near the obex to the level of the genu of the facial nerve. These results suggest that prepositus neurons may play a significant role in the generation and maintenance of both vertical and horizontal saccades and lixation irrespective of whether or not eye movements are induced by vestibular or visual stimuli. That prepositus activity may, in part, be carried to the oculomotor complex by the MLF is consistent with recently described activity in MLF fibers 5,1~ l h e data obtained in this study bear out the stimulation and lesion experiments of Hyde and Elliasson s who supported the concept of a medullary brain stem area TM involved with horizontal eye movement 6,1s. in addition, we now provide evidence for a posterior brain stem area important for vertical eye movement and likely the one (in part) responsible for deficits in vertical eye movement following MLF lesions~L Even though there is little doubt that prepositus neurons are intimately related to the vestibular system a, the fact that these neurons are so closely correlated with eye movement induced by any stimuli (visual or vestibular) suggests that they could, in addition, be part of the visuo-oculomotor pathway, a hypothesis supported by a number of lesion experiments s,~s, In this latter context, it is worth suggesting and testing the hypothesis that this brain stem area may, in fact, be the site where visuomotor signals originating from the midbrain tectum 9 are interfaced with vestibular information and transformed into appropriate motor commands. This idea is attractive because of the intimate relationship of the prepositus hypoglossi nucleus with the overlying vestibulo-cerebellum and the midline vermal areas "~,a,~7 which purportedly have important control functions for motor systems. This research was supported by Public Health Service Grants EY01074. NS09916 and NS-05748.
1 ALLEY, K., BAKER, R., AND SIMPSON, J. t., Afferents to the vestibulo-cerebellum and the origin of the visual climbing fiber in the rabbit, Brain Research, 98 (1975) 582-589. 2 ANGAUT,P., AND BRODAL,At, The projection of the 'vestibulocerebellum' onto the vestibular nuclei in the cat, Arch. ital. Biol., 105 (1967) 441-479. 3 BAKER,R., ANDBERTHOZ,A., Is the prepositus hypoglossi nucleus the source of another vestibuloocular pathway? Brain Research, 86 (1975) 121-127. 4 BRODAL, A., Experimental demonstration of cerebellar connexions from the peri-hypoglossal nuclei (nucleus intercalatus, nucleus praepositus hypoglossi and nucleus of roller) in the cat. J. Anat. (Lond.), 86 (1952) 110-120.
371 5 DAVIS-KING, W. M., LISBERGER, S. G., FUCHS, A. F., AND EVINGER, L. C., Activity of simial MLF fibers related to eye movement and adequate vestibular stimulation, Soc. Neurosci., 4 (1974) 185. 6 EVINGER, C. L., K1NG, W. M., LlSBERGER, S. G., FUCHS, A., AND BAKER, R., The role of MLF in eye movements: functional physiology underlying anterior internuclear ophthalmoplegia, Neurosci. Abstr., 1 (1975) 235. 7 GRAVB1EL,A. M., AND HARTWIEG, E. A., Some afferent connections of the oculomotor complex in the cat: an experimental study with tracer techniques, Brain Research, 81 (1974) 543-551. 8 HYDE, J. E., AND ELIASSON, S. G., Brainstem induced eye movements in cat, J. comp. Neurol., 108 (1957) 139-172. 9 INGLE, D., AND SPRAGUE, J. M., Sensorimotor function of the midbrain tectum, Neurosci. Res. Progr. Bull., 14 (1975) 226-244. 10 KELLER, E. L., Participation of medial pontine reticular fomation in eye movement generation in monkey, J. Neurophysiol., 37 (1974) 316-332. 1 I KELLER, E. L., AND DANIELS, P. D., Oculomotor related interaction of vestibular and visual stimulation in vestibular nucleus cells in alert monkey, Exp. Neurol., 46 (1975) 187-198. 12 LUSCHEI,E. S., AND FUCHS, A. F., Activity of brain stem neurons during eye movements of alert monkeys, J. Neurophysiol., 35 (1972) 445-461. 13 MILES, F. A., Single unit firing patterns in the vestibular nuclei related to voluntary eye movements and passive body rotation in conscious monkeys, Brain Research, 71 (1974) 215-224. 14 POLA, J., MLF fiber activity in monkey during visually elicited and vestibular eye movement, Soc. Neurosci., 4 (1974) 377. 15 ROBINSON, D. A., Oculomotor unit behavior in the monkey, J. Neurophysiol., 33 (1970) 393-404. 16 SZENT/,GOTHAI, J., Recherches exp6rimentales sur les voies oculogyres, Sem. H6p. Paris, 26 (1950) 2989-2996. 17 TORVIK, A., AND BaOOAL, A., The cerebellar projection of the perihypoglossal nuclei (nucleus intercalatus, nucleus praepositus hypoglossi and nucleus of roller) in the cat, J. Neuropath. exp. Neurol., 13 (1954) 515-527. 18 UEMURA, T., AND COHEN, B., Effects of vestibular nuclei lesions on vestibulo-ocular reflexes and posture in monkeys, Acta oto-laryng. (Stockh.), Suppl. 315 (1973) 1-71. 19 WALBERG, F., Fastigiofugal fibers to the perihypoglossal nuclei in the cat, Exp. Neurol., 3 (1961) 525-541.
E l s e v i e r Scicrltiiic P t l b l i s h i n g ( o m p a n y ,
tCraht R e s e a r H i , liH (1975i ?;{)~ 3 ! A m s t e r d a m - P r i n t e d iP. 1-he Ncrhcrl:~Hd~;
Neuronal activity in the prepositus hypoglossi nucleus correlated with vertical and horizontal eye movement in the cat
R. BAKER, M. GRESTY A N n A. BERTHOZ* Division of Neurobiology, Department o/' Physiology and Biophysics, University o[" Iowa, Iowa ~70', Iowa 52242 (U.S.A.)
(Accepted September 25th, 1975)
Many neurons in the prepositus hypoglossi nucleus 4 are ortho- and antidromically activated by electrical stimulation of either the oculomotor complex or cerebellum and exhibit disynaptic potentials from either ipsi- or contralateral vestibular nerve stimulation 3. In part, this finding had been anticipated from prior anatomical studies employing horseradish peroxidase tracers, which suggested that prepositus neurons send afferents to the oculomotor nuclei and cerebelluml,L Thus, it seems that the prepositus hypoglossi nucleus may be a vestibulo-cerebellar center concerned with the regulation of eye movement 3,1s. To determine whether prepositus neurons might have art oculomotor role, we recorded their activities during eye movement evoked by visual and vestibular stimuli in alert cats. In 4 animals, microelectrode tracks were correlated with subsequent histological sections (Fig. 1) and the results indicate that prepositus neurons may play a significant ro!e in the generation of vertical and horizontal saccades, fixation and vestibular or visually guided pursuit eye movements. One to 2 weeks before the experiments, cats were anesthetized with pentobarbital (30 mg/kg) and chlorided silver ball electrodes were placed in the bony orbit for recording both horizontal and vertical EOGs. Eye movement was calibrated by comparing E O G records with photographs (simultaneously at two angles) of an elongated marking device attached to the eye by a suction contact lens. Both an anterior and posterior set of stabilization bolts were cemented with acrylic cement to the cat's skull for head immobilization. The lamboidal ridge overlying the posterior vermis (Fig. l, left) was removed and a round polyethylene tube (diameter l cm) was cemented snugly in place. A nylon plug was sculptured to fit the underlying cerebellar cortical areas. A few days after recovery from the surgery, each animal was gently, but tightly, wrapped in thin cloth, placed on foam cushions in a wooden box and its head immobilized for unit recordings. Recording sessions usually lasted about 3 h and animal alertness was maintained by adequate investigator activity.
* Laboratoire de Physiologie du Travail, 41 Rue Gay-Lussac, Paris, France.
367
L
J
//
Fig. 1. Schematic diagrams and histological profile showing the microelectrode tracks and their relationship to the prepositus hypoglossi nucleus and other brain stem nuclei. The diagram on the left (a sagittal section at 1.2 mm lateral to the midline) depicts access to the prepositus hypoglossi nucleus and those structures traversed by the microelectrode. The diagram in the upper right shows a coronal section at the level indicated by the microelectrode in the left sketch. The histological inset was stained with cresyl violet and Luxol blue. It corresponds to the area indicated by the box in the above transverse section. Microelectrode tracks 1, 2 and 3 correspond to those shown in the histological inset (see text). Abbreviations: MLF, medial longitudinal fasciculus; N6, N10 and NI2, cranial motor nuclei; 7N, VII nerve; M and D, the medial and descending vestibular nuclei; ph, prepositus hypoglossi nucleus; x, vestibular nuclei subgroup; Ncue, accessory cuneate nucleus; Ncu, cuneate nucleus; Npr, dorsal group of paramedian reticular nucleus; Npc, nucleus pontis caudalis; Nrm, nucleus reticularis magnocellularis; Nrg, nucleus reticularis gigantocellularis; Nrtp, nucleus reticularis tegmenti pontis; Ntg, ventral tegmental nucleus; Nio, inferior olivary nucleus; Nfast, fastigial nucleus; IC, inferior colliculus.
368 The microelectrodes tbr extracellular recording were filled with I AI NaCl saturated with Fast green. As shown in Fig. 1, the microelectrode was lov~ercd to the brain stem through a small opening in the dura overlying the posterior vermis. Systematic recordings were taken throughout the anterior-posterior extent of the prepositus hypoglossi nucleus. At each level, tracks were made across the brain stem from the left to right at 0.5 mm intervals and the glass microelectrodes were left at interesting recording sites. This method permitted wide areas of the medulla to be surveyed and a subsequent correlation of unit records with anatomical location; however, it limited the number of recording sessions for each animal to a b o m 5. Samples of the activities of several units which are representative of the various types so far discovered are illustrated in Fig. 2. All the units were recorded from a single microelectrode track (Fig. I, No. 1) through the right posterior prepositus hypoglossi nucleus. In the next microelectrode track (Fig. I, No. 2) the glass microelectrode was replaced with a steel one and a small electrolytic lesion (10 ~A tk)r 15 sec) was placed at the most dorsal level at which neuronal activity related to eye movement was found. Eye movement related responses were not found in other more lateral microelectrode tracks which passed through the posterior part of medial vestibular nuclei (example No. 3). The activity seen in most prepositus neurons suggests that they might conveniently be divided into two classes. Neurons of the first group (called burst-tonic by Luschei and F u c h ¢ z) produce a burst of activity preceding saccades in a preferred direction and have a steady firing rate more or less linearly related to eye position*. Such activity is shown in Fig. 2A by a neuron in which firing was tightly coupled with horizontal eye movement to the right. The sensitivity of this cell to a high velocity eye movement is shown by its response during the first small saccade (filled circle). At this time, tonic background activity is absent because the position threshold for this neuron (filled triangles) had not been attained15. A comparison of activity during the two saccades of equal amplitude, but different velocity, which are indicated by the upward directed arrows, demonstrates that discharge frequency was proportional to eye movement velocity. About 200/zm below the right burst-tonic neuron an up burst-tonic cell was isolated (Fig. 2B). Its sensitivity to eye movement is indicated by the neuronal discharge during first upward eye saccade. A tonic activity is maintained during fixation once its position threshold has been exceeded as shown during the next two upward saccades (second and third arrows). Both an irregular and regular discharge rate during maintained fixation have been observed in these ceils (compare Fig. 2A and B). In all burst-tonic neurons the duration of the burst was equal to that of the saccade. Onset of the burst could precede the saccade by up to 20 msec. When the unit was near its position threshold the latency was about 5-10 msec. However, any tonic
* Appropriately, Fig. 5 of Luschei and Fuchs a2, depicts the activity of two units which according to their anatomical location are likely to have been recorded from the prepositus hypoglossi nucleus in the monkey. The responses of these cells are representative of the two classes of cells we describe in this study.
369
]
right
- up
B
I sec
500 msec
CII
Jill ~ I IItL[I'I IlllllltlllllliUI~ll~[~]lll [~ ................... ~u,,,nj,,,,dllllllJllll!ll|lilllJl[llIlllllll~l[~Jlllh~J .......... l,,,u,J,dd ......... El[ T'TI1 I( TIll IIIIIIIIIIIII[IIINTIJTI TI1 ~llll~lmlll mll[rlllllll'll Ill[llll llRIIl|l~lmlillmIRI/lll fl I NIl~ll[ll~lll[rllllllq[I1[~1 IIllllllllltl'~"l'
~1 ll~ ~!$~t ii~llllll/li/:!Nilill~,i/,l~l
~ _ _ _ . - - - - ~ , ,
~
II~llllllllll~]glNtNIIIIlfl[l/;;ll!lll N/-- ! [I , ,-
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Fig. 2. Representative activity from 4 prepositus neurons during voluntary horizontal and vertical eye movement. These neurons were recorded successively from dorsal to ventral in microelectrode track No. 1 shown in Fig. 1. A: a prepositus neuron correlated with rightward eye movement. B: a prepositus neuron correlated with upward eye movement. C: reciprocally related down (large unit) and up (small unit) neurons. Eye movement calibrations shown in A applicable to B and C. Unit activity recorded from 100 to 5,000 Hz and eye movement from DC to 100 Hz. The straight arrows mark on the EOG trace (A-C) the occurrence of a change in neuronal discharge. The curved arrows in C indicate two occasions where the position-threshold for the down and up neurons overlap. Further explanation in text. activity during fixation was nearly always t e r m i n a t e d 10-20 msec before a saccade in the off-direction. In this p o p u l a t i o n o f cells we have f o u n d a c o n t i n u u m o f c o m b i n e d v e l o c i t y p o s i t i o n sensitivities b u t m o s t o f the n e u r o n s showed a high p o s i t i o n threshold. This m e a n s t h a t when the c a t ' s eyes are m o r e o r less centrally situated in orbit, i.e. n o r m a l position, tonic activity is usually absent. The second class o f responses consisted o f n e u r o n a l activity t h a t c o u l d be correlated p r i m a r i l y with changes in eye position. Very near the u p - b u r s t tonic neurons s h o w n in Fig. 2B, we were able to isolate, simultaneously, the activity o f two reciprocally related vertical units. T h e responses o f the d o w n (large) and up (small) unit were clearly d e v o i d o f a burst (or eye m o v e m e n t sensitivity) shown in the previous two units. As i n d i c a t e d by the curved a r r o w s in Fig. 2C there is a n o v e r l a p p i n g ( a b o u t 5°) p o s i t i o n - t h r e s h o l d for the d o w n a n d up unit. I n addition, the discharge rate o f these units was never m o d u l a t e d until after the onset o f the saccades (in b o t h on- a n d off-directions). A few n e u r o n s with eye p o s i t i o n sensitivities a p p e a r e d to pause for saccades in b o t h the on- a n d off-direction; however, they were l o c a t e d lateral in the nucleus a n d thus c o u l d be vestibular in o r i g i n n , la. W e frequently e n c o u n t e r e d clusters o f
370 neurons (mixed horizontal and vertical directions) responding like the lwo ceils shown in Fig. 2C. The activities of all such neurons described in Fig. 2 were modulated during both voluntary and compensatory vestibular evoked eye movement. In addition, a third type of activity (not illustrated in this paper) was found in prepositus neurons and/or axons. I1 consisted of an intense burst or, in cells with a maintained firing rate, a pause of activity during saccades (both uni- and pandirectional). When tonic activity was present in these neurons, it was not a function of eye position l~ ~a. In summary, we have been able to acquire records, typified by those shown in Fig. 2, from microelectrode tracks throughout the prepositus hypoglossi nucleus, extending from its posterior border near the obex to the level of the genu of the facial nerve. These results suggest that prepositus neurons may play a significant role in the generation and maintenance of both vertical and horizontal saccades and lixation irrespective of whether or not eye movements are induced by vestibular or visual stimuli. That prepositus activity may, in part, be carried to the oculomotor complex by the MLF is consistent with recently described activity in MLF fibers 5,1~ l h e data obtained in this study bear out the stimulation and lesion experiments of Hyde and Elliasson s who supported the concept of a medullary brain stem area TM involved with horizontal eye movement 6,1s. in addition, we now provide evidence for a posterior brain stem area important for vertical eye movement and likely the one (in part) responsible for deficits in vertical eye movement following MLF lesions~L Even though there is little doubt that prepositus neurons are intimately related to the vestibular system a, the fact that these neurons are so closely correlated with eye movement induced by any stimuli (visual or vestibular) suggests that they could, in addition, be part of the visuo-oculomotor pathway, a hypothesis supported by a number of lesion experiments s,~s, In this latter context, it is worth suggesting and testing the hypothesis that this brain stem area may, in fact, be the site where visuomotor signals originating from the midbrain tectum 9 are interfaced with vestibular information and transformed into appropriate motor commands. This idea is attractive because of the intimate relationship of the prepositus hypoglossi nucleus with the overlying vestibulo-cerebellum and the midline vermal areas "~,a,~7 which purportedly have important control functions for motor systems. This research was supported by Public Health Service Grants EY01074. NS09916 and NS-05748.
1 ALLEY, K., BAKER, R., AND SIMPSON, J. t., Afferents to the vestibulo-cerebellum and the origin of the visual climbing fiber in the rabbit, Brain Research, 98 (1975) 582-589. 2 ANGAUT,P., AND BRODAL,At, The projection of the 'vestibulocerebellum' onto the vestibular nuclei in the cat, Arch. ital. Biol., 105 (1967) 441-479. 3 BAKER,R., ANDBERTHOZ,A., Is the prepositus hypoglossi nucleus the source of another vestibuloocular pathway? Brain Research, 86 (1975) 121-127. 4 BRODAL, A., Experimental demonstration of cerebellar connexions from the peri-hypoglossal nuclei (nucleus intercalatus, nucleus praepositus hypoglossi and nucleus of roller) in the cat. J. Anat. (Lond.), 86 (1952) 110-120.
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