Dynamic Gamma Axons Research Articles

Static and dynamic γ‐motor output to ankle flexor muscles during locomotion in the decerebrate cat

In locomotion, the flexor muscles of the leg are mainly concerned with the relatively constant task of raising the foot, whereas the extensors have the more variable task of support and propulsion at different speeds. This suggests that the way in which the fusimotor system works may differ between the two muscle groups. Observations previously made of the static and dynamic gamma-motor firing patterns in the ankle extensor medial gastrocnemius (MG) have therefore been repeated in the flexor tibialis anterior (TA). One or more single gamma-motor axons, dissected from a small filament of TA nerve, were recorded simultaneously with a number of single spindle afferents in dorsal rootlets. Cats were decerebrated and locomoted spontaneously on a treadmill. Identification of each gamma-motor axon depended on relating the changes in firing caused by midbrain stimulation to the changes in static and dynamic behaviour of the spindle afferents in response to repetitive ramp and hold stretches. Static gamma axons all showed a smooth modulation in frequency, increasing in phase with muscle shortening, superimposed on a minimum frequency of about 20-30 impulses s(-1). Dynamic gamma axons showed interrupted firing with the frequency rising abruptly from zero at the onset of shortening, and falling again to zero shortly after the onset of lengthening. The frequency during the active periods was relatively constant, even when movement amplitudes varied. The basic similarity in the static and dynamic gamma discharge patterns for the two muscles suggests that the strategy of gamma-motor control is common to both flexors and extensors. The static gamma pattern is thought to be a 'temporal template' of the expected movement, effectively expanding the dynamic response range of the spindles in active movements. The dynamic gamma pattern sensitizes the primary afferents to detect the onset of muscle lengthening and to detect departures from the intended movement trajectory.

Effects of immobilizing the cat peroneus longus muscle on the activity of its own spindles.

The peroneus longus muscle of 10 cats were immobilized by fixating the distal tendon on the fibula at one of two length: neutral (length for a 90 degrees flexion of the ankle joint; 5 cats) or short (length for a full extension of the joint; 5 cats). Spindle afferent discharges were studied after 2 (4 cats) or 5 wk (6 cats) of immobilization and compared with those of four control animals. In each muscle, the discharges of nearly all primary and one of secondary muscle spindle endings were recorded during 2-mm ramp-and-hold stretches applied at different initial muscle lengths. A very slight increase in both the static discharge and the dynamic index of primary endings was observed in passive spindles. The increase in connective tissue that occurs in immobilized muscle and reduces muscle compliance was likely the sole alteration responsible for this constant effect. The responses to stretches of primary endings during stimulation of static and dynamic gamma-axons were not altered. Muscle immobilization at short length, even if spindle properties are not altered, can be expected to reduce the overall amount of group Ia afferent impulses with possible long-term changes on motoneuron properties.

Where in the muscle spindle is the resting discharge generated?

This is a report of experiments on muscle spindles of the soleus muscle of the anaesthetized cat. Following a step shortening of the muscle, muscle spindles fall silent. At suitable muscle lengths their discharge may restart several seconds later to gradually recover a maintained rate of discharge. These experiments examine the question of where within the spindle the resumption of a resting discharge may originate. It was found that stimulation of some static fusimotor fibres immediately after the shortening led to early recovery of the resting discharge. Stimulation of dynamic and other static gamma motoneurones had much less effect. Since the dynamic gamma axons innervate almost exclusively the bag1 intrafusal fibre, contraction of this fibre appears to have little influence on the mechanisms responsible for restarting the resting discharge. Bag2 and chain fibres do seem to be involved. For primary endings, the bag2 fibre contraction was especially effective since static axons, which did not evoke 'driving' of the afferent response, and which are thought to predominantly innervate bag2 fibres, did restart the resting discharge. For secondary endings, stimulation of nearly all gamma axons led to an early restart of the resting discharge suggesting that here the nuclear chain fibres were responsible.

Responses of cat peroneus brevis muscle spindle afferents during recovery from nerve-crush injury.

The responses of regenerated muscle spindle afferents to ramp-and-hold stretch of the peroneus brevis muscle in the cat were recorded at periods from 26 to 140 days after crushing the common peroneal nerve. During the early stages of recovery a number of abnormally responding afferents were observed. The most marked abnormality was the absence or rapid failure of firing during the held phase of the stretch. The proportion of abnormal afferents became less as recovery progressed. Electrical stimulation of isolated static and dynamic gamma-axons increased the firing rates of the afferents during the ramp-and-hold stretch such that a gamma static axon would restore the response of an abnormal afferent to the held phase of the stretch. The regenerated afferents have been classified according to the degree of abnormality displayed. These abnormalities can be accounted for by assuming a subtractive reduction in the firing frequency of the regenerated afferents. This is attributed to an increase in the pacemaker threshold.

Temporal characteristics of the sensitivity-enhancing after-effects of fusimotor activity on spindle la afferents

The after-effects of fusimotor stimulation which enhance dynamic sensitivity of spindle Ia afferents have been further investigated. The response to small sinusoidal movements was increased during muscle lengthening, following stimulation of single static or dynamic gamma-axons at resting length. This effect could be elicited by low rate stimulation during less than one second, and it persisted for up to two minutes. It might therefore be relevant for the control of spindle sensitivity during postural tasks.

Identification of intrafusal muscle fibres activated by single fusimotor axons and injected with fluorescent dye in cat tenuissimus spindles.

1. Intrafusal muscle fibres of cat tenuissimus spindles have been injected with the fluorescent dye Procion Yellow and identified histologically after recording their changes in membrane potential during 1/sec stimulation of single static or dynamic gamma axons. 2. Thirteen intrafusal muscle fibres innervated by static gamma axons were identified as eight bag2 and five chain fibres. The fact that none proved to be a bag1 fibre is not regarded as significant, for reasons given in the Discussion. 3. In one spindle Procion Yellow was injected into two intrafusal muscle fibres activated by the same static gamma axon; they were identified as a bag2 and a chain fibre. 4. Nine intrafusal muscle fibres innervated by dynamic gamma axons were identified as seven bag1 fibres, one bag2 fibre, and one long chain fibre. 5. In one spindle two bag fibres were injected, one activated by a dynamic gamma axon, the other by a static gamma axon; the former proved to be a bag1 fibre, the latter a bag2 fibre. 6. Stimulation of static gamma axons elicited junctional potentials in seven bag2 fibres and one damaged chain fibre, and action potentials in one bag2 and four chain fibres. In the whole sample of impaled intrafusal muscle fibres (identified and unidentified) activated by static axons, junctional potentials were recorded from twenty-three (62.2%), and action potentials from fourteen (37.8%). Stimulation of dynamic gamma axons always elicited junctional potentials. 7. In a number of instances it was possible to examine the ultrastructure of motor endings belonging to the stimulated gamma axon. The myoneural junctions of trail endings supplied by static gamma axons to bag2 and chain fibres were both smooth and folded; the deepest and most regular folding occurred on chain fibres. The terminals of p2 plates supplied to bag1 fibres by dynamic gamma axons had smooth myoneural junctions.

Control of dynamic and static nuclear bag fibres and nuclear chain fibres by gamma and beta axons in isolated cat muscle spindels.

1. The behaviour of nuclear bag and nuclear chain intrafusal fibres in isolated cat muscle spindles with a blood supply, during stimulation of dynamic gamma axons, dynamic beta axons, or static gamma axons in ventral root filaments was observed and recorded on still and moving film. 2. Most spindles were controlled by one dynamic gamma axon (sometimes a beta axon) and three static gamma axons, one of which was often non-selective in distribution. A large majority of fusimotor axons controlled one pole of the spindle only. 3. Dynamic gamma and beta axons produced focal contraction in only one of the two nuclear bag fibres in any spindle and this fibre was never activated by static gamma axons. Maximal tetanic contraction was attained slowly and the primary sensory spiral on this fibre was stretched by a small amount only. This fibre has been named the 'dynamic nuclear bag fibre'. 4. Static gamma axons produced either: (a) focal contraction in the second of the two nuclear bag fibres only; (b) local contraction in the bundle of nuclear chain fibres only; or (c) contraction in one nuclear bag fibre and the nuclear chain fibres together. Maximum tetanic contraction of this nuclear bag fibre stretched its primary sensory spiral considerably and the time to plateau was relatively short. This fibre has been named the 'static nuclear bag fibre'. 5. 'Driving' of the Ia afferent discharge could always be produced by non-selective static gamma axons, frequently by static gamma axons controlling nuclear chain fibres alone, and was probably due to mechanical oscillation in nuclear chain fibres. It was never produced by dynamic gamma axons and on one occasion only by a static gamma axon controlling a nuclear bag fibre alone. 6. The conduction velocities of dynamic gamma and static gamma axons overlapped extensively, though dynamic gamma axons were absent from the lower end, and static gamma axons innervating nuclear chain fibres only were absent from the upper end, of the range of velocities. 7. The observations are correlated with spindle structure and histochemistry. Dynamic and static nuclear bag fibres are shown to correspond with 'bag1 fibres' and 'bag2 fibres', respectively (Ovalle & Smith, 1972). 8. The possible origin of the dynamic and static actions of fusimotor axons and the role of the dynamic and static intrafusal systems in motor control are discussed.

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.

Cinematographic analysis of contractile events produced in intrafusal muscle fibres by stimulation of static and dynamic fusimotor axons.

1. Muscle spindles with an intact blood supply and uninterrupted connexions with ventral and dorsal spinal roots (Bessou & Pagés, 1967, 1972) have been prepared in cat's tenuissimus muscles with the aim of cinephotographically recording intrafusal movements induced by the stimulation of single static or dynamic gamma axons; the time cours of these movements and the morphological kind of activated intrafusal muscle fibres have been established. 2. Displacements of spindle guiding marks in the equatorial region elicited by stimulating single static gamma axons are 4-20 times greater in amplitude than the ones elicited by stimulating dynamic gamma axons at the same frequency. 3. The dynamic gamma axons induced a contraction only in nuclear bag fibres which, in addition, never received any static gamma innervation. The static gamma axons evoked contractions either in nuclear bag fibres alone, or in nuclear chain fibres alone, or in both types of intrafusal fibres. Two thirds of static gamma axons supplied nuclear bag fibres. For various reasons, one half only of static gamma axons innervating nuclear bag fibres could be shown to simultaneously innervate nuclear chain fibres. Consequently, about one third of static gamma axons supplied both nuclear bag fibres and nuclear chain fibres, but it is highly probable that this latter figure is an underestimate. One third of static gamma axons produced contraction in nuclear chain fibres only. In this work, the distribution of fusimotor axons has been established in only one muscle spindle of the cluster of muscle spindles that each fusimotor axon is generally innervating. 4. Generally speaking, a static gamma axon elicits contraction of several intrafusal fibres whereas a dynamic gamma axon innervates only one intrafusal fibre and frequently only one pole of the fibre. 5. One third of static gamma axons evoked contractions in nuclear chain fibres that seemed to involve the whole pole. The other static gamma axons and all dynamic gamma axons produced, in the intrafusal fibres that they supplied, one or several foci of localized contractions. 6. The nuclear chain fibres contract and relax faster than nuclear bag fibres. The contractions of nuclear bag fibres supplied by static gamma axons are stronger and faster than those of nuclear bag fibres innervated by dynamic gamma axons. Nearly all nuclear bag fibres innervated by static gamma axons, like the nuclear chain fibres, show transient contractions at each pulse of a stimulation at low frequency (2-20/sec). 7. The results are discussed taking into account the available anatomical and physiological data on the muscle spindle. Their consequences with regard to intrafusal working are briefly considered.

Proportion of muscles spindles supplied by skeletofusimotor axons (beta-axons) in peroneus brevis muscle of the cat.

Of 32 cat peroneus brevis spindles, 23 (72%) were found to be supplied by a least 1 skeletofusimotor or beta-axon. A motor axon was identified as skeletofusimotor when repetitive stimulation of it elicited both the contraction of extrafusal muscle fibers and as acceleration of the discharge of primary ending, which persisted after selective block of the neuromuscular junctions of extrafusal muscle fibers. The block was obtained by stimulating single axons at 400-500/s for a few seconds. Of 135 axons supplying extrafusal muscle fibers, 24 (18%) were shown to be beta-axons; 22 beta-axons had conduction velocities ranging from 45 to 75 m/s. All but three beta-axons increased the dynamic sensitivity of primary endings. Beta-innervated spindles may also be supplied by dynamic gamma-axons.

The incidence and properties of beta axons to muscle spindles in the cat hind limb.

The distribution of beta axons to muscle spindles in the tenuissimus and abductor digiti quinti medius (A.D.Q.M.) muscles of the hind limb of the cat was determined by testing the action of single motor axons, capable of producing extrafusal contraction, isolated in the ventral spinal roots on the discharges of individual muscle spindle primary sensory endings recorded in the dorsal spinal roots. The proportion of spindles with beta innervation was 41% in A.D.Q.M. and 30% in tenuissimus. The proportion of fast motor axons that were beta axons was 28% in the A.D.Q.M. and 11% in tenuissimus; usually each beta axon innervated a single spindle while no spindle received more than two beta axons. The beta axons were dynamic in nature and those to any one muscle tended to have slightly lower conduction velocities than the alpha axons though some overlap did occur. The extent to which beta axons can account for the fact that in isolated spindles axons selective to either nuclear bag or nuclear chain fibres are found in about equal proportions whereas a ratio of three static to one dynamic gamma axons is found electrophysiologically is discussed. An explanation for the low incidence of beta innervation previously found electrophysiologically and the considerably higher incidence found histologically is given.