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The effects of electrical stimulation of deiters' nucleus upon hindlimb γ-motoneurons in the cat
BRAIN RESEARCH
385
T H E EFFECTS OF E L E C T R I C A L S T I M U L A T I O N O F DEITERS' N U C L E U S U P O N H I N D L I M B ? - M O T O N E U R O N S IN T H E CAT
MASAMICHI KATO AND JUN TANJ1 Department of Physiology, Hokkaido University School o f Medicine, Sapporo (Japan)
(Accepted January 22nd, 1971)
iNTRODUCTION The cells of Deiters' (lateral) nucleus send their axons as far as the lumbosacral spinal cord is, where they exert mono- and polysynaptic facilitatory effects on extensor a-motoneurons and polysynaptic inhibitory effects upon flexor a-motoneurons9,16,21. Granit et al. 7 and Carli et a l ) investigated the effects of electrical stimulation of Deiters' nucleus upon the discharge rate of spindle afferents of triceps surae muscles. Grillner et al. s observed the synaptic potentials elicited by stimulation o f the nucleus in ?-motoneurons. However, it is not possible to observe direct effects from the nucleus upon ?-motoneurons by the former method, since a muscle spindle is innervated by more than one ?-efferent fiber1,15, and some muscle spindles are so sensitive to mechanical stimuli that contraction of nearby extrafusal muscle fibers could bring a change of afferent discharges, even when their contraction cannot be detected by the myograph 17. It is extremely difficult to keep a microelectrode inside ?-motoneurons for a sufficient period of time to investigate synaptic events. In the present experiments, the effects of electrical stimulation of Deiters' nucleus upon ?-units, studied in thin lumbosacral ventral root filaments, were investigated as a first step. However, since the destination of ?-units isolated in ventral roots is not known, the effects from Deiters' nucleus upon ?-units were also investigated in peripheral nerves innervating extensor as well as flexor muscles as a second step. A part of the experimental results was reported at the 46th Annual Meeting of Physiological Society of Japan 12. MATERIALSAND METHODS The experiments were performed on 38 cats. Under ether anesthesia, the animal was fixed in a metal frame, and laminectomy was performed in the usual manner exposing L1-Sa spinal cord. The cerebellum was removed by suction exposing the floor o f the IVth ventricle, making it possible to insert the stimulating electrode into Deiters' nucleus under visual control. The exposed brain stem was bathed in warmed Brain Research, 30 (1971) 385-395
386
m. KATO AND J. q-ANJI
Ringer's fluid (36-37°C). After precollicular decerebration, the treatment with etl:cr was discontinued. The animal was then immobilized by intravenous application of gallamine triethiodide (Gallamine, Teisan Co.) and respired artificially. Bilateral pneumothorax was performed in order to minimize respiratory movement of tl~e brain stem. The exposed spinal cord and peripheral nerves were co~ered with warn:ed mineral oil, the temperature of the body and the oil pool being maintzdned at 36-38':C with a heating pad and an infrared lamp. Stimulation
In the early experiments a stimulating electrode consisting of an enameled steel wire 80 #m in diameter, exposed at the tip, was inserted several times into Deiters' nucleus and the surrounding structures. However, in the later experiments, a complex electrode array was used; each stimulating electrode consisted of an electrolyticalty sharpened tungsten wire (tip diameter about 80/zm, shaft diameter 120/zm) usually with less than 200 #m uninsulated wire at the tip. Nine electrodes were mounted together separated by 1 mm (3 × 3 electrodes). The indifferent electrode was always placed in the temporal muscle. During insertion of the metal electrodes the vestibule-
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Fig. 1. Identification of the stimulating points in the brain stem. A, Location of stimulating electrode No. 4. Drawing of section shows a lesion (note arrow) made passing current through the electrode at the end of the experiment. D, Deiters' nucleus; m, medial nucleus; i.o., inferior olive. B, Scheme of dorsal view of brain stem after removal of cerebellum showing the locations of the electrodes. Deiters' nucleus is outlined by the dashed line. C, Field potentials recorded from the electrodes shown in B on antidromic stimulation of vestibulospinal tract at L3-4.
Brain Research, 30 (1971) 385-395
387
VESTIBULAR INFLUENCES ON ~.'-MOTONEURONS
spinal tract was stimulated antidromically through the electrodes placed under the spinal cord at La-4. Field potentials produced by stimulation of the spinal cord were recorded with the metal electrodes in the brain stem (Fig. 1C and Wilson et al. 19) and served as a guide for electrode placement. During the experiment, rectangular pulses of 0.05 msec in duration were applied at the rate of 1/sec-500/sec through the electrodes with a stimulus strength below 2.0 V. Sometimes pulses up to 0.5 msec were used in addition.
Recording Watchmaker's forceps were used to isolate y-units under a binocular microscope either in L7 and $1 ventral roots or in peripheral nerves. The hindlimb nerves used were those to the knee flexor semitendinosus (ST); knee flexor tenuissimus (TEN); the ankle flexor tibialis anterior (TA); the ankle extensors gastrocnemius medialis (MG) and gastrocnemius lateralis with soleus (LGS); and the toe extensor plantaris (PL). The isolated nerves were mounted on silver recording electrodes and electrical activity was displayed on a cathode ray oscilloscope. The criteria for the identification of ~,-efferent fibers were (1) smaller amplitudes as compared with those from a fibers (see Fig. 9 and Hunt1°); (2) some units showed 'spontaneous' spikes at rest; (3) the conduction velocity was successfully measured in some cases, those with velocities below 45 m/sec being regarded as y-fibers. Attempts to measure velocities were made whenever units were isolated in the peripheral nerves, but were only sometimes successful because the filaments from which unitary discharges were recorded proved to be composed of several units when the ventral root was stimulated electrically. RESULTS
(I) On the localization of the stimulating points and current spread In the present experiments, descending fibers were activated by stimulation of localized regions of the brain stem, and the effects of the stimulation upon lumbosacral y-motoneurons were investigated. It must be recognized, however, that electrical stimulation of the brain stem involves hazardous problems such as the possibilities (1) of current spread and (2) of exciting fibers coursing through the nucleus a. Special attention was paid, in the present experiments, to these problems and attempts were made to overcome the difficulties (i) by inserting several electrodes into the brain stem, and (ii) by using a very weak stimulus strength as described in Methods. For example, only point 4 of Fig. 1B had an inhibitory effect upon unit 34-104, as shown in Fig. 2, while all other points, except for a doubtful effect from point 8, were ineffective. Upon unit 34-105 only point 8 had a weak, statistically significant facilitatory effect (not shown in the figure). On another unit (unit 34-107, not shown) only point 2 had a facilitatory effect. From these results, it can safely be said that the effect of stimulation is fairly well localized and the possibility of current spread is negligible under the present experimental conditions.
Brain Research, 30 (1971) 385-395
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Fig. 2. The effects of Deiters' nucleus stimulation at point 4 of Fig. 1 upon two 7-motoneurons in a thin ventral root filament. Unit 34-104 was clearly inhibited (P ,~ 0.001) by stimulation of the nucleus at 300/sec, with shocks of 0.1 msec duration and 0.88 V, although no significant effect was observed on unit 34-105.
In many experiments the effective points were distributed in the caudal half of the nucleus, although they were also seen in the rostral half (point 2 of Figs. 1 and 2). This result corresponds to those of Wilson et a13 ° that many L cells (the vestibulospinal neurons which send their axons as far as the lumbosacral level) were located in the caudal half, although some were in the rostral half. (Jr/) Gamma units recorded in ventral roots
Among 61 units recorded from the ventral roots 50 units (82 ~ ) showed spontaneous firing, and the remaining 11 units (18 ~o) showed no or little spontaneous firing. 5
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Fig. 3. The effects of stimulation of Deiters' nucleus with varied stimulus frequencies upon a- as well as 7-units recorded from the ventral root filament. Time marker 500 msec. See text for detail.
Brain Research, 30 (1971) 385-395
389
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On stimulation of Deiters' nucleus 24 (39%) of 61 )'-units showed facilitatory effects: either the spontaneous firing was increased or spikes were initiated in the silent units. Eleven units (18%) among 61 units were inhibited and no visible effect was observed on the remaining 26 units (43 %). The significance of the stimulating effect was determined statistically by the t test. ( a ) F a c i l i t a t o r y effects. Among 24 units that showed a facilitatory effect 16 units (67 %) were spontaneously active and 8 units (33 %) were silent or barely spontaneously firing. The facilitatory effect ranged from 30-100 % in the units that showed spontaneous discharges at rest. One of the facilitated units that was silent at rest is shown in Fig. 3. For this unit, stimuli to Deiters' nucleus were 0.5 msec pulses of 1.35 V at various frequencies from single shock to 500/sec. No appreciable effect was seen at stimulus frequencies less than 50/sec. At 50/sec spikes were initiated with a latency of about 500 msec (measured from the start of stimulation). The spike intervals became shorter as stimulation continued. When the stimulus frequency was increased to 100/sec, 300/sec and 500/see, the latencies were gradually shortened and the discharge frequency increased. At 300/sec large amplitude units (presumably a units) appeared. The effect of stimulation of Deiters' nucleus on the discharge frequency of this ),-unit is plotted with increasing stimulus frequencies in Fig. 4. As the graph shows, with increasing stimulus frequencies facilitatory effects were increased. The facilitatory effect lasted for 15-25 sec after the cessation of stimulation. The effects of stimulation of Deiters' nucleus upon this unit before and after opening of the ),-loop were compared. In order to open the ),-loop, the ventral roots from L5 downwards were cut. The facilitatory effect upon the ),-unit was unchanged during stimulation (Fig. 5), although the facilitatory effect lasted for only 1-2 sec after the cessation of the stimulation, as is seen in Fig. 6. On the other hand there were only a few a-motoneuron spikes. Grillner et al. 8 reported that monosynaptic EPSPs were recorded in some extensor )'-motoneurons on single shock stimulation of Deiters' nucleus. In the present Brain Research, 30 (1971) 385-395
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Fig. 5. Comparison of the effects of stimulation of Deiters' nucleus upon a- and y-units before and after cutting the y-loop. In either case Deiters' nucleus was stimulated at 500/sec, 0.5 msec in duration and 1.35 V. In the upper record, only a thin filameat was cut in the L7 ventral root from which the units were selected, all other ventral and dorsal roots being left intact. The lower record was taken after ventral roots from L3 downwards were cut in order to open the ~,-loop. Time marker 200 msec
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Fig. 6. Graphic'representation of the effects from Deiters' nucleus upon the ~'-motoneuron shown in Fig. 5. As seen~in the graph, increase of discharge of the ~'-unit during stimulation of the nucleus shows identicalfpattern, though the discharges lasted for only 20 msec after the y-loop was opened. tOO/lie. ____~300/N¢,
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Fig. 7. An example of an inhibitory effect. The unit was recorded from an Sz ventral root filament. During stimulation of Deiters' nucleus with 0.05 msee pulses of 1.6 V, at varied frequencies as shown in the graph, a strong inhibitory effect (P ,~ 0.001) was observed. Brain Research, 30 (1971) 385-395
391
VESTIBULAR INFLUENCES ON ~'-MOTONEURONS TABLE I EFFECTSOF STIMULATIONOF I)EITERS' NUCLEUSUPON ~)-UNITSIN THE PERIPHERALNERVES
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study, however, no discharge was initiated in ventral root filaments with single shock stimulation of Deiters' nucleus. (b) Inhibitory effect. Among 50 spontaneously firing ),-units 11 (22 ~ ) showed a decrease of discharge during stimulation of Deiters' nucleus. Maximal inhibitory effect was achieved with relatively weak stimulation, one example being shown in Fig. 7. In 4 cases the effect was tested of stimulation of Deiters' nucleus on the segmental inhibition of ),-units 11, which is evoked by stimulation of either dorsal roots or peripheral afferent fibers. In all these cases the segmental inhibition was prolonged significantly.
(III) The effects on v-units in peripheral nerves Fifty-three ),-units were recorded in the peripheral nerves: 18 MG, 5 LGS, 7 TEN, 19 ST, 3 TA and 1 PL ),-units, as summarized in Table I. (a) Facilitatory effect. As Table I shows a facilitatory effect was observed on M G and LGS )'-motoneurons, which are extensors. However, no facilitatory effect was observed on flexor ?,-neurons such as TA and ST, except for two instances of a weak facilitatory effect on 7-units of TENs which is regarded as a flexor. Among 18 M G ),-units, 4 units (22 ~ ) were facilitated, whereas no visible effect
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Fig. 8. An example of the facilitatory effect on an MG-7-unit. This unit showed spontaneous discharge at 3-8/sec. During stimulation of Deiters' nucleus with shocks at 300/sec, 0.05 msec in duration at 1.4 V, the discharge increased to 10-18 imp/sec. Statistically the effect was highly significant (P ~ 0.001).
Brain Research, 30 (1971) 385-395
392
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Fig. 9. An example of inhibited ;e-unit from the semitendinosus nerve. During stimulation of the nucleus at 300/sec, 0.08 msec in duration at 1.0 V for 5 sec, the y-unit decreased its discharge. The conduction velocity of the unit was 37 m/sec. Sporadic a spikes are seen.
was observed on the remaining 14 units (78~). Two among the 4 facilitated units showed fairly regular spontaneous discharges at 8-12 and 50-58 imp/sec, respectively, and 2 other units showed irregular spikes at 0-9 and 3-8 imp/sec, respectively. One example of the latter is shown in Fig. 8. Three (60 ~ ) out of 5 LGS units increased their discharge frequency during stimulation of Deiters' nucleus, and no visible effect was seen on the remaining 2 units. As to the weak facilitatory effect upon 2 TEN y-units, one showed a gradual increase of discharge frequency with a latency of about 1.6 sec when a stimulus train with a frequency of 300/sec was applied for 3 sec, with pulses 0.05 msec in duration at 1.0 V. Another showed an increase of about 45 ~ in the number of reflex spikes that were evoked by dorsal root stimulation during stimulation of Deiters' nucleus at 300/sec, 1.0 V and 0.05 msec pulses. As was seen with ventral root recording, a facilitatory effect was observed only when repetitive stimuli were applied to the nucleus, and no unit discharge was evoked by single shock stimulation. (b) Inhibitory effect. An inhibitory effect was observed only in flexor },-units. Two (29 ~ ) out of 7 TEN y-units showed inhibitory effects, whereas no appreciable effect was observed on 3 units (43 ~ ) . Inhibitory effects were shown on 9 (47 ?/o) out of 19 ST units, but no visible effect was observed on the remaining 10 units (53 ~o). One of the inhibited ST units is shown in Fig. 9. A m o n g 3 TA units an inhibitory effect was observed on 2 units ( 6 7 ~ ) and no visible effect was seen on the remaining 1 unit (33 ~). DISCUSSION
Reciprocal effects from Deiters' nucleus upon extensor and flexor y-motoneurons In the present study the activity o f y-motoneurons in ventral roots as well as in peripheral nerves was observed, and the effects of electrical stimulation of Deiters' nucleus upon them were investigated. The most prominent effects upon the y-motoneurons innervating hindlimb extensor and flexor muscles were reciprocal ones: a facilitatory effect on extensor y-motoneurons and an inhibitory effect upon flexor y-units. This result corresponds to those of Wilson and Yoshida 21 who obtained, on stimulation of Deiters' nucleus, monosynaptic and polysynaptic EPSPs in some hindlimb extensor a-motoneurons
Brain Research, 30 (1971) 385-395
VESTIBULARINFLUENCESON ~'-MOTONEURONS
393
and a polysynaptic inhibitory effect in some flexor a-motoneurons. Apparently the facilitatory effect from Deiters' nucleus upon extensor a-motoneurons is strengthened by increased spindle afferent discharges from their own as well as from synergistic muscle spindles, and the inhibitory effect upon flexor a-motoneurons is supplemented by decreased sensitivity of flexor muscle spindles. As to the two TEN ),-motoneurons that received a facilitatory effect from Deiters' nucleus, the effect was considered to be exerted indirectly through such structures as the reticular formation rather than through the vestibulospinal tract, since the effect was not marked and the latency was unusually long. Although Grillner et al. 8 reported that there exist monosynaptic connections from Deiters' nucleus to some GS and PL ~,-motoneurons, no ~,-motoneuron in the present study was fired by single shock stimulation with short latency. This discrepancy may be explained by the facts that (1) weak stimuli less than 2.0 V were used in the present experiment and (2) impulses were recorded either in the ventral roots or in the peripheral nerves so that no synaptic potential could be registered. Relation between a and ~ excitation
Granit and Kaada 6 first reported that from several central structures the threshold for excitation of ~-motoneurons is often lower than that of a-motoneurons. In the present experiments, the ~, spikes also appeared before the a spikes (see Fig. 3). There are two possibilities of explaining this observation; firstly, a thicker vestibulospinal tract may connect to 7-motoneurons; and secondly, there may be no difference between the vestibulospinal tracts to the two kinds of motoneuron but since the input resistance of ~,-motoneurons is considerably higher than that of a-motoneurons4,S,9, la, ),-motoneurons may fire in response to a smaller synaptic input. This latter possibility seems more reasonable at the present time. Concerning the former possibility, Brodal 2 suggested that the small vestibulospinal tract neurons may connect to 7" motoneurons, and large vestibulospinal tract neurons to a-motoneurons. Grillner et al. a, however, reported that fast conducting fibers (above 100 m/sec)elicited a monosynaptic EPSP in some ~,-motoneurons. More data will be needed before any conclusive statement can be made on this point. Koeze et al. 14 analyzed the effect of motor cortex stimulation upon a- and ~,motoneurons innervating the extensor digitorum communis muscle of the baboon and stated that when prolonged low-frequency stimulation was given, both a- and ~,motoneurons are activated simultaneously, and this activation hardly outlasts the train of stimuli. These results may mean that the pyramidal system is concerned primarily with phasic movements. On the contrary, Deiters' nucleus is considered to be mainly concerned with maintenance of posture. The differences between the results[of Koeze et al. 14 and ours might be explained by the different functions of the two systems.
Brain Research, 30 (1971) 385-395
394
M, I~.AIO AND .I. IAN.II
SUMMARY
The effects o f electrical s t i m u l a t i o n o f Deiters' nucleus u p o n h i n d l i m b 7 - m o t o n e u r o n s were investigated in 38 d e c e r e b r a t e d and decerebellated cats. V activity was r e c o r d e d in ventral r o o t s as well as in peripheral nerves. A m o n g 61 v-units r e c o r d e d in L7 a n d $1 ventral roots, 24 (39 %) were facilitated, 11 (18 ~ ) were inhibited and no visible effect was observed on the r e m a i n i n g 26 (43 o~;). In p e r i p h e r a l nerves 53 v-units were investigated: 18 medial gastrocnemius, 5 lateral gastrocnemius-soleus, 7 tenuissimus, 19 semitendinosus, 3 a n t e r i o r tibial nerves a n d 1 plantaris nerve. Extensor v - m o t o n e u r o n s such as the medial g a s t r o c n e m i u s (4/18 o r 2 2 ~ ) and lateral g a s t r o c n e m i u s - s o l e u s (3/5 or 60%) were facilitated, and flexor v - m o t o n e u r o n s such as semitendinosus (9/19 or 47~o), tenuissimus (2/7 or 2 9 ~ ) a n d tibialis a n t e r i o r (2/3 or 67~o) were inhibited. T h e meaning o f these effects f r o m Deiters' nucleus upon h i n d l i m b v - m o t o n e u r o n s is discussed. ACKNOWLEDGEMENTS The a u t h o r s express their t h a n k s to P r o f e s s o r B. F u j i m o r i for reading the d r a f t o f this p a p e r . T h e y also express their g r a t i t u d e to P r o f e s s o r V. J. W i l s o n o f The R o c k e feller University for his m a n y v a l u a b l e c o m m e n t s a n d i m p r o v e m e n t o f the English.
REFERENCES 1 BARKER,D., STACEY, M. J., AND ADAL, M. N., Fusimotor innervations in the cat, Phil. Trans. B,
258 (1970) 315-346. 2 BRODAL, A., Anatomical organization of cerebello-vestibulo-spinal pathways. In A. V. S. DE REUCK AND J. KNIGHT (Eds.), Myototic, Kinesthetic and Vestibular Mechanisms, Churchill, London, 1967, pp. 148-169. 3 BRODAL, A., POMPEIANO, O., AND WALBERG, F., The Vestibular Nuclei and their Connections. Anatomy and Functional Correlations, Oliver and Boyd, Edinburgh, 1962, pp. 6-99. 4 BURKE, R. E., Group Ia synaptic input to fast and slow twitch motor units of cat triceps surae, J. Physiol. (Lond.), 196 (1968) 605-630. 5 CARLI, G., DIETE-SPIFF, K., AND POMPEtANO, O., Responses of the muscle spindles and of the extrafusal fibers in an extensor muscle to stimulation of the lateral vestibular nucleus in the cat, Arch. ital. Biol., t05 (1967) 209-242. 6 GRANIT,R., AND KAADA,B. R., Influence of stimulation of central nervous structures on muscle spindles in cat, Actaphysiol. scand., 27 (1952) 130-160. 7 GRANIT, R., POMPEIANO, O., AND WALTMAN,l . , Fast supraspinal control of mammalian muscle spindles: extra- and intrafusal co-activation, J. Physiol. (Lond.), 147 (1959) 385-398. 8 GRILLNER,S., HONGO, T., AND LUND, S., Descending monosynaptic and reflex control of~J-motoneurons, Actaphysiol. scand., 75 (1969) 592-613. 9 GRILLNER,S., HONGO, T., AND LUND, S., The vestibulospinal tract. Effects on alpha-motoneurons in the lumbosacral spinal cord in the cat, Exp. Brain Res., 10 (1970) 94-120. 10 HUNT, C. C., The reflex activity of mammalian small nerve fibres, J. Physiol. (Lond.), 115 (1951) 456-469. II HUNT, C. C., AND PAINTAL, A. S., Spinal reflex regulation of fusimotor neurons, J. Physiol. (Lond.), 143 (1958) 195-212. 12 KATO, M., YAMAUCHI,T., AND TANJI, J., The effects from Deiters' nucleus on ),-motoneurons, J. Physiol. Soc. Jap., 31 (1969) 390. Brain Research, 30 (1971) 385-395
VESTIBULAR INFLUENCES ON ~-MOTONEURONS
395
13 KERNELL,D., Input resistance, electrical excitability and size of ventral horn cells in cat spinal cord, Science, 152 (1966) 1637-1640. 14 KOEZE, T. H., PHILLIPS, C. G., AND SHERIDAN, J. D., Thresholds of cortical activation of muscle spindles and motoneurons of the baboon's hand, J. Physiol. (Lond.), 195 (1968) 419-449. 15 KU~FLER,S. W., AND HUNT, C. C., The mammalian small nerve fibers; a system for efferent nervous regulation of muscle spindle discharge, Res. Publ. Ass. herr. ment. Dis., 30 (1952) 24-47. 16 LUND, S., AND POMPEIANO,O., Monosynaptic excitation of alpha motoneurones from supraspinal structures in the cat, Acta physiol, scand., 73 (1968) 1-12. 17 MATTHEWS,P. B. C., Muscle spindles and their motor control, Physiol. Rev., 44 (1964) 219-288. 18 NYaERG-HANSEN,R., Functional organization of descending supraspinal fiber systems to the spinal cord. Anatomical observations and physiological correlations, Ergebn. Anat. Entwickl.Gesch., 39 (1966) 6-48. 19 WILSON,V. J., KATO, M., THOMAS, R. C., AND PETERSON, B. W., Excitation of lateral vestibular neurons by peripheral afferent fibers, J. Neurophysiol., 29 (1966) 508-529. 20 WILSON, V. J., KATO, M., PETERSON,B. W., AND WYLIE, R. M., A single-unit analysis of the organization of Deiters' nucleus, J. Neurophysiol., 30 (1967) 603-619. 21 WILSON,V. J,, AND YOSHIDA, M., Comparison of effects of stimulation of Deiters' nucleus and medial longitudinal fasciculus on neck, forelimb and hindlimb motoneurons, J. Neurophysiol., 32 (1969) 743-758.
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385
T H E EFFECTS OF E L E C T R I C A L S T I M U L A T I O N O F DEITERS' N U C L E U S U P O N H I N D L I M B ? - M O T O N E U R O N S IN T H E CAT
MASAMICHI KATO AND JUN TANJ1 Department of Physiology, Hokkaido University School o f Medicine, Sapporo (Japan)
(Accepted January 22nd, 1971)
iNTRODUCTION The cells of Deiters' (lateral) nucleus send their axons as far as the lumbosacral spinal cord is, where they exert mono- and polysynaptic facilitatory effects on extensor a-motoneurons and polysynaptic inhibitory effects upon flexor a-motoneurons9,16,21. Granit et al. 7 and Carli et a l ) investigated the effects of electrical stimulation of Deiters' nucleus upon the discharge rate of spindle afferents of triceps surae muscles. Grillner et al. s observed the synaptic potentials elicited by stimulation o f the nucleus in ?-motoneurons. However, it is not possible to observe direct effects from the nucleus upon ?-motoneurons by the former method, since a muscle spindle is innervated by more than one ?-efferent fiber1,15, and some muscle spindles are so sensitive to mechanical stimuli that contraction of nearby extrafusal muscle fibers could bring a change of afferent discharges, even when their contraction cannot be detected by the myograph 17. It is extremely difficult to keep a microelectrode inside ?-motoneurons for a sufficient period of time to investigate synaptic events. In the present experiments, the effects of electrical stimulation of Deiters' nucleus upon ?-units, studied in thin lumbosacral ventral root filaments, were investigated as a first step. However, since the destination of ?-units isolated in ventral roots is not known, the effects from Deiters' nucleus upon ?-units were also investigated in peripheral nerves innervating extensor as well as flexor muscles as a second step. A part of the experimental results was reported at the 46th Annual Meeting of Physiological Society of Japan 12. MATERIALSAND METHODS The experiments were performed on 38 cats. Under ether anesthesia, the animal was fixed in a metal frame, and laminectomy was performed in the usual manner exposing L1-Sa spinal cord. The cerebellum was removed by suction exposing the floor o f the IVth ventricle, making it possible to insert the stimulating electrode into Deiters' nucleus under visual control. The exposed brain stem was bathed in warmed Brain Research, 30 (1971) 385-395
386
m. KATO AND J. q-ANJI
Ringer's fluid (36-37°C). After precollicular decerebration, the treatment with etl:cr was discontinued. The animal was then immobilized by intravenous application of gallamine triethiodide (Gallamine, Teisan Co.) and respired artificially. Bilateral pneumothorax was performed in order to minimize respiratory movement of tl~e brain stem. The exposed spinal cord and peripheral nerves were co~ered with warn:ed mineral oil, the temperature of the body and the oil pool being maintzdned at 36-38':C with a heating pad and an infrared lamp. Stimulation
In the early experiments a stimulating electrode consisting of an enameled steel wire 80 #m in diameter, exposed at the tip, was inserted several times into Deiters' nucleus and the surrounding structures. However, in the later experiments, a complex electrode array was used; each stimulating electrode consisted of an electrolyticalty sharpened tungsten wire (tip diameter about 80/zm, shaft diameter 120/zm) usually with less than 200 #m uninsulated wire at the tip. Nine electrodes were mounted together separated by 1 mm (3 × 3 electrodes). The indifferent electrode was always placed in the temporal muscle. During insertion of the metal electrodes the vestibule-
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Fig. 1. Identification of the stimulating points in the brain stem. A, Location of stimulating electrode No. 4. Drawing of section shows a lesion (note arrow) made passing current through the electrode at the end of the experiment. D, Deiters' nucleus; m, medial nucleus; i.o., inferior olive. B, Scheme of dorsal view of brain stem after removal of cerebellum showing the locations of the electrodes. Deiters' nucleus is outlined by the dashed line. C, Field potentials recorded from the electrodes shown in B on antidromic stimulation of vestibulospinal tract at L3-4.
Brain Research, 30 (1971) 385-395
387
VESTIBULAR INFLUENCES ON ~.'-MOTONEURONS
spinal tract was stimulated antidromically through the electrodes placed under the spinal cord at La-4. Field potentials produced by stimulation of the spinal cord were recorded with the metal electrodes in the brain stem (Fig. 1C and Wilson et al. 19) and served as a guide for electrode placement. During the experiment, rectangular pulses of 0.05 msec in duration were applied at the rate of 1/sec-500/sec through the electrodes with a stimulus strength below 2.0 V. Sometimes pulses up to 0.5 msec were used in addition.
Recording Watchmaker's forceps were used to isolate y-units under a binocular microscope either in L7 and $1 ventral roots or in peripheral nerves. The hindlimb nerves used were those to the knee flexor semitendinosus (ST); knee flexor tenuissimus (TEN); the ankle flexor tibialis anterior (TA); the ankle extensors gastrocnemius medialis (MG) and gastrocnemius lateralis with soleus (LGS); and the toe extensor plantaris (PL). The isolated nerves were mounted on silver recording electrodes and electrical activity was displayed on a cathode ray oscilloscope. The criteria for the identification of ~,-efferent fibers were (1) smaller amplitudes as compared with those from a fibers (see Fig. 9 and Hunt1°); (2) some units showed 'spontaneous' spikes at rest; (3) the conduction velocity was successfully measured in some cases, those with velocities below 45 m/sec being regarded as y-fibers. Attempts to measure velocities were made whenever units were isolated in the peripheral nerves, but were only sometimes successful because the filaments from which unitary discharges were recorded proved to be composed of several units when the ventral root was stimulated electrically. RESULTS
(I) On the localization of the stimulating points and current spread In the present experiments, descending fibers were activated by stimulation of localized regions of the brain stem, and the effects of the stimulation upon lumbosacral y-motoneurons were investigated. It must be recognized, however, that electrical stimulation of the brain stem involves hazardous problems such as the possibilities (1) of current spread and (2) of exciting fibers coursing through the nucleus a. Special attention was paid, in the present experiments, to these problems and attempts were made to overcome the difficulties (i) by inserting several electrodes into the brain stem, and (ii) by using a very weak stimulus strength as described in Methods. For example, only point 4 of Fig. 1B had an inhibitory effect upon unit 34-104, as shown in Fig. 2, while all other points, except for a doubtful effect from point 8, were ineffective. Upon unit 34-105 only point 8 had a weak, statistically significant facilitatory effect (not shown in the figure). On another unit (unit 34-107, not shown) only point 2 had a facilitatory effect. From these results, it can safely be said that the effect of stimulation is fairly well localized and the possibility of current spread is negligible under the present experimental conditions.
Brain Research, 30 (1971) 385-395
M. KATO
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Fig. 2. The effects of Deiters' nucleus stimulation at point 4 of Fig. 1 upon two 7-motoneurons in a thin ventral root filament. Unit 34-104 was clearly inhibited (P ,~ 0.001) by stimulation of the nucleus at 300/sec, with shocks of 0.1 msec duration and 0.88 V, although no significant effect was observed on unit 34-105.
In many experiments the effective points were distributed in the caudal half of the nucleus, although they were also seen in the rostral half (point 2 of Figs. 1 and 2). This result corresponds to those of Wilson et a13 ° that many L cells (the vestibulospinal neurons which send their axons as far as the lumbosacral level) were located in the caudal half, although some were in the rostral half. (Jr/) Gamma units recorded in ventral roots
Among 61 units recorded from the ventral roots 50 units (82 ~ ) showed spontaneous firing, and the remaining 11 units (18 ~o) showed no or little spontaneous firing. 5
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Fig. 3. The effects of stimulation of Deiters' nucleus with varied stimulus frequencies upon a- as well as 7-units recorded from the ventral root filament. Time marker 500 msec. See text for detail.
Brain Research, 30 (1971) 385-395
389
VESTIBULAR INFLUENCES ON )'-MOTONEURONS
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On stimulation of Deiters' nucleus 24 (39%) of 61 )'-units showed facilitatory effects: either the spontaneous firing was increased or spikes were initiated in the silent units. Eleven units (18%) among 61 units were inhibited and no visible effect was observed on the remaining 26 units (43 %). The significance of the stimulating effect was determined statistically by the t test. ( a ) F a c i l i t a t o r y effects. Among 24 units that showed a facilitatory effect 16 units (67 %) were spontaneously active and 8 units (33 %) were silent or barely spontaneously firing. The facilitatory effect ranged from 30-100 % in the units that showed spontaneous discharges at rest. One of the facilitated units that was silent at rest is shown in Fig. 3. For this unit, stimuli to Deiters' nucleus were 0.5 msec pulses of 1.35 V at various frequencies from single shock to 500/sec. No appreciable effect was seen at stimulus frequencies less than 50/sec. At 50/sec spikes were initiated with a latency of about 500 msec (measured from the start of stimulation). The spike intervals became shorter as stimulation continued. When the stimulus frequency was increased to 100/sec, 300/sec and 500/see, the latencies were gradually shortened and the discharge frequency increased. At 300/sec large amplitude units (presumably a units) appeared. The effect of stimulation of Deiters' nucleus on the discharge frequency of this ),-unit is plotted with increasing stimulus frequencies in Fig. 4. As the graph shows, with increasing stimulus frequencies facilitatory effects were increased. The facilitatory effect lasted for 15-25 sec after the cessation of stimulation. The effects of stimulation of Deiters' nucleus upon this unit before and after opening of the ),-loop were compared. In order to open the ),-loop, the ventral roots from L5 downwards were cut. The facilitatory effect upon the ),-unit was unchanged during stimulation (Fig. 5), although the facilitatory effect lasted for only 1-2 sec after the cessation of the stimulation, as is seen in Fig. 6. On the other hand there were only a few a-motoneuron spikes. Grillner et al. 8 reported that monosynaptic EPSPs were recorded in some extensor )'-motoneurons on single shock stimulation of Deiters' nucleus. In the present Brain Research, 30 (1971) 385-395
390
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Fig. 5. Comparison of the effects of stimulation of Deiters' nucleus upon a- and y-units before and after cutting the y-loop. In either case Deiters' nucleus was stimulated at 500/sec, 0.5 msec in duration and 1.35 V. In the upper record, only a thin filameat was cut in the L7 ventral root from which the units were selected, all other ventral and dorsal roots being left intact. The lower record was taken after ventral roots from L3 downwards were cut in order to open the ~,-loop. Time marker 200 msec
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Fig. 6. Graphic'representation of the effects from Deiters' nucleus upon the ~'-motoneuron shown in Fig. 5. As seen~in the graph, increase of discharge of the ~'-unit during stimulation of the nucleus shows identicalfpattern, though the discharges lasted for only 20 msec after the y-loop was opened. tOO/lie. ____~300/N¢,
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Fig. 7. An example of an inhibitory effect. The unit was recorded from an Sz ventral root filament. During stimulation of Deiters' nucleus with 0.05 msee pulses of 1.6 V, at varied frequencies as shown in the graph, a strong inhibitory effect (P ,~ 0.001) was observed. Brain Research, 30 (1971) 385-395
391
VESTIBULAR INFLUENCES ON ~'-MOTONEURONS TABLE I EFFECTSOF STIMULATIONOF I)EITERS' NUCLEUSUPON ~)-UNITSIN THE PERIPHERALNERVES
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study, however, no discharge was initiated in ventral root filaments with single shock stimulation of Deiters' nucleus. (b) Inhibitory effect. Among 50 spontaneously firing ),-units 11 (22 ~ ) showed a decrease of discharge during stimulation of Deiters' nucleus. Maximal inhibitory effect was achieved with relatively weak stimulation, one example being shown in Fig. 7. In 4 cases the effect was tested of stimulation of Deiters' nucleus on the segmental inhibition of ),-units 11, which is evoked by stimulation of either dorsal roots or peripheral afferent fibers. In all these cases the segmental inhibition was prolonged significantly.
(III) The effects on v-units in peripheral nerves Fifty-three ),-units were recorded in the peripheral nerves: 18 MG, 5 LGS, 7 TEN, 19 ST, 3 TA and 1 PL ),-units, as summarized in Table I. (a) Facilitatory effect. As Table I shows a facilitatory effect was observed on M G and LGS )'-motoneurons, which are extensors. However, no facilitatory effect was observed on flexor ?,-neurons such as TA and ST, except for two instances of a weak facilitatory effect on 7-units of TENs which is regarded as a flexor. Among 18 M G ),-units, 4 units (22 ~ ) were facilitated, whereas no visible effect
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Brain Research, 30 (1971) 385-395
392
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Fig. 9. An example of inhibited ;e-unit from the semitendinosus nerve. During stimulation of the nucleus at 300/sec, 0.08 msec in duration at 1.0 V for 5 sec, the y-unit decreased its discharge. The conduction velocity of the unit was 37 m/sec. Sporadic a spikes are seen.
was observed on the remaining 14 units (78~). Two among the 4 facilitated units showed fairly regular spontaneous discharges at 8-12 and 50-58 imp/sec, respectively, and 2 other units showed irregular spikes at 0-9 and 3-8 imp/sec, respectively. One example of the latter is shown in Fig. 8. Three (60 ~ ) out of 5 LGS units increased their discharge frequency during stimulation of Deiters' nucleus, and no visible effect was seen on the remaining 2 units. As to the weak facilitatory effect upon 2 TEN y-units, one showed a gradual increase of discharge frequency with a latency of about 1.6 sec when a stimulus train with a frequency of 300/sec was applied for 3 sec, with pulses 0.05 msec in duration at 1.0 V. Another showed an increase of about 45 ~ in the number of reflex spikes that were evoked by dorsal root stimulation during stimulation of Deiters' nucleus at 300/sec, 1.0 V and 0.05 msec pulses. As was seen with ventral root recording, a facilitatory effect was observed only when repetitive stimuli were applied to the nucleus, and no unit discharge was evoked by single shock stimulation. (b) Inhibitory effect. An inhibitory effect was observed only in flexor },-units. Two (29 ~ ) out of 7 TEN y-units showed inhibitory effects, whereas no appreciable effect was observed on 3 units (43 ~ ) . Inhibitory effects were shown on 9 (47 ?/o) out of 19 ST units, but no visible effect was observed on the remaining 10 units (53 ~o). One of the inhibited ST units is shown in Fig. 9. A m o n g 3 TA units an inhibitory effect was observed on 2 units ( 6 7 ~ ) and no visible effect was seen on the remaining 1 unit (33 ~). DISCUSSION
Reciprocal effects from Deiters' nucleus upon extensor and flexor y-motoneurons In the present study the activity o f y-motoneurons in ventral roots as well as in peripheral nerves was observed, and the effects of electrical stimulation of Deiters' nucleus upon them were investigated. The most prominent effects upon the y-motoneurons innervating hindlimb extensor and flexor muscles were reciprocal ones: a facilitatory effect on extensor y-motoneurons and an inhibitory effect upon flexor y-units. This result corresponds to those of Wilson and Yoshida 21 who obtained, on stimulation of Deiters' nucleus, monosynaptic and polysynaptic EPSPs in some hindlimb extensor a-motoneurons
Brain Research, 30 (1971) 385-395
VESTIBULARINFLUENCESON ~'-MOTONEURONS
393
and a polysynaptic inhibitory effect in some flexor a-motoneurons. Apparently the facilitatory effect from Deiters' nucleus upon extensor a-motoneurons is strengthened by increased spindle afferent discharges from their own as well as from synergistic muscle spindles, and the inhibitory effect upon flexor a-motoneurons is supplemented by decreased sensitivity of flexor muscle spindles. As to the two TEN ),-motoneurons that received a facilitatory effect from Deiters' nucleus, the effect was considered to be exerted indirectly through such structures as the reticular formation rather than through the vestibulospinal tract, since the effect was not marked and the latency was unusually long. Although Grillner et al. 8 reported that there exist monosynaptic connections from Deiters' nucleus to some GS and PL ~,-motoneurons, no ~,-motoneuron in the present study was fired by single shock stimulation with short latency. This discrepancy may be explained by the facts that (1) weak stimuli less than 2.0 V were used in the present experiment and (2) impulses were recorded either in the ventral roots or in the peripheral nerves so that no synaptic potential could be registered. Relation between a and ~ excitation
Granit and Kaada 6 first reported that from several central structures the threshold for excitation of ~-motoneurons is often lower than that of a-motoneurons. In the present experiments, the ~, spikes also appeared before the a spikes (see Fig. 3). There are two possibilities of explaining this observation; firstly, a thicker vestibulospinal tract may connect to 7-motoneurons; and secondly, there may be no difference between the vestibulospinal tracts to the two kinds of motoneuron but since the input resistance of ~,-motoneurons is considerably higher than that of a-motoneurons4,S,9, la, ),-motoneurons may fire in response to a smaller synaptic input. This latter possibility seems more reasonable at the present time. Concerning the former possibility, Brodal 2 suggested that the small vestibulospinal tract neurons may connect to 7" motoneurons, and large vestibulospinal tract neurons to a-motoneurons. Grillner et al. a, however, reported that fast conducting fibers (above 100 m/sec)elicited a monosynaptic EPSP in some ~,-motoneurons. More data will be needed before any conclusive statement can be made on this point. Koeze et al. 14 analyzed the effect of motor cortex stimulation upon a- and ~,motoneurons innervating the extensor digitorum communis muscle of the baboon and stated that when prolonged low-frequency stimulation was given, both a- and ~,motoneurons are activated simultaneously, and this activation hardly outlasts the train of stimuli. These results may mean that the pyramidal system is concerned primarily with phasic movements. On the contrary, Deiters' nucleus is considered to be mainly concerned with maintenance of posture. The differences between the results[of Koeze et al. 14 and ours might be explained by the different functions of the two systems.
Brain Research, 30 (1971) 385-395
394
M, I~.AIO AND .I. IAN.II
SUMMARY
The effects o f electrical s t i m u l a t i o n o f Deiters' nucleus u p o n h i n d l i m b 7 - m o t o n e u r o n s were investigated in 38 d e c e r e b r a t e d and decerebellated cats. V activity was r e c o r d e d in ventral r o o t s as well as in peripheral nerves. A m o n g 61 v-units r e c o r d e d in L7 a n d $1 ventral roots, 24 (39 %) were facilitated, 11 (18 ~ ) were inhibited and no visible effect was observed on the r e m a i n i n g 26 (43 o~;). In p e r i p h e r a l nerves 53 v-units were investigated: 18 medial gastrocnemius, 5 lateral gastrocnemius-soleus, 7 tenuissimus, 19 semitendinosus, 3 a n t e r i o r tibial nerves a n d 1 plantaris nerve. Extensor v - m o t o n e u r o n s such as the medial g a s t r o c n e m i u s (4/18 o r 2 2 ~ ) and lateral g a s t r o c n e m i u s - s o l e u s (3/5 or 60%) were facilitated, and flexor v - m o t o n e u r o n s such as semitendinosus (9/19 or 47~o), tenuissimus (2/7 or 2 9 ~ ) a n d tibialis a n t e r i o r (2/3 or 67~o) were inhibited. T h e meaning o f these effects f r o m Deiters' nucleus upon h i n d l i m b v - m o t o n e u r o n s is discussed. ACKNOWLEDGEMENTS The a u t h o r s express their t h a n k s to P r o f e s s o r B. F u j i m o r i for reading the d r a f t o f this p a p e r . T h e y also express their g r a t i t u d e to P r o f e s s o r V. J. W i l s o n o f The R o c k e feller University for his m a n y v a l u a b l e c o m m e n t s a n d i m p r o v e m e n t o f the English.
REFERENCES 1 BARKER,D., STACEY, M. J., AND ADAL, M. N., Fusimotor innervations in the cat, Phil. Trans. B,
258 (1970) 315-346. 2 BRODAL, A., Anatomical organization of cerebello-vestibulo-spinal pathways. In A. V. S. DE REUCK AND J. KNIGHT (Eds.), Myototic, Kinesthetic and Vestibular Mechanisms, Churchill, London, 1967, pp. 148-169. 3 BRODAL, A., POMPEIANO, O., AND WALBERG, F., The Vestibular Nuclei and their Connections. Anatomy and Functional Correlations, Oliver and Boyd, Edinburgh, 1962, pp. 6-99. 4 BURKE, R. E., Group Ia synaptic input to fast and slow twitch motor units of cat triceps surae, J. Physiol. (Lond.), 196 (1968) 605-630. 5 CARLI, G., DIETE-SPIFF, K., AND POMPEtANO, O., Responses of the muscle spindles and of the extrafusal fibers in an extensor muscle to stimulation of the lateral vestibular nucleus in the cat, Arch. ital. Biol., t05 (1967) 209-242. 6 GRANIT,R., AND KAADA,B. R., Influence of stimulation of central nervous structures on muscle spindles in cat, Actaphysiol. scand., 27 (1952) 130-160. 7 GRANIT, R., POMPEIANO, O., AND WALTMAN,l . , Fast supraspinal control of mammalian muscle spindles: extra- and intrafusal co-activation, J. Physiol. (Lond.), 147 (1959) 385-398. 8 GRILLNER,S., HONGO, T., AND LUND, S., Descending monosynaptic and reflex control of~J-motoneurons, Actaphysiol. scand., 75 (1969) 592-613. 9 GRILLNER,S., HONGO, T., AND LUND, S., The vestibulospinal tract. Effects on alpha-motoneurons in the lumbosacral spinal cord in the cat, Exp. Brain Res., 10 (1970) 94-120. 10 HUNT, C. C., The reflex activity of mammalian small nerve fibres, J. Physiol. (Lond.), 115 (1951) 456-469. II HUNT, C. C., AND PAINTAL, A. S., Spinal reflex regulation of fusimotor neurons, J. Physiol. (Lond.), 143 (1958) 195-212. 12 KATO, M., YAMAUCHI,T., AND TANJI, J., The effects from Deiters' nucleus on ),-motoneurons, J. Physiol. Soc. Jap., 31 (1969) 390. Brain Research, 30 (1971) 385-395
VESTIBULAR INFLUENCES ON ~-MOTONEURONS
395
13 KERNELL,D., Input resistance, electrical excitability and size of ventral horn cells in cat spinal cord, Science, 152 (1966) 1637-1640. 14 KOEZE, T. H., PHILLIPS, C. G., AND SHERIDAN, J. D., Thresholds of cortical activation of muscle spindles and motoneurons of the baboon's hand, J. Physiol. (Lond.), 195 (1968) 419-449. 15 KU~FLER,S. W., AND HUNT, C. C., The mammalian small nerve fibers; a system for efferent nervous regulation of muscle spindle discharge, Res. Publ. Ass. herr. ment. Dis., 30 (1952) 24-47. 16 LUND, S., AND POMPEIANO,O., Monosynaptic excitation of alpha motoneurones from supraspinal structures in the cat, Acta physiol, scand., 73 (1968) 1-12. 17 MATTHEWS,P. B. C., Muscle spindles and their motor control, Physiol. Rev., 44 (1964) 219-288. 18 NYaERG-HANSEN,R., Functional organization of descending supraspinal fiber systems to the spinal cord. Anatomical observations and physiological correlations, Ergebn. Anat. Entwickl.Gesch., 39 (1966) 6-48. 19 WILSON,V. J., KATO, M., THOMAS, R. C., AND PETERSON, B. W., Excitation of lateral vestibular neurons by peripheral afferent fibers, J. Neurophysiol., 29 (1966) 508-529. 20 WILSON, V. J., KATO, M., PETERSON,B. W., AND WYLIE, R. M., A single-unit analysis of the organization of Deiters' nucleus, J. Neurophysiol., 30 (1967) 603-619. 21 WILSON,V. J,, AND YOSHIDA, M., Comparison of effects of stimulation of Deiters' nucleus and medial longitudinal fasciculus on neck, forelimb and hindlimb motoneurons, J. Neurophysiol., 32 (1969) 743-758.
Brain Research, 30 (1971) 385-395