The discharge from primary endings of muscle spindles during reflex activation of fusimotor neurones in the lightly anaesthetised and spinal cat

The discharge from primary endings of muscle spindles during reflex activation of fusimotor neurones in the lightly anaesthetised and spinal cat

Brain Research, 51 (1973) 279-292 279 © Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands T H E D I S C H A R G E F R ...

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Brain Research, 51 (1973) 279-292

279

© Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands

T H E D I S C H A R G E F R O M P R I M A R Y E N D I N G S OF MUSCLE SPINDLES D U R I N G R E F L E X ACTIVATION OF F U S I M O T O R N E U R O N E S IN T H E L I G H T L Y A N A E S T H E T I S E D A N D SPINAL CAT

D. M. LEWIS

Department of Physiology, University of Bristol, Bristol BS8 ITD (Great Britain) (Accepted August 25th, 1972)

SUMMARY

The responses of primary endings in muscle spindles of peroneus brevis of the cat to a single ipsilateral skin nerve stimulus were measured as frequencygrams and post-stimulus histograms. Under light pentobarbitone anaesthesia a brief, short latency, large amplitude frequencygram was observed with a stimulus too weak to elicit a reflex contraction. The response is deduced to have been caused by an almost synchronous discharge of several static fusimotor fibres. It is suggested that the background activity was due to asynchronous activity in static fusimotor fibres. After section of the spinal cord, reflex acceleration of the spindle was less pronounced and the frequencygram had a slower time course. The response was increased during extension of the muscle. The possibility that the response in spinal cats resulted from a dynamic fusimotor reflex is considered.

INTRODUCTION

On stimulation of a cutaneous nerve there may be a response in intrafusal motor nerves. Jansen and Rudjord 11 have shown that the response is greatest in static fusimotor fibres in the decerebrate cat, whereas after spinal section mainly dynamic fusimotor fibres are excited 1. These authors differentiated between the two types of fusimotor fibre during repetitive stimulation of the sensory nerve. However, a full understanding of the role of the static and dynamic fibres requires a knowledge of the time course of their reflex activation. A preliminary approach to this question may be made by studying the response to a single stimulus and a number of studies have shown that not all fusimotor fibres respond with the same time course 1°,17. However, none of these studies distinguished between static and dynamic fusimotor fibres and the present experiments were undertaken in an attempt to make this distinction.

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Post-stimulus histograms and frequencygrams 4 have been used to study the discharge of primary endings from peroneus brevis muscle of the cat following stimuli applied to ipsilateral skin nerves. It was found that lightly anaesthetised animals showed a response to repetitive stimulation similar to that described by Jansen and Rudjord 11. The response to single stimuli resembled the increase in the rate of firing produced by static fusimotor stimulationL Preliminary results are described from spinal animals which show a response with a different time course. METHODS

Cats with weights ranging from 1.4 to 3.1 kg were anaesthetised with pentobarbitone sodium given intraperitoneally in a dose of 40 mg/kg. Anaesthesia was maintained by further intravenous injections of 5-10 mg. Occasionally nitrous oxide was used to allow the administration of pentobarbitone at a lower rate. During the recording period, anaesthesia was maintained at a level at which there was a brisk ipsilateral response to pinching a forepaw. No records were made immediately after an injection of pentobarbitone. A further 8 cats were decerebrated under halothane anaesthesia which was then discontinued. The spinal cords of all these and 6 of the pentobarbitone anaesthetised cats were cut at T12 under brief halothane or propanidid anaesthesia. One to 6 h were allowed to elapse after cord section before measurements were made. The peroneal muscles were chosen as they are activated together with the flexors in the flexor reflex. However they are more accessible for recording, especially peroneus brevis which is a posterior muscle of this group. It was exposed by a posterior midline incision and its tendon was marked to allow identification of its maximum and minimum physiological lengths during recording. The nerves to all other muscles in the limb were cut; sural and superficial peroneal nerves were prepared for stimulation. A laminectomy was made from S1 to L5. The lamina o f T 1 2 was also removed where the spinal cord was to be cut. The tibia and fibula were clamped in metal vices at the ankle and knee and anchored to a massive metal table by magnetic clamps. Exposed tissues were covered in liquid paraffin, temperature of this and of the body was maintained at 36-37 °C. The tendon of the muscle was tied to a tension transducer which had a stiffness of 50 k g / m m and was held on the moving arm of an electromagnetic shaker. Length and velocity feedback were used and the servo had a stiffness of I0 k g / m m and was just overdamped. Details are described by Lewis and Proske 14. The dorsal roots were explored with a single ball electrode and a filament was cut centrally from a region where there was a clear spike evoked by stimulation of the nerve to peroneus brevis. Single primary afferents (group Ia) were isolated from this strand, conduction velocities ranged between 86 and 109 m/sec. The threshold of the dorsal cord potential was measured for each skin nerve, using 100/~sec pulses delivered from an isolated stimulator (Devices). Muscle length was controlled by signals from a modified waveform generator (Servomex L.F. 141). The output of the dynamometer was amplified by a low noise variable gain amplifier (Fenlow A D 103S). The noise

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Fig. 1. Top left, frequencygram recorded from a primary ending with afferent nerve conduction velocity (C.V.) of 93 m/sec. Each dot represents a single action potential and its vertical displacement is proportional to the reciprocal of the time elapsed since the previous action potential, 16 sweeps superimposed. The row of dots below are at intervals of 10 msec but indicate by their vertical position a frequency of 10 imp./sec. The time of the stimulus is indicated by the vertical bar below the first dot. The 3 histograms show the number of action potentials occurring after a stimulus in the same afferent fibre. Top right, the sum of 64 responses counted in 1 msec bins. Below right, 16 responses taken from this series. Below left, these 16 responses recounted in 4 msec bins. Alongside each histogram is shown a scale of the number of spikes per bin. The corresponding frequency is shown in the centre together with the frequency scale for the frequencygram (steps of 100-300 imp./ sec).

level o f this system was equivalent to approximately 200 mg peak to peak. A n a l o g u e signals o f nerve spikes, muscle length and tension were recorded on magnetic tape (Thermionic T3000) to allow later analysis. The other recording channel was used to provide a sweep counter, stinmlus marker and a frequency standard to improve playback accuracy 18.

Analysis of results. The action potentials triggered an instantaneous frequency meter 12 which had been modified so that the dot display could be used without Z modulation o f a storage oscilloscope (A. Taylor, personal communication). It was shown to be linear within 1 ~ over a range f r o m 6 to 700 imp./sec. By superimposing 10-20 responses a frequencygram could be built as seen in Fig. 1 (top left). In this and other illustrations a r o w o f dots is superimposed below the frequencygram at a level corresponding to 10 imp./sec. These dots also provide time markers, at 10 msec in this figure. A vertical bar under one o f the dots indicates that a stimulus was applied at this time. Some limitations have been described in the use o f frequency in the analysis o f spike trains 15. All the results o f these experiments have been confirmed by poststimulus histograms compiled on a special purpose computer. This was a Biomac 500 which had been modified in order to count every spike occurring in a time bin, rather than the one or none counting normally used by this machine. Interval histograms were also made. Post-stimulus histograms are also illustrated in Fig. I. The upper right record was compiled f r o m 64 sweeps using 1 msec counting bins. A response could be seen if a smaller n u m b e r was used but it was often close to the noise level as illustrated by the lower right record o f Fig. I. This was f r o m the same series but comprised only 16 sweeps c o m p a r e d with 64. Noise could be reduced by using 4 msec bins

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(lower left in Fig. 1) but this p r o c e d u r e reduced the m a x i m u m frequency recorded and increased u n c e r t a i n t y in m e a s u r i n g time. It was f o u n d t h a t a response c o u l d be seen in a f r e q u e n c y g r a m after a much smaller n u m b e r o f sweeps than was possible in a post-stimulus histogram. F o r this r e a s o n the f r e q u e n c y g r a m was preferred, as m e a s u r e m e n t s c o u l d be m a d e m o r e quickly a n d were less likely to be affected by changes in reflex excitability. RESULTS The results are d e s c r i b e d in two m a i n sections: the first deals with responses r e c o r d e d from a n i m a l s with an intact spinal c o r d ; the second is a p r e l i m i n a r y r e p o r t o f responses r e c o r d e d f r o m a small n u m b e r o f animals following spinal transection. Initially, in b o t h sections, the change o f d y n a m i c index 7 during repetitive s t i m u l a t i o n o f an afferent nerve is briefly described, in o r d e r to m a k e a c o m p a r i s o n with the results o f o t h e r w o r k e r s 1,11. The r e m a i n d e r o f each section describes responses to single afferent nerve volleys; first the characteristics o f an early reflex increase in the :°

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Fig. 2. Frequencygrams recorded from primary ending (C.V. 98 m/sec) in lightly anaesthetised cat with intact spinal cord. Frequencygrams recorded as in Fig. 1 ; timing dots at 10 msec and 10 imp./ sec. All responses w~re from 16 superimposed oscilloscope sweeps. On the left, background activity; on the right, the responses to a single twice threshold stimulus applied to the ipsilateral sural nerve (indicated by vertical bar below the first time dot). Background and reflex were recorded at maximum body length of the muscle, Lm~,, (below); at Lmax - - 2 mm (middle) and at Lmax --5 mm (top). The calibrations (in imp./sec, bottom left) apply to all the records.

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rate o f discharge are described, followed by an analysis o f the effect o f muscle length on the response. Next a description is given o f dynamic effects which include the changes in the response to a single stimulus b r o u g h t about by constant velocity extension o f the muscle. Finally certain late effects, which occur some hundreds o f milliseconds after a single stimulus, are described.

Responses in animals with intact spinal cord A total o f 39 afferents were studied in 16 animals. In order to measure the dynamic sensitivity o f endings, the muscle was extended for 3 m m at constant velocity finishing near Lmax. The difference between the m a x i m u m instantaneous frequency at the end o f the r a m p and the frequency measured 0.5 sec later (at the same muscle length) is the dynamic index 7. This was measured at a velocity of 10 mm/sec in 17 afferents. In 9 o f these, the effect o f repetitive stimulation o f a skin nerve at 80 pulses/ sec was measured. A decrease o f dynamic index was always observed although in 2 the change was close to the limits o f certainty (5 imp./sec). The mean change was - - 9 . 7 imp./sec. In 5 of these afferents the dynamic index was measured at different times during the period o f nerve stimulation. The decrease was maximal in the first 0.5 sec and became less or disappeared after 1 or 2 sec. A similar time course was seen in the increased firing rate induced by repetitive stimulation of the skin nerve but with muscle length constant. The results are essentially similar to those o f Jansen and R u d j o r d 11 and indicate that static fusimotor fibres are stimulated under barbiturate anaesthesia as they are in the decerebrate animal, however the effects were less marked. In response to a single stimulus, a brief increase in firing rate was seen after a short latency in both the frequencygram (Fig. 2, right) and in the post-stimulus histogram (Fig. 3, right). The threshold for the reflex varied from one experiment to another but was always small, typically between 1.5 and 5 times the threshold voltage for

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Fig. 3. Interval and post-stimulus histograms from a primary ending (C.V. 102 m/sec). On the left, interval histograms (1 msec bins) of background discharge. On the right, post-stimulus histograms (1 msec bins, 64 responses) following a single 5 times threshold stimulus to the ipsilateral sural nerve. A scale of the number of action potentials per bin is shown to the right of the interval histograms, and to the left of the post-stimulus histograms. The corresponding frequency (imp./sec) is also indicated on the left of the post-stimulus histograms. Time scales for all histograms are identical. Background and reflex were recorded at 3 muscle lengths : above at Lmax - - 5 mm, middle at Lrnax - - 2 mm and below at Lmax.

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the most excitable fibres of the skin nerve. In two experiments (5 afferents) a second stimulus at 3 msec was necessary to elicit the response. The frequencygram was particularly useful in searching for minimal responses. In all experiments it was possible to evoke a fusimotor response with a stimulus below threshold for an extrafusal contraction. If stimulus intensity was increased gradually the peak of the reflex frequencygram increased to a maximum or close to it before the extrafusal response could be detected. Beyond this point the form of the frequencygram also changed little despite muscle contraction. The maximal twitch tension averaged 340 g and contractions less than 0.1 ~ of this (i.e. motor unit size) could be detected. All the records presented result from the use of a stimulus that was subthreshold for an extrafusal contraction. Similar responses may be observed in primary afferents from tenuissimus muscle (unpublished observations with U. Proske). They have similar amplitude and time course but cannot be separated by stimulus strength from the twitch-like contraction of the extrafusal fibres. Slow intravenous injection of critical doses of gallamine produced a reduction of the tension with little change in the peak frequency of the response of the afferent fibre and none in its time course. An intravenous injection of pentobarbitone in a dose of 4 mg/kg reduced the response and a dose of 10 mg/kg abolished it for some time. In some animals with very active reflexes there was a second but smaller peak in the falling phase of the initial response with a delay of 20-40 msec. Long repetitive responses to a single stimulus have been seen in decerebrate animals (unpublished observations). Effect of muscle length. Measurements have been made over the full range of muscle lengths possible in the body. The mean range between full ankle flexion and extension measured in the cats was 5.7 mm (Standard Deviation 1.4). The mean optimum lengths for active twitch tension was 2.7 mm less the maximum body length (Lmax). The effect of muscle length on the reflex responses from the spindles in two experiments are shown in Fig. 2, right and in Fig. 3, right. Additionally in the lefthand columns of Fig. 2 background activity is shown as superimposed instantaneous frequency records and the histograms of Fig. 3 (left) indicate the distribution of intervals in the 'spontaneous' spindle discharge. The mean peak increase in rate of firing of 39 primary afferents was 199 imp./sec (S.D. 78 imp./sec); the largest response observed was 450 imp./sec and the smallest 80 imp./sec. In any one animal all afferents isolated (up to 5) had a comparable response. The reflex increase of discharge of all primary afferents was influenced by muscle length. The most obvious effect was on peak firing rate which was always low when the muscle was at a short length (58 _+_24 imp./sec at minimum body length) and increased as the muscle was extended. At maximum body length the peak frequency was also maximal in some fibres (as in that of Fig. 3); in others the peak fell off a little at extreme lengths (see Fig. 2). Proske and Lewis 16 showed that this could be explained in some cases by an autogenetic inhibition of fusimotor fibres by muscle stretch afferents 9. This conclusion is supported by the observation that the peak frequency of the spontaneous activity continued to increase with muscle length even when the reflex peak was reduced (e.g. Fig. 2), indicating that the reduction in the peak of the

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Fig. 4. Effect of muscle pull on the primary ending of Fig. 2. Frequencygrams derived as in Fig. 1. The upper record was the response to muscle extension at 5 mm/sec, beginning before and ending after the oscilloscope sweep. Below an additional twice threshold stimulus to the sural nerve was given. At the time of stimulus the muscle length was Lma,~--1 mm. Time dots are at 10 msec and 10 imp./sec, stimulus marked as in Fig. 1. The scale of frequencies (imp./sec) applies to both traces.

reflex response could not be accounted for by changes in the muscle spindle. The interval histograms of Fig. 3 also illustrate this effect. At short lengths the distribution was almost symmetrical about the mean (apparently slightly skewed to long intervals). At longer lengths, as the mean interval became shorter, the distribution skewed towards short intervals, almost becoming bimodal at Lmax. Peak instantaneous frequencies of up to 200 imp./sec have been observed in the spontaneous discharge. In many experiments the reflex response was smaller, sometimes less than peak background frequencies. The latency of the response also changed a little with muscle length and was minimal at long lengths. Minimum latencies of 15-26 msec (mean, 18; S.D., 4.1 msec; n = 29) were seen in frequencygrams. Measurements of post-stimulus histograms usually gave a shorter latency down to 13 msec. These results are comparable with earlier reports 8. Estimates of intrafusal delays 5 and motor and sensory conduction times add to 14--18 msec and the residual central time must be less than 4 msec. The somewhat longer latencies have been found at short muscle lengths but these could be accounted for by longer intrafusal delays 5. The rise time of the frequencygram decreased twofold with increasing length; typically, a minimal value of 6 msec was found (mean, 6.5; S.D., 1.6 msec; n = 29). Dynamic effects. If a stimulus was applied during a constant velocity pull on the muscle, the peak frequency of the reflex response of the afferent was decreased. This is illustrated in Fig. 4 recorded from the same afferent fibre as Fig. 2. In the upper record are the superimposed responses to a ramp extension at 5 mm/sec starting 200 msec before the beginning of the oscilloscope trace and ending after it at a muscle length corresponding to Lmax. Thus at the beginning of the trace the muscle was 1 mm below Lmax. The lower record was obtained under similar conditions except that a stimulus was applied to the sural nerve. The peak response during stretch was well below that obtained at constant length (see Fig. 2 bottom right), a direct comparison

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Fig. 5. Frequencygram recorded on a slower sweep showing the response of a primary afferent (C.V 89 m/sec) in a lightly anaesthetised cat. Time dots are at 100 msec and 10 imp./sec. Stimulus at twice threshold to superficial peroneal nerve. On the left are 2 single responses; on the right the next 8 were superimposed. is illustrated by the lower pair of records of Fig. 7. A reduction of 50-30 ~ has been seen in 7 afferents tested. This effect is not due to autogenetic inhibition as it has been seen in deafferented animals (unpublished observations with U. Proske). Late effects. The responses of a primary afferent with the muscle held at Lrnax are illustrated in slow sweeps in Fig. 5 where the time marks are at 100 msec. The two left-hand traces were single responses; the right-hand one consists of 8 superimposed traces. The single traces show that the spontaneous activity consisted of a train of low frequency spikes interspersed with sets of 2-3 at higher frequency, each burst had a time course comparable to that of the reflex frequencygram. The spontaneous bursts occur irregularly at about 5-10/sec. In the superimposed trace the bursts were absent for a period of about 100 msec following the reflex. Granit and Holmgren 8 have reported that the response consisted of a train of spikes if the muscle length was long. This may be similar to the responses illustrated in Fig. 5 and may be interpreted here as synchronisation of background fusimotor firing by the stimulus.

Responses in animals with spinal cord section Of the 14 animals examined after spinal section only 7 showed a response in afferent fibres to repetitive stimulation of a skin nerve. In 5 animals (12 afferents) a velocity stimulus of 2 mm/sec produced a mean dynamic index of 25 imp./sec. During

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repetitive stimulation of a skin nerve no change was seen in two fibres and the mean increase was 15 imp./sec. One animal showed a marked effect and in this dynamic index was measured at several times during repetitive stimulation of the nerve. A velocity stimulus of 10 mm/sec produced a dynamic index 150 imp./sec at an interval of 0.1 sec after nerve stimulation but the response fell to control levels (70 imp./sec) after 0.5 sec of stimulation. Thus although unambiguous dynamic responses were seen they were less than has been reported 1. When tested with a single skin nerve volley only two animals (3 afferents examined) showed a spindle response and two other afferents developed one during muscle stretch. Threshold was as low as twice nerve threshold but this stimulus often produced an extrafusal contraction even when there was no spindle acceleration (3 other animals). After section of the spinal cord the discharge of the primary endings was always more regular (see Fig. 6 and 7 top left). Although the number is very small the responses are sufficiently different from those reported above as to merit a preliminary description. Effect of muscle length. The graphs of Fig. 6 show how the peak response, measured from the resting rate, changed with muscle length. One of the two fibres represented (open circles) is that illustrated by the frequencygrams and showed a maximal response at intermediate muscle lengths, the other (filled circles) at minimum body length. Both responses were almost absent at Lmax. The peak increase in frequency was small and never more than 20 imp./sec

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above the resting discharge rate. Latencies were 20-30 msec and rise times not less than 20 msec. Dynamic effects. The spindle response to a single stimulus to a skin nerve in the spinal cat was increased if the stimulus was applied during a constant velocity extension o f the muscle. A n increase o f peak frequency by a factor of 1.5-2 was observed. In one animal this procedure even induced a fusimotor reflex response and this is illustrated in the upper 4 traces of Fig. 7. The upper pair of records show spindle activity in the absence o f a skin nerve stimulus both with the muscle held at constant length (left) and during a 2.5 mm/sec extension (right). The middle pair o f records was obtained under similar conditions o f the muscle but with a stimulus applied at the beginning o f each trace. There was no change in the rate o f firing or tension at constant muscle length but during the r a m p a response occurred in a b o u t half o f the 16 responses. In this experiment the reflex was apparently all or none in both spindle discharge and muscle tension, indeed they changed together. The latency and rise time o f the response during pull were similar to those seen in other afferents with the muscle at constant length. The differences between these

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and reflexes observed in animals with an intact spinal cord are illustrated by the lower records of Fig. 7. Latencies in the spinal cat were 5-10 msec longer but only 2-5 msec of this can be accounted for by the longer intrafusal delays shown by Bessou et aLL Rutledge and Haase 17 have reported long latencies but these were long compared with the background interspike intervals observed in the present exl~eriments at all muscle lengths except those near minimum in the body. Another feature seen whilst stimulating during a pull is illustrated in Fig. 8 in which the spindle afferent response of Fig. 7 was recorded on a slower time base (time marks at 100 msec). The initial response was followed by a 'tail' which continued beyond the end of the constant velocity phase, increasing the frequency of discharge and the dynamic index. The effect is not unambiguously seen in the top trace of Fig. 8 in which the muscle was extended at 2.5 mm/sec but is clear in the other two responses which were obtained during ramps of 5 and 10 mm/sec. The 'tail' increased with ramp velocity more than the initial peak. The prolonged acceleration of the spindle seen during muscle extension in the spinal cat could be due to a repetitive reflex discharge, however, it would be necessary to exclude the possibility that similar prolonged effects follow a single dynamic fusimotor spike 6. The increase in the amplitude of the reflex frequencygram produced during muscle extension in the spinal cat may represent an autogenetic facilitation of the reflex activation of fusimotor fibres similar to that

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produced in a-motoneurones. Alternatively it may be due to an alteration of the response of the spindle afferent to fusimotor fibre activation during muscle stretch. DISCUSSION

In the intact anaesthetised animal the responses of primary afferent endings to repetitive stimulation of skin nerves are similar to those described by Alnaes et al. 1 and may be interpreted as resulting from reflex activation of static fusimotor fibres. The responses to single stimuli are comparable with those described by other authors s-1°,17, for example they show a short latency indicating brief synaptic delays. However examination of the afferent fibre frequencygrams allows the responses to be analysed in more detail, especially as much information is available about frequencygrams resulting from direct fusimotor stimulation4,L The increase in the peak of the frequencygram with muscle length (and possibly the decrease during muscle extension) is due to changes in the muscle spindle and not to autogenetic inhibitory reflexes16 and resembles closely static fusimotor responses. The time course of the reflex frequencygrams was as brief as that of one evoked by stimulation of a single static fusimotor fibre but the peak rate was often greater than that reported by Bessou et al. 5 and usually greater than the maximum rate observed in the background (see below). It may be inferred that often the response consisted of almost synchronous activation of several static fusimotor fibres to one spindle. The simultaneous activation of dynamic fusimotor fibres cannot be excluded but it seems unlikely that the longer dynamic frequencygram would not have been seen. The background activity also showed some points of similarity with the responses to static fusimotor stimulation. Above a baseline rate, bursts of two or more spikes occurred irregularly. Even the longest burst spanned only 20 msec, peak frequencies were at least as high as those described following static fusimotor stimulation and also increased progressively with muscle length. These bursts therefore seem likely to have been afferent responses to spontaneous static fusimotor activity, although additional dynamic fusimotor activity cannot be excluded. The rate of about 10/sec at which the spontaneous bursts occurred is lower than the rates of discharge normally seen in fusimotor fibres in decerebrate animals 9. Even allowing that not all static fusimotor fibres produce a strong response in an afferent, there was a discrepancy here. Perhaps some of the bursts correspond to the synchronous arrival of action potentials in several fusimotor fibres, the high instantaneous frequencies observed in the bursts may support this idea. The period of reduced spontaneous activity which followed the fusimotor reflex (Fig. 5) might suggest an inhibitory process, but an alternative explanation would be that all the fusimotor fibres were recruited in the reflex and then resumed firing at their spontaneous rate of 10/sec corresponding to 100 msec. As has been seen in decerebrate cats 1°, the presumed static fusimotor reflex response occurred in the absence of muscle contraction which came in at higher stimulus strengths. But it is unlikely that the increased muscle afferent activity was directly responsible for the a-motoneurone recruitment as the frequencygram was typically maximal at lower stimulus intensity. The observations fit best the idea of

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tWO separate pathways with the fusimotor activation increasing the rate of discharge of muscle afferents and facilitating a-motoneurones. In this context it is interesting to note how the effect increases with muscle length and might be considered as an increase in gain of a length servo loop. The short delays, brief time course and the absence of background fusimotor activity after the response should be compared with the time course of the twitch which has a rise time of 20 msec and a total duration of 60 msec. I f intrafusal and extrafusal neurones were excited briefly, after an early increase, the loop gain could decrease and even fall below initial levels before the end of the contraction. There would then be no problems arising from the underdamping consequent upon the increase of gain, as this only occurred early in a response when maximal speed might be achieved. Although these arguments apply to the reflexes of single stimuli, they indicate the frequency responses of a system that might be useful in controlling varying physiological demands. In the spinal animal, the absence of bursts of high frequency in the afferent spikes discharge suggests that 'spontaneous' static fusimotor activity no longer occursL The response to repetitive stimulation of a skin nerve indicates that dynamic fusimotor fibres are predominantly activated as in the experiments of Jansen and Rudjord 11. In contrast with animals with intact spinal cords, responses to single stimuli were not often seen. The thresholds were closer to those for a-motoneurone activation and this makes any interpretation difficult because of the possibility of mechanical interaction or of fl fibre activation 8. The parameters of the few single stimulus reflex frequencygrams observed were different from those elicited in cats with an intact cord. The peak frequency, the effect of muscle length on this and the time course (but not the slightly longer mean latency) were all significantly different in the statistical sense but are of limited value because of the small numbers. However it is reasonable to conclude that any differences that do exist could be due to differences in the response of the spindle to dynamic and static fusimotor fibre stimulation and therefore the different frequency components of these responses should be considered in assessing the role of the two types of fusimotor fibres. ACKNOWLEDGEMENT I wish to thank the Medical Research Council of Great Britain for a generous grant in support of this work.

REFERENCES 1 ALNAES,E., JANSEN,J. K. S., AND RUDJORD,T., Fusimotor activity in the spinal cat, Actaphysiol scand., 63 (1965) 197-212. 2 BERGMANS,J., AND GRILLNER,S., Reciprocal control of spontaneous activity and reflex effects in static and dynamic flexor a-motoneurones revealed by an injection of Dopa, Actaphysiol. scand.. 77 (1969) 106-124. 3 BESSOU,P., EMONET-DENAND,F., ANDLAPORTE,Y., Motor fibres innervating extrafusal and intrafusal muscle fibres in the cat, J. Physiol. (Lond.), 180 (1965) 649-672. 4 BESSOU,P., LAPORTE,Y.. ANDPAGES,B., A method of analysing the responses of spindle primary endings to fusimotor stimulation, J. Physiol. (Lond.), 196 (1968) 37-45.

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5 BESSOU, P., LAPORTE, Y., AND PAGES, B., Frequencygrams of spindle primary endings elicited by stimulation of static and dynamic fusimotor fibres, J. Physiol. (Lond.), 196 (1968) 47-64. 6 BROWN, M. C., GOODWIN, G. M., AND MATTHEWS, P. B. C., After-effects of fusimotor stimulation on the responses of muscle spindle primary afferent endings, J. Physiol. (Lond.), 205 (1969) 677-694. 7 CROWE, A., AND MATTHEWS, P. B. C., The effects of stimulation of static and dynamic fusimotc~r fibres on the response to stretching of the primary endings of muscle spindles, J. Physiol. (Lond.), 174 (1964) 109-131. 8 GRANIT, R., AND HOLMGREN, B., Two pathways from brain stem to gamma ventral horn cells, Actaphysiol. scand., 35 (1955) 93-108. 9 HUNT, C. C., The reflex activity of mammalian small nerve fibres, J. Physiol. (Lond.), 115 (1951) 456-469. 10 HUNT, C. C., AND PAINTAL, A. A., Spinal reflex regulation of fusimotor neurones, J. Physivl. (Lond.), 143 (1958) 195-212. 11 JANSEN, J. K. S., AND RUDJORD, T., Fusimotor activity in a flexor muscle of the decerebrate cat, Acta physiol, stand., 63 (1965) 230-246. 12 KAY, R. H., A reciprocal time-interval display using transistor circuits, Electr. e;~gng., 37 (1965) 543-545. 13 LEWIS, D. M., A counter for magnetic tape recording, J. Physiol. (Lond.), 203 (1969) 24P. 14 LEWIS, D. M., AND PROSKE, U., The effect of muscle length and rate of fusimotor stimulation on the frequency of discharge in primary endings from muscle spindles of the cat, J. Physiol. (Lond.), 222 (1972) 511-535. 15 MCKEAN, T. A., POPPELE, R. E., ROSENTHAL, N. P., AND TERZUOLO, C. A., The biologically relevant parameter in nerve impulse trains, Kybernetik, 6 (1971) 168-170. 16 PROSKE, U., AND LEWIS, D. M., The effects of muscle stretch and vibration on fusimotor activity in the lightly anaesthetised cat, Brain Research, 46 (1972) 55-69. 17 RUTLEDGE, L. T., AND HAASE, J., Flexor muscle spindles and reflex firing of early discharging units, J. Neurophysiol., 24 (1961) 182-192.