Exp. Brain Res. 22, 69--86 (1975) 9 by Springer-Verlag 1975

Labyrinthine Influence on Cat Forelimb Motoneurons* M. MAEDA, I~.A. MAu?cz** and V.J. WILSON The P~ockefeller University, New York (USA) Received July 22, 1974 Summary. 1. Intracellular responses in forelimb motoneurons to electrical stimulation of the whole labyrinth and of individual semicircular canal nerves were studied in deeerebrated, unanesthetized eats. 2. Stimulation of the whole labyrinth typically produced EPSPs, usually bilaterally, in forelimb extensor (LON, LAT, MED) and shoulder (SI) motoneurons and bilateral I P S P s in forelimb flexor (BIC) motoneurons. 3. Latencies of PSPs indicated that most of those in extensor motoneurons were trisynaptie and many seen in flexor motoneurons may involve four synapses. 4. I n the cells sampled, stimulation of the anterior, horizontal or posterior canal nerves often evoked EPSPs in extensor and IPSPs in flexor motoneurons, both ipsi- and eontralaterally. Responses to canal stimulation were weaker and more variable than those to stimulation of the whole nerve. 5. Transection of the MLF in the lower medulla had no effect on PSPs evoked in forelimb motoneurons. Lesions in the medulla in the area of the LVST greatly reduced the occurrence of eontralateral EPSPs in extensor and IPSPs in flexor motoneurons. The pathway linking labyrinths to forelimb motoneurons therefore appears to include the LVST. Itemisection shows that the pathway to eontralateral motoneurons descends in the cord on the side of the stimulated labyrinth before crossing to influence these cells. 6. Labyrinthine control of forelimb motoneurons is less direct than control of neck and back motoneurons. I t is suggested that the interneuron in the pathway to forelimb motoneurons is the site of integration of labyrinthine with other reflexes. Key words : Labyrinth - - Forelimb motoneurons - - Lateral vestibulospinal tract

Introduction Activation of labyrinthine receptors results in precise reflex activation of the neck musculature by means of the lateral and medial vestibulospinal tracts (LVST and MVST). In particular, stimulation of individual semicircular canal nerves evokes a pattern of disynaptic excitation and inhibition of neck motoneurons (Wilson and Maeda, 1974) that can account for the head movements produced by similar stimuli (Suzuki and Cohen, 1964). Although it is well known that there * Supported in par~ by N.I.H. grants NS 02619 and NS 05463, ** l~ecipient of N.I.H. Fellowship 1 F02 NS 55199.

70

M. Maeda et al.

are l a b y r i n t h i n e reflexes acting on th e forelimb musculature, earlier e x p e r i m e n t s suggest t h a t connections b e tw e e n l a b y r i n t h a n d forelimb m o t o n e u r o n s are less direct t h a n b e t w e e n l a b y r i n t h a n d neck, a n d t h a t no d i s y n a p t i c p a t h w a y is present (Wilson and Y o s h i d a 1969a, b). I n t h e present experiments, we h a v e rei n v e s t i g a t e d l a b y r i n t h i n e control of forelimb motoneurons. Our goals h a v e been to see how a n y p a t t e r n of s h o r t - l a t e n c y effects is r el at ed to t h e reflexes of balance t h a t h a v e been described (Magnus, 1926; l~oberts, 1967) an d how t h e t w o tracts originating in t h e v e s t i b u l a r nuclei are utilized in t h e p r o d u c t i o n of such effects. Some of t h e results h a v e been p r e s e n t e d in a p r e l i m i n a r y c o m m u n i c a t i o n (Maunz, Maeda a n d Wilson, 1974).

Methods Experiments were performed on 32 adult cats. Surgical procedures were completed under halothane (Fluothane, Ayerst Laboratories, Inc.) anesthesia. The common carotid arteries were ligated. Animals were then decerebrated at the intercollicular level, paralyzed with gallamine triethiodide (Flaxedil, American Cyanamid Co.) and respired artificially; bilateral pneumothorax was performed routinely to improve stability. End-tidal C02 was monitored with a Beckman medical gas analyzer and kept at physiological levels. Blood pressure was monitored from the femoral artery and, when necessary, maintained above 80 mm Hg by intravenous infusion of metaraminol bitartrate (Aramine, Merck) in normal saline, 80/lg/ml; the rectal temperature was kept at 36--38~ by radiant heat. Stimulating electrodes (fine Ag-AgC1 wires insulated except at the spherical tip) were implanted in the ipsi- and contralateral labyrinths to stimulate the peripheral branches of the vestibular nerve (Shimazu and Precht, 1965). At this location both ampullary and macular branches would be stimulated. The stimuli consisted of 0.1 msee rectangular pulses delivered at rates of 2--5/see. The intensity of stimulation for evoking vestibular field responses was usually less than 100/~A. Because the facial nerve runs near the vestibular nerve, the intensity for evoking twitch responses in the facial region caused by spread of stimulating current was checked in some experiments. This intensity wa~ u~ually 10 or more times the threshold for the vestibular N1 field response (10 X NIT). In some experiments animals were decerebrated precollicularly, to avoid damage to the oculomotor nucleus, and bipolar stimulating electrodes made of insulated 40-~ stainless steel wire were implanted near the ampuIlary nerves (Suzuki, Goto, Tokumasu and Cohen, 1969). Implantation was tested by observing the eharacteristic eye movements produced by stimulation of each ampullary nerve with trains of 25 rectangular pulses (Cohen, Suzuki and Bender, 1964). After testing, the decerebration was extended to the intercollicular level. In a few cases we tested, at the middle or the end of experiment, for stimulus spread between ampullary nerves by checking the summation of the N1 field potentials produced by stimulation of individual ampullary nerves (Wilson and Felpel, 1972). The C~--T 1 segments were exposed by dorsal laminectomy to permit intracellular recording from motoneurons. In addition, the spinal cord was transected at mid-thoracic levels. After occipital craniotomy, the medial part of the cerebellum was removed by aspiration to expose the floor of the fourth ventricle. Intracellular recording was done with glass mieropipettes filled with 1M potassium acetate; electrode resistance was usually 3--7 M~. Conventional circuits were used for recording and for passing current through the microelectrode. Motoneurons were identified by antidromic invasion or, occasionally, by the large EPSPs evoked by muscle nerve stimulation. Forelimb nerves prepared were those to the long (LON), lateral (LAT) and medial (MED) heads of triceps; to biceps (BIC); to supra- and infraspinatus (SI). In some experiments the medial longitudinal f~sciculus (MLF) was interrupted bilaterally by section at the caudal levels of the medulla. The cut was made by a fine blade positioned with a manipulator under visual observation. In other experiments a similar procedure was used to m~ke a cut laterally in the caudal medulla, in order to interrupt the LVST. A spinal hemisection was made at the upper cervical level in a few cases. The lesions were reconstructed histologically after each experiment. The brain stem or spinal cord was removed and placed

Labyrinthine Influence on Cat Forelimb Motoneurons

71

in 10% formaldehyde in Ringer solution. After fixation, 100-/l frozen serial sections were cut and stained for fibers and cells (Kliiver and Barrera, 1953). All experimental data were averaged on-line using a Digital Equipment Corporation PDP 11--45 computer. Usually 50 sweeps were averaged, and the result was plotted after preliminary smoothing. This smoothing was equivalent to a low pass filter with a corner frequency of 3.5 KHz. Measurements showed that it had no significant effect on the potentials that we studied. Results

Stimulation of the labyrinth evokes disynaptie potentials in neck motoneurons even under pentobarbital anesthesia (Wilson and Yoshida, 1969a, b). I n contrast, no synaptie potentials are observed in forelimb motoneurons under pentobarbital (Wilson and Yoshida, 1969a), and potentials are depressed by ehloralose. I n agreement with earlier work in which stimulation of the labyrinth evoked activity in forelimb nerves (e.g. Gernandt and Gilman, 1959), we routinely observed labyrinth-evoked activity in cervical motonenrons in decerebrate cats, especially in those with the medial cerebellum removed and the spinal cord transected in the mid-thoracic region (Batini, Moruzzi and Pompeiano, 1957). I n successful preparations there could be considerable variability. For example, after m a n y hours of recording, cyclic excitability changes, paralleled by resting potential changes in motoneurons, sometimes developed. I n such cases large synaptie potentials could be evoked at the peak of the resting potential, whereas there was almost no response during the trough. Even during periods of relatively stable excitability, the amplitude of responses in the same cell to successive stimuli often varied (Figs. 1, 3). Such variability is masked by the computer averaging t h a t was used routinely for better measurement of latency and other parameters of synaptic potentials, which were often rather small. Results were obtained from more t h a n 500 motoneurons. Although a few cells with low resting potential were accepted because synaptic potentials were clear, resting potentials were generally over 40 and very often over 50 inV.

Synaptic Potentials Evot:ed by Stimulation o[ the Whole Labyrinth Characteristics o] the Potentials Stimuli as strong as 5 - - 6 • N1T were generally used to evoke potentials in motoneurons. When the threshold of these potentials was measured, however, it was usually less t h a n 2 - - 3 • Such thresholds are similar to those for monosynaptic and polysynaptic activation of cells in Deiters' nucleus and the medial vestibular nucleus (Wilson, Kato, Peterson and Wylie, ]967; Wilson, Wylie and Marco, 1968). Extensor Motoneurons. Stimulation of the labyrinth with triple shocks typically caused depolarization, usually bilaterally, in extensor motoneurons (Figs. 1, 2). Sometimes temporal summation was required to evoke a depolarization, which appeared only after the second or third shock. I n m a n y other instances there was a short-latency response to each of the stimuli (Figs. 1 and 2B, D). Such shortlatency potentials varied widely in amplitude with the strength of stimulation (Fig. 1 D - - F ) ; responses to successive shocks in the train typically increased in size (Figs. 1 A - - C and 2B, D). This early part of the response could be followed by a later, larger depolarization (for example, arrow in Fig. 2A). Passing current

72

M. Maeda et al.

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Fig. 2. Synaptic potentials in extensor motoneurons. Computer-averaged potentials evoked in two LON cells. Stimulation of either labyrinth with triple shocks at 500/~A evoked an E P S P in the cell illustrated in A, B. In the second cell stimulation of the contrala~eral labyrinth at 125/IA evoked an E P S P (D). Stimulation of the ipsilateral labyrinth at 300 ~A evoked an I P S P followed by a depolarization (C). The early I P S P is shown at higher gain in the upper trace of C. Bottom traces in alI cases are juxtacellular field potentials t h r o u g h t h e r e c o r d i n g e l e c t r o d e o f t e n h a d l i t t l e or n o effect on t h e e a r l y d e p o l a r i zation. I n a n u m b e r of cases it was i n c r e a s e d b y h y p e r p o l a r i z a t i o n a n d d e c r e a s e d b y d e p o l a r i z a t i o n , a l t h o u g h effects in t h e o p p o s i t e d i r e c t i o n w e r e also o b s e r v e d .

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Fig. 3. Synaptic potentials in flexor motoneurons. A and B show computer-averaged IPSPs in a BIC motoneuron, recorded after section of the MLF. Triple shocks at 150/IA were delivered to the ipsilateral (A) and contralateral (B) labyrinths. In B the upper trace was recorded while passing a hyperpol~rizing current of 2.0 • l0 -s A through the recording electrode; the second trace shows the potential without current, the third during an 0.5 • 10-s A depolarizing current. C and D show potentials evoked in another BIC motoneuron by stimulation of the ipsi- and contralateral labyrinth respectively with a train of six shocks. Calibrations under D apply to C, D. Lower traces in all frames are juxtacellular field potentials

The m o s t likely e x p l a n a t i o n of these results is t h a t t h e response is p r e d o m i n a n t l y a n E P S P , b u t t h a t t h e synapses p r o d u c i n g it are l o c a t e d fairly d i s t a l l y on t h e m o t o n e u r o n s (Rall, Smith, Nelson a n d F r a n k , 1967). The p e a k a m p l i t u d e of t h e e a r l y E P S P p r o d u c e d b y a triple shock was u s u a l l y a few h u n d r e d m i c r o v o l t s ; in some cells it could be 1.5 m V or more, a n d it sometimes e v o k e d a spike. A l t h o u g h changes were seen in some cells, n e i t h e r a m p l i t u d e nor l a t e n c y were s y s t e m a t i c a l l y affected b y v a r i a t i o n in t h e s t i m u l u s r e p e t i t i o n r a t e b e t w e e n 1--10/see. A l t h o u g h an E P S P was t h e m o s t p r o m i n e n t e a r l y effect observed in extensor m o t o n e u r o n s , h y p e r p o l a r i z a t i o n was e v o k e d in some cells; i t was decreased b y h y p e r p o l a r i z a t i o n a n d increased b y depolarization, a n d was therefore a n I P S P (Eccles, 1964). I n some cells t h e response consisted of b o t h h y p e r - a n d depolarization, for e x a m p l e a n e a r l y I P S P followed b y a later, long-lasting d e p o l a r i z a t i o n (Fig. 2C). Flexor Motoneurons. I n c o n t r a s t to effects o b s e r v e d in e x t e n s o r cells, t h e m o s t c o m m o n p o t e n t i a l change evoked, bilaterally, in flexor m o t o n e u r o n s was an e a r l y h y p e r p o l a r i z a t i o n (Fig. 3) which b e h a v e d in response to m u l t i p l e shocks similarly

M. Maeda et al.

74

to the E P S P seen in extensor motoneurons. As in extensor cells, the hyperpolariza-

tion was increased b y depolarizing and decreased or reversed b y hyperpolarizing current (Fig. 3B). I t was therefore an I P S P , with the inhibitory synapses located relatively proximally on the motoneuron. I n some cells an E P S P , or a response consisting of a mixture of E P S P and I P S P , was observed instead of an I P S P (Fig. 3C, D).

Latency o/Synaptic Potentials E a r l y E P S P s evoked in ipsilateral and eontralateral extensor motoneurons had ]~teney ranging from 2.5 to just over 5 msee, b u t most lateneies were between 3 and 4 msee (Fig. 4 A, B). I n general there was overlap between lateneies observed in triceps and SI motoneurons, although the shortest values (2.5 msec, Fig. 4A) occurred in the latter, which are located more rostrally t h a n triceps cells (C 5 versus A

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Latency (msec) Fig. 4. Lateneies of synoptic potentiMs evoked in ~orelimb motoneurons. Only cells in which the first shock evoked a response are included and the histograms show the lateneies of the responses to this shock. Symbols: open circles, SI motoneurons; filled circles, LON and LAT; X's, BIC C~--Ti). Inspection of the histograms reveals a t e n d e n c y for contralateral lateneies to be shorter t h a n ipsilateral ones. This tendency was confirmed b y comparing lateneies of ipsi- and contralateral potentials recorded in the same cell : The eontralateral potential had a shorter latency in 24/37 of the eases. The lateney difference was usually 0.5 msec or less, indicating the p a t h w a y s contained the same n u m b e r of synapses. Monosynaptie firing of neurons in the lateral and medial vestibular nuclei m a y occur at 0.8--1.5 msee after stimulation of the labyrinth, with most of the firing early in this period (Wilson et al., 1967, 1968). Adding to these values as m u c h as 1.0 msec for conduction from the vestibular nuclei (Wilson and u I969a),

Labyrinthine Influence on Cat Forelimb Motoneurons hi

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Fig. 5. AnaIysis of the descending pathway. A1 Diagram of the experimental arrangement, described further in the ~ex~(VN, vestibub~r nuclei). A2 Shows the field potential recorded by an electrode in Deiters' nucleus (location confirmed histologically) when the labyrinth ~vas stimulated, A3 lq'ieJd potential recorded at ~he same location in response ~o stimulation at C~. Threshoid of this potential w~s near 2.2 V. :B :EPSP evoked by stimulation ot the Ja,byri~f~ba~ 250/xA. C EPSP evoked by stimulation at C2; ~hresho~do~ th~s~PSP was similar ~o ~ha~of the antidromic field potential. D E Show EPSPs evokecl by stimulation at C 2 with si~gle and double 2.6 V shocks. Potentials i~ B--E computer ~veraged. Lower ~race in all frames is f,he~ juxtacellular field

and 0.5 msec for synaptic delay, gives an expected latency range of 2.3--~.0 msee for a disynaptio p a t h w a y between the lab3~rinth and/bre]imb motoneurons i.n the caudal part of the enlargement, with most of the late~eies in the early part of the range. Clearly then, most E P S P s were evoked b y a pathway containing at least three s3mapses. The properties of EPSPs evoked by stimulating tJoe descending axons at cervical levels suggest that two of the syna,pscs are at the spinal cord level, ~/gure 5 illustrates an experiment in which sy~aptic potentials were evoked by stimulation of the labyrinth and of descending axons at cervical levels. Stimulating electrodes were inserted into the spin~l cord at 0.2, in the vicinity of the LVST, on the side contralateral to the motoneuron (as udll be sJ~own below, the eontrala~era] L V S T is ~be pathway relaying impulses from the contralateral ~aby. rinth): stimulation with t,he spinal electrodes evoked an antidromic field pot, ential in Deiters' nucleus (Fig. 5 A3}, When the contralateral labyrinth was stimulated, an ~ P S P with a latency of 3.2 msec was evoked in the moVoneuron (l~ig. 5B). StimnIation of the LVST evoked a larger E P S P with a latency of 1.6 msee (Fig. 5C~ of ~,'hfch no more than 0.4--0.5 msee is taken up by conduction over the distance of 40 mm between the stimulating electrode and the level of the moteneuron ; the remaining time allows for activation of an intern~uron and an a.ddi~ional synaptic delay. We interpret the first p~sitive peak, 0.5 msec after the stimu. lus, in Fig'. 5C (first arrow) as indicating the arrival of descending volleys at the segmental level, and the second peak, 0.8 msec later (second arrow), as indicating ~he arrival oE interneuron impulses near the motoneuron. Further evidence that

76

M. Maeda et al.

the pathway is disynaptic at the spinal level is shown in Fig. 5 D, E : the response to the second of two submaximal shocks is considerably larger t h a n the response to the first. Such behavior is usually associated with polysynaptic rather than with monosynaptic systems. There is no evidence that an alternate explanation, potentiation of a monosynaptic response, applies to the vestibulospinal system (for example, Fig. 8 in Grillner, Hongo and Lund, 1970). I P S P s evoked in extensor motoneurons had a latency comparable to t h a t of E P S P s (Fig. 4E) and were apparently produced by a pathway no more complex. On the other hand, I P S P s in flexor motoneurons, both ipsi- and eontralateral, had latencies t h a t were often somewhat longer, even though biceps motoneurons are located more rostrally than triceps cells (Fig. 4C, D). I t seems likely t h a t m a n y of these I P S P s are produced via at least four synapses, particularly since slowlyconducting inhibitory fibers in the MLF are not involved in the pathway (see below). Pattern o / S y n a p t i c Potentials We have recorded mostly from motoneurons innervating shoulder and elbow muscles. Shoulder motoneurons were those to supra- and infraspinatus. The former acts to extend the humerus and the latter to rotate it outwards (Reighard and Jennings, 1935). We have stimulated the two nerves together and grouped the motoneurons into one category (SI). Table 1 shows that stimulation of the labyrinth causes excitation bilaterally in a high percentage of SI motoneurons. Motoneurons studied that innervated elbow muscles were those of triceps and biceps. Although the three heads of triceps (LON, LAT, MED) are often considered together as extensors of the elbow (Reighard and Jennings, 1935) the LON head, a double joint, muscle, is excited during the flexion reflex and m a y be considered a shoulder flexor (Sherrington, 1910). Furthermore, although stimulation of the LON nerve evokes sizeable heteronymous monosynaptic EPSPs in other triceps motoneurons, the reverse does not hold (Eccles, Eccles and Lundberg, 1957). Despite these differences, there is a great similarity between the pattern of potentials seen in the various triceps motoneurons. Excitation is the predominant effect, bilaterally, in both LON and LAT motoneurons (Table 1) and in the 5 MED motoneurons studied. Inhibition and mixtures of excitation and inhibition are also seen

Table 1. Distribution of early synaptic potentials SI Ipsi EPSP

Contra

Ipsi

LON Contra

Ipsi

LAT Contr~

BIC Ipsi

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42/53 35/43 95/142 128/137 3 8 / 5 4 29/43 6/71 5/71 (79) (81) (67) (93) (70) (67) (8) (7) IPSP 0/53 0/43 17/142 1/137 3/54 0/43 44/71 50/71 (0) (0) (12) (1) (6) (0) (62) (70) Mixed 1/53 0/43 19/142 2/137 2/54 0/43 9/71. 7/71 (2) (0) (13) (1) (4) (0) (13) (10) No Effect 1 0 / 5 3 8/43 11/142 6/137 11/54 14/43 12/71 9/71 (19) (19) (8) (4) (20) (33) (17) (13) The denominator shows the total number of cells tested, the numerator the number of times a particular response type was seen. The percentage of occurrence of each response type is in brackets.

Labyrinthine Influence on Cat Forelimb Motoneurons

77

in triceps motoneurons, but almost entirely ipsilaterally and more so in L 0 N than in LAT cells. Inhibition occurs in LON cells only a little more ti'equently than in LAT cells, and it is not clear that the difference is due to any functional difference between the two heads of the muscle. I t is possible, however, that our results are not an accurate reflection of I P S P occurrence, because we did not routinely pass depolarizing current through all motoneurons. Inhibition is seen bilaterally in more than half of elbow flexor (BIC) motoneurons, with excitation or mixed effects in a number of cells (Table 1). In addition to these results EPSPs, and some ipsilateral IPSPs, were also observed in a group of motoneurons with their axons in the dorsal interosseus nerve to wrist and digit muscles. Taken together the results show that although stimulation of the labyrinth often excites extensor and inhibits flexor motoneurons there must be, particularly for the two BIC and the ipsilateral LAT and LON nuclei, alternate excitatory and inhibitory pathways linking the vestibular nuclei to motoneurons. Which pathway is activated when the labyrinth is stimulated electrically could depend on a number of variables, including the afferents that are stimulated and the bias of segmental interneurons. Although stimulation of the labyrinth frequently evokes excitation bilaterally in elbow extensor and shoulder motoneurons, there are usually differences between the effects evoked by ipsilateral and eontralateral stimulation. I n cells that responded with an E P S P to both ipsi- and contralateral stimuli the eontralateral stimulus was more likely to evoke a response with the first shock of a short train. When stimuli of comparable intensity (in terms of vestibular N1 threshold) were used, the time to peak for responses to single shocks or the first shock of a train was usually shorter for contralateral EPSPs than for ipsilateral EPSPs (for example, Fig. 2A, B). Medians for time to peak of eontralateral and ipsilateral EPSPs are 1.1 and 1.9 msee for LAT, 1.3 and 2.0 for LON, and 1.0 and 1.5 msee for SI. All differences are highly significant (p < .01, Mann-Whitney U test). I n a polysynaptie pathway the difference in rise time could be due to different locations of synapses on the motoneurons (gall et al., 1967) or to differences in the synehrony of firing of interneurons in the pathway. In addition, the EPSPs evoked by single shocks, or by the first of three shocks, were larger with eontralateral than with ipsilateral stimulation. For example, the medians of the responses to eontralateral and ipsilateral stimuli are 268 and 210/~V for LAT, 240 and 200 for LON, and 195 and 124 for SI, although the difference is significant only for SI (p < .01, Mann-Whitney U test). The differences in latency, shape and amplitude between the ipsilateral and eontralateral responses suggest a difference between the excitatory pathways and show that the eontralateral one exerts a stronger influence on motoneurons.

Synaptic Potentials Evoked by Stimulation o/ Ampullary Nerves Stimulation of individual ampullary nerves evoked responses in a large proportion of the motoneurons in which this was tested. Of cells tested with both ampullary nerve and whole nerve stimulation on the same side, and in which the whole nerve stimulation evoked a response, ampullary nerve stimulation evoked a response in 31/42 motoneurons eontralaterally and 9/9 motoneurons ipsilaterally. Synaptic potential thresholds were generally equal to, or less than, 2--3 • threshold,

78

M. Maeda et al. ANTERIOR

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Table 2. Early and late synaptic potentials evoked b y ampullary stimulation Anterior EPSP IPSP

Horizontal EPSP IPSP

Posterior EPSP IPSP

16 (10) 22 (22)

I0 (3) 27 (27)

16 (2) 17 (17)

5 (2) 5 (5)

2 (0) 5 (5)

4 (0) 5 (5)

7 (7) 12 (12)

4 (4) 12 (12)

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BIC . . . . . . . . . . Ipsilateral LON . . . . . . . . . . LAT . . . . . . . . . . BIC . . . . . . . . . .

not tested

3 (2)

5 (2)

4 (2)

4 (3)

6 (5)

4 (3)

7 (1) s (3)

7 (0) s (3)

not tested 3 (1) 3 (2)

6 (0) 7 (2)

3 (0) 3 (3)

not tested 4 (1) 4 (3)

a (0) 3 (2)

This table compares the responses obtained b y stimulating canals to the responses evoked b y stimulation of the whole vestibular nerve in a selected sample of cells. The denominator of each fraction represents the n u m b e r of responses of a particular type (EPSP, IPSP) obtained with whole nerve stimulation. The numerator gives the n u m b e r of these cells responding to ampullary nerve stimulation. The n u m b e r in brackets indicate how m a n y of the responses were early responses. I t was not possible to test all 3 ampullary nerves for every motoneuron. Lack of an entry means t h a t no response of t h a t type was observed in this sample, although it was looked for.

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The polarity of the potentials evoked by ampullary nerve stimulation was the same as that of the potentials produced by stimulation of the whole nerve: in the cells sampled, stimulation of the anterior, horizontal or posterior canal nerves evoked EPSPs in extensor motoneurons and I P S P s in flexor motoneurons, both ipsi- and contralaterally (Fig. 6 and Table 2). The shape and latency of the response to ampullary nerve stimulation were not necessarily the same as those of the typical response to whole nerve stimulation. Sometimes the E P S P evoked by ampullary nerve stimulation had the same latency and shape as the typical response to stimulation of the whole nerve (Fig. 6A); this was often the ease with the eontralateral anterior canal (Table 2). Often, and particularly with the horizontal and posterior canals, the response occurred later and was slowly rising, and there was no early response (t~'ig. 6 and Table 2). This could be so even in cells in which anterior canal stimulation evoked a typical early response (Fig. 6A). Even though the response to stimulation of individual canal nerves was variable and was absent in some cells, this m a y be due only to the strength of the drive on the interneuron(s) in the pathway. I n any case it is clear that activity in canal afferents contributes to the production of the responses seen when the whole nerve is stimulated.

E~ects o/Lesions oz~ Synaptic Potentials I n several experiments attempts were made to identify the pathways involved in the production of labyrinth-evoked potentials by making lesions in spinal cord or brainstem. We began by looking for the level at which the contralateral p a t h w a y crosses and then assessed the contribution of the MVST and LVST to the responses.

Hemiseetion o/the Spinal Cord I n two experiments the spinal cord was transected on the right side at the C~ level (Fig. 7). Before hemisection, stimulation of either the right or left labyrinth evoked the usual short-latency EPSPs in a number of SI and triceps motoneurons. Typical results after section arc illustrated in Fig. 7. No early EPSPs were seen in 11 triceps cells contralateral to the hemisection (Lt-LON, Fig. 7), or in 4 cells ipsilateral to it (Rt-LON), when the right labyrinth was stimulated. On the other hand, stimulation of the left labyrinth continued to produce typical potentials in

U'LOb

Lt-LON

Rt-LOb

Rt-LON

Lt"Lob

",

,I

'~

~

~' '~'~o~ ' '-

" ~ RI-LOb U'LON Rt-LON

Fig. 7. Effect of spinal cord hemisection. On the left, a diagram of the experimental arrangement and lesion. On the right, computer-averaged synaptie potentials evoked, after hemiseetion, in a left and a right LON cell by triple shocks to the left and right labyrinths. All stimuli 5oo ~A

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motoneurons on the left and right sides. We conclude t h a t the excitatory p a t h w a y to contralateral motoneurons travels down on the side of the spinal cord ipsilateral to the stimulated labyrinth before crossing to influence contralateral motoneurons. Similar observations were made in one experiment on contralateral inhibition of BIC motoneurons, indicating t h a t the inhibitory p a t h w a y also crosses in the spinal cord. Transection o[ the M L F

The M L F was cut bilaterally in the lower medulla in four experiments, with results such as those illustrated in Fig. 8A. After transection typical short-latency E P S P s were observed in 12/12 L O N and L A T motoneurons ipsi- and contralateral to the stimulated labyrinth. Similarly, short-latency I P S P s were present in 11/14 B I C motoneurons ipsilateral, and 16/16 contralateral to the stimulated labyrinth. Therefore, neither slowly conducting inhibitory fibers (Wilson and Yoshida, 1969 b; Akaike, Fanardjian, I t o and 0hno, 1973) nor rapidly conducting excitatory fibers (Akaike et al., 1973 ; Wilson and Maeda, 1974) in the MVST play a significant role in relaying labyrinthine activity to forelimb motoneurons. Lateral Cuts in the Medulla

A lateral cut in the medulla, near the caudal end of the inferior olive, was made in four experiments. I n each case the most medial edge of the lesion either was next to, or impinged on, the ventrolateral tip of the olive (Fig. 8B). I n this area

LI- I.AT

L~-BIC

L

U-LON

i

i , ~ mser

i

I

RI-LON

Imm

Fig. 8. Effect of brain stem lesions. A Interruption of the MLF as illustrated in the drawing. After transection typical EPSPs were still evoked in a LAT motoneuron by stimulating the ipsilateral (400 ZA) and eontralateral (300 ]IA) labyrinths. Typical IPSPs were also evoked in a BIC motoneurons by stimulating the two labyrinths at 150 BA; this motoneuron was studied in a different experiment. B Lateral cut in the caudal brain stem, as illustrated. Results obtained in two LON cells after lesioning are shown. While recording in the left LON cell the left and right labyrinths were stimulated at 250/~A. While recording in the right LON cell the left labyrinth was stimulated at 200 zA, the right at 300/~A. Abbreviations: IO inferior olive, M L F medial longitudinal fascieulus, h r XI1 hypogloss~l nerve, P T pyramidal tract

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the LVST is somewhat dorsolateral to the ventrolateral tip of the olive (lgeinosoSuarez, 1961) and it is therefore likely t h a t the lesion would interrupt, or at least severely damage, the tract. Lesions such as this m a y also interrupt some retieulospinal fibers, but most fibers originating in N. pontis eaudalis or N. giganto-cellularis lie dorsal to the olive and medial to the lesions (Petras, 1967) and should therefore have been spared. The effects of lateral cuts, illustrated in Fig. 8B, are clearest for contralateral synaptie potentials. I n these experiments stimulation of the labyrinth before the lesions were made evoked short latency EPSPs contralaterally in 19/19 LON and 1/1 LAT motoneurons, and early I P S P s eontralaterally in 18/22 BIC cells. After lateral medullary section on the same side as the stimulated labyrinth, the occurrence of potentials in contralateral motoneurons was sharply reduced : there were EPSPs in 6/26 LON cells, I P S P s in 4/17 BIC cells. I n cells without early synaptic potentials small, very late, potentials sometimes remained. Stimulation of the labyrinth on the side contralateral to the cut continued to evoke typical potentials in these motoneurons. As also shown in Fig. 8 B, stimulation of the labyrinth on the side of the lesion usually evoked no early potentials in motoneurons ipsilateral to the cut. The variable ipsilateral results obtained in some of these animals before the lesion make this finding hard to interpret.

Section o] the Cochlear Nerve Even though synaptie potentials were evoked in motoneurons at very low multiples of N I T , the stimulus strengths routinely employed for whole nerve stimulation could result in stimulus spread to the cochlear nerve. Although the latency and other characteristics of the early potentials are not consistent with the observations made by others on the properties of spinal activity evoked by stimulation of auditory pathways (Gernandt and Ades, 1964), a p a t h w a y from cochlear nuclei to motoneurons through the reticular formation is conceivable. Therefore, in one experiment the cochlear nerve was cut on one side in the internal auditory meatus. This cut had no effect on either ipsi- or contralateral potentials. Discussion

Pathways Linking the Labyrinth to Forelimb Motoneurons When the labyrinth is stimulated in decerebrate cats, early synaptie potentials are produced in forelimb motoneurons with a latency t h a t suggests the pathway is usually at least trisynaptie. This interpretation is consistent with the dependence of these potentials on the type of preparation used and with the fact t h a t pentobarbital anesthesia appears to abolish labyrinth-evoked potentials in forelimb motoneurons, although the disynaptic potentials in neck motoneurons remain (Wilson and u 1969a, b). I t is also consistent with the lack of monosynaptic connections between LVST or MVST fibers and forelimb motoneurons (Wilson and Yoshida, 1969a, b). This latter observation a n d the results obtained when the spinal cord is stimulated (Fig. 5A) suggest t h a t the interneuron in the pathway is in the spinal cord. Despite all the evidence pointing to trisynaptie linkage between the labyrinth and forelimb motonenrons, we cannot rule out the possibility t h a t some of the earliest EPSPs are produced b y a disynaptie pathway. Even if this 6

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is the case, such a pathway is rare and can play only a negligible role in relaying labyrinthine activity to forelimb motoneurons. The descending limb of the labyrinth-forelimb pathway could include the LVST and MVST. An important role for the MVST (and therefore for the medial and descending nuclei, see Wilson, 1972) in producing excitation or inhibition of ipsi- and contralateral forelimb motoneurons is ruled out by the lack of effect of MLF cuts on potentials evoked by stimulation of the labyrinth (Fig. 8A). This result emphasizes the importance of the LVST, and the role of this tract in the production of contralateral EPSPs in extensors and I P S P s in flexors is confirmed b y the effect of cuts made laterally in the medulla (Fig. 8B). I t is a reasonable assumption that the LVST is important in the production of ipsilateral potentials as well. The simplest ipsilateral route to extensors probably has the components: labyrinth - - Deiters' nucleus and LVST - - spinal interneuron (excitatory er inhibitory) - - motoneuron. The inhibitory pathway leading to flexor motoneurons is often longer, and in those instances it m a y contain both an excitatory and an inhibitory interneuron. The shortest pathways activated by stimulation of the contralateral labyrinth are also trisynaptie and must include the contralateral Deiters' nucleus and LVST, as is the case with hindlimb motoneurons (Aoyama, tIongo, Kudo and Tanaka, 1971). Although study of the influence of Deiters' nucleus on hindlimb motoneurons has shown interaction, due to convergence on interneurons, between the ipsi- and contralateral pathways, no interneurons are driven monosynaptically by the two LVSTs (Aoyama et al., 1971). The differences observed between ipsi- and contralatera] effects in forelimb motoneurons suggest t h a t the same holds true for connections at t h a t level. Apparently, contralateral LVST axons make synapses with commissural interneurons, known to be present in the general area of termination of the LVST (Sterling and Kuypers, 1968); these in turn must make synapses with motoneurons. While the evidence suggests t h a t the LVST is the main pathway involved in relaying labyrinthine early activity to forelimb motoneurons, a role for reticulospinal fibers cannot be completely ruled out even though the lateral medullary cuts should have spared most retieulospina] fibers. Many reticulospinal neurons excite forelimb motoneurons monosynaptically (Wilson and Yoshida, 1969a} and some are excited disynaptically or later by stimulation of the labyrinth (Peterson and Felpel, 1971). The reticulospinal system could also play a role in evoking the later responses seen after interruption of the LVST.

Labyrinthine Control o] Motoneurons There is obvious contrast between labyrinthine connections with axiM motoneurons on the one hand and forelimb motoneurons on the other. The difference is particularly striking for connections between semicircular canals and neck motoneurons. Not only are there precise functionally meaningful connections between canals and neck motoneurons, but the pathway in all cases is disynaptic (Wilson and Maeda, 1974). I n contrast, canal projections to forelimb motoneurons are weak, do not show a functionally meaningful pattern, and are at least trisynaptic. More generally, while there are extensive disynaptic connections between the labyrinth and neck and back motoneurons (Wilson and Yoshida, 1969 a, b; Wilson, Yoshida and Schor, 1970), all connections between the labyrinth and cat

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83

forelimb motoneurons are at least trisynaptic. I t can be suggested t h a t the same holds true for connections between labyrinth and hindlimb motoneurons, even though LVST axons make monosynaptie contact with some of these (Lund and Pompeiano, 1968; Wilson and u 1969a; Grillner et al., 1970): Wilson and Yoshida (1969 a) saw no potentials in hindlimb motoneurons when they stimulated the labyrinth in cats under pentobarbital anesthesia, evidence of a lack of disynaptie connections. Instead, it seems that in the cat the labyrinth acts on limb motoneurons only through the di- or polysynaptic pathways originating in Deiters' nucleus t h a t have been extensively studied (Wilson and Yoshida, 1969a; Grillncr et al., 1970; Aoyama et al., 1971 ; ten :Bruggencate and Lundberg, 1974). Comparative studies show variation in the connections between labyrinth and limb motoneurons in different vertebrates. For example, in the frog there is a disynaptic p a t h w a y between the labyrinth and hindlimb motoneurons (Magherini, Precht and Richter, 1974). We suggest t h a t these differences reflect mainly the greater complexity of postural and locomotor control in the higher animals, and the need to integrate labyrinthine with other reflexes, such as neck reflexes. The disynaptic pathway by which it acts emphasizes the importance of the labyrinthine input to neck motoneurons. Labyrinthine reflexes acting on the neck can be modulated only at the level of the vestibular nuclei, where the synapse between afferents and second-order neurons is a strong one (Wilson et al., 1967, 1968), or non-specifically at motoneurons. On the other hand, labyrinthine reflexes acting on the forelimbs, and probably hindlimbs, can be enhanced or suppressed by control of the interneurons interposed in the pathway. I n other words, in the eat the labyrinthine reflexes of the limbs are less obligatory, and more modifiable by peripheral or central inputs, than the reflexes of the neck. Functional Considerations The pattern of activity observed in forelimb motoneurons when the labyrinth is stimulated electrically consists principally of bilateral excitation of extensor and inhibition of flexor motoneurons, just as described by Hongo, Kudo and Tanaka (1971) for hindlimb motoneurons. Opposite effects are seen frequently enough, however, to suggest that there are both excitatory and inhibitory pathways to some motor nuclei. The question arises, to what receptors in the labyrinth are these pathways related ? Stimulation of individual semicircular canal nerves m a y evoke synaptic potentials in motoneurons, but, comparison of these potentials with those obtained when the labyrinth as a whole is stimulated suggests t h a t an important contribution to the latter potentials, particularly to the early component, results from stimulation of utricular, and perhaps saccular, afferents. I t is of interest to t r y to relate our results to the reflex movements seen by others as a result of electrical, mechanical, or natural stimulation of different labyrinthine receptors. Suzuki and Cohen (1964) stimulated individual ampullary nerves in alert, unrestrained, cats and obtained ipsilateral forelimb extension and contralateral flexion whichever nerve was stimulated (however, stimulation of both anterior canals caused bilateral extension whereas stimulation of both posterior canals caused bilateral flexion). Generally similar results were obtained earlier by Szents gothai (1952) who, however, saw little reflex response in limb muscles unless 6*

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several canals were stimulated together. Our results are in agreement with these findings only in showing t h a t activation of ampullary nerves m a y influence forelimb motoneurons and that potentials of the same polarity are produced by stimulation of the three canals on one side. On the other hand, the bilateral depolarization of extensor and hyperpolarization of flexor motoneurons that we saw is not consistent with the movements seen by Suzuki and Cohen (1964) and by Szent&gothai (1952). I n response to stimulation of individual ampullary nerves, early potentials were frequently small or absent. This suggests t h a t shol%-latency canal influence on limb motoneurons is not powerful. Perhaps long-lasting stimulation of canal afferents activates more complex pathways, and this in turn m a y lead to movements such as have been described. There has been some disagreement about the positional labyrinthine reflexes that arise in the utricle, de Kleijn and Magnus (1921) deduced from extirpation of one labyrinth that the utricular macula could influence the limbs on both sides of the body, but believed that all limbs were always affected in the same way. More recently it has been shown t h a t during lateral tilt the forelimbs are affected reciprocally, with increased activity in the extensors on the side tilted down and decreased activity eontralaterally (Roberts, 1970; Berthoz and Anderson, 1971; gosenberg and Lindsay, 1973). During forward-backward tilt the forelimbs are affected symmetrically, with bilateral extension in the head down and bilaterM flexion in the head up position (Roberts, i970). The hair cells on different parts of the utricular macula are polarized in different directions (Flock, 1964; Lindeman, 1969), and by postulating particular connections between utricular afferents and the excitatory and inhibitory pathways we have observed it is possible to account for the various positional reflexes described by Roberts and his colleagues (I{oberts, 1967, 1970; Rosenberg and Lindsay, 1973). For example, assume t h a t a utricular afferents and Deiters' neurons, t h a t are excited by side down tilt (Duensing and Schaefer, 1959; Peterson, 1970), cause excitation of ipsilateral extensor and inhibition of ipsilateral flexor motoneurons. Assume further that fl afferents and Deiters' neurons, excited by side up tilt, excite contralateral extensor and inhibit contralateral flexor motoneurons. A similar circuit could be devised t h a t includes type 1 and type 2 afferents, inhibited and facilitated respectively by head down tilt (Duensing and Schaefer, 1959; Peterson, 1970). Such a pattern of connections would not be revealed by electrical stimulation of the vestibular nerve, which to some degree would excite simultaneously all types of afferents, but it is consistent with our results and could produce the changes in forelimb muscles t h a t are the result of tilt. References

Akaike, T., Fanardiian, V.V., :[to, M., Ohno, T. : Eleetrophysiological analysis of the vestibulospinal reflex pathway of rabbit. IL Synaptie actions upon spinal neurons. Exp. Brain l~es. 17, 497--515 (1973) Aoyama, M., tIongo, T., K_udo, N., Tanaka, t~.: Convergent effects lrom bilateral vestibulospinal tracts on spinal interneurons. Brain Res. 35, 250--253 (1971) Batini, C., Moruzzi, G., Pompeiano, 0. : Cerebellar release phenomena. Arch. ital. Biol. 95, 71--95 (1957) Berthoz, A., Anderson, J. H. : Frequency analysis of vestibular influence on extensor motoneurons. I. l~esponse to tilt in forelimb extensors. Brain Res. 34, 370--375 (1971)

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Bruggencate, G. ten, Lundberg, A. : Facilitatory interaction in transmission to motoneurones from vestibulosloinal fibres and contralateral primary afferents. Exp. Brain Res. 19, 248-270 (1974) Cohen, B., Suzuki, J.-I., Bender, M. B. : Eye movements from semicircular canal nerve stimulation in the cat. Ann. Otol. (St. Louis) 73, 153--169 (1964) Duensing, F., Schaefer, K.P. : Uber die Konvergenz verschiedener labyrinth~rer Afferenzen auf einzelne Neurone des Vestibulariskerngebietes. Arch. Psychiat. Nervenkr. 199, 345-371 (1959) Eccles, J.C.: The Physiology of Synapses. Berlin-GSttingen-Heidelberg-New York: Springer 1964 Eccles, J.C., Eccles, R.M., Lundberg, A. : The convergence of monosynaptic excitatory afterents on to many different species of alpha motoneurones. J. Physiol. (Lond.) 137, 22--50 (1957) Flock, A. : Structure of the macula utriculi with special reference to directional interplay of sensory responses as revealed by morphological polarization. J. Cell Biol. 22,413--431 (1964) Gernandt, B.E., Ades, H.W.: Spinal motor responses to acoustic stimulation. Exp. Neurol. 10, 52--66 (1964) Gernandt, B.E., Gilman, S. : Descending vestibular activity and its modulation by proprioceptive, cerebellar and reticular influences. Exp. Neurol. 1,274--304 (1959) Grillner, S., Hongo, T., Land, S. : The vestibulospinal tract. Effects on alpha motoneurons in the lumbosacral spinal cord in the cat. Exp. Brain Res. 10, 94--120 (1970) Hongo, T., Kudo, N., Tanaka, R. : Effects from the vestibulospinal tract on the contralateral hindlimb nmtoneurones in the cat. Brain Res. 31, 220--223 (1971) de Kleijn, A., Magnus, R. : l~ber die Funktion der Otolithen. I. Mitteilung. Otolithenstand bei den tonischen Labyrinthreflexen. Pttiigers Arch. ges. Physiol. 186, 6--38 (1921) Kliiver, tt., Barrera, E. : A method for the combined staining of ceils and fibers in the nervous system. J. Neuropath. exp. Neurol. 12, 400~403 (1953) Lindeman, I-I. H. : Studies on the morphology of the sensory regions of the vestibular apparatus. Ergebn. Anat. 42, 7--110 (1969) Lund, S., Pompeiano, O. : Monosynaptic excitation of alpha motoneurones from supraspinal structures in the eat. Acta physiol, seand. 73, 1--21 (1968) Magherini, P.C., Precht, W., Richter, A. : Vestibulospinal effects on hindlimb motoneurons of the frog. Pfliigers Arch. 348, 211--223 (1974) Magnus, R.: Some results of studies in the physiology of posture. Lancet 211, 531--536, 585--588 (I926) Maunz, R.A., Maeda, M., Wilson, V.J.: Labyrinthine control of cat forelimb motoneurons. 4th Ann. Meeting Soc. Neurosci. 328 (1974) Peterson, 13. W. : Distribution of neural responses to tilting within vestibular nuclei of the cat. J. Neurophysiol. 33, 750--767 (1970) Peterson, B. W., Felpel, L. P. : Excitation and inhibition of retieulospinal neurons by vestibular, cortical and cutaneous stimulation. Brain Res. 27, 373--376 (1971) Petras, J.M. : Cortical, tectal and tegmental fiber connections in the spinal cord of the cat. Brain Res. 6, 275--324 (1967) Rall, W., Burke, R.E., Smith, T.G., Nelson, P.G., Frank, K. : Dendritic location of synapses and possible mechanisms for the monosynaptic E P S P in motoneurons. J. Neurophysiol. 30, 1169-1193 (1967) Reighard, J., Jennings, H.S. : Anatomy of the eat (3d ed.). New York: Holt 1935 Reinoso-Suarez, F.: Topographischer Hirnatlas der Katze. Darmstadt: Merck 1961 Roberts, T.D.M. : Neurophysiology of Postural Mechanisms. London: Butterworths 1967 Roberts, T. D. M. : Changes in stretch reflexes in limb extensor muscles during position reflexes from the labyrinth in the cat. J. Physiol. (Lond.) 211, 45P (1970) Rosenberg, J.l~., Lindsay, K . W . : Asymmetric tonic labyrinthine reflexes. Brain Res. 63, 347--350 (1973) Shcrrington, C.S.: Flexion-reflex of the limb, crossed extension-reflex, and reflex stepping and standing. J. Physiol. (Lond.) 40, 28--121 (1910) 7 Exp. Brain Res. Vol. 22

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Shimazu, It., Precht, W. : Tonic and kinetic responses of cat's vestibular neurons to horizontal angular acceleration. J. Neurophysiol. 28, 991--1013 (1965) Sterling, P., Kuypers, H. G.J.M. : Anatomical organization of the brachial spinal cord of the cat. III. The propriospinal connections. Brain l~es. 7, 419--443 (1968) Suzuki, J.-I., Cohen, B. : Head, eye, body and limb movements from semicircular canal nerves. Exp. 5[eurol. 10, 393--405 (1964) Suzuki, J.-I., Goto, K., Tokumasu, K., Cohen, B. : Implantation of electrodes near individual vestibular nerve branches in mammals. Ann. Otol. (St. Louis) 78, 815--826 (1969) Szentg~gothai, J. : Die Rolle der Einzelnen Labyrinthrezeptorcn bei dcr Orientation yon Augen und Kopf im Raume. Budapest: Akademiai Kiado 1952 Wilson, V.J. : Physiological pathways through the vestibular nuclei. Int. Rev. ~eurobiol. 15, 27--81 (1972) Wilson, V.J., Felpcl, L.P.: Specificity of semicircular canal input to neurons in the pigeon vestibular nuclei. J. Neurophysiol. 85, 253--264 (1972) Wilson, V.J., Kato, M., Peterson, B.W., Wylie, R.M. : A single-unit analysis of the organization of Deiters' nucleus. J. Neurophysiol. 80, 603--619 (1967) Wilson, V.J., Maeda, M.: Connections between semicircular canals and neck motoneurons in the cat. J. Neurophysiol. 37, 346--357 (1974) Wilson, V.J., Wylie, R.M., Marco, L.A.: Synaptic inputs to cells in the medial vestibular nucleus. J. Neurophysiol. al, 176--186 (1968) Wilson, V.J., Yoshida, M. : Comparison of effects of stimulation of Deiters' nucleus and medial longitudinal fasciculus on neck, forelimb, and hindlimb motoneurons. J. Neurophysiol. a2, 743--758 (1969a) Wilson, V.J., Yoshida, M. : Monosynaptic inhibition of neck motoneurons by the medial vestibular nucleus. Exp. Brain Res. 9, 365--380 (1969b) Wilson, V.J., Yoshida, M., Schor, 1~.H. : Supraspinal monosynaptic excitation and inhibition of thoracic back motoneurons. Exp. Brain Rcs. 11, 282--295 (1970) Dr. V.J. Wilson The Rockefeller University New York, N.Y. 10021 USA