Tomoyoshi Komiyama

FUNCTION OF SURAL NERVE REFLEXES DURING HUMAN WALKING

1 The functions of ipsilateral cutaneous reflexes were studied with short trains of stimuli presented pseudorandomly to the sural nerve during human walking. Electromyograms (EMG) of lower (tibialis anterior (TA), soleus, lateral (LG) and medial (MG) gastrocnemius) and upper leg (vastus lateralis and biceps femoris) muscles were recorded, together with ankle, knee and hip joint angles. Net reflex EMG responses were quantified in each of the sixteen parts of the step cycle. The kinematic measurements included ankle eversion‐ inversion, and ankle, knee and hip flexion‐extension. 2 The function of the sural reflexes depended upon the part of the step cycle in which the nerve was stimulated and the intensity of stimulation. During stance, reflexes in MG and TA muscles in response to a medium intensity of stimulation (1.9 × radiating threshold, × RT) were closely associated with ankle eversion and dorsiflexion responses, respectively. These responses could assist in accommodation to uneven terrain that applies pressure to the lateral side of the foot (sural innervation area). Non‐noxious, high intensity (2.3 × RT) stimulation resulted in strong suppression of LG and MG during stance which was correlated to a small reduction in ankle plantarflexion. At this higher intensity the response would function to prevent the foot from moving more forcefully onto a potentially harmful obstacle. 3 During swing, ankle dorsiflexion increased and was significantly correlated to the net TA EMG response after both medium and high intensity stimulation. Knee flexion was increased throughout swing at both intensities of stimulation. These responses may serve in an avoidance response in which the swing limb is brought past an obstacle without destabilizing contact. 4 The net EMG and kinematic responses suggest that cutaneous reflexes stabilize human gait against external perturbations produced by an uneven surface in stance or obstacles encountered during swing.

Modulations of interlimb and intralimb cutaneous reflexes during simultaneous arm and leg cycling in humans

OBJECTIVE We investigated to what extent intralimb and interlimb cutaneous reflexes are altered while simultaneously performing arm and leg cycling (AL cycling) under different kinematic and postural conditions. METHODS Eleven subjects performed AL cycling under conditions in which the arm and leg crank ipsilateral to the stimulation side were moved synchronously (in-phase cycling) or asynchronously (anti-phase cycling) while sitting or standing. Cutaneous reflexes following superficial radial or superficial peroneal nerve stimulation (2.0-2.5 times radiating threshold, 5 pulses at 333 Hz) were recorded at 4 different pedal positions from 12 muscles in the upper and lower limbs. Cutaneous reflexes with a peak latency of 80-120 ms were then analyzed. RESULTS The magnitude of interlimb and intralimb cutaneous reflexes in the arm and leg muscles was significantly modulated depending on the crank position for the relevant limb (phase-dependent modulation). A significant correlation between the magnitude of the cutaneous reflex and background EMG was observed in the majority of muscles during static contraction, but not during AL cycling (task-dependent modulation). No significant difference was found in comparisons of the magnitude of intralimb and interlimb cutaneous reflexes obtained during in- and anti-phase AL cycling. Qualitatively, the same results were obtained during AL cycling while sitting or standing. In addition, the modulation of cutaneous reflexes in arm muscles was identical among in-phase, anti-phase and isolated arm cycling. Results were the same for leg muscles. CONCLUSIONS Cutaneous reflexes in arm muscles are little influenced by rhythmic movement of the legs and vice versa during AL cycling. It is likely that neural components that control interlimb reflexes are loosely coupled during AL cycling while sitting or standing. SIGNIFICANCE Our results provide a better understanding of the coordination between the upper and lower limbs during rhythmic movement.

Load‐related modulation of cutaneous reflexes in the tibialis anterior muscle during passive walking in humans

Although cutaneous reflexes are known to be strongly modulated in a phase‐dependent manner during walking in both human and cat, it is not clear whether the movement‐related or the load‐sensitive afferent feedback plays a more important role in regulating this modulation. To address this issue in humans, we investigated modulation of the cutaneous reflex in the tibialis anterior muscles (TA) of 17 subjects during passive walking with a load (0%, 33%, 66% unloading of body weight) and without a load (100% unloading). These walking tasks were performed passively with a robotic gait trainer system. Cutaneous reflexes in TA, elicited by electrical stimulation to the distal tibial (Tib) and superficial peroneal (SP) nerves, were recorded during 10 different phases of the walking cycle, and the middle latency responses (MLR, 70–120 ms) were analysed. During loaded walking, the magnitudes of the MLR induced by Tib nerve stimulation were strongly increased during the late stance‐to‐early swing phase irrespective of the amount of load (phase modulation), a phenomenon that also occurred without background electromyogram in the TA. Predominant suppression of the MLR following SP nerve stimulation at the early stance phase changed to facilitation at the late stance. By contrast, the MLR following either Tib or SP nerve stimulation was not at all modulated by the stepping phase during both unloaded walking (100% unloading) and standing. These results suggest that phasic changes in the load‐related afferent information in concert with rhythmic lower limb movement play a key role in modulating cutaneous reflexes during walking.

Disinhibition of upper limb motor area by voluntary contraction of the lower limb muscle

It is well known that monosynaptic spinal reflexes and motor evoked potentials following transcranial magnetic stimulation (TMS) are reinforced during phasic and intensive voluntary contraction in the remote segment (remote effect). However, the remote effect on the cortical silent period (CSP) is less known. The purpose of the present study is to determine to what extent the CSP in the intrinsic hand muscle following TMS is modified by voluntary ankle dorsiflexion and to elucidate the origin of the modulation of CSP by the remote effect. CSP was recorded in the right first dorsal interosseous while subjects performed phasic dorsiflexion in the ipsilateral side under self-paced and reaction-time conditions. Modulation of the peripherally-induced silent period (PSP) induced by electrical stimulation of the ulnar nerve was also investigated under the same conditions. In addition, modulation of the CSP was investigated during ischemic nerve block of the lower limb and during application of vibration to the tibialis anterior tendon. The duration of CSP was significantly shortened by phasic dorsiflexion, and the extent of shortening was proportional to dorsiflexion force. Shortening of the CSP duration was also observed during tonic dorsiflexion. In contrast, the PSP duration following ulnar nerve stimulation was not altered during phasic dorsiflexion. Furthermore, the remote effect on the CSP duration was seen during ischemic nerve block of the lower limb and the pre-movement period in the reaction-time paradigm, but shortening of the CSP was not observed during tendon vibration. These findings suggest that phasic muscle contraction in the remote segment results in a decrease in intracortical inhibitory pathways to the corticospinal tract innervating the muscle involved in reflex testing and that the remote effect on the CSP is predominantly cortical in origin.

Neural Mechanisms Influencing Interlimb Coordination during Locomotion in Humans: Presynaptic Modulation of Forearm H-Reflexes during Leg Cycling

Presynaptic inhibition of transmission between Ia afferent terminals and alpha motoneurons (Ia PSI) is a major control mechanism associated with soleus H-reflex modulation during human locomotion. Rhythmic arm cycling suppresses soleus H-reflex amplitude by increasing segmental Ia PSI. There is a reciprocal organization in the human nervous system such that arm cycling modulates H-reflexes in leg muscles and leg cycling modulates H-reflexes in forearm muscles. However, comparatively little is known about mechanisms subserving the effects from leg to arm. Using a conditioning-test (C-T) stimulation paradigm, the purpose of this study was to test the hypothesis that changes in Ia PSI underlie the modulation of H-reflexes in forearm flexor muscles during leg cycling. Subjects performed leg cycling and static activation while H-reflexes were evoked in forearm flexor muscles. H-reflexes were conditioned with either electrical stimuli to the radial nerve (to increase Ia PSI; C-T interval  = 20 ms) or to the superficial radial (SR) nerve (to reduce Ia PSI; C-T interval  = 37–47 ms). While stationary, H-reflex amplitudes were significantly suppressed by radial nerve conditioning and facilitated by SR nerve conditioning. Leg cycling suppressed H-reflex amplitudes and the amount of this suppression was increased with radial nerve conditioning. SR conditioning stimulation removed the suppression of H-reflex amplitude resulting from leg cycling. Interestingly, these effects and interactions on H-reflex amplitudes were observed with subthreshold conditioning stimulus intensities (radial n., ∼0.6×MT; SR n., ∼ perceptual threshold) that did not have clear post synaptic effects. That is, did not evoke reflexes in the surface EMG of forearm flexor muscles. We conclude that the interaction between leg cycling and somatosensory conditioning of forearm H-reflex amplitudes is mediated by modulation of Ia PSI pathways. Overall our results support a conservation of neural control mechanisms between the arms and legs during locomotor behaviors in humans.

Robotic-assisted stepping modulates monosynaptic reflexes in forearm muscles in the human

Although the amplitude of the Hoffmann (H)-reflex in the forelimb muscles is known to be suppressed during rhythmic leg movement, it is unknown which factor plays a more important role in generating this suppression-movement-related afferent feedback or feedback related to body loading. To specifically explore the movement- and load-related afferent feedback, we investigated the modulation of the H-reflex in the flexor carpi radialis (FCR) muscle during robotic-assisted passive leg stepping. Passive stepping and standing were performed using a robotic gait-trainer system (Lokomat). The H-reflex in the FCR, elicited by electrical stimulation to the median nerve, was recorded at 10 different phases of the stepping cycle, as well as during quiet standing. We confirmed that the magnitude of the FCR H-reflex was suppressed significantly during passive stepping compared with during standing. The suppressive effect on the FCR H-reflex amplitude was seen at all phases of stepping, irrespective of whether the stepping was conducted with body weight loaded or unloaded. These results suggest that movement-related afferent feedback, rather than load-related afferent feedback, plays an important role in suppressing the FCR H-reflex amplitude.

Facilitation of agonist motoneurons upon initiation of rapid and slow voluntary movements in man

The time course of facilitation of the agonist motoneurons upon initiation of voluntary ankle dorsiflexion was investigated in eight healthy subjects. The H-reflex and visually guided tracking methods were used for testing the excitability of the motoneuron pool and for controlling the initiation of movement as well as speed and force. Since the onset of voluntary EMG activity (EMG reaction time: EMGvRT) was delayed and/or obscured by test H-reflexes which were evoked very close to the behavioral responses, the subject was instructed to make response movements bilaterally, and EMGvRT was measured on the side without stimulation. In every subject, the EMGvRT was invariably longer in the ramp movement than in the step movement. The onset of H-reflex facilitation prior to EMG onset, which was regarded as indicating the arrival time of the descending motor command to the motoneuron pool, always started earlier in the ramp movement than in the step movement. The difference in facilitation onset between the two tasks was smaller than that in EMGvRT. Since the amplitude of the H-reflex at the onset of the voluntary EMG was equivalent in both movements, the development of H-reflex towards the behavioral EMG onset was more gradual in the ramp movement than in the step movement. The present results demonstrate that the longer reaction time in the slow ramp task depends on 2 factors: delay in the arrival of descending facilitatory impulses to the agonist motoneuron pool, and its slow recruitment thereafter.

Modulation of interhemispheric interactions across symmetric and asymmetric bimanual force regulations

The corpus callosum is essential for neural communication between the left and right hemispheres. Although spatiotemporal coordination of bimanual movements is mediated by the activity of the transcallosal circuit, it remains to be addressed how transcallosal neural activity is involved in the dynamic control of bimanual force execution in human. To address this issue, we investigated transcallosal inhibition (TCI) elicited by single‐pulse transcranial magnetic stimulation (TMS) in association with the coordination condition of bimanual force regulation. During a visually‐guided bimanual force tracking task, both thumbs were abducted either in‐phase (symmetric condition) or 180° out‐of‐phase (asymmetric condition). TMS was applied to the left primary motor cortex to elicit the disturbance of ipsilateral left force tracking due to TCI. The tracking accuracy was equivalent between the two conditions, but the synchrony of the left and right tracking trajectories was higher in the symmetric condition than in the asymmetric condition. The magnitude of force disturbance and TCI were larger during the symmetric condition than during the asymmetric condition. Right unimanual force tracking influenced neither the force disturbance nor TCI during tonic left thumb abduction. Additionally, these TMS‐induced ipsilateral motor disturbances only appeared when the TMS intensity was strong enough to excite the transcallosal circuit, irrespective of whether the crossed corticospinal tract was activated. These findings support the hypotheses that interhemispheric interactions between the motor cortices play an important role in modulating bimanual force coordination tasks, and that TCI is finely tuned depending on the coordination condition of bimanual force regulation.

Effects of Leg Pedaling on Early Latency Cutaneous Reflexes in Upper Limb Muscles

The functional coupling of neural circuits between the upper and lower limbs involving rhythmic movements is of interest to both motor control research and rehabilitation science. This coupling can be detected by examining the effect of remote rhythmic limb movement on the modulation of reflex amplitude in stationary limbs. The present study investigated the extent to which rhythmic leg pedaling modulates the amplitude of an early latency (peak 30-70 ms) cutaneous reflex (ELCR) in the upper limb muscles. Thirteen neurologically intact volunteers performed leg pedaling (60 or 90 rpm) while simultaneously contracting their arm muscles isometrically. Control experiments included isolated isometric contractions and discrete movements of the leg. ELCRs were evoked by stimulation of the superficial radial nerve with a train of rectangular pulses (three pulses at 333 Hz, intensity 2.0- to 2.5-fold perceptual threshold). Reflex amplitudes were significantly increased in the flexor carpi radialis and posterior deltoid and significantly decreased in the biceps brachii muscles during leg pedaling compared with that during stationary isometric contraction of the lower leg muscles. This effect was also sensitive to cadence. No significant modulation was seen during the isometric contractions or discrete movements of the leg. Additionally, there was no phase-dependent modulation of the ELCR. These findings suggest that activation of the rhythm generating system of the legs affects the excitability of the early latency cutaneous reflex pathways in the upper limbs.

Effects of remote muscle contraction on transcranial magnetic stimulation-induced motor evoked potentials and silent periods in humans

OBJECTIVE To determine to what extent tonic contraction of the testing muscle modulates the effect of remote muscle contraction on motor evoked potentials (MEPs) and cortical silent periods (CSPs) in resting and active proximal and distal muscles following transcranial magnetic stimulation (TMS). In addition, we tested whether the remote effect on MEP was observable when the test MEP was small. METHODS While performing tonic abductions of the first dorsal interosseous (FDI), flexor carpi radialis, or anterior deltoid muscles, subjects made phasic dorsiflexions of the right ankle at various forces. MEPs and CSPs were induced by separately optimized TMS intensities and locations in the left motor cortex and recorded electromyographically. RESULTS Phasic dorsiflexion increased MEP amplitude and shortened CSP duration in a dorsiflexion intensity-dependent manner in all muscles tested. At test MEPs <10% of Mmax, remote effects on MEP amplitude and CSP duration were significantly attenuated while the testing muscle was active. CONCLUSIONS Phasic contraction of remote muscles potentiates excitatory- and suppresses inhibitory intracortical neuronal pathways converging on corticospinal tract cells innervating the upper limb muscles even when they are active. However, the magnitude of the remote effect on MEP amplitude strongly depends on the test MEP amplitude. SIGNIFICANCE Although remote effects on MEP amplitude and CSP duration are observed even when the test muscle is active, the magnitude of the remote effect strongly depends on TMS intensity.