Action of static and dynamic fusimotor fibres on secondary endings of cat's spindles

1. The effects exerted on secondary endings by repetitive stimulation of single static or single dynamic fusimotor fibres were studied in nine tenuissimus spindles in cats.2. The discharge of each secondary ending was recorded simultaneously with the discharge of the primary ending belonging to the same spindle.3. All the nineteen static fusimotor fibres studied activated secondary endings.4. Of eight dynamic fusimotor fibres, seven had no action on secondary endings. One dynamic fibre activated an atypical secondary ending which displayed some phasic sensitivity.5. No difference in conduction velocity was found between static and dynamic fibres.6. The implications of these observations for the mechanism of action of static and dynamic fusimotor fibres are discussed.     

Frequencygrams of spindle primary endings elicited by stimulation of static and dynamic fusimotor fibres

1. Frequencygrams of cat spindle primary endings, obtained by the method described by Bessou, Laporte & Pagès (1968), were elicited by the stimulation of single static and dynamic fusimotor fibres.2. Stimulation of static fibres by single stimuli may elicit: (i) no response, (ii) responses of small amplitude, (iii) responses of large amplitude with a pause after the rising phase.3. Stimulation of static fibres by repetitive stimuli gives frequencygrams resembling records of tetanic contraction of skeletal muscle. At a frequency of stimulation of 180-200/sec periodic oscillations are perceptible on the plateau of the frequencygram.4. Stimulation of dynamic fibres by single stimuli may elicit: (i) no response, (ii) responses smaller and longer than the responses given by static fibres.5. When the muscle is stretched the amplitude of the responses elicited by dynamic fibres decreases whereas the amplitude of the responses given by static fibres increases.6. Frequencygrams obtained by repetitive stimulation of dynamic fibres show periodic oscillations only at low rates of stimulation. At rates of stimulation higher than the minimal rate giving frequencygrams with a smooth contour, the amplitude of the frequencygram increases.     

Morphological identification and intrafusal distribution of the endings of static fusimotor axons in the cat

1. Tenuissimus muscles of the cat were prepared in which the motor innervation was reduced to a single gamma axon by cutting all the other motor axons and allowing them to degenerate during a period of 7-12 days. The function of the surviving gamma axon was then determined, and the distribution of its endings ascertained in teased, silver preparations.2. In the ten muscles successfully prepared the function of the surviving gamma axon was static and the motor innervation distributed to the spindles consisted of trail endings. The conduction velocities of the axons ranged from 33 to 48 m/sec.3. A detailed histological analysis was made of thirty spindles innervated by six of the surviving static axons.4. The six static axons distributed trail endings to both bag and chain muscle fibres in the poles of thirty spindles with about twice the frequency of supplying them to poles in which the distribution was restricted exclusively to one type of muscle fibre or the other.5. The density of trail innervation supplied to the bag fibres, in terms of the mean number of terminals per fibre, was typically from one and a half to twice that supplied to the chain fibres. On the other hand, whereas the number of bag fibres supplied with trail endings in a spindle pole was seldom more than one, the number of chain fibres innervated was usually two in a range of one to four.6. The possible effects that partial denervation might have had on the spindles are discussed, but it is concluded that they are unlikely to have affected the results.     

Slowing of the discharge of secondary endings of cat muscle spindles during fusimotor stimulation

Summary Responses of secondary endings of muscle spindles of the peroneus tertius muscle of the anaesthetized cat have been recorded during repetitive stimulation of functionally single fusimotor fibres that produced slowing of the discharge. In a sample of 125 pairs of single fusimotor fibres and secondary spindle afferents 5 examples of slowing were seen. The amount of slowing became less at longer muscle lengths. Conditioning the spindle by stimulating the muscle nerve at fusimotor strength, at a length 2.5 mm longer than the test length, and then returning to the test length 3 seconds later led to a greater degree of slowing of the discharge than after conditioning stimulation at the test length. With one exception, responses to muscle stretch were reduced during stimulation of a fusimotor fibre that produced slowing. On two occasions stimulating a fusimotor fibre that produced slowing of the response of one secondary ending, led to excitation of two other endings. Two possible explanations for the generation of slowing responses have been considered. The first is that the slowing is the result of contraction of the region of intrafusal fibre directly underlying the secondary sensory ending. The second, which we favour since it accounts for the facts more adequately, is that slowing is the result of shortening of the region of nuclear chain fibres on which the sensory ending lies, produced by movement in an adjacent nuclear bag fibre.     

Studies on the site of termination of static and dynamic fusimotor fibres within muscle spindles of the tenuissimus muscle of the cat

1. The site of termination of static and dynamic fusimotor fibres has been mapped by finding which intrafusal muscle fibres have been depleted of glycogen as a result of tetanic stimulation of single gamma fibres. Long periods of stimulation coupled with occlusion of the blood supply were necessary to cause glycogen depletion.2. In cat tenuissimus muscle, dynamic gamma motor fibres always activated bag intrafusal muscle fibres, and occasionally chain fibres. Static gamma fibres always activated chain fibres and frequently activated bag fibres as well.3. It is argued that these results can be fitted into the hypothesis of the mechanism of internal functioning of the spindle originally proposed by Jansen & Matthews (1962). It is also pointed out that the results raise problems concerning the mechanism of development of the spindle motor innervation.     

The effect of muscle length and rate of fusimotor stimulation on the frequency of discharge in primary endings from muscle spindles in the cat

1. Responses from the primary endings of muscle spindles in the soleus muscle of the cat were recorded during repetitive fusimotor stimulation at a number of different muscle lengths.2. An increase in the rate of stimulation increased the size of both the peak and the plateau of the responses to stimulation of both static and dynamic fusimotor fibres.3. Responses, with the exception of the peak frequency of the discharge during dynamic fusimotor stimulation, increased in size on raising the muscle length up to maximum body length. The peak of the dynamic response reached its highest value at intermediate lengths.4. The effect of increasing stimulation rate and muscle length was to reduce both the latency and time to peak of fusimotor responses. The change in latency with muscle length was particularly dramatic at low stimulus rates.5. In an attempt to compare fusimotor responses with the behaviour of extrafusal muscle fibres, a model is proposed which consists of a mixture of extrafusal tension and rate of change of tension. This model could simulate the static fusimotor responses reported here.     

Distribution of fusimotor axons to intrafusal muscle fibres in cat tenuissimus spindles as determined by the glycogen-depletion method.

1. The distribution of fusimotor axons to bag1, bag2 and chain muscle fibres in cat tenuissimus spindles has been studied using a modification of the glycogen-depletion technique of Edstrrom & Kugelberg (1968). Single fusimotor axons were stimulated intermittently at 40-100/sec for long periods (30-90 sec) during blood occlusion. Portions of muscle containing the activated spindles were quick-frozen, fixed in absolute ethanol during freeze-substitution, and then embedded in paraffin wax. Serial transverse sections were stained for glycogen using the periodic acid-Schiff method, and examined for depletion. 2. Dynamic gamma axons (i.e. those that increase the dynamic index of primary-ending responses to ramp stretches of large amplitude) depleted bag1 fibres almost exclusively. 3. Static gamma axons (i.e. those that reduce or abolish the dynamic index) depleted both bag and chain fibres. Bag1 and bag2 fibres were depleted about equally. 4. A single static gamma axon may activate both bag and chain fibres in one spindle (the most common pattern), chain fibres only in another, and bag fibres only in a third spindle. 5. Static gamma axons with conduction velocities less than 25 m/sec also had a non-selective distribution, but no depletion was observed in bag2 fibres. 6. The zones of depletion produced by dynamic gamma axons were distributed more or less equally in the intra- and extracapsular parts of spindle poles, whereas those produced by static gamma axons were mainly intracapsular. 7. The results are compared with the glycogen-depletion studies of Brown & Butler (1973, 1975) and our own study of the distribution of static gamma axons to spindles in which all other motor axons had degenerated (Barker, Emonet-Dénand, Laporte, Proske & Stacey, 1973). The implications of the finding that both static gamma and dynamic gamma axons activate bag1 fibres are discussed.     

A method of analysing the responses of spindle primary endings to fusimotor stimulation

1. The superposition of records of `instantaneous' frequency of discharge of spindle primary endings after stimulation of single fusimotor fibres leads to the construction of graphs called `frequencygrams'.

2. The superposition is made on the screen of a storage oscilloscope, the time base of which is synchronized with the stimulus. It is essential that the stimulus be delivered at all possible intervals with respect to the impulse of the resting discharge which precedes it.

3. Frequencygrams obtained by stimulating some static fusimotor fibres by single stimuli display a response with a fast rising phase, a pause, and a slower decreasing phase.

4. Frequencygrams may give some information on the time course of the contraction of intrafusal muscle fibres elicited by stimulating their motor axons.

     

After-effects of fusimotor stimulation on the response of muscle spindle primary afferent endings

1. The experiments were performed on the soleus muscle of the anaesthetized cat in which the ventral roots had been cut.2. A short period of repetitive stimulation of a single fusimotor fibre which influenced a particular spindle primary ending invariably caused a characteristic alteration in the response of the same ending to a subsequently applied ramp stretch of the muscle. The change consisted in the appearance of a burst of impulses at the beginning of the stretch where none had been present before. Occasionally, such an ;initial burst' was spontaneously present; it was then enhanced following fusimotor stimulation.3. This after-effect of fusimotor stimulation was abolished by a subsequent stretch of the muscle, but otherwise persisted for over a minute.4. When the muscle was released to below the length at which the spindle had been facilitated and a testing stretch applied from the new initial length there was no burst of impulses at the beginning of stretch. There was, however, a burst as the muscle was stretched through the length at which the fusimotor fibre had been stimulated.5. These effects are suggested to be due to the persistence of stable bonds between the actin and myosin filaments of the intrafusal fibres, so that their previously activated regions were ;stuck' at the length they were when the fusimotor stimulation was applied.6. Such effects were produced both by static and by dynamic fusimotor fibres. The effects of the two kinds of fusimotor fibre, however, appeared to be mediated by different intrafusal muscle fibres. This was shown by stimulating one kind of fibre with the muscle slightly stretched, then releasing the muscle a few mm and stimulating the other kind of fibre to the same spindle. A subsequent testing stretch then elicited two bursts, one at the beginning and one in the middle of the stretch.