Spinal projection of spindle afferents of the longissimus lumborum muscles of the cat.

The connections and monosynaptic projections of muscle spindle afferents of individual heads of the longissimus lumborum have been studied in cats by natural stimulation, by electrical stimulation and by spike-triggered averaging from single identified afferents. The spindle afferents were classified by sensitivity to vibration and by the effect of succinylcholine on their response to ramp-and-hold muscle stretches. Axonal conduction and synaptic effects were recorded as field potentials and focal synaptic potentials during systematic exploration of the spinal cord in segments L1 to L4 with extracellular metal microelectrodes, singly and in linear arrays. Ascending branches of afferent axons within the cord had a significantly higher mean conduction velocity (CV: 56.5 m s(-1)) than descending branches (40.8 m s(-1)). The CV of ascending branches was significantly positively correlated with a measure of the strength of intrafusal bag(2) muscle fibre contacts, but not to a measure of bag(1) contacts. Two sites of monosynaptic excitatory projection in the cord were identified, namely to the intermediate region (laminae V, VI and VII) and to ventral horn region (laminae VIII and IX). In tests of 154 single afferents, signs of central projection were detected for 60, providing 122 regions of maximum negative focal synaptic potentials (FSPs) of mean amplitude 7.51 microV. Their longitudinal spacing indicated that axons gave off descending collaterals at intervals of 1.5-3.5 mm. Based on the amplitude of FSPs, the projection of secondary afferents is stronger than that of primaries in the intermediate region and possibly also in the ventral horn region. Evidence is also presented that spindle afferent input from different heads of the longissimus converges into any given spinal segment and that input in one spinal root projects to adjacent segments. It is concluded that the organization of the longissimus monosynaptic spindle input favours relatively tonic and diffuse stretch reflexes.

Classification of longissimus lumborum muscle spindle afferents in the anaesthetized cat.

Recordings have been made from 127 single muscle spindle afferents from the longissimus lumborum muscles of anaesthetized cats. They have been characterized by their responses to passive muscle stretch and the effects of succinylcholine (SCh) and by their sensitivity to vibration. The use of SCh permitted the assessment for each afferent of the influence of bag1 (b1) and bag2 (b2) intrafusal muscle fibres. From this, on the assumption that all afferents were affected by chain (c) fibres, they were classified in four groups: b1b2c (41.9%), b2c (51.4%), b1c (1.3%) and c (5.4%). All the afferents with b1 influence were able to respond one to one to vibration at frequencies above 100 Hz and were considered to belong to primary endings. On the basis of the vibration test, 64% of the b2c type afferents appeared to be primaries and 36% secondaries. Of the units classified as primaries, 41% were designated as b2c and would not therefore be able to respond to dynamic fusimotor activity. The significance of this relatively high proportion of b2c-type spindle primary afferents is discussed in relation to the specialized postural function of the back muscles.

Static and dynamic gamma-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.

Stretch reflex instability compared in three different human muscles.

The possibility of causing instability in the stretch reflex has been examined in three different human muscles: biceps, first dorsal interosseous (FDI) of the hand and digastric. Tremor recorded as fluctuation of isometric force was compared with that occurring during contraction against a spring load. The spring compliance was selected to make the natural frequency of the part in each case appropriate for oscillations in the short latency stretch reflex. A computer model of the whole system was used to predict the frequency at which oscillations should be expected and to estimate the reflex gain required in each case to cause sustained oscillations. Estimates were computed of the autospectra of the force records and of the rectified surface EMG signals and of the coherence functions. Normal subjects showed no evidence of a distinct spectral peak during isometric recording from any of the three muscles. However, in anisometric conditions regular oscillations in force occurred in biceps, but not in FDI or digastric. The oscillations in biceps at 8-9 Hz were accompanied by similar oscillations in the EMG which were highly coherent with the force signal. The results are consistent with the presence of a strong segmental stretch reflex effect in biceps and weak or absent reflex in FDI. Digastric is known to contain no muscle spindles and therefore to lack a stretch reflex. In two subjects who volunteered that they had more tremor than normal, but had no known neurological abnormality, there was a distinct peak in the force spectrum at 8-9 Hz in biceps and FDI in isometric conditions with coherent EMG activity. The peak increased in size in anisometric conditions in biceps but not in FDI. This component appears to be of central rather than of reflex origin. No equivalent component was found in digastric records. The results are discussed in relation to the possible role of the short latency stretch reflex in the genesis of physiological tremor in different muscles.

Direct and indirect assessment of gamma-motor firing patterns.

The study of the patterns of gamma-motor activity which accompany natural contractions has been long and difficult, and has not as yet led to general agreement. In this review we have simplified matters by considering the case of locomotion in the cat only, and we have avoided discussion of the various hypotheses which have been advanced to provide general schemes of gamma control for a wide range of movements. The development of the subject is shown to depend very much on devising ingenious methods applicable to reduced and intact animals. Direct recording from gamma-motoneurones has only been possible in reduced preparations, whereas indirect assessment of gamma activity from spindle afferent recordings was used in these and in intact animals. At this point in time, we still have no direct recordings from gamma-motoneurones in normally behaving animals, but those obtained in decerebrate animals show distinct patterns of modulation for static and dynamic types with particular temporal relation to the stepping movements. The spindle recordings in intact animals potentially provide the most important information, and the problems of interpretation, which have previously caused difficulties, are beginning to be solved through the insights obtained from the reduced preparations.

The influence of bag2 and chain intrafusal muscle fibers on secondary spindle afferents in the cat.

Static gamma-motor activity is strongly modulated by a particular phase relationship to the cyclic movements of locomotion, and this has a profound effect on the firing patterns of muscle spindle afferents. Whilst primary afferents are affected by both static and dynamic gamma-motor output,secondary afferents are affected significantly only by the static system acting via the intrafusal bag2 and chain fibres. It is therefore important to know how fluctuating patterns of static gamma-motor activity affect secondary afferents and to relate this to the actions of bagt and chain fibres. We have studied the action of single static gamma axons on secondary afferents in cat hindlimb muscles. Various physiological methods were explored to identify which of the intrafusal muscle fibres were being activated in each case, including the use of random stimulation and ramp frequency stimulation. The effects were also recorded of I Hz sinusoidally frequency-modulated gamma-axon stimuli and the amplitude and phase of the resulting afferent modulation related to the involvement of the bag2 and chain fibres. It was found that bag2 fibres are effective in biasing the secondary discharge, but their modulating action is relatively weak and involves a marked phase lag. Chain fibres acting alone cause strong modulation with very little phase lag. Mixed bag2 and chain-fibre action is most effective in modulating afferent discharge and causes intermediate values of phase lag. The results are discussed in relation to the control of natural movements and it is concluded that an important function of the static gamma motor system is to provide a signal to sum algebraically with the length-related signal. The results do not suggest that it could also usefully control stretch sensitivity.

Modulation of primary afferent discharge by dynamic and static gamma motor axons in cat muscle spindles in relation to the intrafusal fibre types activated.

1. Recordings were made from muscle spindle primary afferents from medial gastrocnemius and soleus muscles of the cat to study the modulating effects of varying gamma-motor stimulation frequency at constant muscle length. Stimulus trains had a mean frequency of 50 Hz and were sinusoidally frequency modulated at 1 Hz, with an amplitude of modulation of +/- 5 to +/- 30 Hz. 2. When dynamic gamma-axons (gamma(d)) were selected for their pure effect on bag(1) fibres, they were found to have very little modulating effect on afferent firing. 3. Static gamma-axons (gamma(s)) were tested with a random stimulus and correlation method to determine whether they acted purely on bag(2) fibres, purely on chain fibres or on both together. Pure bag(2) gamma(s)-axons had weak modulating effects with large values of phase lag. Pure chain connections were effective in modulating with very little phase lag, but their mean gain was low. Mixed bag(2) and chain axons were most effective and showed phase shifts proportional to gain. 4. The effects of muscle length changes recorded previously from locomotor movements were also tested, with and without accompanying stimulation of mixed gamma(s)-axons with pulse trains recorded from gamma(s)-axons. This gamma(s) stimulation had a powerful effect in increasing afferent discharge during muscle shortening. The difference in afferent firing between the stimulated and non-stimulated conditions accurately predicted the profile of the gamma(s) stimulation. 5. The results are discussed in relation to the ways in which the gamma-motor system may be used in natural movements.

Distinctive patterns of static and dynamic gamma motor activity during locomotion in the decerebrate cat.

Simultaneous recordings were made from gamma (gamma) motor axons and from muscle spindle afferents of the medial gastrocnemius (MG) muscle during locomotion in decerebrate cats. The gamma-neurons were identified as static or dynamic (gammas or gammad) by correlating their behaviour during midbrain stimulation with changes in muscle spindle afferent responses to muscle stretch. On the basis of their behaviour during locomotion, gammas neurons could be divided into two groups. One group (type-1) showed strongly and smoothly modulated discharge increasing in parallel with the active muscle shortening in ankle extension, but with phase advance. The other group (type-2) also showed a modulated pattern, but with increased firing centred on the flexion phase. The proportions of the two were 13 type-1 and 7 type-2. The type-1 firing pattern accurately predicted the difference in firing frequency for secondary afferents obtained by subtracting from the recordings made during active movements the response of the same units to the movements repeated passively in the absence of fusimotor activity. The type-2 pattern also became consistent with the difference signal, when operated on by a phase lag appropriate to the effects of bag2 intrafusal fibres. These results suggest that there may be some degree of separate control of chain and bag2 intrafusal fibres. The discharge of gammad axons was also found to fluctuate with the locomotor cycle, with a pattern very distinct from that of the gammas records. The gammad firing frequency rose very suddenly from zero to a maximum at the onset of muscle shortening and continued into the beginning of lengthening. The term 'interrupted' discharge is suggested as a useful description. The timing of this discharge was shown to be appropriate for sensitising the primary afferents to detect the onset of stretch.

Patterns of fusimotor activity during locomotion in the decerebrate cat deduced from recordings from hindlimb muscle spindles.

1. Recordings have been made from multiple single muscle spindle afferents from medial gastrocnemius (MG) and tibialis anterior (TA) muscles of one hindlimb in decerebrate cats, together with ankle rotation and EMG signals, during treadmill locomotion. Whilst the other three limbs walked freely, the experimental limb was denervated except for the nerves to MG and TA and secured so that it could rotate only at the ankle joint, without any external load. Each afferent was characterised by succinylcholine testing with regard to its intrafusal fibre contacts. Active movements were recorded and then replayed through a servo mechanism to reproduce the muscle length changes passively after using a barbiturate to suppress gamma-motor firing. 2. The difference in secondary afferent firing obtained by subtracting the discharge during passive movements from that during active movements was taken to represent the profile of static fusimotor activity. This indicated an increase before the onset of movement followed by a strongly modulated discharge in parallel with muscle shortening during locomotion. The pattern of static firing matched the pattern of unloaded muscle shortening very closely in the case of TA and with some phase advance in the case of MG. The same effects were observed in primary afferents. 3. Primary afferents with bag1 (b1) contacts in addition showed higher firing frequencies during muscle lengthening in active than in passive movements. This indicated increased dynamic fusimotor firing during active locomotion. There was no evidence as to whether this fluctuated during the movement cycles. 4. When the mean active minus passive difference profile of firing in bag2-chain (b2c) type primary afferents was subtracted from that for b1b2c afferents, the difference was dominated by a peak centred on the moment of maximum lengthening velocity (v). 5. The component of the active minus passive difference firing due to b1 fibre contacts could be modelled by f(t) = av (where a is a constant) during lengthening and by f(t) = 0.2 av during shortening. The remainder of the difference signal matched the predictions of the static fusimotor signal derived from secondary afferents. 6. The findings are discussed in relation to the concept that the modulated static fusimotor pattern may represent a 'temporal template' of the expected movement, though the relationship of the results to locomotion in the intact animal will require further investigation. The analysis of the data indicates that the combined action of muscle length changes and static and dynamic fusimotor activity to determine primary afferent firing can be understood in terms of the interaction between the b1 and b2c impulse initiation sites.

Physiological signs of the activation of bag2 and chain intrafusal muscle fibers of gastrocnemius muscle spindles in the cat.

A method is described for identifying the effect of single gamma static (gamma(s)) axons on bag2 or chain intrafusal fibers using random (Poisson-distributed) stimuli. The cross-correlogram of the stimuli with the firing of spindle primary afferents took one of three forms. A large, simple, brief response was taken to indicate pure chain fiber activation and a small, prolonged response to indicate pure bag2 activation. A compound response with brief and prolonged components was taken to be a sign of mixed innervation. The correlogram components could be well fitted with lognormal curves. They could also be transformed into curves of gain as a function of frequency, which were convenient for estimating the strength of the effects. In 68 effects of gammas axons on Ia afferents, 16 were pure chain, 17 pure bag2, and 35 mixed. This distribution was significantly different (P < 0. 05) from that expected from chance nonspecific innervation of chain and bag2 fibers. Making use of the estimates of the strength of chain and bag2 effects derived from the gain curves, the classification was modified by treating mixed responses that had one effect more than five times stronger than the other as belonging to the dominant type. The distribution was then as follows: chain 16, bag2 28, and mixed 24. This differed very significantly from the prediction of chance distribution (P < 0.001). This evidence for some degree of specific innervation of chain and bag2 fibers is discussed in relation to previous work and with regard to the ways in which the two fiber types might be used in natural movements.

Fusimotor influence on jaw muscle spindle activity during swallowing-related movements in the cat.

1. The activity patterns of muscle spindle afferents in jaw-closer muscles were studied during reflex swallowing movements in anaesthetized cats. Simultaneous records were made of the electromyogram (EMG) in masseter and anterior digastric muscles and of the unloaded jaw movements. The underlying patterns of fusimotor activity were deduced by comparing afferent discharges occurring during active swallowing with those occurring when exactly the same movements were imposed passively. The interpretation of spindle behaviour was greatly facilitated by characterizing the afferents according to the evidence for their contact with the various intrafusal muscle fibres, derived from testing with succinylcholine. It was also valuable to have two different types of afferent recorded simultaneously. 2. There was clear evidence of fusimotor activity occurring during active jaw closing so as to oppose the spindle silencing. This effect was most marked in b2c-type afferents (probably secondaries) and was therefore attributed to a modulation of static fusimotor discharge approximately in parallel with alpha-activity. 3. Afferents with evidence of bag1 fibre contacts (primaries) showed much greater sensitivity to muscle lengthening during active movement than when the movement was imposed. This difference was exaggerated when anaesthesia was deepened for the passive movements. This was interpreted as evidence for a higher level of dynamic fusimotor activity maintained during active movements than at rest. 4. The results support the view that for a variety of active jaw movements, static fusimotor neurone firing is modulated roughly in parallel with alpha-activity but leading it so as to counteract spindle unloading. Dynamic fusimotor neurone firing appears to be set at a raised level during active movements. Anaesthesia appears to depress activity in the alpha-motoneurones more than in gamma-motoneurones.

The use of sinusoidal and ramp stretch stimuli in characterizing fusimotor effects on cat muscle spindles.

Comparisons were made between the results of testing muscle spindle primary afferents with low-frequency, large-amplitude sine waves of muscle stretch and with repeating ramp-and-hold stretches. Three different situations were explored, namely, activation with succinylcholine (SCh), generation of various fusimotor outflow patterns by brainstem stimulation and fusimotor activation by stimulation of single ventral root gamma-axons. With ramp-and-hold stretches the effects of bag1 fibre contraction were thought to be generally better represented by increases in the dynamic response to stretch (delta DD) than by increases in dynamic index. The equivalent effect on the sine wave response was an increase in the magnitude of the fitted sine (delta Mag). Static effects were best measured by increases in the initial frequency for ramps (delta IF) and by increases in the fitted centre frequency (delta CF) for sines. There was good agreement between sine and ramp testing in the case of SCh effects, but much less consistency during brainstem stimulation. Sine wave testing can be regarded as less efficient than ramp testing in distinguishing between static and dynamic actions because dynamic fusimotor stimulation causes equal rises in CF and Mag, but fourfold larger rises in DD than in IF. Ramp responses with combined dynamic and static fusimotor stimulation showed increases of both IF and DD as expected, but whilst sine wave responses always showed increase in CF, they often showed no increase in Mag. Comparisons of the effects of SCh, central stimulation and fusimotor stimulation showed that it is important to recognize the different effects of chain and bag2 intrafusal fibre activation as components of static fusimotor excitation. Stimulation of driving static axons (chain activation) raised the IF and CF often with 1:1 or 1:2 driving during the shortened phase of ramps and sines. However, the stretch response in both cases was either unchanged or reduced. Stimulation of a non-driving static fusimotor axon (bag2 activation) caused a marked rise in CF for sine waves and a fall in Mag, but a modest increase in ramp stretch sensitivity (DD) with no increase in dynamic index. A way is described for measuring flattening of sine wave responses as a possible way of detecting chain fibre activation. The consequences of these findings are discussed in relation to previous reports of the use of sine wave testing for assessing fusimotor mechanisms.

Projection of cat jaw muscle spindle afferents related to intrafusal fibre influence.

1. A method of classification of muscle spindle afferents using succinylcholine (SCh) and ramp stretches has recently been described, which appears to estimate separately the strength of influence of bag1 (b1) and of bag2 (b2) intrafusal fibres. Increase in dynamic difference (delta DD) indicates b1 influence whilst increase in initial frequency (delta IF) indicates b2 influence. The significance of this classification has now been examined by correlation with the strength of synaptic projection of jaw muscle spindle afferents to the fifth motor nucleus (MotV) and the supratrigeminal region (STR) in anaesthetized cats. 2. Projection strength was estimated by computing the extracellular focal synaptic potential (FSP) from spike-triggered averages of 1024 sweeps at 100 microns intervals along tracks through STR and MotV. Trigger pulses were derived from spindle afferent cell bodies of the jaw-closer muscles recorded in the mesencephalic trigeminal nucleus, and characterized by the effect of SCh on their responses to ramp-and-hold stretches. 3. The maximum size of FSPs in tracks traversing STR and MotV ranged from 2.08 to 36.99 microV with a mean of 7.55 microV. The amplitudes were bimodally distributed into roughly equal-sized groups with high and low amplitude FSPs. 4. Mean values of delta IF were significantly greater for the group with large FSPs than for those with small FSPs. There were no significant differences in delta DD. FSP amplitude was significantly positively correlated with delta IF, but not with delta DD. 5. Spindle afferents with high values of FSP amplitude in MotV had a wide range of values of delta DD (b1b2c and b2c groups), while units with large FSPs in STR were all in the b2c category. Some evidence is presented to indicate that this reflects a preferential projection of secondary afferents to the STR. 6. For those units with projection to both STR and to MotV, there was a significant positive correlation between FSP amplitude in the two nuclei. 7. These results indicate that the extent of the b2 influence on spindle afferents predicts the central projection strength better than does the b1 influence. This finding is discussed from the viewpoint of possible developmental and functional issues.

The effect of succinylcholine on cat gastrocnemius muscle spindle afferents of different types.

1. A population of 269 gastrocnemius muscle spindle afferents have been studied in anaesthetized cats for the effects of succinylcholine (SCh) on their response to ramp and hold stretches repeated every 6 s. The effectiveness and reliability of the SCh test was improved by prior stimulation of the muscle at 10 Hz for 30 s to increase the blood flow. 2. Responses have been assessed from averaged cycle histograms before and after a single I.V. dose of SCh of 200 micrograms kg-1. As for previous studies of jaw muscle spindles the basic measurements were initial frequency (IF), peak frequency (PF) and static index (SI), the frequency 0.5 s after the end of the ramp of stretch. Dynamic difference (DD = PF-IF), dynamic index (DI = PF-SI) and static difference (SD = SI-IF) were derived from these and increases caused by SCh indicated by the prefix delta. 3. delta DD and delta IF were each distributed bimodally and since they were uncorrelated formed the basis for a four-way classification. Since delta DD can be attributed to activation of bag1 (b1) intrafusal fibres and delta IF to bag2 (b2) fibres, while all afferents receive input from chain (c) fibres it is proposed as with the jaw spindles that the classes correspond to predominant influence from b1c, b1b2c, b2c and c intrafusal fibres. 4. The proportion of units in the different groups were similar to those in the jaw muscles except for there being very few b1c type in gastrocnemius. 5. Conduction velocity was bimodally distributed with the best dividing line at 63.2 m s-1. The b1b2c units were all, save one, in the fast group, while the b2c units were equally divided between fast and slow. 6. Mean control values for DD did not differ between the b1b2c and the b2c groups, which is taken to indicate that the b1 fibre does not contribute significantly to the dynamic stretch response of spindles with no intrafusal contraction. 7. The results emphasize the importance of recognizing that some apparently primary afferents lack b1 fibre influence, while many secondaries have marked b2 fibre influence. 8. The importance of the SCh classification is discussed in relation to the identification of fusimotor effects on spindle discharge and in relation to studies of central connectivity.

The classification of afferents from muscle spindles of the jaw-closing muscles of the cat.

1. The effects of the muscle-depolarizing drug succinylcholine (SCh) on the stretch responses of jaw-closer muscle spindle afferents were studied in the anaesthetized cat. Using ramp and hold stretches repeated every 6 s the basic measurements made were: initial frequency (IF), peak frequency (PF) and static index (SI), the frequency 0.5 s after the end of the ramp of stretch. Derived from these were: dynamic difference (DD) = PF-IF, dynamic index (DI) = PF-SI and static difference (SD) = SI-IF. Increases in these measures caused by a single I.V. dose of SCh (200 micrograms kg-1) are symbolized by the prefix delta. 2. In a population of 234 units, delta DD and delta IF were each distributed bimodally, but were uncorrelated, thus defining four subgroups. 3. delta DD was argued to be an index of the effect of bag1 intrafusal fibre contraction and delta IF to be an index of the effect of bag2 fibre contraction. On this basis it is proposed that units can be divided into four groups according to the predominant influences of the bag1, bag2 and chain fibres as b1c (6.8%), b1b2c (22.2%), b2c (54.3%) or c (16.7%). 4. Testing with sine wave stretches at 1 Hz showed that changes in mean frequency and amplitude of response caused by SCh correlated with delta IF and delta DD respectively, but separated groups of units much less effectively than did ramp and hold testing. 5. Evidence is presented to indicate that the control value of DD in passive spindles does not relate to the potential strength of bag1 fibre effects in fully activated spindles. The bag1 fibre appears to contribute little to responses of spindle afferents in the passive state. DD is superior to DI as a measure of bag1 effects. 6. Conduction velocity was unimodally distributed in masseter spindle afferents and was not correlated with delta DD or delta IF and was therefore of no value in classifying them. 7. Neither the threshold of afferents to quick transient stretch nor the coefficient of variation of interspike intervals provided any significant additional help in classification. 8. The unexpectedly high proportion of units of b2c type is thought to include primaries lacking appreciable bag1 fibre contacts and secondaries with more or less substantial bag2 contracts.