F Emonet-Dénand

Types of intra- and extrafusal muscle fibre innervated by dynamic skeleto-fusimotor axons in cat peroneus brevis and tenuissimus muscles, as determined by the glycogen-depletion method.

1. The types of intra‐ and extrafusal muscle fibre innervated by dynamic skeleto‐fusimotor (beta) axons were determined by using a modification of the glycogen‐depletion method of Edström & Kugelberg (1968) combined with histochemical tests for various enzyme reactions. A single beta axon was prepared in each of the experiments, which were carried out on six peroneus brevis and two tenuissimus muscles. 2. The intrafusal distribution of dynamic beta axons is almost exclusively restricted to bag1 fibres. The bags fibre was depleted in each of twenty‐four beta‐innervated spindle poles; the only fibres of a different type depleted intrafusally were a bag2 fibre in one pole and a long chain in another. 3. Depletion in the bag1 fibres was usually restricted to one zone in one pole, generally in a mid‐polar location. 4. The extrafusal muscle fibres depleted by dynamic beta axons belong to the slow oxidative type as defined by Ariano, Armstrong & Edgerton (1973). The number of such fibres in each motor unit could not be accurately determined, but is almost certainly small. 5. The slow oxidative muscle fibres innervated by dynamic beta axons were not depleted over their entire length. Since there is no reason to assume that they are not twitch fibres, it would seem that the localized depletions result from the conditions required to obtain glycogen depletion, i.e. long periods of motor stimulation applied during the occlusion of the muscles blood supply. Under similar experimental conditions depletion of glycogen was also restricted to portions of fibres in fast oxidative‐glycolytic motor units, but extended over most of the length of the fibres in fast glycolytic units.

Proportion of fatigue‐resistant motor units in hindlimb muscles of cat and their relation to axonal conduction velocity.

1. A study of motor units to hindlimb muscles of cat has been made, with as complete a sample as possible of the motor axons to an individual muscle. In single experiments as much as 95% of the motor supply to a muscle has been examined. 2. The following muscles have been studied: peroneus brevis, peroneus tertius, peroneus longus, plantaris, gastrocnemius medialis, soleus, tenuissimus and lumbricalis superficialis. 3. Units were identified as slow resistant (S), fast resistant (FR), fast fatigable (FF) and fast intermediate (FI). The proportion of various motor unit types differs from one muscle to another. There is also some variation in the proportions to a given muscle from one animal to another. With the exceptions of soleus, which is entirely slow resistant, and gastrocnemius, which has relatively fewer resistant units, most muscles contain 60% or more of resistant (S and FR) units. 4. The conduction velocity ranges of FF, FR and FI units overlapped. There was little overlap between the conduction velocity ranges of these F units and of S units. 5. In individual experiments there was a strong and significant positive correlation between the logarithm of maximal tetanic tension and axonal conduction velocity in S and in S+FR units. In terms of contractile response the total fatigue‐resistant population appeared to be a continuum. The correlation coefficient between maximal tetanic tension and conduction velocity was also high in the totality of units of all types, although within the FF group there appeared to be little or no correlation. In pooled data there was much more scatter and these relations were less clear. This resulted largely from differences in the ranges of axonal conduction velocity for a given motor unit type from one animal to another. 6. There was a highly significant negative correlation between isometric twitch contraction time and axonal conduction velocity in individual experiments. This relationship could also be seen, but less clearly, in pooled data. 7. The possible bases for these relationships are discussed.

Effects of stretch on dynamic fusimotor after‐effects in cat muscle spindles.

Conditioning stimulation of dynamic fusimotor axons leaves persistent after‐effects which increase the responses of primary endings to test dynamic stimuli. Such after‐effects are abolished by muscle stretch. Destruction of these after‐effects depends on the following. (a) Amplitude of stretch: with symmetrical triangular stretches of moderate velocity, an extension of soleus by 4‐5 mm totally abolishes the after‐effects. Lesser stretches cause a graded reduction. (b) Velocity of relaxation: for a given amplitude of stretch there is greater destruction of after‐effects when it is followed by a slow rate of relaxation than after rapid relaxation. (c) After‐effects tested late in ramp stretch are more resistant to destruction by stretch than those increasing test dynamic responses early in ramp stretch. Stretch itself produces after‐effects which enhance test responses to dynamic but not to static fusimotor stimulation. Interactions between conditioning dynamic stimulation and stretch suggest that both these effects occur in the same intrafusal elements, the bag fibres.

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 γ 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 γ axon was then determined, and the distribution of its endings ascertained in teased, silver preparations.

Skeleto-fusimotor axons in the hind-limb muscles of the cat.

1. Motor axons supplying various hind‐limb muscles of the cat (flexor hallucis lingus, peroneus brevis, peroneus digiti quinti, tibialis anterior, soleus and tenuissimus) were identified as skeleto‐fusimotor or beta axons because their repetitive stimulation elicited both the contraction of extrafusal muscle fibres and an increase in the rate of discharge of spindle primary endings which perisited after selective blockade of extrafusal neuromuscular junctions. 2. The conduction velocity of these axons ranged from 39 to 92 m/sec. 3. Of seventy‐six beta axons, seventy‐two had a dynamic action on the sensitivity to velocity of stretching of primary endings, four had a static action. 4. The dynamic action of six beta axons was observed only after the contraction of extrafusal muscle fibres was selectively suppressed. 5. Tendon organs can be activated by beta motor units.

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.

Summation of tension in motor units of the soleus muscle of the cat

In the cat soleus muscle which is exclusively composed of slow motor units the discrepancy between the sum of individual tensions and the tension on combined stimulation of several motor units was found to be much less than previously reported for slow motor units of peroneus longus. In peroneus the tension on combined stimulation was systematically larger than the value predicted from the sum of individual tensions. For both muscles it was possible to reduce the difference between observed and expected values by comparing the tension on combined stimulation with the sum of tensions, not of single motor units, but of groups of units. It is concluded that whenever tension is measured for single motor units, especially slow units in mixed muscles, the values obtained may be modified by frictional forces. The size of the effect appears to vary from one preparation to the next.

Fusimotor after‐effects on responses of primary endings to test dynamic stimuli in cat muscle spindles.

Conditioning stimulation of individual dynamic fusimotor axons, either gamma or beta, leaves after‐effects which enhance the responses of primary endings to test stimulation of the same axon applied during slow ramp stretch. These after‐effects have a long duration, persisting well over 5 min, but are abolished by stretch of large amplitude. The dynamic after‐effects also enhance frequencygrams elicited by low‐frequency repetitive stimulation during slow ramp stretch, causing single stimuli to become much more effective. When several dynamic axons to the same spindle are isolated, conditioning stimulation of one leaves an after‐effect to test stimulation of itself and of all other dynamic axons. When two dynamic axons are used for conditioning stimulation, facilitation or occlusion can be demonstrated in their interaction, indicating that they converge on the same intrafusal element. Dynamic after‐effects persist during background static fusimotor activity of considerable amplitude, suggesting that static and dynamic actions are quite independent. Dynamic after‐effects appear to result from residual changes in the bag fibre, probably from a persistent increase in the number of cross‐bridges between thick and thin filaments. These after‐effects produce a large increase in the response of primary endings to dynamic fusimotor activity and probably have an important functional role.

Comparison of skeleto‐fusimotor innervation in cat peroneus brevis and peroneus tertius muscles.

1. The skeleto‐fusimotor or beta innervation was compared in cat peroneus brevis and peroneus tertius muscles, which differ in their composition of fatigue‐resistant motor units; the slow (S) units predominate in brevis and the fast units (FR) in tertius. 2. In four brevis muscles, of thirty‐four beta‐axons (from a total of 114 axons supplying extrafusal muscle fibres) twenty‐nine were dynamic (beta D) and only five static (beta S). In contrast, in three tertius muscles, of twenty‐five beta‐axons (from a total of 82 axons) twelve were static and thirteen dynamic. 3. In a population of thirty‐five brevis and thirty tertius spindles, the proportion of beta D‐innervated spindles was greater in the brevis (68.5%) than in the tertius (50%) whereas that of beta S‐innervated spindles was greater in the tertius (40%) than in the brevis (17.1%). In a population of thirty‐two brevis and twenty‐seven tertius spindles in which the presence of bag1 fibres was deduced from the existence of a dynamic innervation, the proportion of spindles innervated by beta D‐axons was 80% in the brevis and 62% in the tertius. 4. In both muscles, the number of beta D effects was greater than that of beta S effects. beta S‐axons were rarely found to supply more than one spindle whereas beta D‐axons supplying more than one spindle (up to four) were common. Spindles were often coinnervated by beta D‐ and beta S‐axons.(ABSTRACT TRUNCATED AT 250 WORDS)

Incidence of non‐driving excitation of Ia afferents during ramp frequency stimulation of static gamma‐axons in cat hindlimbs.

1. The aim of this investigation was to identify static gamma‐axons which do not drive any Ia afferents at any stimulus frequency in any spindle which they supply, and to determine their occurrence in various hindlimb muscles (peroneus tertius, brevis, longus and tenuissimus). 2. Ia responses to static gamma stimulation were classified as ‘non‐driven’ when the discharge did not follow the stimulation frequency, or its subharmonics, at any time during a linear increase in stimulus frequency up to 150 Hz lasting 2‐3 s, and when tested at two muscle lengths‐‐except in the tenuissimus muscle. In almost all experiments, cross‐correlograms were used in addition to evaluate the percentage of these ‘non‐driven’ responses in which a time‐locking of discharge to stimulus pulses was obscured by irregularity of the Ia discharge. 3. In 104 spindles, out of 347 responses to stimulation of single static gamma‐axons 332 (93%) could be characterized, and of these, 57% (183) were of the non‐driven type. The mean number of static gamma effects characterized per spindle was 4.1 (fourteen experiments). In the large majority of spindles (79%, 82 out of 104) at least one response was of the non‐driven type. 4. Of the static gamma‐axons studied 16% were called ‘non driving’ (‘ndr’ gamma s‐axons) because they elicited non‐driven effects, and since they had the same qualitative effect consistently in all spindles whose discharge was modulated by stimulating them they were called specific ‘ndr’ axons. If axons with non‐driven effects, but acting on one spindle were included in the ‘non‐driving’ category the proportion was 23%. Of spindles tested 63% were innervated by at least one ‘ndr’ axon. 5. Absence of Ia driving during ramp frequency stimulation of gamma s‐axons has been equated with selective bag2 contraction. All the non‐driven responses identified in this study cannot be attributed to exclusive bag2 involvement because the total number of ‘ndr’ responses was too high. In fact, in the isolated spindle preparation bag2 and chain co‐contraction were shown to elicit non‐driven responses, so chain contraction is not detected reliably in all experimental conditions. Possibly chain fibre contraction is sometimes too weak to dominate the response, or can be of a non‐driving character.(ABSTRACT TRUNCATED AT 400 WORDS)