Effects of skin cooling and warming on stretch responses of the muscle spindle primary and secondary afferent fibers from the cat's tibialis anterior

Fusimotor activation induced by thermal stimuli to the skin was investigated by recording the stretch responses of primary as well as secondary spindle afferent fibers from the tibialis anterior of the barbiturate-anesthetized, spinal cats. A standard rampand-hold stretch was repeatedly given during warming or cooling (20 to 40°C) the skin of the ipsilateral foot pads. In each response of the spindle afferent fiber to stretch, the peak (P) and static firing rates (S) were measured and the dynamic index was calculated to assess the type of fusimotor fiber influence as dynamic or static. Of 47 primary spindle afferent fibers, 22 (46%) were affected by changes in skin temperature. Cooling of the skin below a certain temperature produced a marked increase in the dynamic sensitivity of their response to stretch, and this also occurred on warming above it. Such a “critical temperature” at which a directional relationship between skin temperature and muscle spindle activity was completely altered was determined (mean ± SD: 35.10 ± 1.66°C, N = 7). However, a marked increase in static firing accompanied by a significant decrease in the dynamic index was observed at the dynamic phase of heating the skin beyond the critical temperature. None of the seven secondary afferent fibers studied showed a detectable temperature response. We conclude that the activation of primary spindle afferent fibers by thermal stimulation of the skin is to be attributed predominantly to activation of dynamic fusimotor neurons and is significant for the initiation of cold shivering.     

Sharing of sensory terminals between the dynamic bag1 and static bag2 fibers in the rat muscle spindle

The nuclear bag1 intrafusal fiber mediates the dynamic (velocity) sensitivity, whereas the nuclear bag2 and nuclear chain fibers mediate the static (length) sensitivity of muscle spindles to stretch. The pattern of branching of primary and secondary afferents, the distribution of their terminals to the 3 types of intrafusal fibers, and the incidence of sensory cross-terminals were determined by reconstruction of 4 spindles from serial 1-micron and ultrathin transverse sections of rat extensor digitorum longus muscles. A single primary afferent supplied each spindle, and secondary afferents innervated intrafusal fibers in 3 spindles. Only static intrafusal fibers shared cross-terminals of the secondary afferents. In contrast, the dynamic bag1 and static bag2 fibers of each spindle shared at least one terminal of the primary afferent. Cross-terminals shared by the dynamic bag1 and static bag2 fiber parallel the presence of fusimotor (gamma) axons which coinnervate these types of intrafusal fibers in muscle spindles of rats. Consequently, the greater degree of overlap of elements comprising the dynamic and static systems of spindles of the rat relative to that of the cat reduces the probability of generating a purely dynamic or purely static response to an applied stretch.     

Effects of changes in pH on the afferent impulse activity of isolated cat muscle spindles

Muscle spindle activity has been shown to decrease in the sustained contracting muscle. The effect has been assumed to result from a declining fusimotor drive. Since accumulation of metabolites including H(+), lactate and CO(2) might also affect the receptor in the fatiguing muscle, the impulse activity of muscle spindles isolated from the cat tenuissimus muscle was characterized under varying degrees of extracellular pH, thus excluding any effect on fusimotor activity, blood supply and extrafusal muscle fibers. The isolated receptor was exposed to bathing fluids of pH 6.4, 7.4 and 8.4, and afferent discharge activity was recorded from the spindle nerve. Both primary and secondary endings responded similarly to changes in pH. Resting discharge frequency usually decreased with decreasing pH and increased with increasing pH. A sudden break-off in activity was observed with about 40% of primary endings and about 30% of secondary endings at pH 6.4. Experiments with slow stretch stimulation indicated that this effect was caused by a rising threshold of firing at the encoder site of the endings. With brief ramp-and-hold stretches, we tested the effects of changes in pH on the dynamic and static sensitivity of primary and secondary endings. When pH was reduced from 7.4 to 6.4, the initial burst activity at the beginning of the ramp phase increased in primary and secondary endings and the dynamic response increased in secondary endings, demonstrating that the dynamic properties of muscle spindle endings were usually augmented in the acidic milieu. The static properties rose as well because the static index of both types of ending increased significantly. By contrast, dynamic and static properties of both primary and secondary endings decreased significantly, when pH was increased from 7.4 to 8.4. The amplitude of tension that was measured during the passive stretch stimuli very slightly decreased in the acidic solution and very slightly increased in the alkaline solution. The decrease in the resting discharge activity at low pH supports those previous observations, which demonstrate a reduced peripheral input from muscle spindle afferents to the spinal motor nuclei during fatigue in the isometric contracting muscle. The present finding indicates that an attenuated afferent discharge is not only caused by a decreasing central activation of gamma-motorneurons, but may additionally be supported by a direct effect of protons on the muscle receptor itself. The accompanying augmentation of stretch sensitivity is suggested to correspond to the well-known increase in physiological tremor during exhaustive exercise.     

Re-afferent effects of individual static and dynamic gamma-stimuli during maintained fusimotor stimulation

The ability of maintained dynamic and static fusimotor stimulation to modulate the primary afferent response of the muscle spindle in the rhythm of gamma-stimulation was investigated using a highly sensitive method for modulation detection. The effect of 41 gamma-fibers (13 dynamic; 28 static) on 38 primary afferents obtained from the tibialis anterior muscle of the cat was studied. It was found that maintained stimulation of 10 out of the 13 dynamic (77%) and of 25 out of the 28 static (89%) gamma-fibers could evoke significant modulations of the primary afferent response in the rhythm of fusimotor stimulation at a minimum of one stimulation rate. Moreover, both static and dynamic gamma-stimulations could evoke significant primary afferent modulations almost over the entire range of stimulation rates studied (30-300 stimuli per second). These results show that both gamma-systems can modulate the primary afferent response in the rhythm of fusimotor stimulation over a wide range of stimulation rates; thus the central nervous system may be provided with re-afferent information about the effect of each individual gamma-motoneuron discharge. Some hypotheses for the internal spindle mechanism responsible for the afferent modulations are discussed.     

Time-dependent fusimotor effects on the discharge of cat primary muscle spindle afferents induced by a long-lasting succinylcholine infusion

The responses of 46 la afferents from the tibial anterior muscle of the cat to repetitive ramp-and-hold stretches were investigated under a succinylcholine (SCh) infusion of 120 μg · kg⁻¹ · min⁻¹ lasting 15 to 25 min. It was possible to distinguish four consecutive phases of the effect of the SCh on the responsiveness of the la afferents. The first three of these four phases have already been described. We analysed in more detail the changes from Phase III to the end of Phase IV. Static fusimotor effects were dominant in the discharge patterns obtained during Phase III; dynamic fusimotor effects prevail at the end of Phase IV. Our observations were quantified by comparing the mean values of initial activity, final static value, dynamic response and slow receptor adaptation read from the discharge patterns obtained during Phase III with the mean values of the same parameters obtained from discharge patterns from the end of Phase IV: the two mean values were significantly different for each of the four measurements. This change from Phase III to the end of Phase IV is highly specific for each spindle. To demonstrate this spindle specificity, discharge patterns were selected from among those produced by each la afferent in Phase III and at the end of Phase IV. Each of these discharge patterns was assigned to one of six categories. Category I displays purely dynamic fusimotor effects and Category VI purely static fusimotor effects. Categories II, IV and V display combinations of static and dynamic fusimotor effects with an increasing admixture of static fusimotor effects. The spindle-specific change from Phase III to the end of Phase IV is defined in terms of the specific degree of change from a higher-number to a lower-number category in the case of each of the 46 la afferents. In the discussion a combination of activity by the two nuclear bag fibres of a spindle is deduced from the specific discharge pattern of each category. The conclusion from these considerations is that results obtained from the administration of SCh have to be interpreted with great caution in making any statement about the existence of a dynamic bag₁ fibre in a spindle.     

Static and dynamic fusimotor interaction and the possibility of multiple pace-makers operating in the cat muscle spindle

The interaction of static and dynamic fusimotor activation on the firing of primary muscle spindle afferents has been studied in the cat soleus muscle at constant length and during sinusoidal stretching. Cycle histogram analysis revealed summation of static and dynamic action during the peak of the afferent response to sinusoidal stretching, while static action completely occluded the dynamic effect during the trough of the response. Occlusion was complete as long as, for single fusimotor activation, the static-induced trough response exceeded the dynamic-induced one by about 25%. The investigation of inter-spike interval distributions obtained at constant muscle length revealed occlusion of dynamic by static action in 8 out of 13 cases. A model of multiple spike generation in primary spindle afferents is considered which is based on two or more pacemakers arranged in parallel, with a common pacemaker in series.     

Re-afferent effects of individual static and dynamic γ-stimuli during maintained fusimotor stimulation

The ability of maintained dynamic and static fusimotor stimulation to modulate the primary afferent response of the muscle spindle in the rhythm of γ-stimulation was investigated using a highly sensitive method for modulation detection. The effect of 41 γ-fibers (13 dynamic; 28 static) on 38 primary afferents obtained from the tibialis anterior muscle of the cat was studied. It was found that maintained stimulation of 10 out of the 13 dynamic (77%) and of 25 out of the 28 static (89%) γ-fibers could evoke significant modulations of the primary afferent response in the rhythm of fusimotor stimulation at a minimum of one stimulation rate. Moreover, both static and dynamic γ-stimulations could evoke significant primary afferent modulations almost over the entire range of stimulation rates studied (30–300 stimuli per second). These results show that both γ-systems can modulate the primary afferent response in the rhythm of fusimotor stimulation over a wide range of stimulation rates; thus the central nervous system may be provided with re-afferent information about the effect of each individual γ-motoneuron discharge. Some hypotheses for the internal spindle mechanism responsible for the afferent modulations are discussed.     

Static and dynamic fusimotor action on the response of spindle primary endings to sinusoidal stretches in the cat

In anaesthetized cats, the discharge of single spindle primary endings of flexor and extensor muscles was studied during sinusoidal stretches of the muscle (3–4 mm peak-to-peak, 1–5 Hz). In the response to each stretch, two main components could be distinguished; they were related respectively to the speed and to the amplitude of lengthening. By analogy with the usual definitions of the ‘dynamic index’ (d) and ‘position sensitivity’ (s) during ramp stretches of the same amplitude at a velocity of 35–60 mm/sec, a ‘sinusoidal dynamic index’ (D) and a ‘sinusoidal position sensitivity’ (S) were defined. Stimulation of dynamic fusimotor fibres increased D and d, S and s, while stimulation of static fusimotor fibres decreased D and d and had a less consistent effect on S and s. The total frequency variation during a sinusoidal stretch was always increased by a dynamic fusimotor action while it could be either decreased or increased by a static fusimotor action, depending on the stretch frequency and on the rate of fusimotor stimulation. These results were obtained in various muscles, without any significant difference related to their flexor or extensor function. It is concluded that in order to identify a fusimotor effect as static or dynamic during sinusoidal muscle stretch, it is necessary to use, as here, stretch parameters which elicit a dynamic component in the primary afferent response.     

Discharges of forelimb spindle primary afferents during locomotor activity in the decorticate cat

In the acute decorticate cat, the discharge patterns of single spindle primary afferents from various forelimb muscles during locomotion have been examined in relation to the extrafusal activity. In a given muscle under isometric conditions, the activation of spindle primary endings was closely related to that of extrafusal muscle fibers. Since this increase in spindle discharge could occur in the absence of detectable electromyographic activity in the parent muscle, it resulted, at least to some extent from an enhanced activity in gamma efferents. The data are discussed in relation to previous studies of forelimb efferent activity and hindlimb fusimotor control in the same preparation.     

Changes in fusimotor outflow during vibration-induced contraction of triceps surae muscles in decerebrate cats

Changes in fusimotor outflow in medial gastrocnemius and lateral gastrocnemius plus soleus nerves were investigated during vibration-induced contraction of triceps surae muscles in decerebrate cats. A sustained increase in spike occurrence appeared in 33 of 58 investigated neurons, and a decrease in 13. Transient changes of an opposite sign occurred in 19 excited and 6 inhibited fusimotor neurons during the rising phase of reflex muscle contraction. The later changes appeared coincidently with silence in the electromyogram. Thus the discharge of one-third of the examined fusimotor population directed to the triceps surae muscles was modulated parallelly with that of the skeletomotor neurons. It is supposed that the changes in fusimotor spike occurrence during the rising phase of reflex muscle tension are induced mainly by changes in afferent input from muscle spindle primary endings and/or Golgi tendon organs. We could not ascertain whether the different responses (excitation vs inhibition) are related to fusimotor type or to changes in transmission through the reflex pathways. The possible influence of the changes in fusimotor outflow on muscle spindle pause and the silent period in skeletomotor discharge at the beginning of reflex muscle contraction induced by vibration is considered.     

‘Fusimotor set’: new evidence for α-independent control of γ-motoneurones during movement in the awake cat

The discharge activity of single muscle spindle receptors was recorded in freely moving cats. Large changes in responsiveness to length variations was observed in different types of movement. In separate simulations on anesthetised cats, the activity of the γ-fusimotor neurones responsible for these changes was reconstructed. The results suggested that fusimotor action on a given spindle afferent during the movements studied was not rigidly α-linked, but ‘set’ by the CNS to steady levels, and that it could switch from largely static (γ_s) to largely dynamic (γ_d) according to the motor tasks performed.     

Effect of catechol on the discharge of muscle spindle afferents from the hind limb of the rat

Previous work had shown that some of the effects of catechol could be via the fusimotor system. In order to determine the extent of fusimotor involvement, recordings have been made from muscle spindle afferents in split dorsal root filaments of anaesthetised rats. Catechol failed to excite de-efferented muscle spindles therefore eliminating many possible non-fusimotor effects. Over 80% of spindle afferents with intact efferents showed increased discharge frequency 1 min after injection, this increase often following a biphasic pattern with a pronounced pre-myoclonic burst and decline followed by a more sustained period of activity during the myoclonic phase. Analysis of spontaneous twitches or twitches evoked by ipsilateral auditory stimulation showed in addition a phasic increase in discharge suggesting alpha-gamma co-activation. Both primary and secondary afferents from many muscle groups around ankle and toes had their discharge frequencies elevated. Elevation of discharge frequencies of secondaries implies increased gamma-s activity confirmed by a decrease in dynamic index. Both gamma-d and gamma-s involvement in catechol action on primaries is suggested by dynamic index measurements. Perhaps a more continuous form of testing such as sinusoidal stretches would reveal any rapid switching between activities in the two systems.     

A new simulation method to deduce fusimotor activity from afferent discharge recorded in freely moving cats

Direct recordings from identified and classified fusimotor γ-motoneurons in freely moving animals have not so far been achieved, and present knowledge on fusimotor activity during natural movements is based on qualitative inferences made from spindle afferent discharge. In order to put such deductions on a firmer basis, a simulation method has been developed, which provides quantitative estimates of the fusimotor drive that shaped the spindle afferent discharge, as recorded in chronically implanted cats during voluntary or imposed movements. Simulations are performed in acute experiments on anesthetized cuts, whereby variations in muscle length and EMG envelopes are reproduced by an electromagnetic servo from digitally stored segments of the original records. The responses of spindle afferents to the simulated movements are then examined, both in the absence of fusimotor action and during concomitant stimulation of functionally single γ-motoneurons, rate modulated according to a variety of stored functions (including the original EMG envelope).     

Summation of responses of cat muscle spindles to combined static and dynamic fusimotor stimulation

This is a study of the process of interaction between the responses of muscle spindles to stimulation of two fusimotor fibres. Combined stimulation of a static and a dynamic fusimotor fibre supplying the same muscle spindle in the soleus muscle of the anaesthetised cat gave a response which was larger than from stimulating each fibre separately, but less than their sum. A similar summation process was observed with pairs of static fusimotor fibres. The mean summation coefficient for the responses to stimulation of 14 pairs of static fusimotor fibres was 0.29 (range 0.14–0.52; S.D. 0.09), while for 42 static:dynamic pairs it was 0.30 (range 0.07–0.89; S.D. 0.20). Mechanisms considered for the summation process were probabilistic mixing of impulse traffic from two or more impulse generators within the terminals of the primary ending of the spindle, the spread of generator current from one encoding site to another and mechanical interactions between contracting intrafusal fibres. In an experiment where single static and dynamic fusimotor fibres were stimulated together, and then stimulation of the static fibre stopped, the size of the continuing dynamic response was larger than when the dynamic fibre had been stimulated alone. This finding suggested some kind of mechanical interaction between the contracting intrafusal fibres and implies that static and dynamic fusimotor effects within a spindle cannot be considered to be entirely independent of one another.     

Invited review: Microneurography and applications to issues of motor control: Fifth annual stuart reiner memorial lecture

Among the hypotheses regarding fusimotor functions based on earlier animal experiments some are inconsistent, others are in conformity with microneurographic observations in man. The human data provide evidence against the following two theories: (1) the length follow-up servo theory; and (2) the theory that fusimotor neurons can be selectively activated to produce spindle sensitization and stretch reflex reinforcements. The human data support the theory of alpha–gamma coactivation. In particular, in the early phase of isometric voluntary contractions fusimotor-driven afferent spindle activity assists in autogenetic activation of alpha motoneurons and in reciprocal relaxation of antagonists. As muscle fatigue develops, the autogenetic reflex drive via the fusimotor route declines. The fusimotor bias during contraction provides for maintenance of spindle sensitivity to minute perturbations and for load-compensating reflex adjustments to such perturbations. Reflex overcorrections may lead to uncontrollable oscillations of the type seen in enhanced physiological tremor.     

Summing responses of cat soleus muscle spindles to combined static and dynamic fusimotor stimulation(1)

This is a study of the summation of responses of primary endings of muscle spindles to combined static and dynamic fusimotor stimulation in the soleus muscle of the anaesthetised cat. Summation, expressed as a summation coefficient, K, was measured under a variety of conditions including (1) at several, fixed muscle lengths using steady rates of stimulation, (2) using ramp-shaped increases in stimulation rates, (3) during passive stretches after muscle conditioning, and (4) during combined stretch plus stimulation. The predominant effect observed was occlusion, that is, the combined response was less than the sum of the two individual responses. The calculated mean K value for responses at fixed length was 0.156 (+/-0.005 S.E.M.). It was hypothesised that summation arose from electrotonic spread of generator current between the afferent terminals, either directly, or as a result of mechanical interactions between the contracting intrafusal fibres. Summation for responses from pairs of static fusimotor fibres gave a larger mean K value, 0.340 (+/-0.020 S.E.M.). These findings were interpreted in terms of a model of the muscle spindle where responses to dynamic fusimotor stimulation arise at one impulse generating site, and static fusimotor responses arise at another.     

Effects of the calcium antagonist nifedipine on the afferent impulse activity of isolated cat muscle spindles

The impulse activity of muscle spindles isolated from the cat tenuissimus muscle was investigated under varying concentrations of the L-type calcium channel blocker nifedipine. At a concentration of 25 microM nifedipine impulse activity was clearly diminished in both primary and secondary endings. However, low concentrations of the drug (5-10 microM) exerted unexpected excitatory effects. The dynamic properties of primary endings in particular were augmented; those of secondary endings were also increased, although only slightly. A detailed analysis of the afferent discharge patterns obtained under ramp-and-hold stretches yielded the following effects of 10 microM nifedipine. (1) The initial burst at the beginning of the ramp phase of a stretch was increased in primary endings; (2) the peak dynamic discharge frequency at the end of the ramp phase was considerably increased in most primary endings; (3) the sensitivity of the peak dynamic discharge value to varying amplitudes and velocities of stretch was significantly enhanced in primary endings, and also increased, although only slightly, in secondary endings; (4) the rise in the discharge frequency during the ramp phase of a stretch was augmented in both types of ending, the effect being again stronger in primary endings; (5) the fast adaptive decay of the impulse frequency following the ramp phase of a ramp-and-hold stretch was significantly increased in primary endings, but remained unaffected in secondary endings. The enhanced dynamic properties of primary endings were also observed under small sinusoidal stretch stimuli (10 microm, 40 Hz), where nifedipine induced a significant shift in the position of the 1:1 driven action potentials toward smaller phase values. In view of an increase in tension in the isolated muscle spindle and an increased initial burst in primary endings in the presence of nifedipine, it is suggested that the drug facilitates the attachment of cross-bridges in the poles of the intrafusal muscle fibers. The increase in the dynamic properties of primary endings points to the possibility that the drug preferentially affects the nuclear bag(1) fiber. The inhibitory effect on the afferent discharge rate at high doses of the drug is interpreted as the consequence of a calcium channel block in the membranes of the sensory endings. The membrane potential of sensory endings appears to be highly dependent on sustained Ca(2+) conductance.     

Summing responses of cat soleus muscle spindles to combined static and dynamic fusimotor stimulation

This is a study of the summation of responses of primary endings of muscle spindles to combined static and dynamic fusimotor stimulation in the soleus muscle of the anaesthetised cat. Summation, expressed as a summation coefficient, K, was measured under a variety of conditions including (1) at several, fixed muscle lengths using steady rates of stimulation, (2) using ramp-shaped increases in stimulation rates, (3) during passive stretches after muscle conditioning, and (4) during combined stretch plus stimulation. The predominant effect observed was occlusion, that is, the combined response was less than the sum of the two individual responses. The calculated mean K value for responses at fixed length was 0.156 (±0.005 S.E.M.). It was hypothesised that summation arose from electrotonic spread of generator current between the afferent terminals, either directly, or as a result of mechanical interactions between the contracting intrafusal fibres. Summation for responses from pairs of static fusimotor fibres gave a larger mean K value, 0.340 (±0.020 S.E.M.). These findings were interpreted in terms of a model of the muscle spindle where responses to dynamic fusimotor stimulation arise at one impulse generating site, and static fusimotor responses arise at another.     

Human muscle afferent responses to tendon taps. 2. Effects of variations in fusimotor bias.

The effect of varying the fusimotor bias on the muscle spindle responses to light tendon taps has been studied in normal human volunteers using surface electrodes at the wrist for recording whole nerve activity. Reinforcement manoeuvres were found to increase the sensitivity of the afferent responses to the mechanical stimulus. Such sensitisation was found to be exhibited more commonly as a decrease in the latency of the peak of the afferent waveform than as an increase in amplitude. Increase in amplitude of the response was seen in cases where the subject was well relaxed and the test muscle quiescent. A change in furimotor drive was also achieved by asking the subjects to close their eyes voluntarily during the test, thus depriving themselves of the visual feedback. The results under these conditions were found to be variable, though showing considerable changes from control recordings. The effect of reinforcement manoeuvres may perhaps result in increasing the dynamic fusimotor drive. Such an effect may be simulated on occluding the blood supply to the test muscle since ischaemia produces an immediate rise in the rate of afferent discharge. The method of recording is suggested as a convenient technique for clinical use.     

Joint angle signaling by muscle spindle receptors

Nerve impulses were recorded from sensory fibers supplying the tibialis anterior and soleus muscles of anesthetized cats as the ankle joint was moved from one end of the flexion-extension axis to the other and back again in steps of 6-7 degrees. The rate of movement from one position to the next was 40 deg/s and each position was held for 16-18 s. Plots were made of receptor discharge frequency as a function of ankle joint angle during joint movement (dynamic input-output (I-O) functions) as well as 2 and 15 s after movement terminated (2 and 15 s static I-O functions). Only receptors with a sustained (5s) static response within the physiological range were studied. A total of 229 tibialis anterior receptors met this criterion, of which 11 were identified as tendon organs. One hundred and five soleus receptors were studied, of which 6 were tendon organs. Thus tendon organ activity accounted for only a small part of the muscle afferent signal under passive conditions. The spindle receptors in soleus and tibialis anterior divided the ankle flexion-extension range about equally between them, those in soleus signaling over the flexion half of the range and those in tibialis anterior over the extension half. At angles where the receptors in a particular muscle did not signal joint angle, the tendon of the muscle was observed to be slack. Thus the total muscle afferent discharge in a relaxed animal is high at one end of the range, declines progressively as the ankle is displaced to an intermediate position, and then increases again as the joint moves toward the opposite end of the range. The spindle receptors within an individual muscle were recruited rather early as the muscle came under tension so that over most of a muscle's signaling range joint angle could have been coded by changes in receptor discharge frequency but not by which spindle receptors were active. To evaluate the information signaled by individual muscle spindle receptors, the following measurements were made from plots of impulse frequency vs joint angle: dynamic response, defined as the frequency difference between the dynamic and 2 s static I-O functions during muscle lengthening; adaptation, defined as the frequency difference between the 2 and 15 s static I-O functions during muscle lengthening.(ABSTRACT TRUNCATED AT 400 WORDS)