Reciprocal change of motor-evoked potentials preceding voluntary movement in humans

Reciprocal change of motor-evoked potentials (MEPs) recorded from the agonist and antagonist muscles of the forearm was studied in 10 normal subjects in whom transcranial magnetic stimulation (TMS) was applied to the hand motor area before voluntary wrist movements. MEP recorded from the agonist muscles, that is, radial extensor muscles for wrist extension and ulnar flexor muscle for wrist flexion, were gradually facilitated with shortening of the interval between the magnetic stimulation and the voluntary muscle contraction. In contrast, MEP recorded from the antagonist muscles, that is, ulnar flexor muscle for wrist extension and radial extensor muscles for wrist flexion, were gradually suppressed as the interval shortened. The reciprocal change of MEP was recognized when TMS was applied within 60 ms prior to the voluntary movements. The present data confirmed that reciprocal change of MEP was recognized before voluntary movements; they further suggest that cortically originated reciprocal control of the corticospinal pathway may exist and that it may be generated just before the voluntary movement. © 1996 John Wiley & Sons, Inc.     

Voluntary movement at the elbow in spastic hemiparesis

The relative importance of hyperreflexia and paresis in disturbances of voluntary arm movement was studied in a group of patients (n = 25) with spasticity arising from a unilateral ischemic cerebral lesion. Patient performance was evaluated against data obtained from normal subjects (n = 15). Spastic patients achieved lower maximum movement velocities during flexion or extension than did normal subjects. The more marked the paresis of the elbow flexor and extensor muscles of the patients, relative to the strength of the normal subjects, the greater was this reduction in maximum velocity. For a given velocity, however, the time taken to complete a movement and the time to reach the peak velocity were normal. No relationship was found between the degree of impairment of voluntary movement and the level of passive muscle hypertonia in the antagonist. Although overactivity of the antagonist muscle may play some role in disturbance of movements made at low velocities without an opposing load, antagonist activity during movements made against a load (i.e., under more natural conditions) was at or below normal levels, even in those patients with the most marked passive muscle hypertonia. It is concluded that agonist muscle paresis, rather than antagonist muscle hypertonia, plays the dominant role in the disturbance of voluntary elbow movement following stroke.     

Reciprocal effect of single corticomotoneuronal cells on wrist extensor and flexor muscle activity in the primate

Action potentials of single motor cortex cells were recorded extracellularly in awake monkeys trained to make alternating wrist movements between flexion and extension position zones. Spike-triggered averaging of rectified EMG activity was used to test each cell's output effect on both the coactivated (agonist) forearm muscles and their antagonists. Five of 18 adequately tested motor cortex cells, whose activity covaried strongly with alternating wrist movement, not only produced postspike facilitation of agonist muscles but also postspike suppression of antagonist muscles. Five additional cells only facilitated the agonist muscles and had no effect on the recorded antagonists; 8 cells had no effect on either agonist or antagonist muscles. We conclude that the synaptic terminations of some motor cortex cells with flexor and extensor spinal motoneurons are reciprocally organized.     

Brain activation during human finger extension and flexion movements

Corticospinal projections to the motor neuron pool of upper-limb extensor muscles have been reported to differ from those of the flexor muscles in humans and other primates. The influence of this difference on the central nervous system control for extension and flexion movements is unknown. Cortical activation during thumb extension and flexion movements of eight human volunteers was measured using functional magnetic resonance imaging (fMRI), which detects signal changes caused by an alteration in the local blood oxygenation level. Although the relative activity of the extensor and flexor muscles of the thumb was similar, the brain volume activated during extension was substantially larger than that during flexion. These fMRI results were confirmed by measurements of EEG-derived movement-related cortical potential. Higher brain activity during thumb extension movement may be a result of differential corticospinal, and possibly other pathway projections to the motoneuron pools of extensor and flexor muscles of upper the extremities.     

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.     

Impairment of voluntary control of finger motion following stroke: role of inappropriate muscle coactivation

Subjects with chronic hemiplegia following stroke attempted to perform voluntary isometric, isokinetic, and free contractions of the extensor muscles of the metacarpophalangeal (MCP) joints. We recorded torque, metacarpophalangeal joint angle and velocity, and electromyographic (EMG) activity of the extrinsic extensors and flexors and the first dorsal interosseous (FDI). We found that voluntary MCP joint extension in hemiparetic subjects was greatly impaired in comparison with control subjects: only two of the 11 stroke subjects were able to generate even 0.21 N-m of isometric extension torque, only two could produce positive finger extension with no load, and none could develop an isokinetic concentric extension. Deficits seemed to result from a combination of coactivation of the finger flexor and extensor muscles and decreased voluntary excitation of the extensors, as normalized flexor and FDI EMG activity were greater for stroke than for control subjects (P < 0.001), but normalized extensor activity was reduced (P < 0.001).     

Laufband locomotion with body weight support improved walking in persons with severe spinal cord injuries.

After low transection of the spinal cord mammalian quadrupeds can be trained to walk on a driven surface indicating that coordinating neuronal circuits persist in the spinal cord segments caudal to the lesion. We trained 8 persons with incomplete spinal cord lesion on a Laufband (driven treadmill) for 1 1/2 to 7 months (5 days a week, 30-60 minutes daily) starting 5 to 20 months after injury and found significant improvement in the utilisation of the paralysed limbs during locomotion. Locomotion is described in one additional patient who had trained independently on parallel bars for several years. Five patients had complete functional paralysis in one lower limb when tested in a resting position. In EMG recordings voluntary activity (ie activity induced upon command) was absent or residual in the main flexor and extensor muscles of this limb. In contrast, during locomotion flexion and extension movements were performed and phasic EMG activity was present. In these 5 patients, and in all others reported here, skin sensibility and proprioception are preserved to different degrees in all limbs. In the course of locomotive training of 4 severely paralysed patients the initially habituating flexion reflexes could be entrained in the paralysed limbs as was the case for knee extension during stance. Subsequently, initial body weight support (BWS) of 40% could be reduced to 0%. The distance covered on the Laufband (0-104 m in the first week) increased significantly (200-410 m) in the last week of training as did speed (0-10 to 14-23 m/min). More importantly, this training subsequently allowed patients to walk on a static surface for 100 to 200 meters while voluntary activity remained absent in the paralysed limb when tested at rest. Similar progress was achieved in the 4 less severely paralysed patients. The one patient who had trained independently on parallel bars for several years is described walking on a static surface for 40 meters with the help of a walker, though he had one completely and one near completely paralysed lower limb. It appears that bipedal stepping with consequent knee extension and stabilisation can be taught after unilateral complete or near complete loss of voluntary activity, suggesting the manifestation of complex reflex motor patterns at the spinal level.     

Was Sherrington right about co-contractions?

Differences in electromyographic (EMG) activity between brief isometric maximum voluntary contractions under conditions of agonist contraction and agonist-antagonist co-contractions were assessed for elbow flexors (biceps brachii) and elbow extensors (triceps, long head). Expressing maximum EMG co-contraction activity as a ratio of agonist maximum EMG activity of the same muscle yielded EMG ratios consistently below 1.0 (mean = 0.48 for flexion and 0.76 for extension). Flexor EMG ratios did not co-vary with elbow position but extensor EMG ratios approached 1.0 or sometimes greater at shorter muscle lengths (elbow extension). Findings were in general accord with Sherrington's original proposal of 'double reciprocal innervation'. Neural circuitry designed to limit full muscle activation during co-contractions may serve to protect the joint against excessive tangential or compressive forces.     

Independent control of voluntary movements and associated anticipatory postural responses in a bimanual task.

OBJECTIVE: When one hand loads the other arm, EMG responses in the stationary arm anticipate the load. This study used transcranial magnetic stimulation over each hemisphere to clarify the relationship between a voluntary movement on one side and the anticipatory postural response on the other. METHODS: Subjects (n = 7) performed elbow flexion movements of one arm as a reaction-time task. Because subjects' arms were linked, flexion about one elbow resulted in extension force about the other, and an anticipatory response occurred in those elbow flexor muscles. After the 'go' signal and before the predicted onset of EMG, transcranial magnetic stimuli were delivered over one or other motor cortex. RESULTS: Stimulation contralateral to the reaction-time movement delayed the onset of voluntary EMG (46 ms in right biceps, 77 ms left) but did not alter the onset of EMG in the postural arm. Stimulation contralateral to the anticipatory postural response delayed only the postural EMG (left 96 ms, right 52 ms). CONCLUSIONS: Thus, the associated voluntary and postural responses were delayed independently by stimuli over their respective contralateral motor cortex. SIGNIFICANCE: This suggests that, although timing of responses may be linked by an initial signal, the response from each motor cortex develops independently.     

Abnormal surface EMG during clinically normal wrist movement in cervical dystonia

We investigated whether patients with cervical dystonia (CD) have abnormal muscle activation in non-dystonic body parts. Eight healthy controls and eight CD patients performed a flexion-extension movement of the right wrist. Movement execution was recorded by surface electromyography (EMG) from forearm muscles. Although patients had no complaints concerning wrist movement and had no apparent difficulty in executing the task, they demonstrated lower mean EMG amplitude (flexor: 0.32 mV and extensor: 0.61 mV) than controls (flexor: 0.67 mV; P  = 0.021 and extensor: 1.18 mV; P  = 0.068; borderline significant). Mean extensor muscle contraction was prolonged in patients (1860 ms) compared with controls (1334 ms; P  = 0.026). Variation in mean EMG amplitude over movements tended to be higher in patients (flexor: 43% and extensor: 35%) than controls (flexor: 34%; P  = 0.072 and extensor: 26%; P  = 0.073). These results suggest that CD patients also have abnormal muscle activation in non-dystonic body parts at a subclinical level. This would support the concept that in dystonia, non-dystonic limbs are in a 'pre-dystonic state'.     

Quantitative evaluation of electromyogram activity in rat extensor and flexor muscles immobilized at different lengths

Because immobilization of muscles in the "long" position mitigates the effects of inactivity and rapid wasting occurs when muscles are immobilized in the "short" position, a study was made of the EMG activity in the soleus (SOL)--an extensor muscle--and the tibialis anterior (TA)--a flexor muscle--in order to clarify the possible role of muscle function in modifying the course of disuse atrophy. EMG activity was recorded in the SOL and TA muscles in adult rats in which the ankle had been immobilized in a plaster cast either in plantar flexion or dorsiflexion. The number of action potentials per minute in samples of the EMG activity from control and immobilized muscles was assessed before, for 10 days during immobilization, and up to 9 days after removal of the cast. Immobilization in the short position (plantar flexion) led to a dramatic reduction in the EMG activity of the SOL (to 10% of the control). On the other hand, fixation of the SOL in the long position was without effect upon resting EMG activity. In the TA, EMG activity was exclusively phasic in character and corresponded to about 3% of that of the SOL. Neither the fixation of the ankle in plantar flexion nor dorsiflexion had any appreciable effect upon EMG activity in the TA. We conclude that, because immobilization in the lengthened position does not increase EMG activity in either extensor or flexor muscles, passive stretch appears to be the factor mainly responsible for mitigating the effects of disuse in this situation. On the other hand, when a typical extensor muscle (SOL) is immobilized in the shortened position and undergoes rapid wasting, an accessory role of decreased activity cannot be excluded.     

Prime mover muscle in finger lift or finger flexion reaction times: identification with transcranial magnetic stimulation.

When recording the onset of the electromyographic (EMG) voluntary response in reaction time (RT) studies, the electrodes should be placed on the muscle which is first and foremost involved in executing the response. It is thus necessary to identify which is the prime mover muscle among active synergic muscles. This has been investigated for index finger lift or flexion RTs by delivering a magnetic stimulus to motor cortical areas prior to the subject's voluntary response. The EMG responses to the magnetic stimulus were selectively facilitated either in the extensor indicis proprius muscle (in index lift RTs) or in the first dorsal interosseous muscle (in index flexion RTs). These effects are robust and provide a method for identifying the prime mover muscle in voluntary movements.     

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.     

Botulinum toxin in post-stroke patients: stiffness modifications and clinical implications

Abstract.Objective: To objectively quantify stiffness and clinical changes in the upper limb of poststroke patients following botulinum toxin (BT) injection.Methods: Eighteen consecutive chronic post-stroke spastic patients were injected Botulinum toxin A in the forearm flexor spastic muscles. Spasticity was clinically evaluated with the Ashworth scale. Stiffness was measured with indices (passive stiffness index (ISI) and total stiffness index (TSI) obtained by mechanical wrist displacements induced by a torque motor,which could also provide the stretch reflex threshold speed (SRTS) from flexor muscles. Functional status was measured with the Barthel index and a specific hand ability scale, pain with a visual analogue scale (VAS). The ranges of voluntary wrist extension (EROM) and flexion (FROM) and wrist isometric extension and flexion (IE—IF) strength were also calculated.Results: IE and EROM significantly increased, being respectively p < 0.01 and p < 0.05; also SRTS was augmented (p < 0.001),while TSI showed lower values (p < 0.001); the Ashworth score decreased at least one point.Hand function for selected tasks improved in 50% of patients, the Barthel index only in 4 (22 %), forearm pain was completely relieved in 3 patients (17 %).Conclusions: BT can be considered a valid therapeutic tool in all spastic patients, because of immediate advantages: reduction of muscle hypertonia, pain relief, improvement in selected motor performances.     

Effect of antagonistic voluntary contraction on motor responses in the forearm.

OBJECTIVE: We investigated the effects of voluntary contraction of agonist and antagonist muscles on motor evoked potentials (MEP) and on myoelectric activities in the target (agonist) muscle following transcranial magnetic stimulation (TMS). METHODS: The left extensor carpi radialis (ECR) and flexor carpi radialis (FCR) muscles were studied in 16 healthy subjects. H reflexes, MEP induced by TMS, and background electromyographic (EMG) activity were recorded using surface electrodes at rest and during voluntary contraction of either agonist or antagonist muscles. RESULTS: Voluntary contraction of antagonist muscles (at 10% of maximum contraction) enhanced the amplitudes of MEP for both muscles. The H reflex of the FCR muscle was inhibited by contraction (10% of maximum) of the ECR muscle. Background EMG activity did not differ between H-reflex trials and TMS trials. Enhancement of MEP amplitudes and background EMG activity during voluntary antagonist contraction was comparable in the two muscles. Appearance rate of MEP recorded by needle electrodes in response to subthreshold TMS was increased by antagonistic voluntary contraction. CONCLUSION: Facilitation occurs during voluntary contraction of antagonist muscles. Differences between the effects of voluntary contraction of the ECR muscle for the MEP and the H reflex of the FCR suggest that cortical facilitatory spread occurs between agonist and antagonist muscles.     

Action of dantrolene sodium in spasticity with low dependence on fusimotor drive.

The effects of dantrolene sodium, an anti-spasticity drug with a site of action within the muscle fibres, were studied in 19 patients with spastic paresis. Oral doses were successively increased from 100 mg/day to a maximal tolerated level or up to 800 mg/day. Trial periods were 8-13 weeks. The responses of stretch reflexes to local cooling over the spastic muscles were used to differentiate alpha and gamma spasticity. In the knee extensor and flexor muscle groups, cryo-negative alpha-spasticity was seen in 25 and cryo-positive gamma-spasticity in 4 muscle groups. Ankle clonus was cryo-positive in 14 of 15 cases. Resistance to passive knee joint movements, ankle clonus and isometric or isokinetic muscle strength was determined quantitatively. The gait was recorded by intermittent-light photography and the muscle activation patterns in gait were studied in recordings of the average EMG from limb muscles. Functional disability and spasms were assessed from clinical examinations and interviews. Passive resistance at slow (6%/sec) and fast (30 degrees/sec) knee joint movements decreased by 32% in the extensor muscles (p = 0.005 resp. 0.001) and by 23-26% in the flexor muscles (not significant). Reduced passive resistance was observed in 16 of the muscles with alpha-spasticity and in all 4 of the muscle groups with gamma-spasticity. Clonus was diminished or abolished in 14 of 15 patients with this sign. Maximal isometric or isokinetic muscle strength was unaltered in the majority of the patients. In a few the strength was increased, in some it was decreased. The averaged EMG activity during walking as studied in 10 patients were increased in 35 of the 57 muscle groups examined. In some muscle groups, exaggerated activity attributable to spastic reflexes was reduced. Motor disability was decreased significantly in 10 patients. It was not significantly changed in 5 and deteriorated in 4 patients. Drowsiness and subjective muscle weakness were the most frequent side-effects. SGOT and SGPT were increased in 3 cases.     

Interactions between imagined movement and the initiation of voluntary movement: A TMS study

ObjectiveThe purpose was to examine motor imagery-induced enhancement in corticospinal excitability during a reaction time (RT) task.MethodsNine young and healthy subjects performed an isometric finger flexion tasks in response to a visual imperative cue. In the pre-cue period, they were instructed to: (1) rest; (2) imagine flexing their fingers isometrically (ImFlex); or (3) imagine extending their fingers isometrically (ImExt). Surface EMGs from the finger flexors and extensors were monitored to ensure EMG silence before movement onset. Transcranial magnetic stimulation (TMS) was used to evaluate changes in motor-evoked potentials (MEP) in the finger flexor and extensor muscles during the response phase. TMS was delivered either with the imperative cue, or 120 ms before and after the imperative cue.ResultsRT was slower when they were imagining finger extension prior to the visual imperative cue. MEPs were significantly increased for the finger flexors during imagined finger flexion and for the finger extensors during imagined finger extension at both TMS delivery time points, reflecting movement specific enhancement in corticospinal excitability during motor imagery. When TMS was delivered 120 ms after the cue, finger flexor MEPs were further facilitated under the Rest and ImFlex conditions, but not under the ImExt condition, suggesting additive interactions between imagery-induced enhancement and early rise in corticospinal excitability during the initiation of a reaction time response.ConclusionsOur results provide neurophysiological evidence mediating dynamic interactions between imagined movement and the initiation of voluntary movement.SignificanceMotor imagery can be integrated into a rehabilitation protocol to facilitate motor recovery.     

Modulation of locomotor-like EMG activity in subjects with complete and incomplete spinal cord injury

Treadmill training with partial body weight support (BWS) is being advocated as a strategy to enhance walking in patients with spinal cord injury (SCI). Clinical reports have not examined the range of sensory inputs that might modulate electromyographic (EMG) output in the legs during training. During passive, manually assisted stepping on a treadmill with partial BWS, we found similar rhythmical EMG activity in the flexor and extensor muscles of the lower extremities in subjects who had chronic, complete thoracic spinal cord injuries and in subject who had incomplete lesions that resulted in minimal motor control and an inability to ambulate. The EMG bursts were temporally synchronized to specific phases of the step cycle, and their amplitudes and durations were modulated by varying the treadmill speed and the level of limb loading. Hip extension at the end of stance often induced involuntary hip flexion that initiated the swing phase. When the incomplete SCI subjects attempted volitional stepping, the EMG bursts in some muscles had a similar waveform but greater amplitude and duration compared to that observed during passive, assisted stepping. This suggests that, as in the model of the cat after a thoracic spinal transection, peripheral sensory inputs that are associated with rhythmical locomotion can enhance the output of lumbosacral neural circuits that contribute to step-like EMG activity, even in the absence of supraspinal descending influences. Attention should be given to optimizing the manipulation of sensory inputs during rehabilitation efforts with body weight supported treadmill training.