The ‘initial burst’ of human primary muscle spindle afferents has at least two components

Ten muscle spindle primary afferents from the extensor digitorum communis muscle of man were studied with single unit afferent recordings. Responses to slow test stretches with three different pre-history conditions were assessed to investigate the contribution of rapid stretches to the stretch sensitization phenomenon. In two of the conditions, the slow test ramps were preceded by rapid stretch after which the parent muscle of the receptor was either (a) kept short for 5 seconds or (b) kept long for 3.2 seconds and then returned to the short muscle length for 5 seconds. The third condition (c) consisted of a slow stretch from short to long muscle length followed by a rapid return to the short muscle length, in turn followed by 5 seconds at the short muscle length. Afferent responses were depressed when the muscle had been kept at the long length after the rapid stretches (condition b) and enhanced when the muscle had been kept at the short length (conditions a & c). A prominent ‘initial burst’ was only present in the afferent discharge when the parent muscles of the primary endings had been kept short (condition a). A second, more prolonged burst was present for conditions (a) and (c) but was lacking or inconspicuous when the muscle had been kept long after rapid stretches (condition b). The rapid stretches in the stretch sensitization paradigm appear to be a primary factor not only for the enhanced responses of sensitized primary afferents but also for the depressed responses of desensitized primary afferents.     

Dynamic response of human muscle spindle afferents to stretch

1. One hundred and twenty-four muscle afferents from the finger extensor muscles were recorded from the radial nerve in human subjects. 2. The afferents were provisionally classified as muscle spindle primary (78/124) and secondary afferents (25/124), and Golgi tendon organ afferents (21/124), on the basis of their response to 1) maximal twitch contractions, 2) 20- and 50-Hz sinusoids superimposed on ramp-and-hold stretches, 3) stretch sensitization, and 4) isometric contractions and sudden relaxations. 3. Ramp-and-hold stretches at two velocities, 10 and 50 degrees/s, were applied to the appropriate metacarpophalangeal (MCP) joint while the parent muscle remained relaxed. For each unit three discrete parameters were assessed: the presence or absence of 1) an initial burst at the commencement of the ramp stretch, 2) a deceleration response at the beginning of the hold phase, and 3) a prompt silencing at muscle shortening. In addition, two kinds of dynamic indexes were calculated for 79 of the muscle spindle afferents. 4. Most spindle afferents responded readily to stretch, whereas the Golgi tendon organ afferents produced very poor stretch responses. All of them lacked a static response, whereas the dynamic response, when present at all, consisted of only a few impulses. 5. The dynamic index was higher for spindle primaries than for secondaries, and this difference was statistically significant although the distribution was unimodal for spindle afferents as a group. Hence, this parameter was a poor discriminator. 6. Initial bursts, deceleration responses, and silences during imposed shortening were more common in spindle primaries than in secondaries. The differences were significant in all these respects. 7. The three discrete parameters were statistically pairwise independent for the spindle afferents, justifying the combination of the three into a useful battery for discrimination between primary and secondary spindle afferents and the use of this battery as a partial data base for a probability approach towards a solid classification of human muscle afferents.     

The effects on primary and secondary spindle afferents of fusimotor reflex during ramp and sinusoidal muscle stretch

Summary Tetanic stimulation of ipsilateral Triceps surae afferents leads to a reflex increase in the initial burst from the primary spindle afferents during ramp stretch in both intercollicular decerebrate and spinal preparations. The dynamic index does not change significantly.Slow, low-amplitude sinusoidal muscle stretches (1.6 Hz, 0.55 mm peak-peak) disclose an increased dynamic sensitivity of primary afferents during reflex activation. The same activation in the statically adapted muscle results in a great many cases in little or no increase in spindle discharge rate.In the frequency-stretch relation, the discharge rates of primary afferents in the spinal cat and of secondaries in decerebrate animals are greatly increased by combined fusimotor activation and low-amplitude sinusoidal stretch.We conclude that both static and dynamic motoneurons are implied in this reflex.     

Physiological evidence for caudal brainstem projections of jaw muscle spindle afferents

Retrograde transport and intra-axonal labeling studies provide convincing evidence that jaw-muscle spindle afferents project to the caudal medulla by way of Probst’s tract. However, functional properties of this caudal projection are not well understood. Extracellular recordings were made in cats at the level of the subnucleus interpolaris (Vi) to identify single units that showed consistent responses to ramp-and-hold stretches of the jaw. In this report, we present data from 20 central units with properties indicating that they received input from trigeminal muscle spindle afferents. All units were activated by gentle palpation of jaw muscles, and none had superficial receptive fields. Two groups of neurons could be defined based on their responses to passive jaw movements. One group (n=12) showed an obvious dynamic response (i.e., a higher level of activity at the onset of stretch than during the hold period). Activity was maintained during the hold phase, and the units stopped firing (unloaded) for a brief period upon jaw closure. The other group (n=8) lacked a dynamic response. Instead, they showed an increase in firing with onset of stretch that was maintained during the hold phase. Thirteen units, which were tested with more than three different jaw stretch speeds and/or amplitudes, were further characterized by analyzing dynamic index (DI) and mean firing rate (MFR) during each phase of the ramp-and-hold movement as well as interspike interval (ISI) variability. All but one unit with a dynamic response showed a speed-sensitivity. In all cases, the MFR was a more sensitive indicator of changes in jaw speed than DI. Neurons in the other group (5/5 tested) showed a high position-sensitivity, i.e., their firing rates varied as a function of amplitude of jaw opening. The percent change in ISI variability for all neurons ranged from 37–84%. The response characteristics of these central neurons were compared to known physiological properties of muscle spindle afferents. The results provided compelling evidence for jaw-muscle-spindle afferent projection onto these neurons. Reconstruction of recording sites showed that medial Vi, and the adjacent reticular formation, are likely recipients for the caudal projections from jaw-muscle-spindle afferents. We suggest that muscle spindle input to this region is well suited for influencing the coordination of motor behavior during feeding and for the integration and processing of kinesthetic information. Received: 22 December 1998 / Accepted: 7 May 1999     

Evidence for presynaptic inhibition of muscle spindle Ia afferents in man

A new method for estimating presynaptic inhibition of soleus (Sol) Ia fibres in man is introduced based on the assessment of the amount of facilitation produced by a preceding homonymous Ia volley onto a Sol monosynaptic reflex. It was found in animal experiments that a reduction of such Ia facilitation reflects the amount of presynaptic inhibition exerted on these Ia fibres. Since, in man, a similar reduction of homonymous Ia facilitation was found after tibialis anterior vibration, this provides evidence for presynaptic inhibition of Sol Ia fibres, elicited here by the afferent discharge due to this flexor vibration.     

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.     

Activity patterns in individual hindlimb primary and secondary muscle spindle afferents during normal movements in unrestrained cats.

1. Chronically implanted microelectrode wires in the L7 and S1 dorsal root ganglia were used to record unit activity from cat hindlimb primary and secondary muscle spindle afferents. Units could be reliably recorded for several days, permitting comparison of their activity with homonymous muscle EMG and length during a variety of normal, unrestrained movements. 2. The general observation was that among both primary and secondary endings there was a broad range of different patterns of activity depending on the type of muscle involved and the type of movement performed. 3. During walking, the activity of a given spindle primary was usually consistent among similar step cycles. However, the activity was usually poorly correlated with absolute muscle length, apparently unrealted to velocity of muscle stretch, and could change markedly for similar movements performed under different conditions. 4. Spindle activity modulation not apparently related to muscle length changes was assumed to be influenced by fusimotor activity. In certain muscles, this presumption leads to the conclusion that gamma-motoneurons may be activated out of phase with homonymous alpha-motoneurons as well as by more conventional alpha-gamma-motoneuron coactivation. 5. Simultaneous recordings of two spindle primary afferents from extensor digitorum longus indicated that spindles within the same muscle may differ considerably with respect to this presumed gamma-motoneuron drive. 6. Spindle secondary endings appeared to be predominantly passive indicators of muscle length during walking, but could demonstrate apparently strong fusimotor modulation during other motor activities such as postural changes and paw shaking. 7. Both primary and secondary endings were observed to undergo very rapid modulation of firing rates in response to presumed reflexly induced intrafusal contractions. 8. It is suggested that the pattern of fusimotor control of spindles may be tailored to the specific muscle and task being performed, rather than necessarily dominated by rigid alpha-gamma coactivation.     

The regularity of primary and secondary muscle spindle afferent discharges

1. The patterns of nerve impulses in the afferent fibres from muscle spindles have been studied using the soleus muscle of the decerebrate cat. Impulses from up to five single units were recorded simultaneously on magnetic tape, while the muscle was stretched to a series of different lengths. Various statistics were later determined by computer analysis.2. After the ventral roots were cut to eliminate any motor outflow to the muscle spindles, both primary and secondary spindle endings discharged very regularly. At frequencies around 30 impulses/sec the coefficient of variation of the interspike interval distributions had a mean value of only 0.02 for the secondary endings and 0.058 for the primary endings. The values obtained for the two kinds of ending did not overlap.3. When the ventral roots were intact, the ;spontaneous' fusimotor activity considerably increased the variability of both kinds of endings. Secondary endings still discharged much more regularly than primary endings, even when the fusimotor activity increased the frequency of firing equally for the two kinds of endings. At frequencies around 30/sec the average coefficient of variation of the interval distributions was then 0.064 for the secondary endings and 0.25 for the primary endings.4. When the ventral roots were intact there was usually an inverse relation between the values of successive interspike intervals. The first serial correlation coefficient often had values down to - 0.6 for both kinds of ending. Higher order serial correlation coefficients were also computed.5. Approximate calculations, based on the variability observed when the ventral roots were intact, suggested that when the length of the muscle was constant an observer analysing a 1 sec period of discharge from a single primary ending would only be able to distinguish about six different lengths of the muscle. The corresponding figure for a secondary ending was twenty-five lengths.6. The increase in variability with fusimotor activity, and the pattern of serial correlations, were probably caused by static fusimotor fibres firing at rates below the fusion frequency of the intrafusal muscle fibres that they supply.     

Classification and response characteristics of muscle spindle afferents in the primate.

A study was made of the response characteristics of spindle afferents in the baboon soleus muscle. Afferents were isolated from the dorsal roots, their conduction velocities were determined, and their responses were recorded to muscle stretch at rates of 2.5-45 mm/s and amplitudes of 2-10 mm. Spindle afferents could be classified as primary or secondary on the basis of two criteria. The first criterion was conduction velocity. The conduction velocity histogram was bimodal, with peaks at about 45 and 80 m/s and an intermediate region from 55 to 70 m/s. The second criterion was the pattern of adaptation following the peak of ramp stretch. This latter criterion has the advantage of allowing units with intermediate conduction velocities also to be confidently classified as primary or secondary. The velocity and position sensitivities of primate spindle afferents were determined. The mean dynamic index and mean dynamic sensitivity of secondary afferents were about 45% of the corresponding values for primary afferents. On the other hand, the position sensitivities of primary and secondary spindle afferents in the baboon were not significantly different.     

Inhibition of extensorγ motoneurons by antagonistic primary and secondary spindle afferents

Summary About 2/3 of the efferents isolated from the medial gastrocnemius nerve were inhibited by longitudinal high-frequency vibration applied to the tendons of the non-contracting pretibial flexors (decerebrate cats). The inhibition appeared at 15–25 m amplitude of vibration and increased up to a maximum at nearly 100 m. Increasing the frequency of vibration from 100 to 300 Hz increased the inhibition. The reflex effects elicited by muscle vibration corresponded well in incidence and magnitude with those evoked by tetanization of the deep peroneal nerve at group I stimulus strength. The reflex disappeared when the nerve supply of the vibrated muscles was cut. The sensitivity of some pretibial proprioceptors to vibration was also tested. It is concluded that primary spindle endings of the pretibial flexors inhibit the extensor motoneurons. Some findings hint at a spinal pathway involving I a inhibitory interneurons.In addition, an inhibitory action of pretibial group II afferents, probably secondary spindle endings, on extensor efferents was demonstrated.The described fusimotor inhibition by antagonistic muscle spindle afferents is a further example of --linkage.