Changes in discharge rate of cat hamstring fusimotor neurones during fatiguing contractions of triceps surae muscles

Changes in discharge rate of cat hamstring fusimotor neurones during fatiguing contractions of triceps surae muscles

246 Brain Research, 579 (1992) 246-252 © 1992 Elsevier Science Publishers B.V. All rights reserved. 0006-8993/92/$05.00 BRES 17687 Changes in disch...

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Brain Research, 579 (1992) 246-252 © 1992 Elsevier Science Publishers B.V. All rights reserved. 0006-8993/92/$05.00

BRES 17687

Changes in discharge rate of cat hamstring fusimotor neurones during fatiguing contractions of triceps surae muscles Milog Ljubisavljevi6, Ksenija Jovanovi6 and Radmila Anastasijevi6 Institute for Medical Research, 11001 Beograd, Dr Subotida 4 (Yugoslavia) (Accepted 17 December 1991) Key words: Fusimotor neuron; Muscle fatigue; Small diameter muscle afferent; Heteronymous fusimotor reflex

Changes in the discharge rate of fusimotor neurones to hamstring muscles during long-lasting, fatiguing, contractions of the triceps surae muscles were studied in decerebrate cats. Discharges of fusimotor neurones were recorded from the nerve filaments. Muscle contractions were elicited by electrical stimulation of the muscle nerves applied until the muscle tension fell to about 30% of its initial value. Early and late changes could be recognized in fusimotor discharge rate. The early changes, at the onset of muscle contraction, occurred in 9 out of 22 neurones and varied in both sign and duration among the cells. The late change, encountered in 16 fusimotor neurones, was an increase in discharge rate developing towards the end of the muscle contraction and outlasting it. When the contracting triceps muscle was made ischaemic the late increase in discharge rate developed earlier, as did the muscle tension fall and started to subside after the arterial clamp was removed. After severing the muscle nerves their stimulation provoked either no changes or a slight sustained decrease in fusimotor discharge rate. It is supposed that the late increase in discharge rate of fusimotor neurones to hamstring muscles appears due to reflex excitation by discharges in group III and IV afferent fibres from the triceps muscle provoked and/or enhanced by metabolic products liberated during its fatiguing contraction. The possibility is raised that the excitation is elicited primarily by the discharges from chemosensitive afferent fibres. Its functional role in muscle fatigue is discussed. INTRODUCTION It has been shown that chemically induced discharges in small diameter muscle afferents provoke autogenetic reflex excitation of fusimotor neurones 17. Evidence was provided indicating that the increase in the discharge rate of fusimotor neurones to triceps surae muscles developing towards the end of a long-lasting fatiguing contraction of these muscles 21 was elicited reflexly by discharges in group III and IV muscle afferents presumably induced, or else enhanced 11, by metabolic products liberated in muscle tissue during contraction. In view of recent findings by Hayward et al. 11 contribution of nonspindle group If afferents should also be taken into account. Since spike discharges from group III, as well as from group If muscle afferents, elicited by electrical stimulation of a muscle nerve, exert strong reflex effects on fusimotor neurones destined to other muscles 3'4, changes in the discharge rate of fusimotor neurones related to muscle fatigue may not be limited to those innervating muscle spindles in the contracting muscle. If an increase in discharge rate occurs also in fusimotor neurones supplying muscle spindles in other muscle groups, it could contribute to and/or support the spread-

ing of activity to these other muscles when the contracting one is fatigued (refs. 20, 31 and L. Schwirtlich, personal communication). The fusimotor system would thus play a role in muscle fatigue beyond that of autogenetic motor control (e.g. ref. 32). We have not found any studies on reflex effects due to muscle afferent activity other than stretch on fusimotor activity to neighboring muscles (cf. ref. 16). In the present experiments changes in the discharge rate of fusimotor neurones to hamstring muscles were looked for during long-lasting fatiguing contractions of the triceps surae muscles and compared with the changes found previously in the discharge rate of fusimotor neurones to these muscles 21. The aim of the experiments was twofold: (1) to show whether the discharges in mechanosensitive and/or chemosensitive small diameter muscle afferents due to muscle contraction and fatigue are as efficient in exerting reflex effects on fusimotor neurones destined to other muscle groups as they were 3'4 when elicited by electrical stimulation of the afferent fibres; and (2) to prove the possibility that these reflex effects might be involved in motor control in muscle fatigue. A preliminary report of this work has been presented 22.

Correspondence: R. Anastasijevi6, Institute for Medical Research, 11001 Beograd, Dr Suboti6a 4, Po-Box 721, Yugoslavia.

247

MATERIALS AND METHODS Experiments were performed on 14 adult decerebrate cats. Three of the cats were spinalized at the T 9 level in the course of the experiments. The operative procedure before decerebration was carded out under halothane in oxygen anaesthesia. The right hind limb was completely denervated except for the triceps surae and hamstring muscles. The nerves to these muscles were freed from the surrounding tissue; those to the triceps muscles (to medial gastrocnemius and to lateral gastrocnemius and soleus muscles) were mounted on platinum wire bipolar stimulating electrodes, while those to the hamstring group (semitendinosus, semimembranosus and biceps femoris) were dissected later for recording of fusimotor spikes. Decerebration was performed by intercollicular section of the brainstem and the nervous tissue rostral to the section removed. Cats were fixed to the stand by clamps on the third lumbar spine and the iliac processes, and screws in the right tibia and femur. The exposed tissues were kept moist in paraffin pools. Blood pressure and the temperature of both the animal and the paraffin pools were monitored and maintained above 90 mmHg and at 3638°C, respectively. Spike discharges of functionally single fusimotor neurones were recorded from thin filaments, dissected free from desheathed fascicles cut out of the nerves to hamstring muscles. In order to avoid any possible indirect effects on the fusimotor neurones of afferent discharges elicited by electrical stimulation of the nerves to triceps and/or by its contraction, the nerves to hamstring muscles were severed at their distal ends, close to the entry in the muscle tissue. The discharging neurones were identified as fusimotor if their conduction velocity was in the range of 10-45 rn/s. It was determined by back-averaging of impulse traffic in the parent nerve, triggered by single impulses recorded from the filament6 in the same way as the conduction velocity of fusimotor neurones to triceps 17'21. An example of records is shown in Fig. 1A. Changes in tension of the triceps surae muscles were recorded by a tension transducer attached to the tendon. The compliance of the transducer was 20 /~m/N. Isometric contractions of the triceps surae muscles were elicited by stimulating the nerves to these muscles with 0.2 ms electrical pulses at 1.3 times motor threshold at a rate of 40 Hz until the muscle tension fell to approximately one third of the initial value. The motor threshold was assessed as described in the previous paper zl by observing muscle tension changes on the oscilloscope screen while the stimulus strength was gradually increased. The muscle was held extended by 3 mm from the length at which the slack was just taken up. Fusimotor discharges were recorded before (60-120 s), during and after (50-300 s) muscle contraction. The records were stored on magnetic tape and/or analysed on-line on a Hewlett-Packard 9817 computer. The spikes were converted to voltage steps which were sampled at either 10 ms- or 20 ms-intervals and the discharge rate (number of impulses per 1 s-interval) computed. This procedure was adopted to obtain, with the available computer memory, an on-line record at the sampling rate high enough to detect every action potential during a 300 s- or 600 s-period. This was the shortest period allowing an immediate visual inspection of either the muscle contraction and the related changes in fusimotor discharge rate or, if taken in the absence of the nerve stimulation, of possible longer-lasting spontaneous oscillations in background firing rate. The output signal from the tension transducer was amplified, stored on magnetic tape, and A/D converted (sampling interval 40 ms) simultaneously with fusimotor discharges. Actual signals of both fusimotor spike discharges (Fig. 1B) and muscle tension were also monitored on an oscilloscope screen and their changes observed during recording. Further analysis of records was performed offline as described in detail in the previous paper 21 and shown in Fig. 1C. In short, timing and magnitude (oblique and vertical arrows in Fig. 1, respectively) of changes in fusimotor discharge rate were estimated from the departure of counts per 10-s interval, expressed in impulses/s, from the mean resting discharge rate computed dur-

ing either the 60 s- or 120 s-period (horizontal arrow) immediately preceding the onset of stimulation. Whenever the increased discharge rate was maintained at a fairly constant level for either 60 or 120 s statistical significance was estimated using the Student t-test. Otherwise the difference between the actual and the mean resting firing rate was roughly estimated to be significant if the interval limited by 2 S.D.'s from the mean resting discharge rate and the interval covering the amplitudes of random fluctuations in the actual discharge rate did not overlap. To check whether the changes in fusimotor discharge rate represent reflex responses to changes in afferent inflow from the contracting muscles and to differentiate the receptors responsible for the reflex effects, the following procedure was adopted: (a) fusimotor discharges were recorded during long-lasting muscle contraction (control); (b) the contraction was provoked while the muscles were made ischaemic by clamping the femoral artery and (c) the same electrical stimulation was applied after severing the nerves distal to the site of stimulation. Half-hour periods of rest were introduced between any procedure. The muscle was considered to have recovered when the tension changes provoked by the same stimulation were the same as before. Also, any metabolic changes due to fatigue could be expected to subside during this period of time (e.g. refs. 7,18).

RESULTS The effects of long-lasting contractions of the triceps s u r a e m u s c l e s w e r e s t u d i e d o n 22 f u s i m o t o r n e u r o n e s t o h a m s t r i n g m u s c l e s f r o m 14 cats. T h e m a j o r i t y o f n e u rones were destined to semimembranosus

muscle since

spontaneous fusimotor discharges were most often enc o u n t e r e d in t h e n e r v e b r a n c h s u p p l y i n g t h i s m u s c l e . S p o n t a n e o u s d i s c h a r g e r a t e o f t h e cells r a n g e d b e t w e e n i n t e r m i t t e n t l o w r a t e s (less t h a n 5 i m p u l s e s / s ) t o sust a i n e d r a t e s o f 42 i m p u l s e s / s a n d t h e c o n d u c t i o n v e l o c i t y o f t h e i r a x o n s f r o m 15 t o 30 m/s. C h a n g e s in d i s c h a r g e r a t e r e l a t e d t o t h e t r i c e p s s u r a e c o n t r a c t i o n o c c u r r e d in 16 f u s i m o t o r n e u r o n e s . T w o o f t h e s e n e u r o n e s , s h o w i n g s p o n t a n e o u s o s c i l l a t i o n s in firing r a t e w e r e d i s c a r d e d f r o m f u r t h e r a n a l y s i s s i n c e t h e e x a c t m a g n i t u d e a n d t i m i n g o f c h a n g e s in d i s c h a r g e r a t e presumably related to the contractions could not be det e r m i n e d . A f t e r a d d i t i o n a l s p i n a l i z a t i o n , t o r e m o v e possible d e p r e s s i o n in reflex t r a n s m i s s i o n 8 t h e c h a n g e s in the discharge rate of fusimotor neurones became larger t h a n b e f o r e in t h e s a m e cats, b u t r e m a i n e d in t h e r a n g e of magnitudes encountered

in d e c e r e b r a t e s . N o differ-

e n c e s w e r e f o u n d r e l a t e d t o t h e f u s i m o t o r n e u r o n e destination within the hamstring group of muscles.

Changes in fusimotor discharge rate E a r l y a n d l a t e c h a n g e s c o u l d b e r e c o g n i z e d in discharge rate of fusimotor neurones to hamstring muscles d u r i n g l o n g - l a s t i n g t r i c e p s c o n t r a c t i o n . A n e x a m p l e is s h o w n in Fig. 1C. T h e initial s h a r p i n c r e a s e in t h e disc h a r g e r a t e at t h e o n s e t o f t h e t r i c e p s c o n t r a c t i o n w a s f o l l o w e d b y a d e c r e a s e b e l o w t h e r e s t i n g firing level. T h e l a t e g r a d u a l i n c r e a s e in d i s c h a r g e r a t e d e v e l o p e d t o w a r d s

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CoOs Fig. 1. Identification (A) and changes in discharge rate (B,C,D) of fusimotor neurones to hamstring muscles during long-lasting contraction of the triceps muscles. A: records of the action potentials of one fusimotor neurone (upper trace) and of the whole nerve activity (lower trace) both spike triggered averaged and delayed. Conduction time (horizontal arrow) 1 ms, distance between the recording sites 26 mm, calculated conduction velocity 26 m/s. B: segments of records of spike discharges of the same neurone. From top to bottom: immediately before the onset of stimulation of the nerves to triceps; immediately after its cessation; 280 s later. C: upper traces, discharge rate (impulses/s calculated from counts per 1 s- and 10 s-interval, thick and thin line, respectively) of the same neurone throughout the recording period. Continuous and broken horizontal lines, mean spontaneous discharge rate and _+ S.D. Lower trace, muscle tension changes (N). Vertical broken line, onset of stimulation; horizontal lowermost line, period of stimulation. D: another fusimotor neurone, upper and lower traces, same as in C. Mean and S.D. shown also for the increased firing level.

the e n d of c o n t r a c t i o n a n d outlasted it for a b o u t 220 s. T h e difference b e t w e e n the m e a n discharge rate d u r i n g this p e r i o d a n d the m e a n s p o n t a n e o u s firing rate was small b u t significant at the 0.01 level. I n the f u s i m o t o r n e u r o n e shown in Fig. 1D the early changes were lacking while an a b r u p t shift in firing level o c c u r r e d towards the e n d of muscle contraction. T h e initial increase in discharge rate, at the onset of

the triceps c o n t r a c t i o n , by 2 - 7 impulses/s ( m e a n value 3.5 impulses/s), was a p p a r e n t in 8 f u s i m o t o r n e u r o n e s . The increase was short-lasting in 6 n e u r o n e s ( 5 - 3 0 s), while in two n e u r o n e s it was p r o l o n g e d (135 a n d 150 s). In o n e f u s i m o t o r n e u r o n e a sharp initial decrease in discharge rate, by 20 impulses/s, o c c u r r e d instead, lasting for a b o u t 20 s. N o a p p a r e n t initial changes in discharge rate b e y o n d the r a n d o m fluctuation level a r o u n d the

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Fig. 2. Control procedure: changes in the discharge rate of a fusimotor neurone. A: during triceps contraction; B: during ischaemic triceps contraction; C: during stimulation of the nerves to triceps severed distal to the site of stimulation. In B, ischaemia started before the recording period, removal of the arterial clamp indicated by the arrow. In C, period of stimulation indicated by horizontal bar. Upper and lower traces same as in Fig. 1C.

mean spontaneous firing rate could be noticed in the remaining 5 fusimotor neurones. The initial increase in discharge rate was followed by a decrease attaining a level below that of the spontaneous firing rate in two fusimotor neurones, by 3 and 13 impulses/s, and lasting for 60 and 50 s, respectively. The late changes in discharge rate were much more uniform. An increase in discharge rate starting towards the end of the triceps surae contraction and outlasting it was encountered in all these 14 fusimotor neurones, as well as in those two discarded from quantitative analysis. It ranged from 1 to 13 impulses/s at its maximum (mean value 4.6 impulses/s, n = 14), remaining within limits of random fluctuations in two neurones. In 12 neurones the increase developed gradually, attaining its maximum usually after the end of the contraction and subsiding gradually thereafter to the resting discharge level. It outlasted the muscle contraction for 30-280 s (mean value 150 s). In two fusimotor neurones the discharge rate increased abruptly and was maintained thereafter at the new level for more than 300 s, i.e. beyond the recording period.

Origin of the late increase in fusimotor discharge rate A control procedure to check the possibility that the late increase in discharge rate was related to muscle fatigue was carded out in 5 fusimotor neurones. An example is shown in Fig. 2. In four of the neurones the late increase in discharge rate was gradual (Fig. 2A). It developed earlier, as did the muscle tension fall, when the contracting triceps surae muscles were made ischaemic by clamping the femoral artery and started to subside after removal of the clamp (Fig. 2B). The shift in firing level of the fifth neurone also occurred earlier, but the discharge rate remained elevated after removing the arterial clamp (not shown). Stimulation of the nerves to the triceps severed distal to the site of stimulation provoked no changes in the discharge rate of 3 fusimotot neurones (as in Fig. 2C), while in two units it elicited a sustained decrease in discharge rate, by about 2 impulses/s, throughout the period of stimulation. The difference between the mean discharge rate during the stimulation period and the mean resting discharge rate was not statistically significant. At the end of the stimulation period the discharge rate returned immediately

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itr~lses ts Fig. 3. A: mean resting discharge rates (left) and the corresponding firing rates during the period of late increase (right) of the 14 fusimotor neurones studied. B,C: histograms of distribution of firing rates (continuous lines, at rest; broken lines, during the period of late increase) and of duration of the late increase respectively. In C, the two neurones showing abrupt shifts in firing level were omitted.

to the resting discharge level. The changes in fusimotor discharge rate occurring either during muscle contraction, during ischaemic muscle contraction or in its absence during stimulation of the severed nerves were reproducible when tested after a half-hour period of rest.

Generality of the late increase in fusimotor discharge rate The late increase in discharge rate varied considerably in both amplitude and duration among the fusimotor neurones to hamstring muscles. General reflex changes in activity pooled data are shown in Fig. 3. While the absolute increase in discharge rate, in impulses/s, of some fusimotor neurones was rather large (A), its values, normalized with respect to the corresponding spontaneous firing rate (not shown), indicated that the relative increase was modest (range 1.11-4.0, mean value 1.5). Though the range of firing rates was shifted by about 5 impulses/s towards the higher frequencies (B) during the period of late increase, there was no increase in the number of units firing at higher rates as encountered in fusimotor neurones to triceps 21. Smaller changes in distribution might, however, have remained unnoticed due to the broad range of firing rates of fusimotor neurones to hamstring muscles and, consequently, a small number of units firing at each particular frequency. On the other hand, the late increase in the discharge rate of fusimotor neurones to hamstring muscles (Fig. 3C) was longer-lasting on the average than in fusimotor neurones to triceps muscles, the discharge rate remaining elevated for more than 2 min after the end of muscle contraction in 11 out of 14 neurones (78%). DISCUSSION The results of our experiments show that changes in the discharge rate of fusimotor neurones to hamstring

muscles do occur during long-lasting fatiguing contractions of the triceps surae muscles. Being similar in pattern to those found in fusimotor neurones to triceps 2t, and different from those provoked by electrical stimulation of the severed nerves, the changes in the discharge rate of fusimotor neurones to hamstring muscles could be supposed to result from reflex influences of afferent discharges from the contracting triceps muscles. The changes occurred in 16 out of 22 neurones studied (73%). A lower incidence of the heteronymous than of autogenetic 2~ reflex effects could, however, be expected in the view of the findings by Appelberg et al. 3"4. The origin of the early changes in discharge rate, bearing obviously no relation to muscle fatigue, will be discussed only briefly. The initial increase, occurring at the onset of muscle contraction, could be ascribed mainly to discharges elicited in group III mechanosensitive afferents from the triceps muscles 1°. Contribution of early discharges from muscle spindle secondary endings 13 and/or of those from non-spindle group II afferents 29 cannot, however, be excluded. The initial sharp decrease in discharge rate, encountered in one fusimotor neurone only, could be provoked by these same afferent discharges 3'4. The transient decrease in discharge rate, following on rare occasions its initial increase, could be due to biphasic effects of the same afferent impulses '° or due to recurrent inhibition 5'9 since bursts of Renshaw interneurone discharges may be expected to occur at the onset of muscle contraction 1'2. The late increase in discharge rate, developing towards the end of the triceps contraction and outlasting it, could be related to fatigue of the contracting muscles. It preserved the same temporal relation to muscle contraction when the tension fall started earlier due to muscle ischaemia and persisted until the arterial clamp was removed. Though its amplitude was smaller on the av-

251 erage, its time course (except for abrupt shifts, see later) was similar to the corresponding changes in discharge rate found in fusimotor neurones to triceps 21. Therefore it seems reasonable to assume that the late increase in the discharge rate of fusimotor neurones to hamstring muscles during fatiguing triceps contraction is also provoked by discharges elicited and/or enhanced by metabolic products liberated during the contraction in both mechanosensitive 11'19'23'2s and chemosensitive 27'3° group III and IV afferents from triceps. The contribution of discharges from the non-spindle group II afferents cannot be wholly excluded though their number might be small 11'29. However, the absence of the early increase in discharge rate, at the onset of muscle contraction, in 5 out of 14 fusimotor neurones in which the late increase developed raises the possibility that the latter is provoked primarily by nerve impulses from chemosensitive rather than from mechanosensitive muscle afferents. The smaller amplitude of the initial increase in firing rate, when present, in fusimotor neurones to hamstring muscles in comparison to the neurones to triceps 2x speaks also in favour of less strong reflex connections of mechanosensitive afferents from the triceps muscles with hamstring fusimotor neurones. Abrupt long-lasting shifts in the discharge rate, though encountered in two neurones only, may deserve some comment. Their reproducibility as well as their temporal relation to muscle contraction similar to that of a gradual late increase in discharge rate, speak against their being spontaneous changes known to occur in decerebrate cats. Further studies, however, are required, before they can be considered with any certainty as bistable behaviour similar to that of skeletomotor neurones ~2. Static fusimotor neurones could not be differentiated from dynamic fusimotor neurones in these experiments. However, since the background discharges of the neurones studied covered a wide range of firing rates, it can

be assumed that both static and dynamic fusimotor neurones were affected if the differences in spontaneous firing rates determined by Murphy et al. 24 hold true also for hamstring neurones.

REFERENCES

305. 6 Bostock, H. and Sears, T. A., Continuous conduction in demyelinated mammalian nerve fibres, Nature, 236 (1976) 786-787. 7 Duchateau, J., De Montigny, L. and Hainaut, K., Electro-mechanic failures and lactate production during fatigue, Eur. J. Appl. Physiol., 56 (1987) 287-291. 8 Eccles, R.M. and Lundberg, A., Supraspinal control of interneurones mediating spinal reflexes, J. Physiol., 147 (1959) 565584. 9 Ellaway, P.H., Recurrent inhibition of fusimotor neurones exhibiting background discharge in the decerebrate and the spinal cat, J. Physiol., 216 (1971) 419-439. 10 Ellaway, P.H., Murphy, P.R. and Tripathi, A., Closely coupled excitation of ),-motoneurones by group III muscle afferents with low mechanical threshold in the cat, J. Physiol., 331 (1982) 481-498. 11 Hayward, L., Wesselmann, U. and Rymer, W.Z., Effects of muscle fatigue on mechanically sensitive afferents of slow conduction velocity in the cat triceps surae, J. Neurophysiol., 65

1 Anastasijevi6, R. and Vu6o, J., The relative dependence of the activity of Renshaw cells on recurrent pathways during contraction of the triceps muscle, Pfliigers Arch., 377 (1978) 255-268. 2 Anastasijevi6, R. and Vu6o, J., Renshaw cell discharge at the beginning of muscular contraction and its relation to the silent period, Exp. Neurol., 69 (1980) 589-598, 3 Appelberg, B., Hulliger, M., Johansson, H. and Sojka, P., Action on gamma motoneurones elicited by electrical stimulation of group II muscle afferent fibres in the hindlimb of the cat, J. Physiol., 335 (1983) 255-273. 4 Appelberg, B., Hulliger, M., Johansson, H. and Sojka, P., Action on gamma motoneurones elicited by electrical stimulation of group III muscle afferent fibres in the hind limb of the cat, J. Physiol., 335 (1983) 275-292. 5 Appelberg, B., Hulliger, M., Johansson, H. and Sojka, P., Recurrent actions on gamma motoneurones mediated via large and small ventral root fibres in the cat, J. Physiol., 335 (1983) 293-

Functional implications It has been supposed that the increase in fusimotor activity directed to muscle spindles outside the contracting muscle elicited reflexly by afferent discharges due to fatigue from the contracting muscle could contribute to spreading of activity (refs. 20, 31 and L. Schwirtlich, personal communication) to other muscle groups when the contracting one is fatigued. The fusimotor system would thus play a role in providing reflex support to the waning function of the fatigued agonist. While the late increase in discharge rate has been found in 73% of fusimotor neurones to hamstring muscles studied during fatiguing contractions of triceps, the relative changes in the discharge rate of individual neurones with respect to the resting firing level, though long-lasting, were rather small. The contribution of this increase per se to the spreading of activity to other muscle groups could only be modest. Whether the afferent discharges from the fatigued muscle can be made more efficient when integrated by the fusimotor neurones with afferent impulses of other origin 4'15, which were largely eliminated by denervation in our experiments, remains to be elucidated. For the same reasons possible after-effects of the changes in fusimotor discharge rate and consecutive increase in sensitivity of muscle spindle sensory endings 14'25, as well as any speculation on their role in motor control 26 postulated to apply also for muscle fatigue, require further investigation.

Acknowledgements. This work has been supported by a Serbian Research Foundation Grant. Thanks are due to Dr. J. Vu6o for both constant encouragement and criticism.

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