Modulation of cutaneous reflexes in arm muscles during walking: further evidence of similar control mechanisms for rhythmic human arm and leg movements

Stimulation of cutaneous nerves innervating the hand evokes prominent reflexes in many arm muscles during arm cycling. We hypothesized that the mechanisms controlling reflex modulation during the rhythmic arm swing of walking would be similar to that documented during arm cycling. Thus, we expected cutaneous reflexes to be modulated by position in the walking cycle (phase dependence) and be different when walking compared to contraction while standing (task dependence). Subjects performed static postures similar to those occurring during walking and also walked on a treadmill while the superficial radial nerve was electrically stimulated pseudorandomly throughout the step cycle. EMG was recorded bilaterally from upper limb muscles and kinematic recordings were obtained from the elbow and shoulder joints. Step cycle information was obtained from force-sensing insoles. Analysis was conducted after averaging contingent upon the occurrence of stimulation in the step cycle. Phase-dependent modulation of cutaneous reflexes at early (~50–80 ms) and middle (~80–120 ms) latencies was observed. Coordinated bilateral reflexes were seen in posterior deltoid and triceps brachii muscles. Task dependency was seen in that reflex amplitude was only correlated with background EMG during static contraction (75% of comparisons for both early and middle latency reflexes). During walking, no significant relationship between reflex amplitude and background EMG level was found. The results show that cutaneous reflex modulation during rhythmic upper limb movement is similar to that seen during arm cycling and to that observed in leg muscles during locomotion. These results add to the evidence that, during cyclical movements of the arms and legs, similar neural mechanisms observed only during movement (e.g. central pattern generators) control reflex output. Electronic Publication     

Modulation of cutaneous reflexes by load receptor input during human walking

To investigate the influence of load on the modulation of cutaneous reflexes, evoked by sural nerve stimulation, electromyographic activity in different leg muscles (tibialis anterior, gastrocnemius medialis (GM), biceps femoris, and soleus muscles (SO)) was recorded in healthy humans during treadmill walking with different body loads. Sural nerve stimulation was applied at two times perception threshold during different phases of the step cycle. Reflex amplitudes increased with body unloading and decreased with body loading. The reflex responses were not a simple function of the level of background activity. For example, in GM and SO, the largest reflex responses occurred during walking with body unloading, when background activity was decreased. Hence, stable ground conditions (body loading) yielded smaller reflexes. It is proposed that load receptors are involved in the regulation of cutaneous reflex responses in order to adapt the locomotor pattern to the environmental conditions.     

Modulation of heteronymous reflexes from ankle dorsiflexors to hamstring muscles during human walking

In 16 human subjects, stimulation of the common peroneal nerve (CPN) was applied during walking and standing. The effect of the stimulation was evaluated from the rectified and averaged biceps femoris (BF) electromyographic (EMG) activity. In the swing phase of walking, the CPN stimulation evoked a suppression in the BF EMG in 12 of the subjects. In the early stance phase, the suppression was replaced by facilitation at a similar latency in 9 of the subjects. Of the other 3 subjects, in whom a suppression was observed during swing, a decrease in the suppression was observed in the stance phase in two of them. During a voluntary co-contraction of BF and tibialis anterior while standing, a suppression similar to that observed in the swing phase was observed. The thresholds of the suppression and facilitation were identical, suggesting that afferents of similar diameter were responsible. Cutaneous stimuli, which mimicked the sensation evoked by the CPN stimulation, but without activation of muscle afferents, did not produce similar effects in the BF EMG activity. It is suggested that the observed response and reflex reversal may reflect opening of an excitatory group I pathway in the early stance phase of walking with a concomitant shut-down of heteronymous group I inhibition.     

Suppression of cutaneous reflexes by a conditioning pulse during human walking

There are two ways in which responses to successive unexpected stimuli are attenuated, namely through habituation and conditioning. For the latter, it suffices that the unexpected stimulus is preceded by another just perceivable stimulus. In spinal cord reflexes this is termed conditioning, while in brainstem reflexes this is usually referred to as prepulse inhibition. Cutaneous reflexes in Tibialis Anterior (TA) are particularly strong during gait and they are thought to involve a transcortical loop. Can these reflexes be suppressed by giving a brief pulse prior to a reflex-evoking pulse given to the same nerve? To examine this question, electromyographic signals were recorded in healthy humans during walking. Sural nerve stimulation (train of five pulses (1 ms duration)) at 200 Hz were applied at two times perception threshold during different phases of the step cycle. The preceding pulse (single pulse of 1 ms at same intensity) was applied to the same nerve 150 ms before the reflex-evoking pulse train. Conditioning stimulation with a single pulse lowered significantly the following reflex response in the ipsilateral TA but much less in other muscles such as biceps femoris. The preceding pulse did not disturb the phase-dependent modulation or the typical reflex reversal. The finding that TA is selectively involved indicates that the suppressing mechanism may involve the motor cortex, which is known to be involved in the control of TA. The conditioning pulse did not cause a reduction in background activity. Therefore, the suppression of the reflex responses points to a premotoneuronal source such as presynaptic inhibition.     

Neural control of rhythmic human arm movement: phase dependence and task modulation of hoffmann reflexes in forearm muscles

Although we move our arms rhythmically during walking, running, and swimming, we know little about the neural control of such movements. Our working hypothesis is that neural mechanisms controlling rhythmic movements are similar in the human lumbar and cervical spinal cord. Thus reflex modulation during rhythmic arm movement should be similar to that seen during leg movement. Our main experimental hypotheses were that the amplitude of H-reflexes in the forearm muscles would be modulated during arm movement (i.e., phase-dependent) and would be inhibited during cycling compared with static contraction (i.e., task-dependent). Furthermore, to determine the locus of any modulation, we tested the effect that active and passive movement of the ipsilateral (relative to stimulated arm) and contralateral arm had on H-reflex amplitude. Subjects performed rhythmic arm cycling on a custom-made hydraulic ergometer in which the two arms could be constrained to move together (180 degrees out of phase) or could rotate independently. Position of the stimulated limb in the movement cycle is described with respect to the clock face. H-reflexes were evoked at 12, 3, 6, and 9 o'clock positions during static contraction as well as during rhythmic arm movements. Reflex amplitudes were compared between tasks at equal M wave amplitudes and similar levels of electromyographic (EMG) activity in the target muscle. Surface EMG recordings were obtained bilaterally from flexor carpi radialis as well as from other muscles controlling the wrist, elbow, and shoulder. Compared with reflexes evoked during static contractions, movement of the stimulated limb attenuated H-reflexes by 50.8% (P < 0.005), 65.3% (P < 0.001), and 52.6% (P < 0.001) for bilateral, active ipsilateral, and passive ipsilateral movements, respectively. In contrast, movement of the contralateral limb did not significantly alter H-reflex amplitude. H-reflexes were also modulated by limb position (P < 0.005). Thus task- and phase-dependent modulation were observed in the arm as previously demonstrated in the leg. The data support the hypothesis that neural mechanisms regulating reflex pathways in the moving limb are similar in the human upper and lower limbs. However, the inhibition of H-reflex amplitude induced by contralateral leg movement is absent in the arms. This may reflect the greater extent to which the arms can be used independently.     

Corticospinal excitability is lower during rhythmic arm movement than during tonic contraction

Humans perform rhythmic, locomotor movements with the arms and legs every day. Studies using reflexes to probe the functional role of the CNS suggest that spinal circuits are an important part of the neural control system for rhythmic arm cycling and walking. Here, by studying motor-evoked potentials (MEPs) in response to transcranial magnetic stimulation (TMS) of the motor cortex, and H-reflexes induced by electrical stimulation of peripheral nerves, we show a reduction in corticospinal excitability during rhythmic arm movement compared with tonic, voluntary contraction. Responses were compared between arm cycling and tonic contraction at four positions, while participants generated similar levels of muscle activity. Both H-reflexes and MEPs were significantly smaller during arm cycling than during tonic contraction at the midpoint of arm flexion (F = 13.51, P = 0.006; F = 11.83, P = 0.009). Subthreshold TMS significantly facilitated the FCR H-reflex during tonic contractions, but did not significantly modulate H-reflex amplitude during arm cycling. The data indicate a reduction in the responsiveness of cells constituting the fast, monosynaptic, corticospinal pathway during arm cycling and suggest that the motor cortex may contribute less to motor drive during rhythmic arm movement than during tonic, voluntary contraction. Our results are consistent with the idea that subcortical regions contribute to the control of rhythmic arm movements despite highly developed corticospinal projections to the human upper limb.     

Cutaneous reflexes during rhythmic arm cycling are insensitive to asymmetrical changes in crank length

The neural control of a movement depends upon the motor task performed. To further understand the neural regulation of different variations of the same type of movement, we created three dissimilar bilateral rhythmic arm cycling tasks by unilaterally manipulating crank length (CL). Modulation in the amplitude and sign of cutaneous reflexes was used as an index of neural control. Neurologically intact subjects performed three bilateral cycling trials at ∼1 Hz with the ipsilateral crank arm at one of three different lengths. Cutaneous reflexes were evoked during each trial with trains (5 × 1.0 ms pulses at 300 Hz) of electrical stimulation delivered to the superficial radial nerve at the ipsilateral wrist. EMG recordings were made bilaterally from muscles acting at the shoulder, elbow, and wrist. Analysis was conducted after phase-averaging contingent upon the timing of stimulation in the movement cycle. CL variation created an asymmetrical cycling pattern and produced significant changes in the range of motion at the ipsilateral shoulder and elbow. Background EMG amplitude in muscles of the contralateral arm generally increased significantly as CL decreased. Therefore at a given phase in the movement cycle, the background EMG was different between the three cycling trials. In contrast, cutaneous reflex amplitudes in muscles of both arms were similar at each phase of the movement cycle between the different CLs trials at both early and middle latencies. This was particularly evident in muscles ipsilateral to nerve stimulation. We suggest that variations of arm cycling that primarily yield significant changes in the amplitude of muscle activity do not require significant task-specific change in neural control.     

Effect of rhythmic arm movement on reflexes in the legs: modulation of soleus H-reflexes and somatosensory conditioning

During locomotor tasks such as walking, running, and swimming, the arms move rhythmically with the legs. It has been suggested that connections between the cervical and lumbosacral spinal cord may mediate some of this interlimb coordination. However, it is unclear how these interlimb pathways modulate reflex excitability during movement. We hypothesized that rhythmic arm movement would alter the gain of reflex pathways in the stationary leg. Soleus H-reflexes recorded during arm cycling were compared with those recorded at similar positions with the arms stationary. Nerve stimulation was delivered with the right arm at approximately 70 degrees shoulder flexion or 10 degrees shoulder extension. H-reflexes were evoked alone (unconditioned) or with sural or common peroneal nerve (CP) conditioning to decrease or increase soleus IA presynaptic inhibition, respectively. Both conditioning stimuli were also delivered with no H-reflex stimulation. H-reflex amplitudes were compared at similar M-wave amplitudes and activation levels of the soleus. Arm cycling significantly reduced (P < 0.05) unconditioned soleus H-reflexes at shoulder flexion by 21.7% and at shoulder extension by 8.8% compared with static controls. The results demonstrate a task-dependent modulation of soleus H-reflexes between arm cycling and stationary trials. Sural nerve stimulation facilitated H-reflexes at shoulder extension but not at shoulder flexion during static and cycling trials. CP nerve stimulation significantly reduced H-reflex amplitude in all conditions. Reflexes in soleus when sural and CP nerve stimulation were delivered alone, were not different between cycling and static trials; thus the task-dependent change in H reflex amplitude was not due to changes in motoneuron excitability. Therefore modulation occurred at a pre-motoneuronal level, probably by presynaptic inhibition of the IA afferent volley. Results indicate that neural networks coupling the cervical and lumbosacral spinal cord in humans are activated during rhythmic arm movement. It is proposed that activation of these networks may assist in reflex linkages between the arms and legs during locomotor tasks.     

Abeta fibers mediate cutaneous reflexes during human walking

During human gait, transmission of cutaneous reflexes from the foot is controlled specifically according to the phase of the step cycle. These reflex responses can be evoked by nonnociceptive stimuli, and therefore it is thought that the large-myelinated and low-threshold Abeta afferent fibers mediate these reflexes. At present, this hypothesis is not yet verified. To test whether Abeta fibers are involved the reflex responses were studied in patients with a sensory polyneuropathy who suffer from a predominant loss of large-myelinated Abeta fibers. The sural nerve of both patients and healthy control subjects was stimulated electrically at a nonnociceptive intensity during the early and late swing phases while they walked on a treadmill. The responses were studied by recording electromyographic (EMG) activity of the biceps femoris (BF) and tibialis anterior (TA) of the stimulated leg. In both phases, large facilitatory responses were observed in the BF of the healthy subjects. These facilitations were reduced significantly in the BF of the patients, indicating that Abeta fibers mediate these reflexes. In TA similar results were obtained. The absolute response magnitude across the two phases was significantly smaller for the patients than for the healthy subjects. The TA responses for the healthy subjects were on average facilitatory during early swing and suppressive during end swing. Both facilitations and suppressions were considerably smaller for the patients, indicating that both types of responses are mediated by Abeta fibers. It is concluded that low-threshold Abeta sensory fibers mediate these reflexes during human gait. The low threshold and the precise phase-dependent control of these responses suggest that these responses are important in the regulation of gait. The loss of such reflex activity may be related to the gait impairments of these patients.     

Modulation of short latency stretch reflexes during human hopping

To gain insight into central and peripheral reflex control mechanisms in moving humans we have investigated short latency stretch reflex activity in m. tricgif surae during two legged hopping. The objectives were: (1) to compare movement induced short latency stretch reflexes in soleus and medial gastrocnemius (MG) muscles, (2) to determine the relationship between the size of these reflexes and the muscle spindle stretch velocities, and (3) to compare the size of the movement induced short latency stretch reflexes and the H-reflexes simultaneously. Six well-trained healthy male subjects participated and they hopped at three different work rates. Surface electromyogram (EMG) and H-reflexes were recorded during hopping. Muscle spindle length changes were estimated as the difference between estimated origin-to-insertion length changes and tendon length changes. The important findings were that during hopping: (1) movement induced short latency stretch reflexes were observed consistently in soleus, (2) the EMG amplitude of this stretch reflex was negatively correlated with the estimated peak muscle spindle stretch velocity (r_s=?0.52, P < 0.02), and (3) the amplitude of the soleus H-reflex at touchdown did not change in parallel with the stretch reflex. The negative correlation observed between the stretch reflex and the estimated peak muscle spindle stretch velocity in soleus is opposite to the basic velocity sensitive behaviour of stretch reflexes mechanically elicited during resting conditions. Possible control mechanisms are discussed. Additionally, muscle spindle length changes estimated from changes in the skeletal movements (joint angles) should be inferred cautiously because of tendon compliance, especially at high tendon forces.     

Slowing of human arm movements during weightlessness: the role of vision

The human motor system responds to weightlessness by the slowing of movement. It has been suggested that deficits in visuo-motor co-ordination cause this effect. We studied the mechanisms of the slowing of movement in three long-term missions to the Russian space station Mir. In particular, the role of vision in the control of movement in microgravity has been studied in these experiments on seven cosmonauts, pre-, in-, and post-flight. The cosmonauts made arm movements to visual targets under the following conditions of visual control: no visual control, interrupted visual control, and undisturbed visual control. The results showed that the slowing of movement during weightlessness was manifested by decreases of peak velocity and peak acceleration, was not associated with a prolongation of the movement phase of deceleration, and was not affected by manipulation of the conditions of visual control. The slowing of movement tended to subside after the months of the flight and completely disappeared within days after the landing. Accuracy of the movements strictly depended on the constraints imposed on the vision and remained unaffected in-flight. The data presented demonstrate that the slowing of movement in microgravity is not directly related to deficits in sensori-motor co-ordination and is not associated with a reduction of the accuracy of movement. The strategy for motor control in microgravity seems to be directed towards the generation of smooth movements and the maintenance of their accuracy. Electronic Publication     

Neural regulation of rhythmic arm and leg movement is conserved across human locomotor tasks

It has been proposed that different forms of rhythmic human limb movement have a common central neural control ('common core hypothesis'), just as in other animals. We compared the modulation patterns of background EMG and cutaneous reflexes during walking, arm and leg cycling, and arm-assisted recumbent stepping. We hypothesized that patterns of EMG and reflex modulation during cycling and stepping (deduced from mathematical principal components analysis) would be comparable to those during walking because they rely on similar neural substrates. Differences between the tasks were assessed by evoking cutaneous reflexes via stimulation of nerves in the foot and hand in separate trials. The EMG was recorded from flexor and extensor muscles of the arms and legs. Angular positions of the hip, knee and elbow joints were also recorded. Factor analysis revealed that across the three tasks, four principal components explained more than 93% of the variance in the background EMG and middle-latency reflex amplitude. Phase modulation of reflex amplitude was observed in most muscles across all tasks, suggesting activity in similar control networks. Significant correlations between EMG level and reflex amplitude were frequently observed only during static voluntary muscle activation and not during rhythmic movement. Results from a control experiment showed that strong correlation between EMG and reflex amplitudes was observed during discrete, voluntary leg extension but not during walking. There were task-dependent differences in reflex modulation between the three tasks which probably arise owing to specific constraints during each task. Overall, the results show strong correlation across tasks and support common neural patterning as the regulator of arm and leg movement during various rhythmic human movements.     

Modulation of sensory transmission in cat lemniscal system during voluntary movement

Summary Adult cats were trained to lift their forepaw, depress a lever and then replace their paw on the ground. The potential recorded in the medial lemniscus to stimulation of the superficial radial nerve in the forelimb involved in the movement is depressed both prior to and during displacement of the limb. These changes did not result from movement of the stimulating electrode. The timing of the suppression in lemniscal transmission suggests a central origin of this effect.This investigation was supported by P.H.S. research grant NB 07685-02 from the National Institute of Neurological Diseases and Blindness, N.I.H., Public Health Service, U.S.A. and by a research grant from the Consiglio Nazionale delle Ricerche, Italy.     

Absence of nerve specificity in human cutaneous reflexes during standing

Cutaneous reflexes in lower limb muscles were recorded from healthy human subjects after non-noxious electrical stimulation of superficial peroneal (SP), sural and distal tibial nerves while subjects: (1) made graded voluntary contractions of the ankle and knee extensor and flexor muscles while mimicking late stance or heel strike limb positions; and (2) walked on a treadmill at speeds of 2 and 4 km/h. During standing, net reflexes were predominantly suppressive and graded with background EMG. In contrast, during walking net reflexes were mostly facilitatory and uncorrelated with background EMG. Opposite signs (negative during standing, positive during walking) and significant differences of the reflex ratio (net reflex/background EMG) were seen in most leg muscles. The nerve stimulated did not determine the sign of the net reflex while standing: nerve specificity was absent. We suggest that during standing, where maintenance of posture is of primary importance, there is a reduction of effort that led to increased cutaneous input (i.e., a global suppressive response), while during walking there is a modulation of reflexes which is independent of muscle activation level but closely tied to events occurring in the step cycle.     

Gating and reversal of reflexes in ankle muscles during human walking

Summary Phase-dependent reflex modulation was studied by recording the electromyographic (EMG) responses in ankle flexors (Tibialis Anterior, TA) and extensors (Gastrocnemius Medialis, GM and Soleus, SOL) to a 20 ms train of electrical pulses, applied to the tibial or sural nerve at the ankle, in human volunteers walking on a treadmill at 4 km/h. For low intensity stimuli (i.e. 1.6 times perception threshold), given during the swing phase, the most common response was a suppression of the TA activity with a latency of 67 to 118 ms. With high intensity of stimulation (i.e. 2.8 × T), a facilitatory response appeared in TA with a latency of 74 ms. This latter response was largest during the middle of the swing phase, when it was correlated with exaggerated ankle dorsiflexion. The TA reflex amplitude was not a simple function of the level of spontaneous ongoing activity. During stance, TA responses were small or absent and accompanied by a suppression of the GM activity with a latency ranging from 62 to 101 ms. A few subjects showed an early facilitatory, instead of a suppressive, GM response (88 to 136 ms latency). They showed a phase-dependent reflex reversal from a dominant TA response during swing to a facilitatory GM response with an equivalent latency during stance. The GM facilitation occurred exclusively during the early stance phase and habituated more than the TA responses. It is concluded that phase-dependent gating of reflexes occurs in ankle muscles of man, but only when vigorous extensor reflexes are present. More commonly, a phase-dependent modulation is seen, both of facilitatory and suppressive responses.     

Muscle activation and cutaneous reflex modulation during rhythmic and discrete arm tasks in orthopaedic shoulder instability

In orthopaedic shoulder instability, muscle activity (EMG) is altered during unconstrained discrete arm movement tasks (e.g. elevation against a load). These findings have been ascribed to deficits in afferent feedback and neural control with glenohumeral instabilities resulting from orthopaedic injury. However, the integrity of neural control during shoulder movements in those with unstable shoulders is unclear. It is not known if there are altered EMG patterns during rhythmic arm movement or during discrete tasks involving no load, as would be experienced in many arm motions performed in daily living. The primary objective of this study was to evaluate neural control of arm movements between those with unstable shoulders and control participants, within a constrained arm movement paradigm involving both rhythmic arm cycling and discrete reaching. To achieve this objective, we determined if the amplitude and timing of EMG related to the movement pattern (background EMG) was significantly different between groups. Cutaneous reflexes were used to simulate a perturbation to the upper limb that would typically evoke a coordinated response. In the elevation phase of the movement path for anterior and posterior deltoid, upper trapezius, infraspinatus and serratus anterior, background EMG during rhythmic arm cycling was significantly (24%, p < 0.05) larger in unstable shoulders than in controls. No differences were found in background EMG between the groups during the discrete task. Significant differences (p < 0.05) were also noted in cutaneous reflexes between groups for both the rhythmic and discrete tasks with the reflex amplitudes being either increased or reduced in unstable shoulders as compared to controls. The differences in the background EMG and the cutaneous reflexes patterns in those with shoulder instabilities suggest that neural control is altered during rhythmic movement.     

Neuromagnetic motor fields accompanying self-paced rhythmic finger movement at different rates

We have studied the effect of movement rate on MEG activity associated with self-paced finger movement in four subjects to determine whether the amplitude or latency of motor-evoked activity changes across a range of rates. Subjects performed a continuation paradigm at 21 distinct rates (range: 0.5–2.5 Hz) chosen because of their relevance for many types of sensorimotor coordination (e.g. musical performance). Results revealed a pair of field patterns whose topography and temporal dynamics were similar across all subjects. The strongest pattern was a movement-evoked field (MEF) that emerged during the response and exhibited one or two polarity reversals in time depending on the subject. The MEF complex was tightly coupled to the biphasic response profile but neither latency nor peak amplitude of each MEF component had significant dependence on the temporal duration between successive responses, i.e. movement rate. In contrast, the maximal amplitude of a second, weaker pattern decreased by over 50% when movement rates exceeded 1.1 Hz (inter-response interval <1 s). This pattern was characterized by a change in field line direction over the midline of the scalp and a gradual accumulation of amplitude prior to movement onset. Both characteristics are suggestive of a readiness field. The observed rate-dependent changes in this field may contribute to known transitions in sensorimotor coordination that emerge when the frequency of coordination is increased.