Modulation of reflex and voluntary EMG activity in wrist flexors by stimulation of digital nerves in hemiplegic humans

Changes in EMG activity in the wrist flexor muscles were studied in response to electrical stimulation of digital nerves and to sudden extension perturbations at the wrist produced by a torque motor in human subjects with unilateral cerebral hemisphere lesions. With the subjects maintaining a steady voluntary contraction against a constant load, digital nerve stimulation produced a series of excitatory and inhibitory changes in tonic EMG activity from the wrist flexors in both the normal and paretic arm. The most consistent response was a period of EMG inhibition beginning approximately 38 msec after the stimulus and lasting approximately 35 msec. With relatively weak electrical stimuli, there was less EMG inhibition in the paretic arm than in the normal arm; with stronger stimuli, the inhibitory response was similar in the two arms. The electrical stimuli and mechanical perturbations were then delivered together, with the interval between them adjusted so that the expected period of inhibition following electrical stimulation coincided with either the early (M1) or the long latency (M2) components of the stretch reflex. In the normal arm electrical stimulation produced more inhibition of the M2 component than of the M1 component. In the paretic arm, inhibition during the M2 component was less marked and similar in degree to that which occurred during M1. These results are compatible with the view that M1 and M2 are normally mediated by separate neural pathways. The long latency EMG activity evoked by muscle stretch in the paretic arm of hemiplegic patients may be generated by pathways or mechanisms different from those in the intact arm.     

Changes in electromyographic responses to muscle stretch, related to the programming of movement parameters.

Three experiments are reported that used the advance information paradigm which consists of providing subjects with either no or partial information about an upcoming movement. Subjects moved handles to control the vertical displacements of CRT beams, to point to eight targets. The illumination of different combinations of these targets prior to movement execution provided advance information about which hand, movement direction, or movement extent would be required. Reaction time (RT), integrated EMG activity in the forearm extensor and flexor muscles, and M1, M2, and M3 components of the stretch reflex responses triggered in these muscles were analysed as a function of the precued movement parameter. Compared to the no-information condition, RT decreased in all precue conditions; however, the reduction was greater when direction than when hand was precued, and greater when hand than extent was precued. The EMG activity of forearm muscles increased during the preparatory period in all precue conditions, but generally did not differ among them. An overall facilitation of the stretch reflex components was observed in all precue conditions. This facilitation: (1) was greater for flexor than extensor muscles, (2) was similar regardless of the degree of extent precued, (3) differed for the M2 and M3 components depending on whether the responding hand precued was ipsilateral or contralateral. When the precued movement direction was considered, similar changes in the M3 component were found in extensor and flexor muscles. M3 was facilitated when the muscle was precued as an agonist and was inhibited when it was precued as an antagonist. Collectively these data provide support for a motor programming conception of movement organization.     

Spastic dystonia in stroke subjects: prevalence and features of the neglected phenomenon of the upper motor neuron syndrome

ObjectiveSpastic dystonia is one of the positive phenomena of the upper motor neuron syndrome (UMNS). It is characterised by the inability to relax a muscle leading to a spontaneous, although stretch-sensitive, tonic contraction. Although spastic dystonia is a recognized cause of muscle hypertonia, its prevalence among hypertonic muscles of stroke subjects has never been investigated. Differently from spasticity, which is an exaggerated stretch reflex, spastic dystonia is viewed as an efferent phenomenon, due to an abnormal central drive to motoneurons.MethodsIn 23 hemiparetic stroke subjects showing increased muscle tone of wrist flexors, surface EMG was used to investigate the presence of spontaneous, stretch-sensitive EMG activity in flexor carpi radialis.ResultsSpontaneous, stretch-sensitive EMG activity was found in 17 subjects. In the remaining 6 subjects, no spontaneous EMG activity was found.ConclusionsThe majority of stroke subjects is affected by spastic dystonia in their hypertonic wrist flexor muscles. Only a minority of subjects is affected by spasticity.SignificanceTo stop spastic dystonia from being the neglected aspect of UMNS, it is essential to link its definition to increased muscle tone, as occurred for spasticity. Recognizing the real phenomena underling muscle hypertonia could improve its management.     

Changes of forearm EMG and cerebral evoked potentials following sudden muscle stretch during isometric contractions in patients with Parkinson''s disease

Various investigators have reported that the late reflex EMG activity following muscle stretch is increased in patients with Parkinson's disease. To explore the basis of this increased activity, we have now recorded the late EMG responses together with associated cerebral responses following muscle stretch in parkinsonian patients. Nine patients and eight controls participated in two sets of experiments in which they grasped a handle attached to a torque motor and maintained the wrist isometrically against a constant flexor force. The force was changed unpredictably (first set) or predictably (second set of experiments), causing a stretch of wrist extensors or flexors. Cerebral responses and muscle responses from the forearm were recorded and averaged separately depending upon condition. The late muscle responses to unpredictable muscle stretch were enhanced in parkinsonian patients while the cerebral responses were attenuated when compared to controls. The alteration of the electrocerebral response began approx. 25 ms prior to the late M2 muscle response. Both controls and patients showed a markedly attenuated cerebral response when the muscle stretch was predictable. These results indicate that the electrocerebral response to muscle stretch is altered prior to the onset of M2 in patients with Parkinson's disease, and suggest that these cerebral events reflect components of a long-latency transcerebral reflex pathway that is affected in this disorder.     

Changes of forearm EMG and cerebral evoked potentials following sudden muscle stretch in patients with Huntington's disease.

Various investigators have reported that the late-reflex electromyographic (EMG) activity following muscle stretch is decreased in Huntington's disease. To explore the basis of this decreased activity, we recorded the late EMG responses together with associated cerebral responses following muscle stretch in patients with Huntington's disease. Five patients and seven controls voluntarily participated in two sets of experiments in which they grasped a handle attached to a torque motor and maintained the wrist isometrically against a constant flexor force of 2.3 newtons (N). The force was changed unpredictably (first set of experiments) or predictably (second set) to 10.4 N, causing a stretch of wrist extensors or flexors. Rectified surface EMG from the extensor and flexor carpi radialis muscles was integrated for the M2 and M3 components of the late responses. Cerebral responses were recorded from F3, F4, C3, C4, and Cz and averaged separately depending upon condition. The late muscle responses to unpredictable muscle stretch were decreased or absent in patients with Huntington's disease. The cerebral responses recorded at Cz differed markedly between patients and controls, beginning approximately 15 ms prior to the onset of the late M2 muscle response. Although the initial positivity was similar in amplitude, all other cerebral components were markedly reduced in the patient group. Both controls and patients showed a markedly attenuated cerebral response when the muscle stretch was predictable. The electrocerebral response to muscle stretch is thus altered prior to the onset of M2 in patients with Huntington's disease, suggesting that the long-latency reflex involves transcerebral pathways that are affected in this disease.     

Anticipatory changes of long-latency stretch responses during preparation for directional hand movements

We have investigated, in 9 normal subjects, the time course of amplitude changes in the automatic long latency stretch reflex of wrist flexors during the preparatory period as a function of the precued direction of hand movement. Subjects maintained right hand position against a weak force and learned to compensate precisely for brief ramp stretch (250 deg./s, 50 ms) which imposed wrist extension. This probe stretch was applied randomly at different times during the 1 s preparatory period of a reaction time task. The warning signal gave directional advance information (DAI) about the voluntary movement that had to be performed. The EMG activity, recorded between 20 and 80 ms after the stretch started, was measured in terms of 3 successive components, M1, M2 and M3, identified on the basis of their respective latency.There was no significant change in the M1 component. Following a warning signal which precued an extension movement, M2 was depressed prior to the response signal. The time course of M3 was clearly different according to DAI: it increased following a warning signal which precued a flexion movement and decreased in the alternative case. This difference reached statistical significance 400 ms before the response signal. In fast-performing subjects the differential development of M3 was more marked than for slow-performing subjects. This underlines its preparatory significance. These results suggest that the neuronal pathways involved in the M3 response to stretch: i, are partly different from those conveying the earlier components, and ii, include structures which take part in the pre-programming of rapid movements.     

The shortening reaction of forearm muscles: the influence of central set.

OBJECTIVE: The EMG of the forearm muscles shortened by an imposed wrist joint displacement has been studied at different levels and distribution of background muscle activity and with different instructions to the subjects, in order to test the hypothesis that the recorded EMG response (shortening reaction, ShoRe) could be deliberate in origin. METHODS: Ten normal subjects were examined. A torque motor induced 50 degrees wrist extension or flexion at 500 degrees /s. The subjects were relaxed or exerted a 10% maximal voluntary contraction. They were instructed either not to intervene, or to oppose the displacement, or else to assist it. Several trials were repeated at different initial angles. RESULTS: We found a short-latency reflex (SR) in the stretched muscle, be it flexor or extensor, and a later inconstant ShoRe in the antagonist. ShoRe latency was compatible with that of a reaction time (RT), and was not influenced by the initial wrist angle. When subjects assisted the movement, the EMG burst in the shortening muscle was in every respect a RT; when they opposed the movement, the ShoRe disappeared. There was a strict temporal relationship between SR duration and ShoRe latency. CONCLUSIONS: We suggest that the brain would deliberately trigger the ShoRe on recognizing the displacement direction. The occurrence of such activity in the shortened muscle makes the SR to abruptly stop. The temporal relationship between the duration of the SR and onset of the ShoRe can be an expression of the inhibition on the SR burst by the cortical drive to the antagonist muscle being shortened, possibly through the action of spinal inhibitory interneurones. The ShoRe would complete the movement momentarily braked by the SR and redistribute the muscle tone across antagonists, appropriate for the new muscle length.     

Relation between changes in long-latency stretch reflexes and muscle stiffness in Parkinson's disease--comparison before and after unilateral pallidotomy.

OBJECTIVE: To study the effects of posteroventral pallidotomy on both the size of long-latency stretch reflex (LLR) and the muscle stiffness in the wrist flexor muscles. PATIENTS AND METHODS: Eleven consecutive patients (right-handed, 6 men and 5 women) underwent left-side microelectrode-guided pallidotomy. The LLR of the contralesional forearm was studied at baseline and 2-3 months after surgery while patients continued to take their optimal medical regimens ('on' period). Patients were instructed not to respond to the perturbation (passive mode) or to oppose the mechanical extensor perturbation (active mode). RESULTS: The stretch reflex evoked by extension perturbations of the wrist consisted of a short-latency reflex (M1) and an LLR (M2). Pallidotomy had no effects on the size of M1 components in both passive and active mode and on that of M2 component in the passive mode, however, it significantly reduced M2 component in the active mode (P<0.05). The inherent muscle stiffness over 60 ms period of mechanical stretch was not influenced by pallidotomy in any experimental condition (preoperative vs. postoperative or passive mode vs. active mode). The hand displacement following M2 component increased significantly after pallidotomy in both passive (P<0.005) and active mode (P<0.05). The inverted value of the displacement following M2 component correlated with the size of M2 component (r=0.60, P<0.001). CONCLUSIONS: Pallidotomy decreased the transcortical reflex gain, probably at cortical level, and consequently reduced muscle stiffness.     

The basis and functional role of the late EMG activity in human forearm muscles following wrist displacement.

The present paper examines the hypothesis that the long latency EMG activity produced by muscle stretch is the result of long loop reflex pathways involved in the control of limb stiffness. We recorded the cerebral responses and late EMG activity in agonist and antagonist muscles following sudden stretch of the wrist extensor muscles under 4 experimental conditions in 11 subjects. In each experiment subjects held their right wrist extended isometrically against a constant force of 2.3 N and a trial was begun with a step increase in the force from 2.3 N to 18.4 N, to stretch the extensor muscle. In the first and second experiments the force change occurred unpredictably and subjects had to either oppose the perturbation (Unpredictable Oppose) or relax the forearm muscles once the increase in force was detected (Unpredictable Let-Go). In the third and fourth experiments the force change occurred predictably when subjects pressed a thumb switch with the left hand to cause it. As before, subjects were instructed to either oppose the perturbation (Predictable Oppose) or relax the forearm muscles (Predictable Let-Go). Responses were recorded from the flexor and extensor carpi radialis muscles and from the scalp. When the perturbing force occurred unpredictably, early latency EMG activity (the MI response) was seen in the stretched extensor muscle, and longer latency EMG activity was seen simultaneously in both extensor and flexor muscles. When the force change occurred predictably the late EMG activity was considerably attenuated, especially in the Predictable Let-Go condition. Cerebral responses similarly depended upon the predictability of the perturbation.(ABSTRACT TRUNCATED AT 250 WORDS)     

Attenuation of the effect of remote muscle contraction on the soleus H-reflex during plantar flexion.

OBJECTIVE: We investigated to what extent the facilitation of the soleus (Sol) Hoffmann (H-) reflex during a phasic voluntary wrist flexion (Jendrássik maneuver, JM) can be modulated by graded plantar flexion force and conditioning wrist flexion force. METHODS: The subjects were asked to perform phasic wrist flexion under a reaction time condition. Sol H-reflex was evoked by stimulating the right tibial nerve at various time intervals (50-400ms) after the 'Go' signal for initiating JM while the ankle was at rest and while plantarflexing. The level of tonic plantar flexion force (isometric contraction of 10, 20 and 30% of maximal EMG) and conditioning wrist flexion (isometric contraction of 30, 50 and 80% of maximum voluntary contraction) during JM was graded systematically. RESULTS: Although JM facilitation could be seen 80-120ms after the flexor carpi radialis (FCR) EMG onset even while plantarflexing, the magnitude of JM facilitation under plantar flexion was significantly decreased compared to that at rest. The degree of decrease in JM facilitation did not depend on the level of plantar flexion force. In contrast, the degree of JM facilitation was proportional to the level of wrist flexion force while the ankle was at rest and while plantarflexing, though the amount of JM facilitation significantly decreased while plantarflexing. CONCLUSIONS: JM facilitation of Sol H-reflex is decreased while performing tonic voluntary contraction of the homonymous muscle. The degree of decrease in JM facilitation is independent of the level of homonymous muscle contraction, but depends on the level of remote FCR contraction. In clinical application, when we intend to elicit a maximum stretch reflex by JM, full relaxation of homonymous muscle should be carefully confirmed. SIGNIFICANCE: Our results provide evidence for better understanding of the features of JM and insight into its clinical application.     

Effects of ischemic nerve block on the early and late components of the stretch reflex in the human forearm

To investigate the peripheral afferent mechanisms which mediate the short latency (M1) and long latency (M2) components of the stretch reflex, we have recorded EMG responses to extension perturbations at the wrist before and following inflation of a blood pressure cuff around the upper arm. After approximately 30 min of ischemia, the reflexes had almost completely disappeared, although subjects were still able to activate the forearm muscles voluntarily. As the ischemic block developed, the M2 component began to decrease in amplitude sooner than M1, and up to the time of complete loss of reflex activity, the suppression of M2 was relatively greater than that of M1. These results suggest that M2 may be mediated by a population of afferent fibers different from the Ia afferents which are believed to generate the M1 response.     

Effects of changing wrist positions on finger flexor hypertonia in stroke survivors

We sought to establish whether spastic hypertonia results from changes in intrinsic muscle properties or from altered stretch reflex properties. We hypothesized that finger flexor spastic hypertonia is primarily of neural origin, and that the dynamics of spastic muscle responses to stretch should therefore reflect the dynamics of muscle spindle receptor responses. In 12 stroke survivors, we recorded torque and electromyographic (EMG) responses of extrinsic finger flexors to constant-velocity rotation of the metacarpophalangeal (MCP) joints of the affected hand, over a range of initial muscle lengths. Stretch velocity was set to 6 degrees, 50 degrees, 150 degrees, or 300 degrees per second. Muscle length changes were imposed by changing wrist angle between 0 degree, 25 degrees, and 50 degrees of flexion. We found that reflex torque and EMG responses exhibited both velocity and length dependence, and there were significant interactions between velocity and length, replicating known characteristics of muscle spindle receptors. Our results support the hypothesis that finger flexor hypertonia is primarily of neural origin, and that it accurately reflects spindle receptor firing properties.     

The relationship of voluntary movement to spasticity in the upper motor neuron syndrome

Hyperactive strethch reflexes in the upper motor neuron (UMN) syndrome are frequently cited as an impediment to volitional movement. The assumption is that neural or mechanical activity of the hyperactive antagonist interferes with agonist function. The validity of this assumption was examined by evaluating quantitative and qualitative relationships between stretch reflexes and voluntary movement. Sixteen patients with chronic UMN symptoms and 8 normal volunteers were tested. Joint position and integrated electromyograms from primary flexors and extensors were recorded. Quantitated values of (1) reflex response to controlled passive motion by an automated system, (2) a maximal voluntary isometric contraction, and (3) the time required for ten voluntary rapid repetitive movements (RRM) of alternating elbow flexion and extension were obtained. Passive movement elicited tonic reflexes, which predominated during muscle stretch in patients and during muscle shortening in the volunteers. Ratios of the EMG activity elicited during stretch, shortening, and isometric activity were used as measures of spasticity and were compared with the time for RRM. A positive correlation between elbow flexor spasticity and the time for RRM was shown. Qualitative analysis of the EMG activity during voluntary isotonic movement, however, showed that primary impairment of movement is not due to antagonist stretch reflexes, but rather to limited and prolonged recruitment of agonist contraction and delayed cessation of agonist contraction at the termination of movement.     

The flexor reflex--influence of stimulus parameters on the reflex response

The flexor reflex evoked in the tibialis anterior muscle by stimulation of the medial plantar nerve was investigated in 54 normal subjects. Three main reflex components were identified (excitation--inhibition-- excitation), the early excitation being composed of two subcomponents. Occasionally, a fourth (excitatory) reflex component was seen breaking through EMG inhibition. The individual reflex components were differentially susceptible to facilitatory influences which suggested transmission via a central multichannel system. Methodological experiments showed that the amplitudes and to some degree also the latencies of the individual reflex components were modified by both the parameters of the stimulus as well as by the degree of pre-innervation. However, the patterning of the reflex response was basically independent from methodological permutations.     

Contralateral intramuscular acupuncture-like electrical stimulation differentially changes the short-latency responses to muscle stretch

Measurements were made from the human first dorsal interosseous and extensor digitorum communis muscles of the surface electromyographic activity reflexly produced by brief stretch of the muscle. For the first dorsal interosseous muscle, reflex EMG activity was also produced by electrical stimulation of the ulnar nerve at the wrist. The procedures were carried out before, during, and after 25 min of nonspecific, low-frequency electrical stimulation to the contralateral arm delivered through intramuscular electrodes. Control stimulation was delivered subcutaneously. The EMG recorded during a maintained contraction was rectified, filtered, and averaged. Two reflex components (M1 and M2) of the EMG response to muscle stretch or ulnar nerve stimulation were investigated. During nonspecific intramuscular stimulation to the contralateral arm, M1 responses of the extensor digitorum communis were depressed, initially by 37%. The effect began to fade during stimulation but extended beyond it. Reflex responses were elicited alternately by brief stretch of the first dorsal interosseus muscle and by electrical stimulation of the ulnar nerve in the same experiment. Nonspecific intramuscular stimulation to the contralateral arm depressed the M1 response to stretch, but had no effect on the M1 response to electrical stimulation. It is concluded that nonspecific intramuscular electrical stimulation reduces the amplitude of the M1 component of the response to brief stretch of contralateral muscle, either through depression of fusimotor activity or inhibition of oligosynaptic pathways that contribute to the early reflex response.     

Neural development in children: a neurophysiological study

In adult human subjects torque motor imposed angular displacements of the upper limb joints result in two major reflex EMG components as identified by their latency. The shorter latency (SL) component is probably the spinal stretch reflex and the longer latency (LL) reflex component may involve supraspinal structures. Tendon jerk, arising via the spinal reflex pathway, is present in children at birth. In this study the presence and the development of the LL component in wrist flexors was investigated in children between the ages of 2 and 13 years. Kinaesthetic reaction times were tested simultaneously. In young children, the duration of the LL component was much longer than that in adults. The duration decreased slowly from 2 to 6 years, following which a relatively abrupt decrease between the ages of 6 and 8 years took place. After 8 years of age responses looked more adult-like. Kinaesthetic reaction times attained adult-like values after 10 years of age. Various possibilities underlying these observations are discussed.     

The role of action reflexes in the damping of mechanical oscillations

Reflex responses measured during voluntary contraction of the muscle being stretched are known to differ markedly from reflex responses elicited from passive muscle. The term 'action tonic stretch reflex' or 'action TSR' has been used previously to describe a reflex response to continuous stretch, separated from voluntary activity by means of a cross-correlational and spectrographic analysis. In this paper it is proposed that the action TSR play a functional role during voluntary movement by damping the transient oscillations associated with the natural resonant frequencies of the limbs. It is suggested that oscillations excite an action TSR force response with phase lead ahead of muscle stretch. This force response can be resolved into two force components, one of which has a 90 degree phase lead ahead of muscle stretch and behaves like a viscous friction reaction force causing damping of oscillations. Three experiments which support this proposition are described. (1) Analog computer model stimulation studies of a muscle supporting a mass-spring load reveal that damping only occurs when the force response has a phase lead ahead of muscle stretch. When the force response has a phage lag behind muscle stretch, the system is unstable and the amplitude of oscillation increases with time. (2) It is demonstrated that when a mass-spring load is supported as rigidly as possible by the human arm, reaction forces from the arm damp and mass-spring oscillations more rapidly than when the mass-spring is rigidly supported. Electromyogram (EMG) recordings reveal that mass-spring oscillations excite action TSR responses with phase lead ahead of muscle stretch. (3) Recordings of elbow angle and biceps EMG during rapid forearm flexion or extension movements followed by sudden stops reveal critically damped oscillations in the elbow angle signal (i.e. no more than one or two small overshoots), which are accompanied by EMG action TSR responses with phase lead ahead of muscle stretch.     

Reorganization of flexion reflexes in the upper extremity of hemiparetic subjects.

We examined spatiotemporal abnormalities in the flexor reflex response in the impaired upper extremity of hemiparetic subjects. Electrical stimulation was used to elicit flexion reflexes in both upper extremities of 8 hemiparetic brain-injured and 6 control subjects. Electromyograms (EMGs) were recorded from 12 arm muscles, and reflex forces and moments were recorded at the wrist with a load cell, and converted to shoulder and elbow torques. We found that the onset of reflex torque and EMG was delayed in the impaired arm and delays were greater at the shoulder than at the elbow. The normal reflex torque response consisted of elbow flexion, shoulder extension, and shoulder adduction. In contrast, in the impaired limb shoulder, flexion torque was observed in 7 subjects and shoulder abduction in 3. The delays in reflex onset and altered torque patterns in the impaired arm may be related to the abnormal movement synergies observed following stroke. © 1999 John Wiley & Sons, Inc.     

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.