Effect of medication on EMG patterns in individuals with Parkinson's disease.

Individuals with Parkinson's disease show dramatic improvements in their ability to move when medicated. However, the neural cause of this improvement is unclear. One hypothesis is that neural activation patterns, as measured by surface electromyography (EMG), are normalized by medication. We tested this hypothesis by investigating the effect of medication on the electromyographic (EMG) patterns recorded when individuals with idiopathic Parkinson's disease performed elbow flexion movements over three movement distances while off and on antiparkinsonian medication. When the subjects were off medication, they lacked the ability to modulate the agonist EMG burst duration with changes in movement distance. The ability to modulate agonist EMG burst duration is characteristic of the EMG patterns observed in healthy subjects. Also, multiple agonist bursts were exhibited during the acceleration phase. As expected, medication diminished the clinical signs of Parkinson's disease, increased movement speed, and increased the magnitude of the first agonist burst. Medication did not restore agonist burst duration modulation with movement distance, did not change the frequency of agonist bursting, and did not alter the timing of the antagonist activation. These results show that medication does not alter the temporal profile of EMG activation.     

Control of movement distance in Parkinson's disease.

Studies of electromyographic (EMG) patterns during movements in Parkinson's disease (PD) have often yielded contradictory results, making it impossible to derive a set of rules to explain how muscles are activated to perform different movement tasks. We sought to clarify the changes in modulation of EMG parameters associated with control of movement distance during fast movements in patients with PD. Specifically, we studied surface EMG activity during rapid elbow flexion movements over a wide range of distances (5-72 degrees) in 14 patients with relatively mild symptoms of PD and 14 control subjects of similar age, sex, height, and weight. The PD group exhibited several changes in EMG modulation including impaired modulation of agonist burst duration; increased number of agonist bursts; reduced scaling of agonist EMG magnitude in the more severely impaired subjects; and increased temporal overlap of the antagonist and agonist signals in the most severely impaired subjects. These findings suggest that progressive motor dysfunction in PD is accompanied by increasing deficits in modulating muscle activation. These results help clarify previous disparate and sometimes contradictory results of EMG patterns in subjects with PD.     

Ballistic elbow flexion movements in patients with amyotrophic lateral sclerosis.

Patients with amyotrophic lateral sclerosis made stereotyped 20 degrees elbow flexion movements as rapidly as possible while surface EMG was recorded from biceps and triceps. The characteristic ballistic movement EMG pattern could be recognised in almost all the patients. The first agonist burst and the first antagonist burst, which are normally limited in duration, were prolonged in patients with clinical signs of pyramidal tract disease or alpha motor neurone disease or both. Prolongation of these components permits the muscles to generate sufficient forces to accomplish the movements.     

Effects of subthalamic nucleus stimulation on characteristics of EMG activity underlying reaction time in Parkinson's disease.

We examined the effects of high-frequency deep brain stimulation of the subthalamic nucleus (STN-DBS) on characteristics of electromyographic (EMG) activity of the agonist muscle in 8 patients with Parkinson's disease (PD). Patients were examined during STN-DBS (ON), and 30 minutes after switching off both stimulators (OFF). They were asked to make a ballistic movement in paradigms of simple reaction time (SRT) and choice reaction time (CRT) tasks. Onset of movement (MOVonset) was measured as the latency of the initial displacement from baseline of the signal from an accelerometer attached to the dorsum of the hand. In the associated EMG activity, recorded from wrist extensor muscles, we measured onset latency (EMGonset), size of the first EMG burst (EMGsize), and number of EMG bursts (EMGbursts) counted between EMGonset and task execution. MOVonset and EMGonset were significantly shorter in ON than in OFF conditions in CRT. EMGsize was larger, EMGbursts were reduced, and peak of the acceleration profile was larger in ON compared with OFF conditions in both SRT and CRT. Our results indicate that STN-DBS induces a significant improvement in motor performance of reaction time tasks in PD patients. Such improvement is associated with a change in features of the EMG activity suggesting an increase in the excitability of the motor pathways engaged in ballistic movements.     

The first agonist and antagonist burst in patients with an upper motor neuron syndrome

Rapid elbow flexion movements were studied in patients with an upper motor neuron syndrome following a stroke. The velocity of movements was slower than normal. The initial bursts of electromyographic (EMG) activity in both the agonist and antagonist muscles were prolonged. As in normal subjects, the first agonist burst increased in duration with larger movements, but it generally remained about 40 ms longer than normal. The size of the first agonist burst also increased with larger movements. A fixed linkage between burst duration and level of motor unit recruitment, together with a deficient corticospinal command, could explain the prolonged burst duration with preserved ability to modulate the burst.     

EMG remains fractionated in Parkinson''s disease, despite practice-related improvements in performance

OBJECTIVE: We studied the ability of patients with Parkinson's disease to improve their performance in a motor task requiring both speed and accuracy in the execution of elbow flexion movements. Our goal was to investigate the changes in electromyographic activity associated with the changes in movement performance. METHODS: Eleven patients on anti-Parkinsonian medication were tested. The patients were selected for being bradykinetic, having little or no resting tremor or dyskinesias, and being in stages II or III of the Hoehn and Yahr rating scale. RESULTS: The untrained patients displayed multiple bursts of agonist activity, characteristic of Parkinsonian EMG recordings. All patients improved their performance by increasing peak velocity while maintaining movement accuracy within strict boundaries. With practice, the patients' performance changed in a manner similar to that which has been previously observed for performance curves in neurologically normal subjects. As movement duration decreased (i.e. peak velocity increased), we observed a slight decrease in the number of agonist bursts and an increase in the average burst duration. However, the patients continued to generate a fractionated, multi-burst agonist pattern. CONCLUSIONS: We conclude that Parkinsonian patients benefit from practice by improving their performance but remain fundamentally impaired in the generation of muscle activation patterns. This study has shown that the generation of fractionated, multiple short bursts of EMG activity that is characteristic of movements made by Parkinsonian patients is not normalized by practice.     

Analysis of stereotyped voluntary movements at the elbow in patients with Parkinson''s disease.

Patients with Parkinson's disease performed several different stereotyped elbow flexion tasks, and the electromyographic (EMG) patterns from biceps and triceps were compared with previously established normal standards. The EMG pattern during a smooth flexion task was almost always abnormal and was characterized by alternating activity in biceps and triceps. The EMG patterns during a fast flexion task were also usually abnormal although they were always composed of bursts of EMG activity of normal duration appearing alternately in the agonist and antagonist muscles. These bursts, associated with movements of the limb, have a superficially similar appearance to the EMG bursts seen with tremor-at-rest, but certain physiological differences are demonstrated. This study demonstrates that both slow (ramp) and fast (ballistic) movements are clearly abnormal in these patients with disease of the basal ganglia. In a task designed to investigate antagonist inhibition before agonist activity, a majority of the patients performed normally. This suggests that, contrary to previous claims, slowness of movement (akinesia/bradykinesia) is not due either to failure to relax or to rigidity of antagonist muscle.     

Modification of motor output to compensate for unanticipated load conditions during rapid voluntary movements

Mechanisms responsible for load compensation during fast voluntary movements were investigated in 20 normal subjects trained to carry out rapid wrist flexions against a standard load. When an unanticipated increase in load occurred, there was a compensatory increase in agonist EMG and decrease in antagonist EMG. Unanticipated decreases in load produced reciprocal changes with a decrease in agonist EMG and an increase in antagonist EMG. The latency of these EMG changes was quite short and compatible with a spinal reflex mechanism rather than a long loop response. The results suggest that mechanisms exist at the spinal level to allow rapid modification of motor programs when unanticipated load conditions are encountered on initiation of movement.     

Effects of expected perturbations on the velocity control of fast arm abduction movements

A triphasic electromyographic pattern of sequential activation of agonist, antagonist, and again agonist muscles underlies rapid or ballistic limb movements in humans. The first agonist burst reflects muscular force accelerating the limb, the antagonist burst is mainly related to the braking process of movement, while the second agonist burst is considered a reactive adjustment to the deceleration. The duration of the first agonist burst has been reported to be constant for movements of different amplitudes, thus suggesting that only changes in its amplitude contribute to the velocity control of movement. The present research has been undertaken to investigate the strategy whereby the nervous system increases agonist impulsive force for ballistic performance in response to experimental conditions requiring perceptual and/or provisional processes related to expected changes in load or accuracy constraints. The effects of expected perturbations of different strengths on some kinematic and electromyographic variables of fast arm abduction movements performed in a step-tracking task and in an outer-stop terminated task were analyzed in normal subjects. All motor performances were characterized by triphasic electromyographic patterns. In the absence of expected perturbations, the mean velocity of the movements was markedly higher in the outer-stop terminated task. Correspondingly, greater amplitudes and durations of the first agonist burst were observed. In both types of motor tasks, when expected perturbations were inserted, the velocity of the movement increased as well as the amplitude and the duration of the first agonist burst. These results, in agreement with previous observations, indicate that the normal mechanism, whereby the nervous system increases agonist impulsive force in rapid movements, comprises changes not only in the amplitude but also in the duration of the first agonist burst.     

Step-tracking movements of the wrist in humans. II. EMG analysis

We asked human subjects to make accurate step-tracking movements of the wrist to targets that required 5 degrees-30 degrees of radial or ulnar deviation. Speed instructions were given prior to each trial. Muscle activity was recorded from extensor carpi radialis longus (ECRL) and extensor carpi ulnaris (ECU) using surface electrodes. The agonist muscle initiated each movement with a brief burst of activity which began approximately 45 msec before movement onset. Then, the antagonist muscle displayed a brief burst of activity which began approximately 10 msec after movement onset. The magnitude, but not the timing, of these bursts was modulated by changes in the task requirements. The area of the initial agonist burst varied with changes in both displacement and intended speed. This burst was most highly correlated with the initial peaks of acceleration and jerk. In contrast, the area of the initial antagonist burst varied with changes in intended speed and was less well modulated by changes in displacement. This burst was highly correlated with the reciprocal of movement duration. Some small, fast movements had the same agonist bursts as some large, slow movements. However, the antagonist bursts for these movements differed greatly. This observation provides clear evidence that the magnitudes of the agonist and antagonist bursts are independently controlled. In a prior paper (Hoffman and Strick, 1986b), we proposed that step-tracking movements of different amplitudes and intended speeds are centrally generated by adjusting 2 kinematic variables: (1) the peak value and (2) the duration of a derivative of displacement. The present results suggest that these 2 kinematic parameters are separately generated by independently modulating the magnitudes of the agonist and antagonist bursts. Thus, the peak displacement of a step-tracking movement must be determined by the appropriate adjustment of both bursts of muscle activity.     

Motor cortex excitability during ballistic forearm and finger movements

In a ballistic forearm flexion movement, a centrally programmed triphasic pattern of electromyogram (EMG) is seen with two bursts in biceps and a single burst in triceps. Rapid abduction of the index finger, in contrast, is achieved with a single agonist burst. Transcranial magnetic and electrical stimuli, triggered at the onset of the EMG burst, have been used to probe cortical and spinal cord excitability during and after self-paced ballistic finger and forearm movements. In both, the motor cortex has two phases of increased excitability. The first phase is coincident with the initial agonist burst. The second phase in biceps is associated with the second agonist burst, but in the finger movement, the raised motor cortical excitability is not associated with any EMG. It is argued that the motor program for the two movements may be similar, despite there being large differences in the EMG pattern generated. © 1996 John Wiley & Sons, Inc.     

Responses to force perturbations preceding voluntary human arm movements

Brief force perturbations were applied 30–120 ms prior to onset of step-tracking forearm movements by normal humans. The perturbations altered the first agonist burst of the movement-related triphasic EMG pattern. Perturbations opposing the movement resulted in an increase in the magnitude of the late part of the first agonist burst, the early part being unchanged. Conversely, in movements which would be assisted by the perturbation, EMG magnitude decreased during the late part of the burst. No reflex EMG responses were elicited during the period following the perturbation and preceding onset of the first agonist burst.     

Jaw movement dysfunction related to Parkinson's disease and partially modified by levodopa.

OBJECTIVES--To test the hypotheses that Parkinson's disease can differentially produce deficits in voluntary and rhythmic jaw movements, which involve different neuronal circuits, and that levodopa treatment improves specific components of the motor deficit. METHODS--Patients with idiopathic Parkinson's disease and control subjects were tested on a series of jaw motor tasks that included simple voluntary movement, isometric clenching, and natural and paced rhythmic movements. Jaw movements were measured by changes in electromagnetic fields and EMG activity. Patients with Parkinson's disease with fluctuations in motor responses to levodopa were tested while off and on. RESULTS--During the off state, patients with Parkinson's disease were significantly worse than the control subjects on most tasks. The deficits included a decrease in amplitude and velocity during jaw opening and closing, aberrant patterns and low amplitude of EMG activity during clenching, and low vertical amplitude and prolonged durations of occlusion during rhythmic movements. No decrements were found in the amplitude of voluntary lateral jaw movements or the frequency of rhythmic movements. During the on state, improvements occurred in the patterns and level of EMG activity during clenching and in the vertical amplitude and duration of occlusion during rhythmic movements, although a significant decrement occurred in the lateral excursion of the jaw. CONCLUSIONS--Parkinson's disease affects the central programming of functionally related muscles involved in voluntary and rhythmic jaw movements and levodopa replacement influences only certain aspects of jaw movement, most likely those requiring sensory feedback.     

Impaired compensation for mechanical loads in a patient with hemiballismus following stroke

Flexion movements of the wrist were studied in a patient who showed signs of hemiballismus following a unilateral infarction, which damaged the region neighboring the subthalamic nucleus. The experiments were designed to test whether a lesion of this nature impairs load compensation and, specifically, whether antagonist activity can be appropriately suppressed when initiating a movement. The latency between movement onset and agonist EMG onset changed from the normal relationship where agonist onset precedes movement to one where agonist onset followed movement when an extensor load was placed on the affected limb. This was found to result from the inability to inhibit tonic activity in the antagonist and simultaneously activate the agonist muscle. The results suggest that the indirect pathway through the basal ganglia may be necessary to compensate for mechanical loads and to suppress antagonist activity when a movement is initiated.     

Physiological analysis of simple rapid movements in patients with cerebellar deficits.

Patients with cerebellar deficits made elbow flexion movements as rapidly as possible for three different angular distances. Electromyographic activity of biceps and triceps and the kinematics of the movements were analysed. Results were compared with those of normal subjects making both rapid and slow movements. In the patients, the first agonist burst of the biceps was frequently prolonged regardless of the distance or speed of the movement. The most striking kinematic abnormality was prolonged acceleration time. The pattern of acceleration time exceeding deceleration time was common in patients but uncommon in normal subjects. The best kinematic correlate of the duration of the first agonist burst was acceleration time. Altered production of appropriate acceleration may therefore be an important abnormality in cerebellar dysfunction for attempted rapid voluntary movements.     

Activity of wrist muscles during step-tracking movements in different directions

Human subjects made step-tracking movements of the wrist in 12 different directions while electromyographic activity was recorded from the long and short heads of the extensor carpi radialis. Three basic patterns of muscle activity were observed from a single muscle. The agonist pattern consisted of a large burst of activity beginning about 40 ms before movement onset, followed by relative inactivity during the movement. The antagonist pattern consisted of a large burst of activity beginning at or just after movement onset. The third pattern appeared to be a combination of agonist and antagonist patterns in a single muscle. These observations lead us to hypothesize that the nervous system has simplified the task of generating wrist movements in different directions by limiting the patterns of muscle activity to combinations of two basic patterns: agonist and antagonist.     

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.     

Fast complex arm movements in Parkinson''s disease.

Fast arm movements involving the shoulder and elbow joints have been analysed in normal controls and in patients with Parkinson's disease. The subjects were requested to draw on a graphic tablet triangles and squares of different size and shape. The patients produced a larger number of EMG burst compared with controls. The movements were accurate, and each segment of the geometric figures was performed with a roughly straight trajectory, but the time necessary to trace the geometric figures and the pauses at the vertices were prolonged. We conclude that in Parkinson's disease the disability in generating two joint ballistic movements depends on a difficulty in running motor programmes for complex trajectories.     

Effects of deep brain stimulation and medication on strength, bradykinesia, and electromyographic patterns of the ankle joint in Parkinson's disease.

We investigated the control of movement in 12 patients with Parkinson's disease (PD) after they received surgically implanted high-frequency stimulating electrodes in the subthalamic nucleus (STN). The experiment studied ankle strength, movement velocity, and the associated electromyographic patterns in PD patients, six of whom had tremor at the ankle. The patients were studied off treatment, ON STN deep brain stimulation (DBS), on medication, and on medication plus STN DBS. Twelve matched control subjects were also examined. Medication alone and STN DBS alone increased patients' ankle strength, ankle velocity, agonist muscle burst amplitude, and agonist burst duration, while reducing the number of agonist bursts during movement. These findings were similar for PD patients with and without tremor. The combination of medication plus STN DBS normalized maximal strength at the ankle joint, but ankle movement velocity and electromyographic patterns were not normalized. The findings are the first to demonstrate that STN DBS and medication increase strength and movement velocity at the ankle joint.     

Inhibition in the human motor cortex is reduced just before a voluntary contraction.

OBJECTIVE: To examine inhibition in the human motor cortex before and during voluntary movements. METHODS: The balance between the excitation and inhibition of corticospinal neurons in the human motor cortex was tested by conditioning the motor evoked potentials (MEP) evoked in forearm muscles by transcranial magnetic stimulation with a preceding subthreshold stimulus delivered through the same coil. RESULTS: When normal individuals (n = 9) made a tonic wrist extension, inhibition of the forearm extensor MEP decreased, whereas that of the forearm flexors was unchanged. When these individuals made a tonic wrist flexion, inhibition of the forearm flexor MEP diminished, whereas that of the forearm extensors was unchanged. When normal individuals (n = 10) made a phasic wrist extension in response to an auditory signal, inhibition of the extensor MEP began to decline about 95 msec before the onset of the agonist EMG activity. CONCLUSIONS: The changes in balance of excitation and inhibition of corticospinal neurons associated with a voluntary movement precede the movement and are directed at the corticospinal neurons projecting to the agonists. These changes may help to select the population of cortical neurons responsible for the movement.