Long-latency Stretch Reflex Research Articles

Parkinsonian Rigidity and Long-Latency Stretch Reflex Activity

Parkinsonian Rigidity and Long-Latency Stretch Reflex Activity

Evidence for a contribution of the motor cortex to the long‐latency stretch reflex of the human thumb.

1. In normal subjects, transcranial magnetic stimulation of the hand region of the motor cortex evokes motor responses only in contralateral hand muscles at a latency of about 19-24 ms. In contrast, stimulation of the motor cortex of three mirror movement subjects evoked, nearly simultaneously, motor responses in hand muscles on both sides of the body at latencies similar to those of normal subjects. In these subjects no other neuroanatomical pathways appear to be abnormally directed across the mid-line. Thus, their mirror movements are probably due to a projection of the corticospinal tract to homologous motoneurone pools on each side of the body. 2. We reasoned that if the motor cortex contributes to the generation of long-latency stretch reflex responses then in these mirror movement subjects stretching a muscle on one side of the body should produce long-latency reflex responses in the ipsilateral and the homologous contralateral muscle. 3. To test this idea experiments were done on normal human subjects and on the subjects with mirror movements. The electromyographic (EMG) activity of the flexor pollicis longus muscle (FPL) on each side of the body was recorded. Stretch of the distal phalanx of the thumb of one hand produced a series of distinct reflex EMG responses in the ipsilateral FPL. The earliest response, when present, began at 25 ms (S.D. = 3.5 ms) and was followed by responses at 40 (S.D. = 3.9 ms) and 56 ms (S.D. = 4.3 ms). There was no difference, either in timing or intensity, between the ipsilateral FPL EMG responses of normal subjects and those of the mirror movement subjects. 4. No response of any kind was observed in the contralateral (unstretched) FPL of normal subjects. In contrast, we observed in all three mirror movement subjects EMG responses in the contralateral (unstretched) FPL beginning at 45-50 ms. The latency of this response is considerably shorter than the fastest voluntary kinaesthetic reaction time, which was on average 130 ms (S.D. = 11 ms). The contralateral long-latency EMG response observed in the mirror movement subjects was on average 30% (range 5-60%) of that on the ipsilateral side. No short-latency response (25 ms) was ever observed in the contralateral FPL of these subjects. 5. These observations are quite consistent with the idea that the long-latency stretch reflex responses of hand and finger muscles are produced, at least in part, by the motor cortex.

Evidence that low-threshold muscle afferents evoke long-latency stretch reflexes in human hand muscles

1. The aim of the present study was to identify the type of spinal afferents involved in the generation of the long-latency response in intrinsic human hand muscles. Position-controlled extensions were imposed on the index finger or on the wrist of healthy subjects who were exerting a steady voluntary flexion force at the relevant joint. Averaged surface electromyographic (EMG) responses of the first dorsal interosseus muscle (FDI) or of the wrist flexors were evaluated with respect to latency and size. 2. Small transient angular displacements of the index finger (1 degree, as measured at the metacarpophalangeal joint), which are supposed to excite primary rather than secondary afferents, evoked two clearly discernible EMG responses with mean latencies of 32.3 ms (M1 response) and 54.7 ms (M2 response), respectively. The size of the M2 response exceeded the size of the M1 response by 60%. In the wrist flexors, transient stretch (1 degree) gave rise to a large M1 response (latency 22.8 ms) and a small, inconstent M2 response. 3. Small-amplitude vibration of the index finger elicited EMG responses in the FDI that were qualitatively and quantitatively similar to those seen in response to small transient stretches of the index finger. This was also true for fast ramp-and-hold stretches (stretch velocity 400 degrees/s, amplitude 5 degrees), whereas slow ramp-and-hold stretches (125 degrees/s, 5 degrees) elicited predominantly M2 responses. 4. In the FDI, the mechanical threshold of the M1 and M2 response to the transient angular displacement was approximately 0.15 degrees, with a tendency for the M2 response to appear at a lower threshold.(ABSTRACT TRUNCATED AT 250 WORDS)

Changes in the response to magnetic and electrical stimulation of the motor cortex following muscle stretch in man.

1. The effect of muscle stretch on the EMG response from the stretched muscle to transcranial magnetic stimulation of the motor cortex was studied in eight subjects. Muscle stretch was produced by increasing the torque of a motor acting through a lever which was held at constant position by a flexion force of the index and middle fingers. EMG responses were recorded from fine-wire electrodes inserted into flexor digitorum profundus muscle in the forearm. They consisted of a spinal latency component and a long-latency component which could in some subjects be separated into an early and a late phase. 2. In four subjects, four intervals between the stretch and the cortical stimulus were explored using three intensities of cortical stimulation. At all three intensities, when the magnetic cortical stimulus was timed to produce an EMG response in the period of the later part of the long-latency stretch reflex the response was larger than when it was timed to produce a response in the period of the short-latency spinal reflex or when superimposed on the tonic muscle activity used to resist the standing torque of the motor. 3. When the intensity of magnetic cortical stimulation was reduced so that it was just below threshold to produce an EMG response in the short-latency reflex period or on the background tonic EMG activity, it still was capable of producing a response when superimposed on the long-latency stretch reflex. 4. In four subjects the time course of this effect was studied in more detail using only one intensity of magnetic cortical stimulus set to be just above threshold to produce a response in tonically active muscles. The time course of the facilitatory effect was similar to the time course of the later part of the long-latency stretch reflex. From these data it was not possible to determine whether the early part of the long-latency stretch reflex also was accompanied by the facilitatory effect since this component was present in only one of the four subjects. 5. The facilitatory effect persisted after the ulnar and median nerves were totally blocked at the wrist by injections of local anaesthetic. This suggests that inputs from muscle receptors of the stretched muscle contribute to the effect.4=

MODULATION OF THE STRETCH REFLEX DURING VOLITIONAL SINUSOIDAL TRACKING IN PARKINSON'S DISEASE

Sinusoidal visually-guided wrist tracking, in normal and parkinsonian subjects, was perturbed by torque transients every 90 degrees throughout the movement. Long-latency stretch reflex and volitional EMG amplitude modulations were assessed as functions of the tracking phase. Reflex modulation during tracking, both in wrist flexor and extensor muscles, was found to differ significantly between parkinsonian and normal subjects. In the parkinsonian group, the abnormality consisted of an increased reflex activity during tracking phases in which the muscle was lengthening. At these phases the reflex generated torque is opposite in direction to the volitionally generated torque and the tracking movement. No differences in the unperturbed volitional EMG modulation were observed between groups for this error constrained tracking paradigm. Significant correlations were found between ratings of bradykinesia and the amount of abnormal reflex modulation in the wrist flexor. These data suggest that a component of bradykinesia results from a defective coordination of supraspinal reflex and volitional control systems.

Lack of fusimotor modulation in a motor adaptation task in man

Single-unit activity was recorded from the radial nerve of human subjects along with surface electromyogram, joint angle, velocity, and torque at a metacarpophalangeal joint. Nine afferents from muscle spindles in the extensor digitorum muscles were studied in a motor adaptation task which involved modulations of the long-latency stretch reflex. While subjects slowly moved one finger, a perturbation which rapidly stretched the parent muscle was applied. The subjects' task was to return their finger as fast as possible. In a series of identical control experiments, electromyographic activity and performance alone were recorded, but not spindle afferents. Subjects improved their performance by a varying degree when the test was repeated. Optimal performance was usually associated with increased electromyographic activity at a latency of about 60 ms, which was interpreted as a long-latency stretch reflex. The response of the individual spindle afferents to perturbation was uniform in repeated tests regardless of the size of the reflex, e.g. whether it was large or lacking altogether. It was concluded that modulations of the size of the long-latency stretch reflex in the present motor adaptation task were accounted for by mechanisms other than adjustments of the fusimotor activity, because spindle response to an invariant perturbation remained invariant when the size of the reflex varied substantially.

Responses of monkey precentral neurones to passive movements and phasic muscle stretch: relevance to man

Single cell recordings were made from movement-related neurones from the precentral cortex of two monkeys, trained to perform a simple lever-pulling task. They were also trained to remain relax while the arm was explored with passive movements at different joints, cutaneous stimuli and during the application of two types of phasic muscle stretch: percutaneous vibration and percussion of muscle tendons. Recordings were made of the responses of cortical neurones both to the ‘natural’ stimuli and to vibration of specific muscle tendons or percussion of the triceps tendon. Both tendon percussion and vibration excited neurones within area 4 with an average latency for tendon percussion of 21.0 msec. There was a high degree of consistency in the effects on single neurones of tendon percussion and vibration at the same site. Although long-term facilitation was not seen, vibration-induced discharge in the motor cortex should be considered as a potential mechanism of its effects in intact man. In contrast to the similarity of the effect of the two forms of phasic stretch, the relationship between a single neurone's response to either tendon percussion or vibration and to passive movement was complex. The dissociation seen between the effects of phasic muscle stretch and that of passive movement may underlie the failure, in man, to find uniformly increased long-latency stretch reflexes in clinical states of extrapyramidal rigidity.

Impaired habituation of long‐latency stretch reflexes of the wrist muscles in Huntington's disease

Electromyographic responses to sudden wrist extension were recorded from the forearm and finger flexor muscles in 10 patients with Huntington's disease (HD) and in 10 normal controls. Stretch reflexes were characterized by a short-latency (SL) and a long-latency (LL) component both in patients and controls. Latency, duration, and size of the SL component were not different in the two groups, whereas the LL component was delayed in latency and reduced in size in HD patients. Increasing the stretch repetition rate from 0.1 to 0.4 cycles/s did not affect the SL component of either group, whereas the LL stretch reflex was reduced in size and duration in normal controls, but not in HD patients. These findings suggest an impairment of the "gain" mechanisms of the sole LL component, responsible for a desaturation of this component. This study supports the hypothesis that LL stretch reflexes are mediated by a transcortical long loop, possibly damaged in HD.

Chapter 9 Analysis of human long-latency reflexes by cooling the peripheral conduction pathway; which afferents are involved?

This chapter first outlines current views on the afferents of origin of human "long-latency stretch reflexes", and especially whether they are fast or slow. Attention is concentrated on methodology; other approaches can be found elsewhere with appropriate bibliography (Marsden et al., 1983; Matthews, 1985, 1986a; Wiesendanger, 1986). Recent experiments involving cooling of the human arm are then described. They were performed on the abductor digiti minimi and first dorsal interosseus muscles. The arm was cooled from wrist to axilla by circulating cold water through a tube wrapped round it. Cooling slows conduction by a constant proportion, hence the conduction delay introduced by cooling a segment of nerve is greater for small slow axons than for large fast ones. On this basis it was concluded that group I muscle afferents (presumably Ia) can elicit a long-latency reflex with a long central delay, as also can fast cutaneous afferents. No evidence was found for a long-latency reflex with the delay introduced peripherally by conduction along slow axons (i.e. spindle group II afferents). However, the co-existence of such a mechanism has yet to be excluded.

Long-latency stretch reflexes of the human elbow extensors during voluntary relaxation: Differences between agonistic muscles

Reflex electromyographic (EMG) responses of elbow extensor muscles to unexpected elbow flexion were recorded in the absence of initial tonic activity from subjects instructed not to resist the stretch. The monosynaptic component M1 was present only in the anconeus muscle and only for high accelerations. The acceleration value at which the long-latency components M2 and M3 appeared was lower for anconeus than for triceps brachii. Increases in peak acceleration of stretch resulted in decreases in M2 and M3 latencies and increases in M2 and M3 magnitudes in both muscles. However, M2 and M3 latencies for anconeus were shorter than those of triceps brachii, except at high acceleration values. Furthermore, the magnitude of M2 and M3 components of anconeus activity increased faster for low accelerations than for high accelerations, whereas those of triceps brachii increased in proportion to the acceleration. These differences between anconeus and triceps brachii were similar to those described earlier for voluntary movements. It is suggested that the motoneurons of all elbow extensor muscles may be recruited as a single motoneuron pool following Henneman's size principle, irrespective of whether the activity is voluntary or reflex in origin.

Modulation of the long-latency reflex to stretch by the supplementary motor area in humans

Surface-recorded, electromyographic responses to 200-ms ramp stretches were studied in the wrist flexor muscles from both arms of a patient with clinical and radiographic evidence of infarction in the right supplementary motor area (SMA). They were compared with those from 8 age-matched control subjects. The latencies of the spinal component of the stretch reflex were slightly longer than normal in both arms of the patient (normal subjects: 28.5±2.6 ms; patient: 35 ms, right arm and 32 ms left arm). However, the amplitude and duration of the short-latency response were identical in both arms. The onset of the long-latency response to stretch was symmetrical in both the patient's arms and was slightly later than normal (normal subjects 55.5±4.0 ms, patient: 72 ms right arm and 70 ms left arm); however, its duration was considerably prolonged in the arm contralateral to the SMA lesion (normal subjects: 44.8±6.0 ms; patient: 48 ms right arm, 105 ms left arm). These results are consistent with the hypothesis that the long-latency stretch reflex is mediated via a transcortical loop.

Hypotonia: an erroneous clinical concept?

Muscle tone, if defined as the resistance felt during passive movement of an extremity, is generally explained by the appearance of stretch reflexes. Consequently, hypotonia would be caused by a decrease or disappearance of these reflexes. This notion has never been challenged by experiments that reproduce the clinical situation. In this study two clinical tests, passive extension and flexion movements at the knee joint and a free fall of the lower leg with gravity, were applied to 72 control legs and 35 'hypotonic' legs. EMG activity was measured in the quadriceps muscle. Despite special care to obtain relaxation in the subjects, the majority of control legs showed voluntary EMG activity on passive movement. During free fall, long-latency reflexes were present in a minority of normal subjects, but the velocity of falling in these legs was within the range obtained in the legs without any EMG spikes. If the fall time was prolonged beyond the upper limit of relaxed legs, this was the result of voluntary activity, confirmed by EMG measurements. Therefore, long-latency stretch reflexes play no role in the clinical assessment of 'normal tone'. This conclusion was further supported by the observation that 'hypotonic' legs did not fall faster than relaxed control legs. If patient's legs feel flaccid this is the result of weakness preventing voluntary activity. Passive movements during the clinical examination are of great value, but only to detect spasticity or rigidity.

Shortening reaction of human tibialis anterior.

The shortening reaction of tibialis anterior was observed in 6 of 25 normal subjects, in 6 of 40 patients with upper motor neuron syndromes, and in 11 of 17 patients with Parkinson's disease. The latency of the shortening reaction was comparable with that of the latter part of the long-latency stretch reflexes. The magnitude of the shortening reaction increased with the velocity of the movement that produced it and increased with background voluntary force of plantar flexion in all but the patients with Parkinson's disease. It was not affected by vibration in the patients with Parkinson's disease. The presence of the shortening reaction was not correlated with the clinical impression of increased tone.

Interaction between the long-latency stretch reflex and voluntary electromyographic activity prior to a rapid voluntary motor reaction

The size of the long-latency component of the stretch reflex has been examined in the time interval between a signal to move and the required rapid voluntary contraction of triceps and flexor pollicis longus in 8 normal subjects. Bilateral movements of the elbow and thumb were made following an auditory signal. In 50% of the trials a torque pulse was applied unilaterally in order to elicit a stretch reflex response in one arm. The voluntary response in the contralateral arm was uncorrupted by a stretch reflex response, so was used as an indicator of voluntary reaction time. Control experiments, using an electrical stimulus to the fingers rather than muscle stretch, verified that both arms reacted almost simultaneously to the auditory cue, even when the reaction time was shortened by the presence of a unilateral electrical stimulus. Similarly, an interposed muscle stretch stimulus considerably reduced the reaction time to the audio signal. Because of this, the start of the voluntary EMG response frequently ‘overlapped’ the end of the long-latency stretch reflex. Failure to take this shortening of voluntary reaction time into consideration can lead to the erroneous conclusion that reflex gain is increased prior to a rapid movement. If the ‘overlap’ of EMG responses is accounted for, very little change in the size of the long-latency stretch reflex is evident prior to activation of the muscles responsible for the movement of either the elbow or the thumb.

The behaviour of the long-latency stretch reflex in patients with Parkinson's disease.

The size of the long-latency stretch reflex was measured in a proximal (triceps) and distal (flexor pollicis longus) muscle in 47 patients with Parkinson's disease, and was compared with that seen in a group of 12 age-matched normal control subjects. The patients were classified clinically into four groups according to the degree of rigidity at the elbow or tremor. Stretch reflexes were evaluated while the subject was exerting a small force against a constant preload supplied by a torque motor, and the size of the reflex response was measured as fractional increase over basal levels of activity. When stretches were given at random intervals by increasing the force exerted by the motor by a factor of 2 or 3, there was a clear trend for the more severely affected patients to have larger long latency responses in the triceps muscle, although there was no change in the size of the short-latency, spinal component of the response. In contrast, there was no change in the size of the long-latency response of the flexor pollicis longus in any group of patients with Parkinson's disease. Despite any differences in reflex size, the inherent muscle stiffness of both muscles appeared to be normal in all groups of patients with Parkinson's disease, since the displacement trajectory of the limb following the force increase was the same as control values in the short (25 ms) period before reflex compensation could intervene. In 20 of the patients and in seven of the control subjects, servo-controlled, ramp positional disturbances were given to the thumb. Up to a velocity of 300°/s, the size of the long-latency stretch reflex was proportional to the log velocity of stretch. This technique revealed, in both moderately and severely rigid patients, increases in the reflex sensitivity of the flexor pollicis longus, which had not been clear using step torque stretches alone. However, whether using ramp or step displacements, long latency stretch reflex gain was not closely related to rigidity; reflex size was within the normal range in many patients with severe rigidity. Enhanced long latency stretch reflexes thus contribute to, but may not be solely responsible for, rigidity in Parkinson's disease.

Automatic and ‘voluntary’ responses compensating for disturbances of human thumb movements

We have investigated in single trials the relationship between the automatic long-latency stretch reflex of flexor pollicis longus and subsequent ‘voluntary’ corrections when human subjects were instructed to compensate rapidly for maintained external disturbances applied to the top joint of the thumb. Subjects were instructed to maintain a constant thumb position with reference to a visual display before them against a small force supplied by a torque motor to the thumb pad. At irregular intervals (4–5 s) the interphalangeal joint suddenly was extended by about 10° by increasing the force in the motor for 1–2 s, and the subjects were required to restore the original thumb position as rapidly as possible. Visual feedback was excluded during this period. Positional compensation was achieved by the flexor pollicis longus in two phases: the first was caused by the automatic long-latency stretch reflex and the second appeared to be a triggered ‘voluntary’ response since it was under the complete conscious control of the subjects. There was a great deal of variation in the size of the automatic response from trial to trial in each individual, yet thumb position was restored within approximately 300 ms by the ‘voluntary’ activity, which was inversely related in size to the preceding automatic response. The inverse relationship between these events was not caused by any conscious adjustment of the size of the ‘voluntary’ response since the interval between the electromyographic (EMG) bursts in flexor pollicis longus producing the positional corrections of the thumb was only some 25–50 ms. The relationship also could be abolished at will by the subjects changing their movement strategy such that the initial thumb disturbance became a signal for them to flex their thumb by a constant amount, rather than to compensate for the perturbation. This did not change the reaction time or affect the size and variability of the preceding automatic response. It appeared that when subjects were instructed to compensate for external thumb displacements, the interaction between automatic long-latency reflex events and later ‘voluntary’ phases of correction made the variability in size of the automatic response from trial to trial unimportant since the required end position was achieved despite varying underlying patterns of muscle activation. Possible mechanisms responsible for this reciprocal relationship are discussed.

Accurate repositioning of the human thumb against unpredictable dynamic loads is dependent upon peripheral feed-back.

1. The strategy of accurate movement of the human thumb has been studied in nine subjects. An open-loop hypothesis, which states that a new final position is defined by re-setting the agonist/antagonist spring constants, was tested2. Subjects were trained to flex the top joint of the thumb rapidly through 20 deg in about a third of a second from a fixed starting position against a load. Occasionally, and unpredictably, the viscous friction of the load was altered prior to it's being moved. The spring hypothesis predicts that such a change in load should have no effect on final position accuracy.3. Under normal conditions no final position error developed when the viscous friction was increased. A small overshoot occurred when the viscous friction was decreased.4. The electromyogram recorded from surface electrodes over the belly of flexor pollicis longus in the forearm revealed an increase in activity in response to an increase in viscous friction and a decrease in activity when the viscous friction was reduced.5. When the joint and cutaneous afferents from the thumb were anaesthetized, the e.m.g. response to a change in viscous friction was severely attenuated and consistent final position errors developed.6. Even though the compensatory open-loop muscle properties went some way towards maintaining accuracy, the change in final position error that occurred as a result of thumb anaesthesia correlated well (r = 0.84) with the amount of muscle e.m.g. response that was lost.7. The latency of the e.m.g. response to a change in viscous friction was compared to that of a voluntary response by asking the subject to push down or let go upon perception of the load change. Approximately the first 100 ms of the e.m.g. response was unaffected by the voluntary intervention of the subject.8. We conclude that the spring hypothesis does not explain human thumb movement. It is argued that the long-latency stretch reflex machinery is responsible for some automatic compensation for unexpected interference with movement.

Behavior of the long-latency stretch reflex prior to voluntary movement

Attempts to elicit stretch reflexes from the ‘relaxed’ human long thumb flexor were made at various times prior to the onset of a voluntary contraction of that muscle. When the muscle was fully relaxed, there were no short or long-latency responses at the rates of stretch employed (about 600°/sec). Without complete relaxation there was a small long-latency response, which occasionally increased in amplitude as the time for voluntary activation approached. This augmentation seemed to be result of a subtle parallel augmentation of background EMG, anticipating the major voluntary contraction, thereby increasing the gain of long-latency stretch response.

Reliability and efficacy of the long-latency stretch reflex in the human thumb.

1. The amount of positional compensation afforded by the long-latency reflex in the flexor pollicis longus has been investigated in ten normal human subjects. 2. The interphalangeal joint of the thumb was extended by between 2 and 40 degrees at up to 900 deg/s by suddenly increasing the standing force applied to the lever against which the subject was pressing with the pad of the thumb. 3. Electromyographic (e.m.g.) responses at spinal-latency were very small or absent for stretches of this magnitude. The long-latency stretch reflex produced an average positional correction of about 50% for disturbances in the range of 5-25 degrees. The response began to saturate for disturbances of greater than 25 degrees. 4. The e.m.g. response was pulsatile, lasting only some 50 ms, even during continuously increasing disturbances; frequently it terminated despite a remaining positional error. 5. There was a large variation from subject to subject in the average amount of positional correction provided by the stretch reflex. Examination of single responses to the same stretch in individual subjects showed an even greater variation from trial to trial. 6. Variation in the compensation produced by the long-latency stretch reflex from trial to trial could not be explained by the slight variation in size or maximum velocity of the individual stretches.

Influence of voluntary intent on the human long-latency stretch reflex.

In man, sudden stretch of an actively contracting muscle evokes a classical monosynaptic spinal reflex followed by an automatic ‘long-latency’ response, both evident as bursts of activity in the electromyogram (EMG)1. This long-latency response, extensively investigated in the human long thumb flexor, but present in many other muscles2, occurs too early to be voluntary and much indirect evidence suggests it represents the operation of a ‘long-loop’, perhaps transcortical, stretch reflex mechanism3,4. Some investigators have found that the long-latency responses may be modified substantially by the subject's intent, possibly by pre-setting of excitability levels within the central nervous system thereby influencing the ‘long-loop’ mechanism5–9. However, others have observed little effect of voluntary set on the automatic long-latency stretch response10,11. It is notable that these studies, which have yielded conflicting results, have involved different muscles in a variety of experimental conditions. In some studies a warning signal preceded muscular stretch, while in others control trials were interspersed with stretches. To resolve the dilemma we have examined the influence of these variables, and found that the automatic long-latency response can be modified most strongly in conditions when the voluntary reaction time is shortest, for example, when the timing of the stimulus can be predicted accurately. We suggest that modification of a long-loop stretch response is not due to some central pre-setting process, but merely represents interaction between a reflex of long latency and a subsequent very rapid voluntary event, occurring early because of predictability of the stimulus.