Stimulation Of Ventral Root Filaments Research Articles

Reference frames for spinal proprioception: kinematics based or kinetics based?

This second paper of the series deals with another issue regarding sensorimotor representations in the CNS that has received much attention, namely the relative weighting of kinematic and kinetic representations. The question we address here is the contribution of muscle tension afferent information in dorsal spinocerebellar tract (DSCT) sensory representations of foot position. In five anesthetized cats, we activated major hindlimb muscle groups using electrical stimulation of ventral root filaments while passively positioning of the left hind foot throughout its workspace. In general, as the parameters of the joint angle covariance planes indicated, muscle stimulation did not significantly change hindlimb geometry. We analyzed the effects of the muscle stimulation on DSCT neuronal activity within the framework of a kinematic-based representation of foot position. We used a multivariate regression model described in the companion paper, wherein indicators of the experimental condition were added as firing rate predictors along with the limb axis length and orientation to account for possible effects of muscle stimulation. The results indicated that the response gain of 35/59 neurons studied (59%) was not changed by the muscle activations, although most neurons showed some change in their overall firing level with stimulation of one or more muscles. Most of the neurons responded to pseudorandom stimulation of the same muscle groups with complex temporal patterns of activity. For a subpopulation of 42 neurons, we investigated the extent to which their representation of foot position was affected by a rigid constraint of the knee joint and at least one type of muscle stimulation. Although they could be divided into four subgroups based on significance level cutoffs for the constraint or stimulation effect, these effects were in fact quite distributed. However, when we examined the preferred directions of spatial tuning relative to the limb axis position, we found it was unchanged by muscle stimulation for most cells. Even in those cases in which response gain was altered by muscle stimulation, the cell's preferred direction generally was unaltered. The invariance of preferred direction with muscle stimulation lead us to the conclusion that the reference frame for DSCT coding may be based primarily on limb kinematics.

Effects of muscle length on the EMG-force relationship of the cat soleus muscle studied using non-periodic stimulation of ventral root filaments.

The effects of changing the length of the cat soleus muscle on electromyographic (EMG) signals, muscle force and the corresponding EMG-force relationship were assessed using distributed stimulation of ten ventral root filaments and irregular interpulse intervals. EMG-force relationships were first determined for four muscle lengths using a protocol of simultaneous addition and rate modulation of ventral root filaments. In the second test, three submaximal levels of stimulation were applied at eight muscle lengths. EMG signals were obtained using surface and wire electrodes, and force was measured using a strain transducer. For most muscle lengths, the relationships between integrated EMG and mean force obtained using wire and surface electrodes were sigmoid with a linear intermediate region. The effects of muscle length on EMG signals were likely to be associated with movement of the recording electrodes relative to each other and to the active motor units. Mean forces increased with increasing muscle length and with increasing levels of stimulation. Mean force-length relationships obtained using submaximal stimulation were not simply scaled down versions of the force-length relationship obtained using supramaximal stimulation of the soleus nerve, but appeared to be shifted towards longer muscle lengths.

EMG-force relationship of the cat soleus muscle studied with distributed and non-periodic stimulation of ventral root filaments.

Distributed stimulation of ventral root (VR) filaments and pseudo-random interpulse intervals (based on a Gaussian distribution with a coefficient of variation of 12.5%) were used to modulate electromyographic activity (EMG) and force of the cat soleus muscle to assess the EMG-force relationship. A protocol consisting of addition and rate modulation of ten VR filaments that contain alpha motoneurones to the soleus muscle was adopted. EMG was measured using indwelling electrodes and forces were measured at the distal tendon using a strain transducer. EMG records obtained using this approach were similar in the time and frequency domains to those obtained during voluntary contractions. Force records obtained from stimulation of single VR filaments showed summation effects typical of irregular interpulse intervals. The overall relationship between integrated rectified EMG (IEMG) and mean force was found to be non-linear. At low and high stimulation levels, IEMG tended to increase proportionally more than mean force. In the intermediate stimulation region (i.e. producing forces between approximately 5% and 88% of the maximal tetanic force), the IEMG-mean force relationship was virtually linear. Muscles with a homogeneous fibre type composition, such as the cat soleus muscle, have been reported to have a linear EMG-force relationship.

Effects of muscle length on EMG, force and EMG-force relation of the cat soleus muscle using stimulation of ventral root filaments

Effects of muscle length on EMG, force and EMG-force relation of the cat soleus muscle using stimulation of ventral root filaments

Extrafusal and intrafusal motor units in the kitten

In the lateral flexor digitorum longus muscle (FDL) of anaesthetized kittens aged 3–21 days, alpha (α) and gamma (γ) motoneurone conduction velocities were measured together with motor unit tensions. Conduction velocity lay in the range 8–27 msec−1 for α motoneurones and 2–10 msec−1 for γ motoneurones. Motor unit tetanic tensions were 3–47 mN with the largest units being 2–2.2% of whole muscle tension. The hypothesis was tested that motor axons conducting within the γ range and presumed to be innervating the intrafusal fibres of muscle spindles, on stimulation, produced measurable tension. Stimulating γ motoneurones in the adult produces no tension. The hypothesis was based on histological observations that while in the adult, intrafusal fibres were about one third of the size of extrafusal fibres, in kittens the two were nearly equal, both in length and diameter. It was shown by means of signal averaging during stimulation of ventral root filaments that whenever tension was recorded in the muscle an impulse could be detected in the muscle nerve conducting at α motoneurone tempo. It is concluded that in the kitten, despite the fact that intrafusal and extrafusal fibres are of similar size, stimulating single γ motoneurones does not develop measurable tension.

In‐series compliance of gastrocnemius muscle in cat step cycle: do spindles signal origin‐to‐insertion length?

1. It has been claimed that stretch in the non-contractile (extramysial) portion of muscles is substantial, and may produce large discrepancies between the origin-to-insertion muscle length and the internal length variations 'seen' by muscle spindle endings. 2. In eight pentobarbitone-anaesthetized cats, we estimated stretch in the extramysial portion of medial gastrocnemius (MG) muscle with a method similar to the spindle null technique. 3. Length variations of MG previously monitored in a normal step cycle were reproduced with a computer-controlled length servo. The responses of test MG spindle endings were monitored in dorsal root filaments. Distributed stimulation of ventral root filaments, rate-modulated by the step-cycle EMG envelope, served to reproduce step-cycle forces. The filaments were selected so as to have no fusimotor action on the test spindle. 4. Spindle responses in active cycles were compared with those in passive cycles (stretch, but no distributed stimulation). In some cases concomitant tonic fusimotor stimulation was used to maintain spindle responsiveness throughout the cycle, both in active and passive trials. Generally, small discrepancies in spindle firing were seen. The passive trials were now repeated, with iterative adjustments of the length function, until the response matched the spindle firing profile in the active trial. The spindle 'saw' the same internal length change in the final passive trial as in the active trial. Any difference between the corresponding length profiles was attributed to extramysial displacement. 5. Extramysial displacement estimated in this was was maximal at short mean muscle lengths, reaching about 0.5 mm in a typical step cycle (force rising from 0 to 10 N). At longer mean muscle lengths where muscle force rose from say 2 to 12 N in the cycle, extramysial displacement was in the range 0.2-0.4 mm. 6. Except at very short lengths, the displacement was probably mainly tendinous. On this assumption, our results suggested that the stiffness of the MG tendinous compartment was force related, and about double that of cat soleus muscle at any given force. Calculations indicated that though the stretch was small, the MG tendon would store and release enough strain energy per cycle to contribute significantly to the E3 phase of the step cycle. The discrepancies in spindle firing were generally quite subtle, so we reject the claim that extramysial stretch poses a serious difficulty for inferences about fusimotion from chronic spindle afferent recordings.

Comparison of physiological and histochemical properties of motor units after cross-reinnervation of antagonistic muscles in the cat hindlimb.

1. Physiological and histochemical properties of the cat ankle extensor muscles, the lateral and medial gastrocnemius, and the soleus were studied after cross-reinnervation by flexor motoneurons. 2. Tibial and common peroneal nerves were cut and cross-united in the popliteal fossa of 2- to 6-mo-old cats. Eighteen to 24 mo later, single motor units were isolated by dissection and stimulation of ventral root filaments and classified into four types: fast-twitch, fatigable (FF), fast-twitch with intermediate fatigue resistance (FI), fast-twitch, fatigue-resistant (FR), and slow, fatigue-resistant (S). Muscle fibers were classified as fast glycolytic (FG), fast, oxidative glycolytic (FOG), and slow oxidative (SO) on the basis of histochemical staining. 3. Although motor-unit force was normally well correlated with the size of the innervating motor axon in the cross-reinnervated muscles, the force of different unit types overlapped considerably. The reinnervated motor units also showed a higher than normal degree of fatigability. 4. The range of muscle unit forces in cross-reinnervated triceps surae muscles was the same as in the normally innervated triceps surae muscles. This range is 2-3 times greater than the flexor muscles, which the common peroneal nerve normally supplies. The range of contraction speed of units in the cross-reinnervated extensor muscles was comparable to that in the flexor muscles, consistent with a motoneuron-specific determination of muscle speed (28). 5. SO and FOG muscle fibers were found in all reinnervated triceps surae muscles, but FG fibers were only found in reinnervated medial gastrocnemius (MG) and lateral gastrocnemius (LG) muscles, consistent with previous findings of the resistance of soleus muscles to complete conversion (10, 16, 20, 21). Type grouping of muscle fibers was characteristic of the reinnervated muscles. 6. Reinnervated SO muscle fibers were larger than the corresponding fibers in normally innervated muscles as were the estimated number of muscle fibers innervated by slow motor axons. Nonetheless, the force generated by the S motor units remained relatively smaller than FR and FF units. The relative contributions of the number, cross-sectional area and specific tension to the force generation of reinnervated motor units are discussed.

Synaptic rearrangements and alterations in motor unit properties in neonatal rat extensor digitorum longus muscle.

1. We have used in vitro intracellular recordings and measurements of the contractile properties of single motor units to examine the changes in muscle innervation occurring during the post-natal development of a fast-twitch muscle in the hindlimb of the rat, the extensor digitorum longus (EDL). 2. Intracellular recordings of end-plate potentials evoked in response to graded stimulation of the nerve supply to the muscle indicate that during the first day after birth, each muscle fibre receives synaptic input from at least two motoneurones and that some muscle fibres receive as many as six such inputs. With subsequent development, most of this polyneuronal innervation is eliminated: the first singly innervated fibres are encountered on day 3; by day 18 fewer than 5% of the fibres remain polyneuronally innervated. These results show that there are quantitative differences in post-natal synapse elimination in EDL compared to its well-studied counterpart, the soleus. Although the great majority of fibres in both muscles become singly innervated at about 18 days, the first singly innervated fibres appear at least a week earlier in the EDL. None the less, synapses are lost from EDL at about half the rate they are lost from soleus. 3. The number of motor units, determined by counting the number of twitch increments produced by graded stimulation of ventral root filaments teased to contain only a few EDL motor axons, remains unchanged from an average of forty-one from post-natal day 1 to day 17. In addition, the number of muscle fibres counted in muscle cross-sections stained with an anti-myosin antibody increases less than 10% from birth to adulthood. Therefore, synapse elimination in EDL occurs with a largely constant population of muscle fibres as well as motoneurones. 4. Measurements of tensions generated by single motor units indicate that the average size of a motor unit declines from 6.8% of the muscle fibres at day 1 to 2.3% at 17 days. This result indicates that each motoneurone, on average, comes to innervate threefold fewer muscle fibres. Motor units derived from each of the spinal segments innervating the muscle undergo equivalent reductions in motor unit size, indicating that there is no segmental disproportion to synapse elimination in this muscle. At all ages, there is a large diversity of motor unit sizes in the muscle. Synapse elimination therefore appears to maintain rather than decrease this diversity.(ABSTRACT TRUNCATED AT 400 WORDS)

Stiffness of cat soleus muscle and tendon during activation of part of muscle.

Experiments have been carried out on the soleus muscle and its tendon in the anesthetized cat. Measurements of isometric tension and muscle stiffness were made during contraction of whole or part of the muscle in response to stimulation of ventral root filaments. In an attempt to determine the distribution of tension in different portions of the tendon during activation of only part of the muscle, the free tendon of insertion was split longitudinally into two halves and a strain gauge attached to each piece. From a large number of measurements, it was found that the mean fraction of tension recorded in one-half of the tendon remained about the same, over a wide range of tensions. However, the scatter of values, which increased as the portion of muscle contracting was reduced, was greater than expected if muscle fibers were randomly distributed throughout the muscle. Measurements of muscle and tendon stiffness were made from length and tension changes during stretch of the actively contracting muscle. Ventral root stimulation that engaged 20% or more of the muscle yielded a value for tendon compliance (0.09 mm/N), which was the same as for stimulating the whole muscle. This result suggested that for contraction of portions as small as 20% of the muscle, fibers were effectively attached to the whole tendon, indicating that tendinous attachments of individual muscle fibers ran independent of one another over only a short distance and were bound together over most of their remaining course. It was concluded that groups of muscle fibers selected by stimulation of ventral root filaments are not entirely randomly distributed throughout the muscle. However, for groups representing larger fractions of the total tension, (greater than 20%) the distribution is uniform enough and the connections between their tendinous attachments firm enough for the force applied by such a group to act through a tendon compliance, which is the same as that seen by the whole muscle.

Motor innervation, motor unit organization and afferent innervation of m. extensor digitorum communis of the baboon's forearm

1. One hundred and fifty efferent axons innervating m. extensor digitorum communis (EDC) were isolated in filaments of C7 and C8 ventral roots of baboons. Conduction velocities were measured antidromically by stimulating the muscle nerve and recording from the filaments, and fell into two groups: a fast (49-84 m/sec) and a slow (22-41m/sec), presumably fusimotor group. The threshold for these latter axons exceeded the strength needed to elicit the maximal motor twitch.2. Stimulation of ventral root filaments containing slow axons produced no contractile tension in EDC.3. Stimulation of ventral root filaments containing fast-group axons elicited all-or-nothing twitches of motor units of EDC. The twitch tensions of 66.3% of the units were < 2.0 g wt.; only 8.7% were > 5.0 g wt. Tetanus-twitch ratios were 1.4-4.7 in a sample of 14 units. Contraction times were between 15 and 35 msec in 97% of the units. There was no correlation between contractile properties and axonal conduction velocity.4. Afferent volleys from the stimulated EDC nerve were recorded from C6 or C7 dorsal roots. The threshold was below the threshold for a just-detectable motor twitch in ten out of eleven baboons. Conduction velocity of the earliest component of the muscle afferent volley was 67-83 m/sec.5. The conduction velocities of twenty-eight spindle afferents, identified by their responses to linear stretches of EDC and by their unloading by maximal twitches, were all < 70 m/sec. Higher dynamic sensitivity tended to be associated with higher conduction velocity.

Fractionation of motor units by curare

The effect of curare upon the population of muscle fibers innervated by a single motor neuron has been investigated. Observations were made on motor units driven by stimulation of ventral root filaments and on units discharging reflexly in response to pinch of the ipsilateral hind paw. Recordings were made from the surface of the gastrocnemius and gracilis muscles of the rat with pairs of closely spaced electrodes. Curare was found to reduce reversibly the amplitude of responses from motor units in either of two patterns: (1) the amplitude remained at control levels until it abruptly dropped to zero or a very low value; (2) the amplitude declined gradually, with one or more abrupt downward “steps” and a large terminal “step.” Analysis of these effects with a fast sweep showed that decline in the amplitude of response was accompanied by an alteration in its form. Units which declined gradually in amplitude with “steps” were found to be made up of two or more components, each of which responded in all-or-none fashion. As the effect of curare developed, these components became distinguishable as separate entities because of unequal delays at their neuromuscular junctions. The originally synchronized responses, that is, began to fall more and more out of phase, which produced a gradual decline in amplitude. “Steps” occurred whenever a component dropped out entirely. An electronic analog of this desynchronization and fractionation of motor units was devised to help explain the results.