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The stretch reflex and H-reflex of the human soleus muscle during walking.

Due to the complexity of applying a well-defined stretch during human walking, most of our knowledge about the short latency stretch reflex modulation in humans is based on H-reflex studies. To illuminate the difference between the two methodologies, both types of reflexes were evoked in the same subjects, same experiment. Stretch reflexes were evoked via a stretch device capable of evoking stretch reflexes of the human soleus muscles during walking. H-reflexes were elicited by an electrical stimulation of the tibial nerve at the popliteal fossa at the knee. A significantly different modulation of the two reflexes was found in the late stance where the stretch reflex decreased in relation to the H-reflex. This was consistent with the unloading of the muscle spindles during the push-off in the late stance, suggesting a complex alpha-gamma coactivation, if any, at this time of the step. The soleus stretch reflex and H-reflex were compared during the stance phase of walking and sitting at matched soleus activity. No difference was found in the amplitude of the stretch reflex. However, there was a significant decrease of the H-reflex during the stance phase of walking, consistent with a task-specific presynaptic mediated reflex control. It is proposed that the short latency stretch reflex during walking is not sensitive to such a presynaptic inhibition.

Adult↗

Effect of tonic muscle pain on short-latency jaw-stretch reflexes in humans.

The modulation of human jaw-stretch reflexes by experimental muscle pain was studied in three experiments. Short-latency reflex responses were evoked in the masseter and temporalis muscles by fast stretches (1 mm displacement, 10 ms ramp time) before, during and 15 min after a period with tonic pain. In Expt. I, a dose of 5.8% hypertonic or 0.9% isotonic (control) saline was infused in random order into the left masseter for up to 15 min (n=12). The level of excitation of the left masseter was kept constant at 15% of maximal effort by visual feedback and on-line calculation of the root-mean-square value of the surface electromyogram (sEMG). In Expt. II, a dose of 5.8% saline was infused into the left masseter but with feedback from the right masseter sEMG (n=12). In Expt. III, both sEMG and intramuscular (im) EMG was recorded from the left and right masseter muscles. The feedback was from either the sEMG or imEMG of the left masseter in which 5.8% saline was infused (n=12). In all experiments, subjects continuously rated their perceived pain intensity on a 10-cm visual analogue scale (VAS). Infusion of 5.8% saline caused moderate levels of pain (mean VAS 4.9-5.0 cm) whereas infusion of 0.9% saline was almost pain-free (mean VAS 0.3 cm). The pre-stimulus EMG activity in the masseter, which served as the feedback muscle during the recording, was constant across the different conditions. During painful infusion of 5.8% saline in Expts. I and III, the pre-stimulus sEMG activity in the non-painful masseter was significantly higher than baseline when the sEMG on the painful side was used as feedback signal, and in Expt. II significantly lower on the painful side when the non-painful side served as feedback signal (Student-Newman-Keuls: P<0.05). Isotonic saline did not affect the pre-stimulus sEMG activity or the jaw-stretch reflex parameters. The peak-to-peak amplitude of the stretch reflex in the painful masseter normalized to the pre-stimulus EMG activity was significantly higher during the pain conditions compared with the pre- and post-infusion conditions in all experiments. These results indicate that experimental jaw-muscle pain facilitates the short-latency (8-9 ms), probably monosynaptic, jaw-stretch reflex as revealed by both sEMG and imEMG. This effect could not be accounted for by variability in pre-stimulus EMG activity. An increased sensitivity of the fusimotor system at this level of static muscle excitation is suggested as a possible mechanism, which could contribute to an increased stiffness of the jaw-muscles during pain.

Adult↗

Modulation of short latency stretch reflexes during human hopping.

To gain insight into central and peripheral reflex control mechanisms in moving humans we have investigated short latency stretch reflex activity in m. triceps surae during two legged hopping. The objectives were: (1) to compare movement induced short latency stretch reflexes in soleus and medial gastrocnemius (MG) muscles, (2) to determine the relationship between the size of these reflexes and the muscle spindle stretch velocities, and (3) to compare the size of the movement induced short latency stretch reflexes and the H-reflexes simultaneously. Six well-trained healthy male subjects participated and they hopped at three different work rates. Surface electromyogram (EMG) and H-reflexes were recorded during hopping. Muscle spindle length changes were estimated as the difference between estimated origin-to-insertion length changes and tendon length changes. The important findings were that during hopping: (1) movement induced short latency stretch reflexes were observed consistently in soleus, (2) the EMG amplitude of this stretch reflex was negatively correlated with the estimated peak muscle spindle stretch velocity (rs = -0.52, P < 0.02), and (3) the amplitude of the soleus H-reflex at touchdown did not change in parallel with the stretch reflex. The negative correlation observed between the stretch reflex and the estimated peak muscle spindle stretch velocity in soleus is opposite to the basic velocity sensitive behaviour of stretch reflexes mechanically elicited during resting conditions. Possible control mechanisms are discussed. Additionally, muscle spindle length changes estimated from changes in the skeletal movements (joint angles) should be inferred cautiously because of tendon compliance, especially at high tendon forces.

Adult↗

Correction for the influence of background muscle activity on stretch reflex amplitudes.

Background muscle activity (BGR) exerts a strong influence on stretch reflex amplitudes. While it is considered important to correct for this influence, which method best able to eliminate the effects of BGR remains unknown. We have therefore compared one previously described and one novel correction method which respectively consisted of calculating (1) the difference between reflex amplitude and BGR, and (2) the ratio of reflex amplitude to BGR. These correction methods were evaluated in a group of 23 healthy individuals. BGR and stretch reflexes were recorded from the gastrocnemius muscle of standing subjects who received sudden toe-up perturbations of a supporting platform upon which they were standing. Calculation of differences markedly reduced the influence of BGR on stretch reflex amplitudes in most, although not all, subjects. Calculation of ratios failed to correct for BGR in most subjects and caused a net increase in the influence of BGR on stretch reflex amplitudes. Because both correction methods insufficiently corrected for BGR in normal subjects, we introduce the use of analysis of covariance (ANCOVA) to reliably remove the influence of BGR on stretch reflex amplitudes. The use of ANCOVA is exemplified by showing that stretch reflex amplitudes are enhanced in patients with Parkinson's disease even if the influence of high BGR is completely taken into account.

Adult↗

Identification of time-varying dynamics of the human triceps surae stretch reflex. II. Rapid imposed movement.

We examined the time-varying dynamics of the human triceps surae stretch reflex before, during, and after a large stretch was imposed upon the ankle joint, during a constant voluntary contraction of 15% of maximum voluntary contraction. Stretch reflex dynamics were estimated by superimposing a small stochastic displacement on many such stretches and using an "ensemble-based" time-varying identification procedure to compute impulse response functions relating the perturbation to the evoked electromyogram (EMG) at each point throughout the task. We found that stretch reflex magnitude (relating joint velocity to EMG) varied directly with baseline EMG activity during steady-state conditions before and after the large imposed stretch. Following the large stretch and the reflex activity it evoked, both background EMG and stretch reflex magnitude declined for up to 100 ms; changes in the stretch reflex were substantially greater in magnitude and followed a different time course from the corresponding changes in background EMG, however, indicating that stretch reflex properties were modulated independently of motoneuron pool activation level. Based on timing and the invariance of stretch reflex dynamics across time, it is argued that this behavior is largely mediated via peripheral neural mechanisms. This peripheral modulation of the stretch reflex presumably supplements various descending influences to adjust reflex properties.

Adult↗

Effect of contraction level and magnitude of stretch on tonic stretch reflex transmission characteristics.

Electromyogram tonic stretch reflex responses were recorded from biceps brachii muscles in normal and cerebral palsied subjects sustaining either 10% or 20% of maximum voluntary contraction and attempting to keep the elbow stiff in a fixed position. The muscle was stretch by a sinusoidal perturbation applied by the experimenter to the elbow angle. Five different amplitudes of stretch were employed ranging 1.67 to 10.0 degrees peak to peak variation of elbow angle. Spectral analysis of the rectified and filtered electromyogram revealed "noisy" sinusoidal reflex responses with negligible harmonic distortion but the amplitude of the reflex responses did not increase linearly with the amplitude of stretch. An analysis of variance showed that for both groups of subjects the gain of the tonic stretch reflex increased significantly (p less than 0.001) with contraction level and decreased significantly (p less than 0.001) with magnitude of stretch. This finding illustrates that both magnitude of stretch and level of contraction need to be carefully controlled when measures of tonic stretch reflex responses are used to assess changes of muscle tone.

Adult↗

Diurnal rhythm in the spinal stretch reflex.

We studied primate spinal stretch reflex (SSR) amplitude as a function of time of day. SSR amplitude was greatest around midnight and smallest around noon. The diurnal rhythm was not simply a function of number of trials, or of the lighting cycle. This rhythm offers an opportunity to study the neuronal and synaptic mechanisms producing a diurnal change in CNS function. Its existence indicates that the CNS response to a given limb disturbance, and thus the CNS activity underlying a given performance, varies with time of day.

Animals↗

A numeric study of the noise-induced tremor in a mathematical model of the stretch reflex.

A mathematical model of the stretch reflex for the cat soleus muscle is presented. The time-delay differential equations of the model are solved using the fourth-order Runge-Kutta algorithm, introducing a Gaussian-noise term to simulate the environmental noise. The muscle response dynamics are then studied under various levels of average muscle activation. Finally, the feasibility of explaining the so-called physiological tremor from the properties of the stretch reflex mechanisms is discussed by comparing our results with reported experimental evidence.

Animals↗

System identification of human stretch reflex dynamics: tibialis anterior.

System identification methods have shown that the stretch reflex in the human ankle extensor (triceps surae, TS) may be modeled as velocity feedback via a single, short latency pathway containing a uni-directional rate-sensitive nonlinearity. Evidence of differences in the reflex organization in flexors and extensors led us to use the same methods to examine stretch reflexes in the ankle flexor (tibialis anterior, TA). Five normal subjects maintained a tonic contraction of TA while subjected to repeated, stochastic perturbations of ankle position. Position, torque, and smoothed, rectified EMGs from TA and TS were recorded and ensemble averaged over 25 stimulus presentations. Linear impulse response functions relating TA EMG to ankle velocity were then determined. The results confirmed the existence of significant differences between stretch reflexes in TA and TS. In particular: 1. TA impulse response functions were characterized by two distinct peaks of excitation separated by a period of inhibition. The impulse response function amplitude increased with increasing mean torque and decreased with displacement amplitude although the sensitivity of the two peaks to these changes was different. This was interpreted as suggesting that TA stretch reflexes involve two separate pathways both involving muscle spindle information. 2. TA stretch reflexes modulate tonic activity much less than do those in TS. 3. The strong uni-directional rate-sensitive nonlinearity seen in TS was not present in TA. The functional significance of these differences remains to be determined.

Adult↗

Stretch reflex and servo action in a variety of human muscles.

1. In the long flexor of the thumb the latency of the stretch reflex and of other manifestations of servo action is some 45 msec, roughly double the latency of a finger jerk. 2. Tendon jerks are feeble or absent in the long flexor of the thumb even in subjects with brisk long-latency stretch reflexes in this muscle. This, and other facts, suggests that the nervous mechanism of the tendon jerk is different from that of the stretch reflex. 3. A muscle that has feeble tendon jerks may show a late component in the response to a tendon tap, with a latency similar to that of the long-latency stretch reflex. 4. On the hypothesis that the excess latency of the stretch reflex over that of a tendon jerk is because the stretch reflex employs a cortical rather than a spinal arc, the excess would be expected to be larger in magnitude for the long flexor of the big toe and smaller for the jaw closing muscles. This is confirmed, 5. An alternative hypothesis that the long latency of stretch reflexes in thumb and toe is because they are excited by slow-conducting afferents is made improbable by the finding that stretch reflexes with an equal or greater excess latency are also found in proximal arm muscles. 6. The long-latency stretch reflex in proximal muscles was seen most distinctly in a healthy subject who happened to have feeble or absent tendon jerks. In ordinary subjects there is often a large, short-latency, presumably spinal component of the stretch reflex in proximal muscles; and short-latency responses to halt and release are also seen, The significance of this spinal latency servo action in proximal muscles remains to be explored. 7. The Discussion argues that the available data on conduction time to and from the cerebral cortex are compatible with the hypothesis that the long-latency component of the stretch reflex uses a transcortical reflex arc, and that none of the experiments described in the present paper are inimical to this view.

Biomechanical Phenomena↗

The cerebellum and initiation of movement: the stretch reflex.

Studies of the stretch reflex in decerebrate cats indicate a phase advance of peak sinusoidal tension in steady-state cycles between 0.1 and 10 Hz. This phase advance is reduced in acute and chronic cerebellectomy, as shown in previous investigations. Also, the augmentation of muscle peak tension in initial sinusoidal stretch cycles at 0.5-5 Hz has been found to be reduced during the time of reflex and motor instability in the several months following cerebellar ablation. This report shows the increased amplitude and phase lead of integrated electromyographic activity in initiating sinusoidal stretch cycles in the decerebrate cat. These reflex aspects are demonstrated in relation to the discharge of neurons in the dorsal spinocerebellar tract and of cerebellar cortical Purkinje cells in initial sinusoidal cycles. The intensity and phase advance of the discharge in dorsal spinocerebellar tract neurons is altered little, but these features are usually increased in Purkinje cells during initial stretches compared to continuous cycling. In terms of overall motor control, these findings are compatible with concepts of movement control, modulated by the cerebellum, in which the discharge of antagonist motor neurons is regulated in concert with that of agonist muscles upon initiation and termination of movement.

Action Potentials↗

Is the long-latency stretch reflex in human masseter transcortical?

A long-latency stretch reflex (LLSR) has been described in the human masseter muscle, but its pathway remains uncertain. To investigate this, the excitability of corticomotoneuronal (CM) cells projecting to masseter motoneurons during the LLSR was assessed with transcranial magnetic stimulation (TMS). A facilitated response to TMS would be evidence of a LLSR pathway that traverses the motor cortex. Surface electromyogram electrodes were placed over the left or right masseter, and subjects ( n=10) bit on bars with their incisor teeth at 10% of maximal electromyographic activity (EMG). Servo-controlled displacements were imposed on the lower jaw to evoke a short- and long-latency stretch reflex in masseter. TMS intensity was just suprathreshold for a response in contralateral masseter. Trials consisted of: (1) stretch alone, (2) TMS alone, and (3) TMS with a preceding conditioning stretch at varied conditioning-testing (C-T) intervals chosen to combine TMS with the short-latency stretch reflex (3 ms, 5 ms) and the LLSR (23-41 ms). Masseter EMG was rectified and averaged. With TMS alone, mean (+/- SE) MEP area above baseline was 56+/-9%. The area of masseter MEPs above baseline in the C-T trials was calculated from each EMG average following subtraction of the response to stretch alone. Conditioning muscle stretch had no significant effect on masseter MEPs evoked by TMS with any C-T interval (ANOVA; P=0.90). In addition, subjects were unable to modify the SLSR or LLSR by voluntary command. It is concluded that the long-latency stretch reflex in the masseter does not involve the motor cortex and is not influenced by "motor set".

Adult↗

Interaction of pre-programmed control and natural stretch reflexes in human landing movements.

Pre-programmed mechanisms of motor control are known to influence the gain of artificially evoked stretch reflexes. However, their interaction with stretch reflexes evoked in the context of unimpeded natural movement is not understood. We used a landing movement, for which a stretch reflex is an integral part of the natural action, to test the hypothesis that unpredicted motor events increase stretch reflex gain. The unpredicted event occurred when a false floor, perceived to be solid, collapsed easily on impact, allowing the subjects to descend for a further 85 ms to a solid floor below. Spinal stretch reflexes were measured following solid floor contact. When subjects passed through the false floor en route to the solid floor, the amplitude of the EMG reflex activity was double that found in direct falls. This was not due to differences in joint rotations between these conditions. Descending pathways can modify H- and stretch-reflex gain in man. We therefore manipulated the time between the false and real floor contacts and hence the time available for transmission along these pathways. With 30 ms between floors, the enhancement of the reflex was extinguished, whereas with 50 ms between floors it reappeared. This excluded several mechanisms from being responsible for the doubling of the reflex EMG amplitude. It is argued that the enhanced response is due to the modulation of reflex gain at the spinal level by signals in descending pathways triggered by the false platform. The results suggest the future hypothesis that this trigger could be the absence of afferent signals expected at the time of false floor impact and that salient error signals produced from a comparison of expected and actual sensory events may be used to reset reflex gains.

Adult↗

Position dependence of stretch reflex dynamics at the human ankle.

The purpose of this study was to examine the effect of ankle position on the human ankle stretch reflexes during tonically-maintained contractions over most of the range of motion. The ankle was placed at randomly selected mean positions. Target levels of triceps surae (TS) or tibialis anterior (TA) tonic contractions were generated while the ankle was displaced by small amplitude, stochastic perturbations. System identification techniques were used to identify the stretch reflex dynamics at each combination of tonic level and ankle angle. As shown previously, the TS stretch reflex was characterized by an unidirectional, velocity-sensitive impulse response function whereas the TA stretch reflex was characterized by a linear impulse response function between ankle velocity and TA EMG. TS stretch reflexes showed a strong dependence on ankle position while TA stretch reflexes did not. Thus the TS stretch reflex magnitude increased greatly as the ankle was progressively dorsiflexed. In contrast, ankle mean position had only a minor effect on the TA stretch reflex magnitude. Our results indicate that the position-dependent facilitation of the TS stretch reflex is not due to changes in the level of skeletal motoneuron excitability. Rather, this effect may be accounted for by mechanisms that modulate the efficacy of the stochastic ankle perturbation. Such mechanisms could include position-induced: modulation of monosynaptic and polysynaptic afferent inputs to skeletal motoneurons, alterations in the extent of fusimotor drive and changes in the transmission of the joint perturbation to spindle receptors. Such mechanisms are discussed in terms of the differences between TS and TA stretch reflexes. Finally, the functional significance of position-dependent reflex responses are considered.

Adult↗

Quantitative relations between hypertonia and stretch reflex threshold in spastic hemiparesis.

The relative contributions of variations in stretch reflex threshold and total joint stiffness to changes in stretch-evoked torque were assessed in the spastic elbow muscles of 14 hemiparetic spastic subjects. For a given subject, variations in torque, measured after a constant angular deflection, were mediated largely by changes in stretch reflex threshold, rather than by changes in reflex stiffness. Between-subject comparisons were sensitive to stiffness differences between limbs, but reflex thresholds were still broadly correlated with torque magnitude, suggesting that reductions in stretch reflex threshold are uniformly present in spastic muscles. These findings, coupled with the apparent similarity of reflex stiffness estimates in voluntarily activated spastic and normal muscles, suggest that the central disturbance in spasticity is a reduction in the threshold of the stretch reflex, without a significant enhancement of reflex gain.

Adult↗

No correlation between number of MRI-evident lesions in cerebrum and the soleus stretch reflex in multiple sclerosis patients.

The aim of the study was to investigate if the stretch reflex of the soleus muscle was useful in quantifying upper motor neuron lesions. The soleus stretch reflex was recorded in 10 healthy subjects and 20 patients with active relapsing-remitting multiple sclerosis and correlated to the number of MRI lesions in cerebrum and clinical scores (expanded disability status scale and regional functional scoring system). The short latency stretch reflex was elicited by rotating the left ankle joint 4 degrees with a rise time in the interval of 40-640 ms. The amplitude of the stretch was larger in multiple sclerosis patients being 88.5 microV in patients and 12.8 microV in controls, P = 0.007. The sensitivity of the stretch reflex expressed as the slope of the best linear fit was increased in MS patients to 2.6 microVs/degree compared with 0.6 microVs/degree (0.1-2.2) in controls, P = 0.009. There was no correlation between amplitude of the stretch reflex and number of MRI lesions (r = -0.03). In conclusion, the soleus stretch reflex might be useful to quantify spasticity but is not useful in detecting dysfunction of upper motor neurons in MS.

Adult↗

Spinal stretch reflex and cortical evoked potential amplitudes versus muscle stretch amplitude in the monkey arm.

While investigating operant conditioning of the primate spinal stretch reflex (SSR), we studied SSR amplitude and cortical somatosensory evoked potential (SEP) amplitude as stretch amplitude changed in the monkey arm. Initial muscle length and background EMG activity remained constant. With change in stretch amplitude (and proportional change in stretch velocity and acceleration), changes in SSR and SEP amplitudes were respectively 0.75 and 0.66 as great. The lesser change in SSR amplitude may reflect saturation of Ia afferents, while that in SEP amplitude may also reflect participation of other peripheral receptors.

Animals↗

Stretch reflex variation in the relaxed and the pre-activated quadriceps muscle of normal humans.

The stretch reflex to patellar tendon taps was quantified by force measurements at the ankle in 7 normal subjects. In each experiment the stretch reflex was elicited from 14 consecutive stretches by two types of hammers (an ordinary hand-held hammer and a motorized hammer) in the relaxed and the pre-activated quadriceps muscle. The coefficient of variation for the 14 stretch reflexes fell from 54% in the relaxed muscle to 39% in the contracting muscle (p less than 0.05). The stretch reflex varied less between the different levels of active contraction than between the relaxed state and the contracted level (p less than 0.05). The experiment was repeated in all subjects and at all contraction levels. The coefficient of variation of the mean for the two experiments fell non-significantly from a mean value of 27% in the relaxed muscle to 14% in the contracting muscle. The coefficients of variation for the two hammers were almost identical. It is concluded that quantification of the stretch reflex can be made more precisely in the contracting muscle.

Adult↗