Golgi tendon organ reflex inhibition following manually applied acute static stretching.

Golgi tendon organ disinhibition may contribute to exercise-associated muscle cramp (henceforth referred to as "cramps") genesis. Static stretching pre-exercise is prescribed to prevent cramps based on the assumption golgi tendon organ inhibition remains elevated post-stretching. We determined whether stretching increased gastrocnemius golgi tendon organ inhibition and, if so, the time course of this inhibition post-stretching. Twelve participants' dominant limb medial gastrocnemius inhibition was measured before, and at 1, 5, 10, 15 and 30 min after investigators applied three, 1-min duration stretches. Participants maintained voluntary contraction intensities of 5% of their maximum while the Achilles tendon was stimulated transcutaneously 50 times. Five-hundred millisecond epochs of raw electromyographic activity were band-pass filtered, full-wave rectified and averaged. An algorithm identified inhibitory points and calculated the area, maximum and duration of inhibition. Area of inhibition (F1,14 = 1.5, P = 0.25), maximum inhibition (F1,14 = 0.2, P = 0.72) and duration of inhibition (F1,14 = 1.5, P = 0.24) were unaffected by static stretching over the 30-min post-stretching period. If pre-stretching does prevent fatigue-induced cramping, the mechanism is unlikely to involve the autoinhibition produced by the golgi tendon organ reflex. Further empirical research is needed to validate the proposed link between static stretching and cramping and then to investigate alternative mechanisms.

Comparison of the inhibitory response to tendon and cutaneous afferent stimulation in the human lower limb.

A powerful early inhibition is seen in triceps surae after transcutaneous electrical stimulation of the Achilles tendon [tendon electrical stimulation (TES)]. The aim of the present study was to confirm results from surface electromyogram (SEMG) recordings that the inhibition is not wholly or partly due to stimulation of cutaneous afferents that may lie within range of the tendon electrodes. Because of methodological limitations, SEMG does not reliably identify the time course of inhibitory and excitatory reflex components. This issue was revisited here with an analysis of changes in single motor unit (SMU) firing rate [peristimulus frequencygram (PSF)] and probability [peristimulus time histogram (PSTH)] to reexamine the time course of inhibitory SMU events that follow purely cutaneous (superficial sural) nerve stimulation. Results were then compared with similar data from TES. When compared with the reflex response to TES, sural nerve stimulation resulted in a longer onset latency of the primary inhibition and a weaker effect on SMU firing probability and rate. PSF also revealed that decreased SMU firing rates persisted during the excitation phase in SEMG, suggesting that the initial inhibition was more prolonged than previously reported. In a further study, the transcutaneous SEMG Achilles tendon response was compared with that from direct intratendon stimulation with insulated needle electrodes. This method should attenuate the SEMG response if it is wholly or partly dependent on cutaneous afferents. However, subcutaneous stimulation of the tendon produced similar components in the SEMG, confirming that cutaneous afferents made little or no contribution to the initial inhibition following TES.

An electromyographic study of parkinsonian swallowing and its response to levodopa.

BACKGROUND: Few studies have investigated the effect of levodopa on parkinsonian swallowing with findings thus far being equivocal. METHODS: We used surface electromyography and accelerometry to investigate submental and laryngeal muscle activation during swallowing in 14 parkinsonian subjects before and after levodopa and in 22 age-matched controls. Our aims were (1) to demonstrate the clinical utility of noninvasive electromyography, (2) to identify electromyographic features of parkinsonian swallowing, and (3) to investigate the effect of levodopa on parkinsonian swallowing. RESULTS: The parkinsonian group showed increased burst amplitudes and durations and increased swallow duration, clearing activity and latency between submental and laryngeal bursts (P < .05) and used more swallows than did controls to consume water boluses (P < .001). Levodopa decreased the latency between submental and laryngeal bursts (P < .05) but did not produce effects on individual muscle bursts. CONCLUSIONS: The clinical utility of electrophysiological and biomechanical methods of swallowing assessment was demonstrated. Levodopa tended to normalize the timing of the combined swallow response but not the activity of individual muscles.

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.

Continuous wavelet transform in the evaluation of stretch reflex responses from surface EMG.

OBJECTIVE: This is the first reported use of the continuous wavelet transform (CWT) of the surface EMG (sEMG) to extract the reflex response to muscle stretch. We used a modulus-based method to estimate instantaneous amplitude-envelopes from ridges of the CWT (referred in this work as sEMG intensity) to extract the dynamic reflex response from sEMG. We tested the method on tendon reflexes where excellent temporal resolution is required to identify the different latency components, and on the tonic stretch reflex (tonic SR) response to an ongoing perturbation that characteristically has a low signal to noise ratio. METHODS: Eight subjects without neurological impairment were subjected to a series of archilles tendon taps and a 2 min continuous perturbation of the ankle using a pseudo-sinusoidal stretch profile containing frequencies from 0.1 to 8.0 Hz. The tendon reflexes were assessed in the soleus muscle at 10% of MVC and the tonic SR in tibialis anterior while the muscle was relaxed, at 5 and 10% of maximal voluntary contraction. Root mean square (RMS) and wavelet ridge extraction was applied to the sEMG signal to extract sEMG amplitudes (RMS) and intensities for all reflexes. To obtain the tonic SR, these estimates and those from the sEMG-RMS were subsequently cross-correlated with the perturbation record to yield 2 sets of estimates of reflex gain and coherence for comparison. RESULTS: The sEMG intensities were highly correlated with the torques resulting from a ramped voluntary contraction. Following tendon taps, the method resolved the M1, M2, M3 response components at accurate latencies and with more complete reconstruction of the components than RMS-derived estimates. The wavelet ridge estimates extracted the tonic SR from resting and contracting muscles with significantly higher coherence than RMS estimates. Reflex gain, when estimated from sEMG intensity or sEMG-RMS, demonstrated similar relationships to the perturbation frequency and background contraction level. When the sEMG intensity reflex gain estimates from different subjects were pooled, they showed significantly lower variance about the mean than gain estimates derived from the rectified sEMG. CONCLUSIONS: Wavelet-ridge extraction provides a valid approach to reflex evaluation from sEMG that does not depend on the absolute amplitude of the potentials measured at the EMG electrodes. This may have substantial advantages in more directly comparing responses between subjects on an absolute frequency scale without the need for normalisation against maximal contraction levels.

Synaptic potentials contributing to reflex inhibition in gastrocnemius following tendon electrical stimulation.

OBJECTIVE: To investigate the synaptic potentials underlying reflex inhibition in gastrocnemius following electrical stimulation of the Achilles tendon using single motor unit recordings. METHODS: Surface electromyography (SEMG) and single motor unit (SMU) action potentials were recorded from the medial head of left gastrocnemius muscle in eight healthy human subjects. The left Achilles tendon was stimulated electrically while subjects maintained a low contraction level sufficient to record one or two motor units. SMU responses were analysed using peri-stimulus time histogram (PSTH) and peri-stimulus frequencygram (PSF) techniques and compared with SEMG results. RESULTS: A total of 22 SMU experiments were completed. In all trials, a large reflex inhibition (I1) was observed in both SEMG and PSTH followed by a later inhibition (I2). In 50% of trials, SEMG and PSTH showed that both I1 and I2 were followed by excitation (E1 and E2, respectively). PSF analysis showed only a prolonged reduction in SMU discharge rate. This inhibition had a latency of 38 ms and duration of 13 ms, extending into the E1 period in 14 units and more than 200 ms extending into the E2 period in six units. CONCLUSIONS: PSF data suggest that tendon electrical stimulation results in a long-lasting inhibition, most likely through the autogenic inhibitory reflex pathway mediated by group I tendon afferents. SIGNIFICANCE: These findings emphasise the importance of using both probability (SEMG, PSTH) and frequency (PSF) based techniques in error free estimation of synaptic potentials.

Inhibitory mechanisms following electrical stimulation of tendon and cutaneous afferents in the lower limb.

Electrical stimulation of the Achilles tendon (TES) produced strong reflex depression (duration>250 ms) of a small background contraction in both heads of gastrocnemius (GA) via large diameter electrodes localized to the tendon. The inhibitory responses were produced without electrical (M wave) or mechanical (muscle twitch) signs of direct muscle stimulation. In this study, the contribution of presynaptic and postsynaptic mechanisms to the depression was investigated by studying conditioning effects of tendon afferent stimulation on the mechanical tendon reflex (TR) and magnetic motor evoked potential (MEP). TES completely inhibited the TR over an ISI of 300 ms that commenced before and continued during and after the period of voluntary EMG depression. Tendon afferent conditioning stimuli also partially inhibited the MEP, but over a short time course confined to the period of voluntary EMG depression. The strength and extended time course of tendon afferent conditioning of the TR and its failure to produce a similar depression of the MEP are consistent with a mechanism involving presynaptic inhibition of Ia terminals. Cutaneous (sural nerve) afferent conditioning partially inhibited the TR and MEP over a short time course (ISI <100 ms) resembling the inhibition seen in the voluntary EMG. This was consistent with the postsynaptic origin of cutaneous inhibition of the motoneurons.

Afferents contributing to autogenic inhibition of gastrocnemius following electrical stimulation of its tendon.

Electrical stimulation of the Achilles tendon produced strong reflex inhibition of the ongoing voluntary EMG activity in the two heads of the gastrocnemius (GA) muscle in all tested subjects. The inhibition was seen clearly in both averaged and single sweep surface EMG records. The inhibitory response was produced without electrical (M wave) or mechanical, (muscle twitch) signs of direct muscle stimulation. The onset latency and duration for the first period of inhibition (I(1)) were 47-49 ms and 67 ms, respectively. A second inhibition (I(2)) had an onset latency of 187-193 ms and duration under 40 ms. Non-noxious stimuli in the range of 2.6-7.6 x mean perceptual threshold, when delivered to four locations over the GA tendon, all produced clear inhibition of the voluntary muscle activity. The inhibition was maximal when the cathode was a large metal plate located near the musculotendinous junction and decreased approximately linearly with distances more distal to that site. The effect of passive muscle stretch on the electrically induced tendon reflex inhibition (TRE) was tested at ankle joint angles incremented in steps of 20 degrees. It was found that TRE is strongly dependent on joint angle, being maximal in the fully stretched muscle. TRE was lost completely after partial tibial nerve block. In comparison, GA inhibition produced by cutaneous (sural) nerve stimulation was of a higher threshold, longer latency and persisted after partial tibial nerve block. We thus demonstrated a powerful autogenic inhibition in the lower limb arising from tendon afferents in conscious subjects that is increased by passive muscle stretch and likely to originate from group I tendon afferents.

Reflex inhibition of normal cramp following electrical stimulation of the muscle tendon.

Muscle cramp was induced in one head of the gastrocnemius muscle (GA) in eight of thirteen subjects using maximum voluntary contraction when the muscle was in the shortened position. Cramp in GA was painful, involuntary, and localized. Induction of cramp was indicated by the presence of electromyographic (EMG) activity in one head of GA while the other head remained silent. In all cramping subjects, reflex inhibition of cramp electrical activity was observed following Achilles tendon electrical stimulation and they all reported subjective relief of cramp. Thus muscle cramp can be inhibited by stimulation of tendon afferents in the cramped muscle. When the inhibition of cramp-generated EMG and voluntary EMG was compared at similar mean EMG levels, the area and timing of the two phases of inhibition (I(1), I(2)) did not differ significantly. This strongly suggests that the same reflex pathway was the source of the inhibition in both cases. Thus the cramp-generated EMG is also likely to be driven by spinal synaptic input to the motorneurons. We have found that the muscle conditions that appear necessary to facilitate cramp, a near to maximal contraction of the shortened muscle, are also the conditions that render the inhibition generated by tendon afferents ineffective. When the strength of tendon inhibition in cramping subjects was compared with that in subjects that failed to cramp, it was found to be significantly weaker under the same experimental conditions. It is likely that reduced inhibitory feedback from tendon afferents has an important role in generating cramp.

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.

Muscle loading as a method to isolate the underlying tremor components in essential tremor and Parkinson's disease.

Tremor is clinically evaluated and classified on the basis of its response to limb posture (resting, postural, and kinetic tremor), but the mechanisms underlying this powerful influence remain unclear and no satisfactory method exists to identify or quantify underlying tremor subtypes. Postural change is closely linked to changes in gravitational load. We therefore assessed the effect of changes in muscle load on essential tremor (ET) and parkinsonian tremor (PT) independently of postural change. A motor accurately delivered a series of constant (0.2-1.2 Nm) flexion and extension torques about the affected wrist while subjects maintained a constant wrist angle by isometrically contracting wrist flexors or extensors against the applied loads. Linear regression of tremulous electromyogram (EMG) spectral peak amplitude against the applied loads estimated the magnitudes of the load-dependent (LDT) and load-independent (LIT) tremor components. The amplitude of ET was linearly related to increase in gravitational load. It thus contained a large LDT component and a small or absent LIT component. Muscle loading revealed significant LDT and LIT components in PT. LIT was dominant at zero load (classic rest tremor) but both components were present during loading (classic postural tremor). Muscle loading more clearly identifies tremor subtypes than postural effects alone. The method could be applied in clinical and pathophysiological studies.

Loss of reflex inhibition following muscle tendon stimulation in essential tremor.

Electrical stimulation of human upper limb muscle tendons produces a reflex inhibition (I(1)) in the same muscles. This inhibition is reduced in Parkinson's disease (PD), prompting a similar study of essential tremor (ET). In essential tremor, two of eight subjects had no discernible inhibition, even following supramaximal stimulation (< 80 mA) of the tendons from extensor digitorum communis and extensor pollicis brevis. In the remaining six subjects, the mean thresholds for I(1) in these muscles were increased by 270 and 320%, respectively, relative to controls. The maximal amplitude of the inhibition was significantly reduced in the ET group, as was the following excitation (E(1)). The latency and duration of I(1) were not different in ET subjects and controls. The maximal duration of I(1) was correlated with tremor frequency in individuals, and tendon stimulation was effective in initiating ongoing tremor cycles. These results disclose a peripheral reflex abnormality in ET that is mediated by tendon afferents and can be linked to the coexistent tremor. The response in ET was distinguished from that in PD by its different time-course and by failure of the response to appear in the antagonist muscle. The abnormality may prove a useful marker for ET, which currently lacks a definitive pathological or neurophysiological marker to support objective clinical diagnosis.