The tonic stretch reflex and spastic hypertonia after spinal cord injury

The operational definition of spasticity is focused on increased resistance of joints to passive rotation and the possible origin of this increased resistance in the induced tonic stretch reflex (TSR). This term is applied in the context of both cerebral and spinal injury, implying that a similar reflex mechanism underlies the two disorders. From recent studies it is clear that increased passive joint resistance in resting limbs following stroke is highly correlated with the induced TSR, but this evidence is lacking in spinal injury. The contribution of the TSR to hypertonia in spinal cord injury (SCI) is unclear and it is possible that hypertonia has a different origin in SCI. The contribution of resting and activated TSR activity to joint stiffness was compared in SCI and normal subjects. The magnitude of the TSR in ankle dorsiflexors (DF) and plantarflexors (PF) and mechanical ankle resistive torque were measured at rest and over a range of contraction levels in normal subjects. Similar measures were made in 13 subjects with SCI to the limits of their range of voluntary contraction. Normals and SCI received a pseudo-sinusoidal stretch perturbation of maximum amplitude +/- 20 degrees and frequency band 0.1-3.5 Hz that was comparable to that used in manual clinical testing of muscle tone. Elastic resistance and resonant frequency of the ankle joint, after normalization for limb volume, were significantly lower in complete and incomplete SCI than normal subjects. No reflex response related to stretch velocity was observed. Resting DF and PF TSR gain, when averaged over the tested band of frequencies, were significantly lower in complete SCI than in resting normal subjects (<0.5 microV/deg). Linear regression analysis found no significant relationship between TSR gain and resting joint stiffness in SCI. Mean TSR gain of DFs and PFs at rest was not correlated with the subject variables: age, time since SCI, level of injury, Frankel score, number of spasms per day, Ashworth score or anti-spastic medication. DF and PF reflex gain were linearly related to voluntary contraction level and regression analysis produced similar slopes in incomplete SCI and normal subjects. Hence TSR loop gain was not significantly increased in SCI at any equivalent contraction level. Extrapolation of the regression lines to zero contraction level predicted that reflex threshold was not reduced in SCI. Low frequency passive stretches did not induce significant TSR activity in the resting limbs of any member of this SCI group. The TSR thus did not contribute to their clinical hypertonia. Other reflex mechanisms must contribute to hypertonia as assessed clinically. This result contrasts with our similar study of cerebral spasticity after stroke, where a comparable low frequency stretch perturbation produced clear evidence of increased TSR gain that was correlated with the hypertonia at rest. We conclude that a low frequency stretch perturbation clearly distinguished between spasticity after stroke and SCI. Spasticity in the two conditions is not equivalent and care should be taken in generalizing results between them.     

Identification of intrinsic and reflex ankle stiffness components in stroke patients

Reflex and intrinsic contributions to ankle stiffness were examined in 11 stroke patients with clinical evidence of ankle spasticity and nine gender-matched and age-matched controls. Subjects lay supine with one foot placed in a custom-fitted boot attached to an electro-hydraulic actuator. They were instructed to relax while pseudo-random binary sequence perturbations were applied to their ankle joint. The ankle position and torque, as well as EMG from the ankle dorsiflexors and plantarflexors were recorded. These were used to identify reflex and intrinsic components of ankle stiffness, using a non-linear, parallel-cascade, system identification method. Results demonstrated that the majority of stroke patients (7/11) had ankle stiffness similar to that of control subjects. In contrast, a minority of stroke patients (4/11) had an abnormal increase in ankle stiffness, most of which could be attributed to an increased reflex gain. Reflex stiffness increased as the ankle was dorsiflexed in all subjects. These results differ from a previous study showing that reflex gain and intrinsic stiffness were increased in all patients with spinal cord injury. This difference may reflect the different topography of the lesions in the two neurological conditions.     

Intrinsic and reflex contributions to human ankle stiffness: variation with activation level and position

A parallel-cascade system identification method was used to identify intrinsic and reflex contributions to dynamic ankle stiffness over a wide range of tonic voluntary contraction levels and ankle positions in healthy human subjects. Intrinsic stiffness dynamics were described well by a linear pathway having elastic, viscous, and inertial properties. A velocity-sensitive pathway comprising a delay, a static non-linearity, resembling a half-wave rectifier, followed by a low-pass filter, described reflex stiffness dynamics. The absolute magnitude of intrinsic and reflex stiffness parameters varied from subject to subject but the relative changes with contraction level and position were consistent. Intrinsic stiffness increased monotonically with contraction level while reflex stiffness was maximal at low contraction levels and then decreased. Intrinsic and reflex stiffness both increased as the ankle was dorsiflexed. As a result, reflex mechanics made their largest relative contributions near the neutral position at low levels of activity. The size of the maximum reflex contribution varied widely among subjects, in some it was so small (ca 1%) that it would be unlikely to have any functional importance; however, in other subjects, reflex contributions were large enough (as high as 55% in one case) to play a significant role in the control of posture and movement. This variability may have arisen because stretch reflexes were not useful for the torque-matching task in these experiments. It will be of interest to examine other tasks where stretch reflexes would have a direct impact on performance.     

Voluntary modulation of human stretch reflexes

It has been postulated that the central nervous system (CNS) can tune the mechanical behavior of a joint by altering reflex stiffness in a task-dependant manner. However, most of the evidence supporting this hypothesis has come from the analysis of H-reflexes or electromyogram (EMG) responses. Changes in overall stiffness have been documented but, as yet, there is no direct evidence that the CNS can control reflex stiffness independently of the intrinsic stiffness. We have used a novel identification algorithm to estimate intrinsic and reflex stiffness and feed it back to subjects in real-time. Using this biofeedback, subjects could learn to control reflex stiffness independently of intrinsic stiffness. At low torque levels, subjects could vary their reflex stiffness gain by a factor of 4, while maintaining elastic stiffness and torque constant. EMG measurements confirmed that the contraction levels of the ankle muscles remained constant. Further experiments showed that subjects could change their reflexes rapidly on command. Thus, we conclude that the CNS can control reflex stiffness independently and so has great flexibility in adjusting the mechanical properties of a joint to meet functional requirements.     

Frequency response characteristics of ankle plantar flexors in humans following spinal cord injury: relation to degree of spasticity

Frequency response characteristics of the ankle plantar flexors were studied in adults both with and without spinal cord injury (SCI) to determine how the muscle contractile properties change after SCI, and to see if there is a relation between the severity of spasticity and how the properties change. Ten controls and ten complete, chronic spinal cord injured subjects were tested, where the tibial nerve was stimulated electrically in a stochastic manner with the ankle fixed isometrically at various joint angles. A nonparametric linear frequency response function was derived, from which a second-order transfer function was calculated. The contractile dynamics were then characterized by the three classic second-order parameters: gain, damping ratio, and natural frequency. We found that in subjects with low degrees of spasticity (as determined by clinical evaluation), the contractile dynamics presented the largest changes, in which the speed of contraction increased significantly while there were no statistical differences in the gains between the two groups. This similarity emerged even though there was noticeable atrophy in the SCI patient group. Differences between the controls and subjects with high levels of spasticity were markedly different, in that these SCI subjects had slower contractile speeds than the controls, but significantly lower gains. Moderately spastic subjects fell somewhere in between, where the speed of muscle contraction increased modestly yet the gain was significantly smaller than that of the control subjects. These findings indicate that in subjects with chronic spinal cord injury, the severity of spasticity can significantly influence the degree of change in muscle contractile properties. It appears that high degrees of spasticity tend to preserve contractile dynamics, while in less spastic subjects, muscle contractile properties may display faster response characteristics. © 2002 Biomedical Engineering Society. PAC2002: 8719Ff, 8717Nn, 8754Dt, 8719Rr     

Stiffness regulation by reflex action in the normal human hand

1. The torque and electromyographic (EMG) responses to stretch of the first dorsal interosseous muscle (externally imposed joint rotation) were recorded in five normal human subjects. The total measured stiffness was decomposed into three individual stiffness components; passive, intrinsic, and reflex. 2. The passive component was measured with the subject relaxed. Compared with the total response at the height of short latency reflex action, the passive component comprised 6-32% of the total stiffness recorded at an initial torque level of 20 N-cm [15-39% maximum voluntary contraction (MVC)]. The passive response also reflected a significant acceleration component during rapid joint rotation due primarily to digit inertia. 3. The intrinsic stiffness component, attributed to the mechanical properties of the active muscle fibers, was estimated by recording the response to joint rotation with the muscle activated in a distributed manner using a single intramuscular electrode. The dynamic stiffness (measured at the end of a ramp displacement) and the static stiffness (measured 1 s after onset of the displacement) both scaled in a straight-line manner with the initial torque level. This relationship held whether the initial torque level was varied by changes in recruitment or temporal summation. 4. The reflex component was calculated by subtracting the passive and the estimated intrinsic component from the total response. The timing of the EMG signal recorded during measurement of the total response and the fact that the estimated intrinsic component matched the total active response over the first 65-100 ms after displacement onset supported the case that this was the true reflex component. The peak of the reflex activity occurred 155-360 ms after displacement onset and, at this peak, accounted for 18-44% of the total stiffness (at an initial torque level of 20 N-cm). 5. Over the low to intermediate torque range employed, we observed that both intrinsic muscle stiffness and total stiffness increased with initial torque. Because total stiffness increased more rapidly than intrinsic stiffness, the difference between them (equal to reflex stiffness) also increased with initial torque. Furthermore, when the total active response trials (passive stiffness removed) were shifted vertically so that the initial torque levels matched, it was seen that reflex action did not reduce the stiffness range to less than the stiffness range encountered for the intrinsic response alone.(ABSTRACT TRUNCATED AT 400 WORDS)     

Flexor reflex responses triggered by imposed knee extension in chronic human spinal cord injury

Hypersensitivity of the flexor reflex pathways to input from force-sensitive muscle afferents may contribute to the prevalence and severity of muscle spasms in patients with spinal cord injury (SCI). In this study, we triggered flexor reflexes with constant velocity knee movements in 15 subjects with SCI. Ramp and hold knee extension perturbations were imposed on one leg while the hip and ankle were held in an isometric position using an instrumented leg brace. Knee, ankle and hip torque responses and electromyograms from six muscles of the leg were recorded following controlled knee extension at four different velocities. Tests were conducted with the hip in both flexed and extended positions. During the movement into knee extension, a velocity-dependent stretch reflex, represented by a progressively increasing knee flexion torque, was observed. In addition, another type of reflex that resembled a flexor reflex (flexion of the hip and ankle) was also triggered by the imposed knee extension. The magnitude of the ankle dorsiflexion torque responses was significantly correlated to the stretch reflex torque at the knee in 9 of the 15 subjects. We concluded that stretch reflexes initiate a muscle contraction that then can contribute to a flexor reflex response, possibly through muscle group III/IV afferent pathways. These results suggest that spasticity in SCI consists of a myriad of complex reflex responses that extend beyond stretch reflexes.     

Muscle stiffness in human ankle dorsiflexors: intrinsic and reflex components

1. The purpose of this study was to evaluate the mechanical response to stretch in normal human ankle dorsiflexors at different levels of voluntary contraction. In an active muscle, the total mechanical response is the sum of the intrinsic response from the contractile apparatus, the response from passive tissues, and the reflex mediated response. Each of these components was investigated. 2. The total incremental stiffness was defined as the ratio between the torque increment and the amplitude of the stretch. In 14 subjects the total stiffness increased from approximately 0.6 N.m/deg to approximately 2.5 N.m/deg at 50% of MVC and remained constant (+/- 10%) from 30 to 80% of MVC. 3. The contribution to incremental stiffness from intrinsic muscle properties was measured during electrical stimulation of the deep peroneal nerve at 7-50 Hz. Intrinsic stiffness increased linearly with torque from approximately 0.5 N.m/deg to approximately 2.5 N.m/deg at 80% of MVC. 4. The reflex component (total minus intrinsic stiffness) had a maximum of 0.5-1.5 N.m/deg at 30-50% of MVC and was approximately zero at no and maximal contraction. For intermediate levels of contraction the reflex increased the stiffness with 40-100% of the intrinsic stiffness in this flexor muscle. 5. The reflex contribution to total stiffness began approximately 50 ms after onset of stretch and peaked 150-300 ms after onset of stretch. 6. Total, intrinsic, and reflex mediated stiffness were all nearly independent of the amplitude of stretch in the range from 2 to 7 degrees. The higher stiffness observed for 1 degree stretches could be due to "short range stiffness" of the cross bridges. 7. Stretching of a contracting muscle generates large force increments even for moderate amplitudes of stretch. Approximately half of this force increment is due to the stretch reflex, which makes the muscle stiffer than predicted from the intrinsic stiffness. These findings in human flexor muscles are surprisingly similar to previous findings in extensor muscles of the decerebrate cat.     

Time course quantification of spastic hypertonia following spinal hemisection in rats

Progressive changes in the muscle tone and stretch reflex after spinal cord injury (SCI) provide insight into the time-course development of spasticity. This study quantified the time-course changes of hypertonia for rats following SCI of T8 hemisection. A miniature manual stretching device measured the reactive torque via a pair of pressure sensing balloons; the angular displacement was measured via an optoelectronic device. Various stretching frequencies were tested, specifically 1/3, 1/2, 1, 3/2 and 2 Hz. The reactive torque and angular displacement were used to derive the viscous and elastic components representing the viscosity and stiffness of the rat's ankle joint. The enhanced velocity-dependent properties of spasticity were observed in the SCI hemisection rats (n=9) but not in the controls (n=9). Time-course measurements from pre-surgery to 56 days following SCI showed that the muscle tone of the hemisection rats dropped immediately after spinal shock and then gradually increased to reach a peak around 21 days postinjury (P<0.01). The muscle tone remained at least 75% of the peak value up to the end of an 8 week observation period (P<0.05). The changes of muscle tone can also be verified from the electrophysiological evaluations of electromyography (EMG) (P<0.05). In addition to conventional BBB motor behavior score, our results provided time-course quantification of the biomechanical and electrophysiological properties of muscle tone from the onset of SCI. Such data are useful for investigating progressive recovery of spinal damage in animal model and for future objective assessment of improved treatment for SCI human subjects.     

Bilateral oscillatory hip movements induce windup of multijoint lower extremity spastic reflexes in chronic spinal cord injury

After spinal cord injury (SCI), alterations in intrinsic motoneuron properties have been shown to be partly responsible for spastic reflex behaviors in human SCI. In particular, a dysregulation of voltage-dependent depolarizing persistent inward currents (PICs) may permit sustained muscle contraction after the removal of a brief excitatory stimulus. Windup, in which the motor response increases with repeated activation, is an indicator of PICs. Although windup of homonymous stretch reflexes has been shown, multijoint muscle activity is often observed following imposed limb movements and may exhibit a similar windup phenomenon. The purpose of this study was to identify and quantify windup of multijoint reflex responses to repeated imposed hip oscillations. Ten chronic SCI subjects participated in this study. A custom-built servomotor apparatus was used to oscillate the legs about the hip joint bilaterally and unilaterally from 10° of extension to 40° flexion for 10 consecutive cycles. Surface electromyograms (EMGs) and joint torques were recorded from both legs. Consistent with a windup response, hip and knee flexion/extension and ankle plantarflexion torque and EMG responses varied according to movement cycle number. The temporal patterns of windup depended on the muscle groups that were activated, which may suggest a difference in the response of neurons in different spinal pathways. Furthermore, because windup was seen in muscles that were not being stretched, these results imply that changes in interneuronal properties are also likely to be associated with windup of spastic reflexes in human SCI.     

Stretch reflexes and joint dynamics in rheumatoid arthritis

In clinically diagnosed rheumatoid arthritis (RA), studies were conducted to investigate the reflex and passive tissue contribution to measured increases in joint stiffness in the resting upper limb and during constant contractions of an attached muscle. The tonic stretch reflex was induced by a servo-controlled sinusoidal stretch perturbation of the metacarpophalangeal joint of RA patients, and age- and sex-matched controls. The resulting reflexes and mechanical changes in the RA affected joint were explored. Surface electromyographic (EMG) measurements were obtained from first dorsal interosseus muscle. Reflex gain (EMG/joint angle amplitude ratio), phase difference (reflex delay after stretch), coherence square (proportion of EMG variance accounted for by joint angle changes), joint mechanical gain (torque–joint angle amplitude ratio) and mechanical phase difference (torque response delay after stretch) were determined. RA patients showed decreased reflex gain that was partly due to coexistent severe muscle weakness, as determined from maximum voluntary contraction and grip pressure estimates. The decreased reflex gain was most evident at high stretch frequency suggesting a disproportionate loss of the large diameter afferent response and also increased reflex delay in the patients. These changes ensemble suggest significant loss of neural drive to the motor unit population. Patients also showed increased joint stiffness (measured as torque gain) in the contracting muscle, but there was no evidence of reflex activity or increased stiffness at rest. This suggests that the increased joint stiffness in RA was due to changes in the mechanical properties of the active muscle–joint system rather than changes in reflex properties.     

Neuromuscular abnormalities associated with spasticity of upper extremity muscles in hemiparetic stroke

Our objective was to assess the mechanical changes associated with spasticity in elbow muscles of chronic hemiparetic stroke survivors and to compare these changes with those recorded in the ankle muscles of a similar cohort. We first characterized elbow dynamic stiffness by applying pseudorandom binary positional perturbations to the joints at different initial angles, over the entire range of motion, with subjects relaxed. We separated this stiffness into intrinsic and reflex components using a novel parallel cascade system identification technique. In addition, for controls, we studied the nonparetic limbs of stroke survivors and limbs of age-matched healthy subjects as primary and secondary controls. We found that both reflex and intrinsic stiffnesses were significantly larger in the stroke than in the nonparetic elbow muscles, and the differences increased as the elbow was extended. Reflex stiffness increased monotonically with the elbow angle in both paretic and nonparetic sides. In contrast, the modulation of intrinsic stiffness with elbow position was different in nonparetic limbs; intrinsic stiffness decreased sharply from full- to mid-flexion in both sides, then it increased continuously with the elbow extension in the paretic side. It remained invariant in the nonparetic side. Surprisingly, reflex stiffness was larger in the nonparetic than in the normal control arm, yet intrinsic stiffness was smaller in the nonparetic arm. Finally, we compare the angular dependence of paretic elbow and ankle muscles and show that the modulation of reflex stiffness with position was strikingly different.     

Spastic reflexes triggered by ankle load release in human spinal cord injury

The rapid decrease in firing of load-sensitive group Ib muscle afferents during unloading may be particularly important in triggering the swing phase of gait. However, it still remains unclear whether load-sensitive muscle afferents modulate reflex activity in human spinal cord injury (SCI), as suggested by studies in the cat. The right hip of 12 individuals with chronic SCI was subjected to ramp (60 degrees /s) and hold (10 s) movements over a range from 40 degrees flexion to 0-10 degrees extension using a custom servomotor system. An ankle dorsiflexion load was imposed and released after the hip reached a targeted position using a custom-designed pneumatic motor system. Isometric joint torques of the hip and knee, reaction torque of the ankle, and surface electromyograms (EMGs) from eight muscles of the leg were recorded following the imposed hip movement and ankle load release. Reflexes, characterized by hip flexion torque, knee extension, and coactivation of ankle flexors and extensors, were triggered by ankle load release when the hip was in an extended position. The ankle load release was observed to enhance the reflexes triggered by hip extension itself, suggesting that ankle load afferents play an important role in spastic reflexes in human SCI and that the reflex pathways associated with ankle load afferents have important implications in the spinal reflex regulation of human movement. Such muscle behaviors emphasize the role of ankle load afferents and hip proprioceptors on locomotion. This knowledge may be especially helpful in the treatment of spasms and in identifying rehabilitation strategies for producing functional movements in human SCI.     

Reflex and intrinsic changes induced by fatigue of human elbow extensor muscles

Fatigue-induced changes in intrinsic and reflex properties of human elbow extensor muscles and the underlying mechanisms for fatigue compensation were investigated. The elbow joint was perturbed using small-amplitude and pseudorandom movement patterns while subjects maintained steady levels of mean joint extension torque. Intrinsic and reflex properties were identified simultaneously using a nonlinear delay differential equation model. Intrinsic joint properties were characterized by measures of joint stiffness, viscous damping, and limb inertia and reflex properties characterized by measures of dynamic and static reflex gains. Fatigue was induced using 15 min of intermittent voluntary isometric (submaximal) exercise, and a rest period of 10 min was taken to allow the fatigued muscles to recover from acute fatigue effects. Identical experimental and data analysis procedures were used before and after fatigue. Our findings were that after fatigue, joint stiffness was significantly reduced at higher torque levels, presumably reflecting the reduced force-generating capacity of fatigued muscles. Conversely, joint viscosity was increased after fatigue potentially because of the reduced crossbridge detachment rate and prolonged relaxation associated with intracellular acidosis accompanying fatigue. Static stretch reflex gain decreased significantly at higher torque levels after fatigue, indicating that the isometric fatiguing exercise might be associated with a preferential change in properties of spindle chain fibers and bag(2) fibers. For matched pre- and postfatigue torque levels, dynamic reflexes contributed relatively more torque after fatigue, displaying higher dynamic reflex gains and larger dynamic electromyographic responses elicited by the controlled small-amplitude position perturbations. These changes appear to counteract the fatigue-induced reductions in joint stiffness and static reflex gain. The compensatory responses could be partly due to the effects of increasing the number of active motoneurons innervating the fatiguing muscles. This shift in operating point gave rise to significant compensation for the loss of contractile force. The compensation could also be due to fusimotor adjustment, which could make the dynamic reflex gain much less sensitive to fatigue than intrinsic stiffness. In short, the reduced contribution from intrinsic stiffness to joint torque was compensated by increased contribution from dynamic stretch reflexes after fatigue.     

Afferent mechanisms for the reflex response to imposed ankle movement in chronic spinal cord injury

We have reported earlier that externally imposed ankle movements trigger ankle and hip flexion reflexes in individuals with spinal cord injury (SCI). In order to examine the afferent mechanisms underlying these movement-triggered reflexes, controlled ankle movements were imposed in 17 SCI subjects. In 13 of these subjects, reflex torques were recorded at the hip, knee and ankle in response to 5 ankle movement ranges, and 4 movement speeds. Subjects were tested using both ankle plantarflexion and dorsiflexion movements. The principal outcome measure, peak hip flexion torque of the induced reflexes, was used for comparing the effects of movement range and speed on the reflex response. We found that movement-triggered reflexes were sensitive to the angular range of ankle deflection, but insensitive to the velocity of the movement. Movement amplitudes sufficient to trigger hip and ankle flexion were routinely associated with increases in ankle passive force, suggesting that force-sensitive receptors participated in the reflex response. However, increases in angular range also corresponded to increases in muscle length, making it difficult to distinguish whether the response was triggered by a load-sensitive receptor (e.g., Golgi tendon organ or muscle free nerve ending) or a position-sensitive receptor responsive to absolute ankle angle (e.g., muscle spindle secondary afferent). The absence of velocity dependence of the reflex suggested that spindle Ia afferents were not major contributors. These results suggest movement-triggered reflexes originate in muscle receptors that are sensitive to either absolute muscle length, to muscle force or to both. Although receptors that are sensitive to absolute muscle length cannot be excluded with certainty, the finding that reflex responses require that ankle movements elicit an increase in passive force argues for a prominent role of nonspindle mechanoreceptors, such as group III/IV muscle afferents. These afferents are activated preferentially as muscles are stretched to near maximum length, and they appear to have potent reflex effects in spinal cord injury.     

The Effects of Sex,Joint Angle,and the Gastrocnemius Muscle on Passive Ankle Joint Complex Stiffness

OBJECTIVE: To assess the effects of sex, joint angle, and the gastrocnemius muscle on passive ankle joint complex stiffness (JCS). DESIGN AND SETTING: A repeated-measures design was employed using sex as a between-subjects factor and joint angle and inclusion of the gastrocnemius muscle as within-subject factors. All testing was conducted in a neuromuscular research laboratory. SUBJECTS: Twelve female and 12 male healthy, physically active subjects between the ages of 18 and 30 years volunteered for participation in this study. The dominant leg was used for testing. No subjects had a history of lower extremity musculoskeletal injury or circulatory or neurologic disorders. MEASUREMENTS: We determined passive ankle JCS by measuring resistance to passive dorsiflexion (5 degrees.s(-1)) from 23 degrees plantar flexion (PF) to 13 degrees dorsiflexion (DF). Angular position and torque data were collected from a dynamometer under 2 conditions designed to include or reduce the contribution of the gastrocnemius muscle. Separate fourth-order polynomial equations relating angular position and torque were constructed for each trial. Stiffness values (Nm.degree(-1)) were calculated at 10 degrees PF, neutral (NE), and 10 degrees DF using the slope of the line at each respective position. RESULTS: Significant condition-by-position and sex-by-position interactions and significant main effects for sex, position, and condition were revealed by a 3-way (sex-by-position, condition-by-position) analysis of variance. Post hoc analyses of the condition-by-position interaction revealed significantly higher stiffness values under the knee-straight condition compared with the knee-bent condition at both ankle NE and 10 degrees DF. Within each condition, stiffness values at each position were significantly higher as the ankle moved into DF. Post hoc analysis of the sex-by-position interaction revealed significantly higher stiffness values at 10 degrees DF in the male subjects. Post hoc analysis of the position main effect revealed that as the ankle moved into dorsiflexion, the stiffness at each position became significantly higher than at the previous position. CONCLUSIONS: The gastrocnemius contributes significantly to passive ankle JCS, thereby providing a scientific basis for clinicians incorporating stretching regimens into rehabilitation programs. Further research is warranted considering the cause and application of the sex-by-position interaction.     

Spacing practice sessions across days earlier rather than later in training improves performance of a visuomotor skill

Reduced depression of transmitter release from Ia afferents following previous activation (post-activation depression) has been suggested to be involved in the pathophysiology of spasticity. However, the effect of this mechanism on the myotatic reflex and its possible contribution to increased reflex excitability in spastic participants has not been tested. To investigate these effects, we examined post-activation depression in Soleus H-reflex responses and in mechanically evoked Soleus stretch reflex responses. Stretch reflex responses were evoked with consecutive dorsiflexion perturbations delivered at different intervals. The magnitude of the stretch reflex and ankle torque response was assessed as a function of the time between perturbations. Soleus stretch reflexes were evoked with constant velocity (175°/s) and amplitude (6°) plantar flexion perturbations. Soleus H-reflexes were evoked by electrical stimulation of the tibial nerve in the popliteal fossa. The stretch reflex and H-reflex responses of 30 spastic participants (with multiple sclerosis or spinal cord injury) were compared with those of 15 healthy participants. In the healthy participants, the magnitude of the soleus stretch reflex and H-reflex decreased as the interval between the stimulus/perturbation was decreased. Similarly, the stretch-evoked torque decreased. In the spastic participants, the post-activation depression of both reflexes and the stretch-evoked torque was significantly smaller than in healthy participants. These findings demonstrate that post-activation depression is an important factor in the evaluation of stretch reflex excitability and muscle stiffness in spasticity, and they strengthen the hypothesis that reduced post-activation depression plays a role in the pathophysiology of spasticity.     

Passive stiffness of the gastrocnemius muscle in athletes with spastic hemiplegic cerebral palsy

The passive properties of the muscle–tendon unit are regularly assessed in individuals with cerebral palsy (CP). However, no information is available on the passive properties of adult muscle, and whether any differences exist between the paretic and control muscles. Eleven ambulant male athletes with spastic hemiplegic CP (21.2 ± 3.0 years) and controls without neurological impairment (age = 21.8 ± 2.2 years) completed two and one passive stretch session, respectively. During each session, the ankle was passively dorsiflexed until end range of motion (ROM), whilst recording passive ankle angle, torque and gastrocnemius medialis (GM) myotendinous junction (MTJ) displacement. In addition, GM cross-sectional area (CSA) and length were measured. Subsequently, in vivo stress and strain were determined to calculate elastic modulus. Passive stiffness, MTJ displacement and ROM of the paretic GM were not different from the control muscles. However, the elastic modulus of the paretic GM was two times stiffer than the control GM muscles. In conclusion, athletes with CP exhibit absolute passive muscle stiffness similar to the controls; however, the elastic modulus of the CP muscle was significantly greater. Therefore, throughout the same ROM a smaller GM CSA in CP athletes has to dissipate larger relative torque compared to the control muscles, consequently causing the muscle to elongate to the same extent as the non-paretic muscle under stretch.     

The passive, human calf muscles in relation to standing: the non-linear decrease from short range to long range stiffness

During human standing, tonic ankle extensor torque is required to support the centre of mass (CoM) forward of the ankles, and dynamic torque modulation is required to maintain unstable balance. Passive mechanisms contribute to both but the extent is controversial. Some groups have revealed a substantial intrinsic stiffness (65–90%) normalized to load stiffness, ' mgh '. Others regard their methodology as unsuitable for the low-frequency conditions of quiet standing and believe the passive contribution to be small (10–15%). Here we applied low-frequency ankle rotations to upright subjects who were supported at the waist allowing the leg muscles to be passive and we report normalized stiffness. The passive calf muscles provided: (i) an extensor torque capable of sustaining unstable balance without tonic activity at a mean CoM–ankle angle of 1.6 deg, (ii) a long range stiffness of 13 ± 2% and (iii) a short range (< 0.2 deg) stiffness of 67 ± 8%. Chordal ankle stiffness, derived from the torque versus angle relationship for 7 deg rotations, shows a non-linear decrease (stiffness α rotation^{−0.33±0.04}) from 101 ± 9% to 19 ± 5% for rotations of 0.03–7 deg, respectively. Thus, passive stiffness is well adapted for the continuum of postural and movement activity and has a substantial postural role eliminating the need for continuous muscle activity and increasing the unstable time constant of the human inverted pendulum. Ignoring the non-linear dependence of passive stiffness on sway size could lead to serious misinterpretation of experiments using perturbations and sensory manipulations such as eye closure, sway referencing and altered support surfaces.     

Direct measurement of human ankle stiffness during quiet standing: the intrinsic mechanical stiffness is insufficient for stability

During quiet standing the human 'inverted pendulum' sways irregularly. In previous work where subjects balanced a real inverted pendulum, we investigated what contribution the intrinsic mechanical ankle stiffness makes to achieve stability. Using the results of a plausible model, we suggested that intrinsic ankle stiffness is inadequate for providing stability. Here, using a piezo-electric translator we applied small, unobtrusive mechanical perturbations to the foot while the subject was standing freely. These short duration perturbations had a similar size and velocity to movements which occur naturally during quiet standing, and they produced no evidence of any stretch reflex response in soleus, or gastrocnemius. Direct measurement confirms our earlier conclusion; intrinsic ankle stiffness is not quite sufficient to stabilise the body or pendulum. On average the directly determined intrinsic stiffness is 91 ± 23 % (mean ± s.d. ) of that necessary to provide minimal stabilisation. The stiffness was substantially constant, increasing only slightly with ankle torque. This stiffness cannot be neurally regulated in quiet standing. Thus we attribute this stiffness to the foot, Achilles' tendon and aponeurosis rather than the activated calf muscle fibres. Our measurements suggest that the triceps surae muscles maintain balance via a spring-like element which is itself too compliant to guarantee stability. The implication is that the brain cannot set ankle stiffness and then ignore the control task because additional modulation of torque is required to maintain balance. We suggest that the triceps surae muscles maintain balance by predictively controlling the proximal offset of the spring-like element in a ballistic-like manner.