Spasticity and spastic dystonia: the two faces of velocity-dependent hypertonia

BackgroundSpasticity and spastic dystonia are two separate phenomena of the upper motor neuron syndrome. Spasticity is clinically defined by velocity-dependent hypertonia and tendon jerk hyperreflexia due to the hyper-excitability of the stretch reflex. Spastic dystonia is the inability to relax a muscle leading to a spontaneous tonic contraction. Both spasticity and spastic dystonia are present in patients who are at rest; however, only patients with spasticity are actually able to kept their muscles relaxed prior to muscle stretch. The idea that has inspired the present work is that also in patients with spastic dystonia the stretch reflex is likely to be hyper-excitable. Therefore, velocity-dependent hypertonia could be mediated not only by spasticity, but also by spastic dystonia.MethodsTonic stretch reflexes in the rectus femoris muscle were evoked in 30 patients with multiple sclerosis showing velocity-dependent hypertonia of leg extensors and the habituation of the reflex was studied. Moreover, the capability of relax the muscle prior to muscle stretch (spastic dystonia) was also investigated.ResultsA tonic stretch reflex was evoked in all the enrolled patients. 73% of the patients were able to relax their rectus femoris muscle prior to stretch (spasticity). In the overwhelming majority of these patients, the tonic stretch reflex decreased during repeated stretches. In the remaining 27% of the subjects, the muscle was tonically activated prior to muscle stretch (spastic dystonia). In the patients in whom spastic dystonia progressively increased over the subsequent stretches (50% of the subjects with spastic dystonia), the habituation of the reflex was replaced by a progressive reflex facilitation.DiscussionThis study shows for the first time that velocity-dependent hypertonia can be caused by two distinct phenomena: spasticity and spastic dystonia. The habituation of the tonic stretch reflex, which is a typical feature of spasticity, is replaced by a reflex facilitation in the half of the subject with spastic dystonia. These preliminary findings suggest that differentiating the two types of velocity-dependent muscle hypertonia (spasticity and spastic dystonia) could be clinically relevant.     

Time-course analysis of stretch reflexes in hemiparetic subjects using an on-line spasticity measurement system

Spasticity after a stroke is usually assessed in a score form by subjectively determining the resistance of a joint to an externally imposed passive movement. This work presents a spasticity measurement system for on-line quantifying the stretch reflex of paretic limbs. Four different constant stretch velocities in a ramp-and-hold mode are used to elicit the stretch reflex of the elbow joint in spastic subjects. The subjects are tested at supine position with the upper limb stretched towards the ground, in contrast with the horizontally stretched movement used in other studies. By subtracting the baseline torque, reflex torque measured at a selected low stretch velocity of 5 deg/sec, the influence of gravity torque and inertial in vertical stretching mode can be minimized. The averaged speed-dependent reflex torque (ASRT), defined as the measured torque deviated from the baseline torque, is used for quantifying the spastic hypertonia. Four subjects having incurred cerebrovascular accident (CVA) are recruited for time-course study in which the measurements are taken at 72 hours, one week, one month, three months, and six months after onset of stroke. During the development of spasticity, the changes of ASRT and velocity sensitivity of ASRT of the involved and the intact elbow joints are discussed.     

Measurements of human forearm viscoelasticity

In human subjects, stiffness of the relaxed elbow was measured by three methods, using a forearm manipulandum coupled to a.d.c. torque motor. Elbow stiffness calculated from frequency response characteristics increased as the driving amplitude decreased. Step displacements of the forearm produced restoring torques linearly related to the displacement. The stiffness was very similar to that calculated from natural frequencies at amplitudes above 0.1 rad. Thirdly, elbow stiffness was estimated from brief test pulses, 120 ms in duration, by mathematically simulating the torque-displacement functions. Stiffness values in the limited linear range (under +/- 0.1 rad) were higher than in the linear range of the first two methods. A major component of elbow stiffness appears to decay within 1 s. The coefficients of viscosity determined from the simulation were, however, very similar to those calculated from the frequency response. Test pulse simulation was then used to determine joint impedance for different, actively maintained elbow angles. Joint stiffness and viscosity increased with progressive elbow flexion.     

Superimposing noise linearizes the responses of primary muscle spindle afferents to sinusoidal muscle stretch

Experiments were conducted in anaesthetized and spinalized cats to measure the extent to which the non-linear response of Ia afferent fibers to sinusoidal muscle stretch as expressed by the peristimulus-time-histograms, PSTHs, can be transformed into a linear one by means of the superposition of random stretch ("mechanical noise"). The gastrocnemius muscles of one hind leg were stretched and the response to sinewave muscle stretch (amplitudes between 0.01 and 4.0 mm, frequencies between 0.1 and 20 Hz) were investigated while band-limited mechanical noise was superimposed on the sinewave stretch. The random stretch upper cut-off frequency was varied between 60 and 300 Hz; the displacements were normally distributed. The noise amplitude sigma, i.e. the standard deviation of the displacement distributions, was varied systematically between 0.002 and 0.4 mm. Mechanical noise was very effective in raising the mean discharge rate. Added to the sinusoidal stretch it prevented the cessation of firing during the release phase of the stretch cycle, or at least reduced the duration of discharge pauses, i.e., a linearization occurred. In general, the larger the noise amplitude, the more the amplitude of the fundamental harmonic component was attenuated and the phase lead reduced. Apart from this rule the particular combination of superimposing small noise (sigma less than 0.02 mm) on small sinewave stretch (A less than 0.02 mm) could enhance the depth of sinusoidal modulation of cycle histograms (compared with responses to pure sinusoids). Linearizing the sinewave response by additional noise allowed the estimation of frequency response characteristics in the otherwise non-linear range of amplitudes (sinewave amplitude 0.5-1.0 mm).(ABSTRACT TRUNCATED AT 250 WORDS)     

Viscous properties of human muscle during contraction.

The purpose of this study was to determine viscous properties of human muscle during plantarflexion efforts. Experiments were performed on 17 subjects with an ankle ergometer allowing sinusoidal oscillations during isometric contractions and isokinetic movements. Sinusoidal oscillations led to the expression of (i) Bode diagrams of the musculo-articular system allowing the determination of a damping coefficient (Bbode); and (ii) a viscous coefficient (Bsin) using an adaptation of Hill's equation to sinusoidal oscillations. Isokinetic movements led to torque-velocity relationships. They showed a fall in torque associated to an increase in angular velocity what was quantified by calculating a damping coefficient (Biso). Both experiments gave consistent results indicating that Bbode was the lowest viscous parameter. This difference is discussed in terms of (i) "analog" viscosity originating from muscle cross-bridges; and (ii) real mechanical damping of passive structures.     

Differences in stretch reflex responses of elbow flexor muscles during shortening, lengthening and isometric contractions

Stretch reflexes were evoked in elbow flexor muscles undergoing three different muscle contractions, i.e. isotonic shortening (SHO) and lengthening (LEN), and isometric (ISO) contractions. The intermuscle relationships for the magnitude of the stretch reflex component in the eletromyographic (EMG) activities of two main elbow flexor muscles, i.e. the biceps brachii (BB) and the brachioradialis (BRD), were compared among the three types of contractions. The subjects were requested to move their forearms sinusoidally (0.1 Hz) against a constant pre-load between elbow joint angles of 10° (0° = full extension) and 80° during SHO and LEN, and to keep an angle of 45° during the ISO. The perturbations were applied at the elbow angle of 45° in pseudo-random order. The EMG signals were rectified and averaged over a period of 100 ms before and 400 ms after the onset of the perturbation 40–50 times. From the ensemble averaged EMG waveform, the background activity (BGA), short (20–50 ms) and long latency (M2, 50–80, M3, 80–100 ms) reflex and voluntary activity (100–150 ms) components were measured. The results showed that both BGA and reflex EMG activity of the two elbow flexor muscles were markedly decreased during the lengthening contraction compared to the SHO and ISO contractions. Furthermore, the changes of reflex EMG components in the BRD muscle were more pronounced than those in the BB muscle, i.e. the ratios of M2 and M3 magnitudes between BRD and BB (BRD:BB) were significantly reduced during the LEN contractions. These results would suggest that the gain of long latency stretch reflex EMG activities in synergistic muscles might be modulated independently according to the model of muscle contraction. Accepted: 1 September 1997     

Muscular torque generation during imposed joint rotation: torque-angle relationships when subjects' only goal is to make a constant effort

It is a reasonable expectation that voluntarily activated spinal motoneurons will be further excited by increases in spindle afferent activity produced by muscle stretch. Human motor behavior attributed to tonic stretch reflexes and to reflexes recruited by relatively slow joint rotation has been reported from several laboratories. We reinvestigated this issue by rotating the elbow joint over the central portion of its range while subjects focused on keeping their elbow flexion effort constant at one of three different levels and made no attempt to control the position, speed or direction of movement of their forearm. There is evidence that subjects' voluntary motor status is constant under these conditions so that any change in torque would be of involuntary origin. On average, torques rose somewhat and then fell as the elbow was flexed through a range of 80 degrees at 10, 20 and 60 degrees/s and a similar pattern occurred during elbow extension; i.e., both concentric and eccentric torque-angle profiles had roughly similar shapes and neither produced consistent stabilizing cross-range stiffness. The negative stiffness (rising torque) during the early part of a concentric movement and the negative stiffness (falling torque) during the later part of an eccentric movement would not have occurred if a stabilizing stretch reflex had been present. Positive stiffness rarely gave rise to torque changes greater than 20% in either individual or cross-subject averaged data. When angular regions of negative stiffness are combined with regions of low positive stiffness (torque change 10% or less), much of the range of motion was not well stabilized, especially during eccentric movements. The sum of the EMGs from biceps brachii, brachioradialis and brachialis showed a pattern opposite to that expected for a stretch reflex; there was an upward trend in the EMG as the elbow was flexed and a downward trend as the elbow was extended. There was little change in the shape of this EMG-angle relationship with either direction or velocity. The individual EMG-angle relationships were distinctive for each of these three elbow flexor muscles in four of the six subjects; in the remaining two, biceps was distinctive, but brachioradialis and brachialis appeared to be coupled. Although the EMGs of individual muscles were modulated over the angular range, no consistent stretch reflexes could be seen in the individual records. Thus, we could find no clear evidence for stretch reflex stabilization of human subjects maintaining a constant effort. Rather, muscle torque appears to be reflexly modulated across a much used portion of the elbow's angular range so that any appreciable stabilizing stiffness that is sustained for more than fractions of a second is associated with a change in effort.     

Muscular torque generation during imposed joint rotation: torque-angle relationships when subjects' only goal is to make a constant effort

It is a reasonable expectation that voluntarily activated spinal motoneurons will be further excited by increases in spindle afferent activity produced by muscle stretch. Human motor behavior attributed to tonic stretch reflexes and to reflexes recruited by relatively slow joint rotation has been reported from several laboratories. We reinvestigated this issue by rotating the elbow joint over the central portion of its range while subjects focused on keeping their elbow flexion effort constant at one of three different levels and made no attempt to control the position, speed or direction of movement of their forearm. There is evidence that subjects' voluntary motor status is constant under these conditions so that any change in torque would be of involuntary origin. On average, torques rose somewhat and then fell as the elbow was flexed through a range of 80° at 10, 20 and 60°/s and a similar pattern occurred during elbow extension; i.e., both concentric and eccentric torque-angle profiles had roughly similar shapes and neither produced consistent stabilizing cross-range stiffness. The negative stiffness (rising torque) during the early part of a concentric movement and the negative stiffness (falling torque) during the later part of an eccentric movement would not have occurred if a stabilizing stretch reflex had been present. Positive stiffness rarely gave rise to torque changes greater than 20% in either individual or cross-subject averaged data. When angular regions of negative stiffness are combined with regions of low positive stiffness (torque change 10% or less), much of the range of motion was not well stabilized, especially during eccentric movements. The sum of the EMGs from biceps brachii, brachioradialis and brachialis showed a pattern opposite to that expected for a stretch reflex; there was an upward trend in the EMG as the elbow was flexed and a downward trend as the elbow was extended. There was little change in the shape of this EMG-angle relationship with either direction or velocity. The individual EMG-angle relationships were distinctive for each of these three elbow flexor muscles in four of the six subjects; in the remaining two, biceps was distinctive, but brachioradialis and brachialis appeared to be coupled. Although the EMGs of individual muscles were modulated over the angular range, no consistent stretch reflexes could be seen in the individual records. Thus, we could find no clear evidence for stretch reflex stabilization of human subjects maintaining a constant effort. Rather, muscle torque appears to be reflexly modulated across a much used portion of the elbow's angular range so that any appreciable stabilizing stiffness that is sustained for more than fractions of a second is associated with a change in effort.     

Characterization of muscle spindle afferents in the adult mouse using an in vitro muscle-nerve preparation

We utilized an in vitro adult mouse extensor digitorum longus (EDL) nerve-attached preparation to characterize the responses of muscle spindle afferents to ramp-and-hold stretch and sinusoidal vibratory stimuli. Responses were measured at both room (24°C) and muscle body temperature (34°C). Muscle spindle afferent static firing frequencies increased linearly in response to increasing stretch lengths to accurately encode the magnitude of muscle stretch (tested at 2.5%, 5% and 7.5% of resting length [Lo]). Peak firing frequency increased with ramp speeds (20% Lo/sec, 40% Lo/sec, and 60% Lo/sec). As a population, muscle spindle afferents could entrain 1:1 to sinusoidal vibrations throughout the frequency (10-100 Hz) and amplitude ranges tested (5-100 μm). Most units preferentially entrained to vibration frequencies close to their baseline steady-state firing frequencies. Cooling the muscle to 24°C decreased baseline firing frequency and units correspondingly entrained to slower frequency vibrations. The ramp component of stretch generated dynamic firing responses. These responses and related measures of dynamic sensitivity were not able to categorize units as primary (group Ia) or secondary (group II) even when tested with more extreme length changes (10% Lo). We conclude that the population of spindle afferents combines to encode stretch in a smoothly graded manner over the physiological range of lengths and speeds tested. Overall, spindle afferent response properties were comparable to those seen in other species, supporting subsequent use of the mouse genetic model system for studies on spindle function and dysfunction in an isolated muscle-nerve preparation.