The role of muscle spindle afferents in stretch and vibration reflexes of the soleus muscle of the decerebrate cat

The role of muscle spindle afferents in stretch and vibration reflexes of the soleus muscle of the decerebrate cat

366 Brain Research, 146 (1978) 366-372 © Elsevier/North-Holland Biomedical Press The role of muscle spindle afferents in stretch and vibration refle...

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366

Brain Research, 146 (1978) 366-372 © Elsevier/North-Holland Biomedical Press

The role of muscle spindle afferents in stretch and vibration reflexes of the soleus muscle of the decerebrate cat

J. J. B. JACK and R. C. ROBERTS University Laboratory of Physiology, Oxford (Great Britain)

(Accepted November 15tb, 1977)

In the decerebrate cat it has, until recently, been assumed that the only source of excitation to extensor motoneurones from their own muscle afferents during stretch is the group Ia fibres (see ref. 15 for a review). In 1969 Matthews la presented strong circumstantial evidence for a net excitatory effect from group II muscle spindle afferents. Subsequent workin the decerebrate cat has added further weight to his conclusions 2,7,12. Furthermore, several groups have reported evidence in anaesthetized preparations of both monosynaptic and polysynaptic excitatory actions from group II afferents on extensor motoneurones 8.n,x6 (see also ref. 17). In this communication we wish to present evidence that in some decerebrate cats the only significant excitatory action contributing to stretch and vibration reflexes of the soleus muscle is by Ia afferents. Adult cats were decerebrated intercollicularly after initial surgery under anaesthesia (Fluothane, ICI, with an equal mixture of N 2 0 and 02). With the exception of the nerve to soleus, the left hindlimb was denervated. The soleus muscle was attached to a stretcher/vibrator built to a design similar to that used by McGrath and Matthewsle; the total compliance of the system, including the tension transducer, was about 25 #m/N. A lumbosacral laminectomy was performed and a portion of L7 or S1 ventral root selected, which contained about half of the skeletomotor nerve supply to the soleus muscle (as judged by the tension produced). This was cut centrally, and used to selectively stimulate the g a m m a efferents by a technique similar to that we have previously used for stimulating group II afferents 6. Freshly chlorided silver electrodes were used, with an interelectrode distance of 4-5 mm. Strong shocks (e.g. 20 V, 1 msec duration, rectangular pulses at 200 Hz for approximately 30 sec) were given and after a 10-20 min recovery period a 'Floyd' stimulus waveform (see ref. 6) was delivered. The cathode was on the cut central end of the ventral root. Monophasic recordings made from muscle nerves such as medial gastrocnemius revealed that we could usually stimulate half or more of the gamma efferents without any significant alpha contamination. We used two checks on the selectivity and effectiveness of the stimulus to soleus efferent axons: (1) the volley produced no (or minimal) tension in the muscle when all reflex tension was inhibited by stimulating the ipsilateral peroneal nerve (lack of alpha

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Length (relotive to M.RL.) Fig. 1. Active tension developed by the soleus muscle and the frequency of discharge of a muscle spindle primary afferent (conduction velocity 81 m/sec) and of a muscle spindle secondary afferent (conduction velocity 63 m/sec) plotted against the length of the muscle in millimetres relative to its maximum physiological length (MPL). The open squares show the maintained response to stretch alone, and the open circles the response to stretch and vibration (200 Hz, 100/~m). The closed squares and circles respectively show the responses to stretch, and to stretch and vibration, during gamma stimulation at 100 Hz delivered via a centrally cot part of the ventral root containing44 ~ of the alpha motor supply to the muscle. Note that gamma stimulation causes no change in the vibration reflex tension (or the rate of Ia discharge in response to stretch and vibration), in spite of a substantial increase in the rate of secondary afferent discharge in response to stretch and vibration.

m o t o r stimulation), a n d (2) p r o d u c t i o n of additional reflex t e n s i o n when the muscle was stretched b u t n o t vibrated (effectiveness of g a m m a stimulation). I n some of the later experiments we also cut a small dorsal root filament centrally a n d isolated single group I or group II afferent fibres c o m i n g from the soleus muscle. Recordings of soleus muscle t e n s i o n a n d afferent discharge were made at least 2 h after decerebration a n d cessation of anaesthesia.

368 Results were obtained in 15 experiments and in 4 of them, although a selective gamma volley in the cut ventral root produced a marked increase in reflex tension on top of a stretch reflex, no additional reflex tension was seen when the muscle was also being vibrated (usually 200 Hz, 100 or 150/~m amplitude) or 'pulsed' (i.e. a continuous mechanical waveform at 200 Hz, similar in shape to that described in ref. 12, see their Fig. 13). The principle of this type of experiment is that during gamma efferent stimulation, when the muscle is stretched, there should be an increase in the firing rate of both the group Ia and group II afferents; but when the muscle is also vibrated only the group II afferents should increase their firing because the group Ia afferents should be held at a constant firing frequency equal to that of the vibratory stimulus 13. Fig. 1 displays the results for one such experiment, in which the activity of both a muscle spindle primary and a muscle spindle secondary afferent were monitored. The stretch reflex stiffness between the muscle lengths of 5.5 mm less than maximum physiological length ( M P L 5.5 mm) and MPL-0.5 mm was 0.88 N/ram, and it was increased by gamma stimulation at 100 Hz to 1.22 N/ram. Since 44 ~ of the skeletomotor supply to the soleus muscle was cut, these figures become equivalent to 1.55 N/mm and 2.18 N/mm if the ventral root supply had been left intact. When the muscle was also vibrated the gamma volley had no significant effect in producing extra reflex tension. Note that in the presence of vibration the sample Ia fibre followed vibration one to one and its firing was not affected by gamma stimulation, in contrast to the observation with stretch alone. However the sample group II spindle afferent did show an increase in firing to the gamma volley whether the muscle was only stretched or stretched and vibrated. The simple conclusion that may be drawn from this experiment is that the increased activity of group II spindle afferents had no significant net effect on motoneurone excitability. In keeping with this conclusion the increment in tension produced by vibration at different muscle lengths shows substantial occlusion, such that the total active tension produced by stretch and vibration remains fairly constant at different muscle lengths (an increase from 7.8 N to 9.0 N between MPL --8 mm and MPL - - 0.5 ram). Given the conclusion that there is no net excitatory effect from the group lI, this suggests that the active length tension curve of the muscle (due solely to its contractile properties) can be fairly flat, as Matthews13,14 has suggested (cf. refs. 3 and 4). We have obtained similar results, showing no net group II excitation, in three other preparations. In the 11 other experiments the selective gamma volley did produce changes in the amount of reflex tension generated by stretch and vibration. The commonest result, observed at some stage in all 11 of the experiments, was an increase in tension, raising the possibility of excitation from spindle secondaries. In 5 of these experiments the tonic stretch reflex was negligible or absent. In 9 of them we measured the total active tension in response to stretch and vibration at two or more lengths and found that in all 9 of them the active tension increased considerably with increase in length. On Matthew's la interpretation this is evidence for a net group II excitation, but on Grillner's a this might simply reflect the contractile properties of the muscle. In 9 of the 11 experiments we performed additional tests that have raised another possible interpretation. We were initially concerned that the gamma volley might so excite the Ia

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endings that they would sometimes fire more than once to each lengthening stroke of vibration. Although we did observe this occasionally, especially if we used 'pulses '12, the main problem we found was that in some of these experiments a sample Ia fibre would misbehave during vibration in the sense that it did not reliably follow vibration one to one. Fig. 2 shows an example of this and also illustrates that the gamma volley restores the Ia behaviour during vibration to that of one to one following. In accord with the behaviour of the Ia, the reflex tension generated during gamma stimulation was greater. In 6 of the 9 experiments we observed the behaviour of one or occasionally two Ia afferents. In 5 of the 6, one of the sample Ia fibres did not follow vibration one to one at all lengths; they tended to be less reliable at shorter lengths. (Spindle afferent fibres were defined as group Ia or group II on the basis of conduction velocity, but in addition all the fibres classified as of group Ia showed high dynamic sensitivity to a ramp stretch. The conduction velocity of units that misbehaved were: 100, 94.4, 90, 89.4, 86, 79.5 m/sec and of those that behaved included ones of 81 and 79 m/sec.) If a proportion of the unsampled Ia fibres, which contributed to the development of tension during stretch and vibration, behaved similarly, the increase in tension produced by the gamma volley, and the increase of vibration reflex tension with length, might be explained solely by this effect. However in order to prove this quantitatively one would have to obtain a substantial sample of the soleus Ia afferents, dissecting them in continuity so that they would continue to contribute to the development of reflex tension.

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Fig. 3. A: the middle trace of the experimental records shows the tension developed by the soleus muscle during a stretch from MPL --7 mm to MPL --5 mm; pulses (200 Hz, 80/zm) were applied for 4 see during the stretch, and gamma stimulation at 150 Hz was delivered for the last 2 sec of the pulses via a centrally cut part of the ventral root containing 69 ~ of the alpha motor supply to the muscle. The upper trace shows the tension developed when, in addition to the 150 Hz gamma stimulation for the 2 sec, 30 Hz gamma stimulation was delivered throughout the remainder of the record. The lower trace shows the tension developed when active reflex tension was inhibited by stimulation of the ipsilateral peroneal nerve at 50 Hz. The gamma volley was delivered at 150 Hz for 2 sec as in the other traces, and it is seen that in this experiment there was a small amount of alpha fibre stimulation. Each trace is the average of 4 trials. The maximal possible reflex tension that could be developed in ths preparation was 5.7 N. B: as for A, except in each trace the soleus muscle was stretched from MPL --7 mm to MPL --3 ram.

As a n alternative to this ideal we sought m o r e c i r c u m s t a n t i a l evidence for I a ' m i s b e h a v i o u r ' d u r i n g vibration. Fig. 3 shows the kinds o f tests p e r f o r m e d . The two sets o f curves display t o t a l tension d e v e l o p e d when the muscle was stretched f r o m M P L - - 7 m m to M P L - - 5 m m (A) a n d to M P L - - 3 m m (B) respectively. In each o f t h e m pulses (200 Hz, 8 0 / z m ) were delivered to the muscle on t o p o f the stretch for 4 sec, a n d a g a m m a volley at 150 H z was generated for 2 sec d u r i n g the pulses. The l o w e r m o s t curves show the result when all reflex tension was inhibited by s t i m u l a t i o n o f the ipsilateral p e r o n e a l nerve; in this e x p e r i m e n t the g a m m a volley was c o n t a m i n a t e d by a small a m o u n t o f a l p h a stimulation. The middle curves show the results w i t h o u t p e r o n e a l nerve s t i m u l a t i o n ; n o t e that the increment in tension p r o d u c e d by the high frequency g a m m a volley was smaller at the longer length. The t o p m o s t curves show the effects o f the high frequency g a m m a volley on t o p o f stretch a n d pulses, when it was p r e c e d e d a n d followed by a low frequency (30 Hz) g a m m a volley. The low frequency g a m m a volley a l m o s t entirely eliminated the i n c r e m e n t in tension p r o d u c e d by the high frequency g a m m a volley. This a p p a r e n t s a t u r a t i o n in the effectiveness o f the g a m m a volley with increasing frequency is n o t o b s e r v e d when the increments in tension p r o d u c e d by it are studied on stretch alone. In experiments in which we p e r f o r m e d q u a n t i tative studies, the increment o f tension on stretch a n d v i b r a t i o n p r o d u c e d by a g a m m a volley s a t u r a t e d at frequencies o f 15-50 Hz, whereas the i n c r e m e n t o f tension on stretch alone c o n t i n u e d to grow as the g a m m a volley frequency was increased to 150 or 200 Hz. The simplest i n t e r p r e t a t i o n o f these results is that some o f the Ia endings were n o t

371 following vibration one to one (more not following at the shorter length), and a low frequency gamma volley was sufficient to ensure that they did; hence, switching to a higher frequency gamma volley would not be expected (in the absence of double firing of any Ia fibres to vibration) to produce any further increment of tension, unless the group II afferents had a net excitatory effect (since their firing would increase further with the high frequency gamma volley). Another feature of Fig. 3, which is in general agreement with this interpretation, is that lack of occlusion of the stretch plus vibration reflexes was observed without a gamma volley (middle curves, early part of the vibration reflex) but adding the low frequency gamma volley converted this into perfect occlusion, with the total active tension being the same at the two lengths. In the 6 experiments in which some or all of these test were performed it was found that in 4 the high frequency gamma volley only produced an increase in tension at shorter lengths, and in the other two the high frequency gamma volley produced no further increase in tension over that produced by a low frequency gamma volley. In addition it was observed in two of the experiments that the increase in tension produced by a high frequency gamma volley was abolished if vibration was started before the muscle had been stretched rather than afterwards. McGrath and Matthews 12 have already noted that if vibration precedes stretch there is less likelihood of Ia 'misbehaviour' when the muscle develops tension. If to these 6 experiments we add 3 other experiments in which it was observed that the Ia monitor misbehaved, we can conclude that in all 9 of these 11 experiments, in which some evidence of Ia misbehaviour was sought, it was found. This does not prove that the only excitatory effect from the soleus muscle proprioceptors was via the Ia fibres, since a small group II excitation, which might saturate at higher frequencies of firing of the group II afferents, cannot be excluded. Nevertheless, the most economical interpretation of our data in all 13 experiments where we performed suitable tests is that the only major excitatory effect on soleus motoneurones during stretch and vibration comes from the group Ia fibres. The experiments do not determine what fraction of the Ia contribution is monosynaptic and what polysynaptic 5. Furthermore, it is clear that vibration is not always a reliable method to lock the firing of all the Ia fibres in the soleus muscle when it is developing tension. It should be noted, however, that the design of our experiments may tend to favour Ia misbehaviour, because a large fraction of the tonically active gamma efferent supply to the muscle spindle has been interrupted by the ventral root section. Other workers using the technique of muscle vibrationT,l~, a3, with ventral roots intact, have provided some evidence that Ia misbehaviour was not a problem. It is still to be settled whether this reflects a difference in the experimental preparation or not, although in 3 animals with ventral roots intact we have observed misbehaviour of a sample Ia fibre. In the mechanically much less favourable circumstance of vibration of the human leg muscles, Burke et al. 1have also reported that the Ia fibres do not always follow vibration one-to-one. We would like to thank our colleagues, especially Dr. P. B. C. Matthews, for their helpful comments throughout the course of this work. The work was supported by the Medical Research Council (Project Grant G974/359.).

372 1 Burke, D., Hagbarth, K.-E., L6fstedt, L. and Wallin, B. G., The responses of human muscle spindle endings to vibration during isometric contraction, J. Physiol. (Lond.), 261 (1976) 695-711. 2 Fromm, C., Haase, J. and Wolf, E., Depression of the recurrent inhibition of extensor motoneurons by the action of group II afferents, Brain Research, 120 (1977) 459-468. 3 Grillner, S., Is the tonic stretch reflex dependent upon Group II excitation?, Actaphysiol. scand., 78 (1970) 431-432. 4 Grillner, S. and Udo, M., Motor unit activity and stiffness of the contracting muscle fibres in the tonic stretch reflex, Acta physiol, scand., 81 (1971) 422-424. 5 Hultborn, H., Wigstr6m, H. and W~ingberg, B., Prolonged activation of soleus motoneurones following a conditioning train in soleus Ia afferents - a case for a reverberating loop?, Neurosci. Lett., 1 (1975) 147-152. 6 Jack, J. J. B. and Roberts, R. C., Selective electrical activation of group II muscle afferent fibres, J. Physiol. (Lond.), 241 (1974) 82-83P. 7 Kanda, R. and Rymer, W. Z., An estimate of the secondary spindle receptor afferent contribution to the stretch reflex in extensor muscles of the decerebrate cat, J. Physiol. (Lond.), 264 (1977) 63-87. 8 Kato, M. and Fukushima, K., Selective activation of group lI muscle afferents and its effects on cat spinal neurones. In S. H o m m a (Ed.), Understanding the Stretch Reflex, Progr. Brain Res., Vol. 44, Elsevier, Amsterdam, 1976, pp. 185-196. 9 Kirkwood, P. A. and Sears, T. A., Monosynaptic excitation of motoneurones from muscle spindle secondary endings of intercostal and triceps surae muscle in the cat, J. Physiol. (Lond.), 245 (1975) 64-66P. 10 Lundberg, A., Malmgren, K. and Schomburg, E. D., Characteristics of the excitatory pathways from group II muscle afferents to alpha motoneurones, Brain Research, 88 (1975) 538-542. 11 Lundberg, A., Malmgren, K. and Schomburg, E. D., Comments on reflex actions evoked by electrical stimulation of group II muscle afferents, Brain Research, 122 (1977) 551-555. 12 McGrath, G. J. and Matthews, P. B. C., Evidence from the use of procaine nerve block that the spindle group II fibres contribute excitation to the tonic stretch reflex of the decerebrate cat, J. Physiol. (Lond.), 235 (1973) 371-408. 13 Matthews, P. B. C., Evidence that the secondary as well as the primary endings of muscle spindles may he responsible for the tonic stretch reflex of the decerebrate cat, J. PhysioL (Lond.), 204 (1969) 365-393. 14 Matthews, P. B. C., A reply to criticism of the hypothesis that the group II afferents contribute excitation to the stretch reflex, Actaphysiol. scand., 79 (1970) 431-433. 15 Matthews, P. B. C., Mammalian Muscle Receptors and their Central Actions, Edward Arnold, London, 1972. 16 Stauffer, E. K., Watt, D. G. D., Taylor, A., Reinking, R. M. and Stuart, D. G., Analysis of muscle receptor connections by spike-triggered averaging. 2. Spindle group II afferents, J. NeurophysioL, 39 (1976) 1393-1402. 17 Westbury, D. R., A study of stretch and vibration reflexes of the cat by intracellular recording from motoneurones, J. PhysioL (Lond.), 226 (1972) 37-56.