The investigation of control mechanisms of stepping rhythm in human in the air-stepping conditions during passive and voluntary leg movements

In unloading condition the degree of activation of the central stepping program was investigated during passive leg movements in healthy subjects, as well as the excitability of spinal motoneurons during passive and voluntary stepping movement. Passive stepping movements with characteristics maximally approximated to those during voluntary stepping were accomplished by experimenter. The comparison of the muscle activity bursts during voluntary and imposed movements was made. In addition to that the influence of artificially created loading onto the foot to the leg movement characteristics was analyzed. Spinal motoneuron excitability was estimated by means of evaluation of amplitude modulation of the soleus H-reflex. The changes of H-reflexes under the fixation of knee or hip joints were also studied. In majority of subjects the passive movements were accompanied by bursts of EMG activity of hip muscles (and sometimes of knee muscles), which timing during step cycle was coincided with burst timing of voluntary step cycle. In many cases the bursts of EMG activity during passive movements exceeded activity in homonymous muscles during voluntary stepping. The foot loading imitation exerted essential influence on distal parts of moving extremity during voluntary as well passive movements, that was expressed in the appearance of movements in the ankle joint and accompanied by emergence and increasing of phasic EMG activity of shank muscles. The excitability of motoneurons during passive movements was greater then during voluntary ones. The changes and modulation of H-reflex throughout the step cycle without restriction of joint mobility and during exclusion of hip joint mobility were similar. The knee joint fixation exerted the greater influence. It is supposed that imposed movements activate the same mechanisms of rhythm generation as a supraspinal commands during voluntary movements. In the conditions of passive movements the presynaptic inhibition depend on afferent influences from moving leg in the most degree then on central commands. It seems that afferent inputs from pressure receptors of foot in the condition of "air-stepping" actively interact with central program of stepping and, irrespective of type of the performing movements (voluntary or passive), form the final pattern activity.     

The influence of the afferent input from receptors of the foot on the excitability of spinal α-motoneurons during air-stepping

The excitability of α-motoneurons was studied in healthy subjects during voluntary and passive air-stepping with imitation of foot loading. The foot loading induced reduction of the H-reflex during both immobility and stepping. Thus, sensory inputs from load receptors play an important role in phase-dependent modulation of the H-reflex, and excitability of α-motoneurons is considerably dependent on the foot afferent input.     

The influence of vibration on spinal alpha-motoneurons excitability in static conditions and during evoked stepping in human

In healthy human the excitability of spinal alpha-motoneurons under application of vibrostimulation (20-60 Hz) to different leg muscles was investigated both in stationary condition and during stepping movements caused by vibration in the condition of suspended leg. In 15 subjects the amplitude of H-reflex were compared under vibration of rectus femoris (RF) and biceps femoris (BF) muscles of left leg as well during vibration of rectus femoris of contralateral, motionless leg in three spatial positions: upright, supine and on right side of body with suspended left leg. In dynamic conditions the amount of H-reflex was compared during evoked and voluntary stepping at 8 intervals of step cycle. In all body positions the vibration of each ipsilateral leg muscles caused significant suppression of H-reflex, this suppression was more prominent in the air-stepping conditions. The vibration of contralateral leg RF muscle had a weak influence on the amplitude of H-reflex. In 7 subjects the muscle vibration of ipsilateral and contralateral legs generated stepping movements. During evoked "air-stepping" H-reflex had different amplitudes in different phases of step cycle. At the same time the differences between responses under voluntary and non-voluntary stepping were revealed only in stance phase. Thus, different degree of H-reflex suppression by vibration under different body position in space depends on, it seems to be, from summary afferent inflows to spinal cord interneurons, which participate in regulation of posture and locomotion. Seemingly, the increasing of spinal cord neurons excitability occurs under involuntary air-stepping in swing phase, which is necessary for activation of locomotor automatism under unloading leg conditions.     

The investigation of locomotor activity control system in humans under the air-stepping conditions during passive and voluntary leg movements

The degree of activation of the central stepping program during passive leg movement was studied in healthy subjects under unloading conditions; the excitability of spinal motoneurons was studied during passive and voluntary stepping movements. Passive stepping movements with characteristics maximally close to those during voluntary stepping were accomplished by the experimenter. The bursts of muscular activity during voluntary and imposed stepping movements were compared. In addition, the influence on the leg movement of artificially created loading onto the foot was studied. The excitability of spinal motoneurons was estimated by the amplitude of modulation of the m. soleus H reflex. Changes in the H reflex (Hoffmann’s reflex) after fixation of the knee and hip joints were also studied. In most subjects, passive movements were accompanied by bursts of electromyographic (EMG) activity in the hip muscles (sometimes in shank muscles); the timing of the EMG burst during the step cycle coincided with the burst’s timing during voluntary stepping. In many cases, the bursts in EMG activity exceeded the activity of homonymous muscles during voluntary stepping. Simulation of foot loading influenced significantly the distal part of the moving extremity during both voluntary and passive movements, which was expressed in the appearance of movements in the ankle joint and an increase in the phasic EMG activity of the shank muscles. The excitability of motoneurons during passive movements was higher than during voluntary movements. Changes and modulation of the H reflex throughout the step cycle were similar without restriction of joint mobility and without hip joint mobility. Fixation of the knee joint was of great importance. It is supposed that imposed movements activate the same mechanisms of rhythm generation as supraspinal commands during voluntary movements. During passive movements, presynaptic inhibition depends mostly on the afferent influences from the moving leg rather than on the central commands. Under the conditions of “air-stepping,” the afferent influences from the foot pressure receptors are likely to interact actively with the central program of stepping and to determine the final activity pattern irrespective of the movement type (voluntary or passive).     

Neural adaptation to resistance training: changes in evoked V-wave and H-reflex responses.

Combined V-wave and Hoffmann (H) reflex measurements were performed during maximal muscle contraction to examine the neural adaptation mechanisms induced by resistance training. The H-reflex can be used to assess the excitability of spinal alpha-motoneurons, while also reflecting transmission efficiency (i.e., presynaptic inhibition) in Ia afferent synapses. Furthermore, the V-wave reflects the overall magnitude of efferent motor output from the alpha-motoneuron pool because of activation from descending central pathways. Fourteen male subjects participated in 14 wk of resistance training that involved heavy weight-lifting exercises for the muscles of the leg. Evoked V-wave, H-reflex, and maximal M-wave (M(max)) responses were recorded before and after training in the soleus muscle during maximal isometric ramp contractions. Maximal isometric, concentric, and eccentric muscle strength was measured by use of isokinetic dynamometry. V-wave amplitude increased approximately 50% with training (P < 0.01) from 3.19 +/- 0.43 to 4.86 +/- 0.43 mV, or from 0.308 +/- 0.048 to 0.478 +/- 0.034 when expressed relative to M(max) (+/- SE). H-reflex amplitude increased approximately 20% (P < 0.05) from 5.37 +/- 0.41 to 6.24 +/- 0.49 mV, or from 0.514 +/- 0.032 to 0.609 +/- 0.025 when normalized to M(max). In contrast, resting H-reflex amplitude remained unchanged with training (0.503 +/- 0.059 vs. 0.499 +/- 0.063). Likewise, no change occurred in M(max) (10.78 +/- 0.86 vs. 10.21 +/- 0.66 mV). Maximal muscle strength increased 23-30% (P < 0.05). In conclusion, increases in evoked V-wave and H-reflex responses were observed during maximal muscle contraction after resistance training. Collectively, the present data suggest that the increase in motoneuronal output induced by resistance training may comprise both supraspinal and spinal adaptation mechanisms (i.e., increased central motor drive, elevated motoneuron excitability, reduced presynaptic inhibition).     

Somatosensory graviception inhibits the soleus H-reflex in standing man - a parabolic flight experiment-

The purpose of this study was to investigate how gravity level affects the excitability of the soleus muscle (SOL) motoneuron pool to la afferent input while erect posture is maintained in humans. Three healthy male subjects participated in an experiment whereby three different gravity conditions (micro gravity (MG), normal gravity (NG), and hyper gravity) were imposed using a parabolic flight procedure. The SOL H-reflex was evoked every 2 seconds while the subjects kept an erect posture. The background electromyographic activity (BGA) of the SOL was almost absent during MG. The SOL H-reflex amplitude was significantly larger during MG than during NG. These results suggest that the somatosensory systems detecting a load at the lower limbs and/or vertebral column play a role in reducing the excitability of the SOL motoneuron pool to la afferent inputs by presynaptic inhibition.     

Modulation of soleus H-reflex during dorsal and plantar flexions in the human ankle joint

Recording of the H-reflex was used to study the changes in the reflex excitability of soleus motoneurons during dorsal and plantar flexions of the ipsilateral and contralateral feet performed with different strengths by 15 healthy subjects. The dorsiflexion of the ipsilateral foot was accompanied by the “classic” reciprocal inhibition of the soleus motoneurons, the degree of the inhibition being directly proportional to the strength of the contraction of pretibial muscles and depending on the presence of foot support. The plantar flexion of the ipsilateral foot was accompanied by changes in reflex excitability, which were inversely proportional to the strength of the flexion. This was apparently related to the activation of a mechanism protecting the muscle against excessive contraction. The dorsal and plantar flexions of the contralateral foot were accompanied by similar changes in the reflex excitability of soleus motoneurons, namely, an increase in the case of weak contraction and a decrease in the case of strong contraction. However, the increase in reflex excitability during contralateral dorsiflexion was smaller and its decrease began at a weaker contraction than in the case of contralateral plantar flexion. The changes in the reflex excitability of soleus motoneurons during movements of the contralateral foot, which were also strength-dependent, confirmed the presence of cross-projections that are likely to be part of the generator of the central pattern of lower limb movement coordination.     

Changes in the reflex excitability of spinal motor neurons in newborn infants during sleep and increases in environmental temperature

Reflex excitability of the spinal motor centres was studied in newborns by the monosynaptic testing (H-reflex) method during the rise of air temperature in the cunette up to 32 degrees and 34 degrees as compared to the control data obtained at 30 degrees C. It was shown that at temperatures of 32 degrees and 34 degrees C the reflex excitability of spinal motoneurones is lower than in the control. A narrowing of the range and a weakening of the stimuli were recorded at which the H-reflex could be elicited. The possible ways are discussed in which the surrounding temperature affects reflex excitability of the spinal motor centres.     

Enhanced stretch reflex excitability in the soleus muscle during passive standing posture in humans

The purpose of this study was to test whether the spinal reflex excitability of the soleus muscle is modulated as posture changes from a supine to a passive upright position. Eight healthy subjects (29.6 ± 5.4 yrs) participated in this study. Stretch and H-reflex responses were elicited while the subjects maintained passive standing (ST) and supine (SP) postures. The passive standing posture was accomplished by using a gait orthosis to which a custom-made device was mounted to elicit stretch reflex in the soleus muscle. This orthosis makes it possible to elicit stretch and H-reflexes without background muscle activity in the soleus muscle. The results revealed that the H-reflex amplitude in the ST was smaller than that in the SP condition, which is in good agreement with previous reports. On the other hand, the stretch reflex was significantly larger in the ST than in the SP condition. Since the experimental conditions of both the stretch and H-reflex measurements were exactly the same, the results were attributed to differences in the underlying neural mechanisms of the two reflex systems: different sensitivity of the presynaptic inhibition onto the spinal motoneuron pool and/or a change in the muscle spindle sensitivity.     

Relationship between the discharge rate of a firing motoneuron and the effectiveness of excitatory la afferent volleys in man

The H-reflex was evoked after producing regular unit firing in the flexor carpi ulnaris set up by moderate voluntary isometric muscular contraction. The firing index was used to quantify the effectiveness of the monosynaptic afferent signal traveling to the firing motoneuron. An analysis was made of the 3.3–16.0 spikes/sec firing range characteristic of naturally occurring muscular contraction. Effectiveness of afferent signals for motor units in the "fast" muscles under study were found to depend on motoneuronal background firing rate; the former declined as the latter rose, as previously discovered during research into "slow" soleus muscle units [2]. Afferent signals were most effective for motoneurons belonging to the "fast" muscles over the entire range of firing rates. It was found from analyzing afferent signal efficacy in relation to its point of occurrence within the interspike interval that variations in motoneuronal excitability within this interval are the reason for this relationship.Institute for Research into Information Transmission, Academy of Sciences of the USSR, Moscow. Translated from Neirofiziologiya, Vol. 19, No. 5, pp. 595–600, September–October, 1987.     

Mirror symmetric bimanual movement priming can increase corticomotor excitability and enhance motor learning

Repetitive mirror symmetric bilateral upper limb may be a suitable priming technique for upper limb rehabilitation after stroke. Here we demonstrate neurophysiological and behavioural after-effects in healthy participants after priming with 20 minutes of repetitive active-passive bimanual wrist flexion and extension in a mirror symmetric pattern with respect to the body midline (MIR) compared to an control priming condition with alternating flexion-extension (ALT). Transcranial magnetic stimulation (TMS) indicated that corticomotor excitability (CME) of the passive hemisphere remained elevated compared to baseline for at least 30 minutes after MIR but not ALT, evidenced by an increase in the size of motor evoked potentials in ECR and FCR. Short and long-latency intracortical inhibition (SICI, LICI), short afferent inhibition (SAI) and interhemispheric inhibition (IHI) were also examined using pairs of stimuli. LICI differed between patterns, with less LICI after MIR compared with ALT, and an effect of pattern on IHI, with reduced IHI in passive FCR 15 minutes after MIR compared with ALT and baseline. There was no effect of pattern on SAI or FCR H-reflex. Similarly, SICI remained unchanged after 20 minutes of MIR. We then had participants complete a timed manual dexterity motor learning task with the passive hand during, immediately after, and 24 hours after MIR or control priming. The rate of task completion was faster with MIR priming compared to control conditions. Finally, ECR and FCR MEPs were examined within a pre-movement facilitation paradigm of wrist extension before and after MIR. ECR, but not FCR, MEPs were consistently facilitated before and after MIR, demonstrating no degradation of selective muscle activation. In summary, mirror symmetric active-passive bimanual movement increases CME and can enhance motor learning without degradation of muscle selectivity. These findings rationalise the use of mirror symmetric bimanual movement as a priming modality in post-stroke upper limb rehabilitation.     

The relationship between the soleus H-reflex amplitude and vibratory inhibition in controls and spastic subjects. II. Computer model

A computer model is presented that describes soleus H-reflex recruitment as a function of electric stimulus intensity. The model consists of two coupled non-linear transfer functions. The first transfer function describes the activation of muscle spindle (Ia) afferent terminals as a function of the electric stimulus intensity; whereas the second describes the activation of a number of motoneurons as a function of the number of active Ia afferent terminals. The effect of change in these transfer functions on the H-reflex recruitment curve is simulated. In spastic patients, a higher average maximal H-response amplitude is observed in combination with a decreased H-reflex threshold. Vibration of the Achilles tendon reduces the H-reflex amplitude, presumably by reducing the excitatory afferent input. Vibratory inhibition is diminished in spasticity. In the model, the afferent-motoneuron transfer function was modified to represent the possible alterations occurring in spasticity. The simulations show that vibratory suppression of the H-reflex is determined only in part by the inhibition level of the afferent input. With a constant level of presynaptic inhibition, the suppression of reflexes of different sizes may vary. A lowering of the motoneuron activation thresholds in spastic patients will directly contribute to a decrease of vibratory inhibition in spasticity.     

Effect of angular velocity on soleus and medial gastrocnemius H-reflex during maximal concentric and eccentric muscle contraction

At rest, the H-reflex is lower during lengthening than shortening actions. During passive lengthening, both soleus (SOL) and medial gastrocnemius (MG) H-reflex amplitudes decrease with increasing angular velocity. This study was designed to investigate whether H-reflex amplitude is affected by angular velocity during concentric and eccentric maximal voluntary contraction (MVC). Experiments were performed on nine healthy men. At a constant angular velocity of 60°/s and 20°/s, maximal H-reflex and M-wave potentials were evoked at rest (i.e., H_max and M_max, respectively) and during concentric and eccentric MVC (i.e., H_sup and M_sup, respectively). Regardless of the muscle, H_max/M_max was lower during lengthening than shortening actions and the H_sup/M_sup ratio was higher than H_max/M_max during lengthening actions. Whereas no action type and angular velocity effects on the MG H_sup/M_sup were found, the SOL H_sup/M_sup was lower during eccentric than concentric MVC and this depression was increased with higher angular velocity. Our findings indicate that the depression of the H-reflex amplitude during eccentric compared to concentric MVC depends mainly on the amount of inhibition induced by lengthening action. In conclusion, H-reflex should be evoked during both passive and active dynamic trials to evaluate the plasticity of the spinal loop.     

Threshold of the soleus muscle H-reflex is less sensitive to the change in excitability of the motoneuron pool during plantarflexion or dorsiflexion in humans

In the present study, we investigated whether weak (10% of maximal voluntary contraction) tonic dorsiflexion (DF) and plantarflexion (PF) affects the two conventional parameters used for evaluating the excitability of the soleus motoneuron (MN) pool, i.e. the ratio of the threshold of H-reflex to that of M-response (H_th:M_th) and the ratio of the maximal amplitude of H-reflex to that of M-response (H_max:M_max) in human subjects. The results showed that the H_max:M_max decreased during DF and increased during PF compared with that during rest, whereas no clear alteration was observed in H_th:M_th. These results are consistent with the scheme proposed by earlier workers, who have argued that neither inhibitory nor facilitatory effects of the conditioning stimulus apply to specific spinal reflex circuits occurring around the threshold of the test H-reflex. It is suggested, therefore, that the conventional use of the H_th:M_th ratio as a parameter reflecting the excitability of the MN pool should be reconsidered.     

Central nervous adaptations following 1 wk of wrist and hand immobilization.

Plastic neural changes have been documented in relation to different types of physical activity, but little is known about central nervous system plasticity accompanying reduced physical activity and immobilization. In the present study we investigated whether plastic neural changes occur in relation to 1 wk of immobilization of the nondominant wrist and hand and a corresponding period of recovery in 10 able-bodied volunteers. After immobilization, maximal voluntary contraction torque decreased and the variability of submaximal static contractions increased significantly without evidence of changes in muscle contractile properties. Hoffmann (H)-reflex amplitudes and the ratios of H-slope to M-slope increased significantly in flexor carpi radialis and abductor pollicis brevis at rest and during contraction without changes in corticospinal excitability, estimated from motor-evoked potentials (MEPs) elicited by transcranial magnetic stimulation. Corticomuscular coherence measures were derived from EEG and EMG obtained during static contractions. After immobilization, corticomuscular coherence in the 15- to 35-Hz range associated with maximum negative cumulant values at lags corresponding to MEP latencies decreased. One week after cast removal, all measurements returned to preimmobilization levels. The increased H-reflex amplitudes without changes in MEPs may suggest that presynaptic inhibition or postactivation depression of Ia afferents is reduced following immobilization. Reduced corticomuscular coherence may be caused by changes in afferent input at spinal and cortical levels or by changes in the descending drive from motor cortex. Further studies are needed to elucidate the mechanisms underlying the observed increased spinal excitability and reduced coupling between motor cortex and spinal motoneuronal activity following immobilization.     

The response of alpha-motoneurons of different size to stretch and vibration of extensor muscles after injection of 5-hydroxytryptophan in spinal cats.

1. Vibration of the GS muscle at 100/sec, and the peak-to-peak amplitude of about 100 mu, produced slight reflex activity of homonymous and heteronymous alpha-motoneurons in the spinal, unanesthetized cat. 2. Intravenous injection of the 5-HT precursor 5-HTP (25 mg/kg, L-form) performed in the spinal preparation facilitated the responses of single extensor alpha-motoneurons to both vibration and stretch of the corresponding muscle. The 5-HT antagonist methysergide (0-5 mg/kg i. v.) blocked almost completely the facilitation of the vibration and stretch induced motoneuronal discharges produced by 5-HTP in the spinal cat, indicating that the facilitation was 5-HT specific. 4. A comparison of the types of alpha-motoneurons participating in the reflex responses elicited by the different stimuli in the spinal cat following injection of 5-HTP showed that both small-tonic and large-phasic alpha-motoneurons take part in both stretch and vibration reflexes. 5. It is concluded that the alpha-motoneuron pool of the GS muscle represents an homogenous population, no matter what kind of synaptic drive is used for its activation, and that the susceptibility of a motoneuron to discharge depends on the amount of the afferent excitatory input rather than on the modalities of sensory stimulation.     

Somatosensory graviception inhibits the soleus H-reflexin standing man - an underwater experiment-

H-reflexes were elicited in the soleus muscle in subjects standing on a force platform in a water tank, under different loading conditions at the ankle joint. The joint loading was altered by changing the combination of buoys and weights attached to lower limb segments, while the total body mass was kept the same. The results revealed that as the joint load was reduced the H-reflex was significantly enhanced as compared to that under the control condition, while it decreased as the joint load was increased, despite the same background EMG activity level. It was demonstrated that the augmented load information from the lower limb joints has an inhibitory effect on the soleus H-reflex, suggesting that this might be one of underlying neural mechanisms responsible for the suppression of H-reflex during human upright standing.     

The relationship between dynamic balancing ability and posture-related modulation of the soleus H-reflex

Soleus H-reflex reveals down modulation with increased postural difficulty. Role of this posture-related reflex modulation is thought to shift movement control toward higher motor centers in order to facilitate more precise postural control. Present study hypothesized that the ability to modulate H-reflex is related to one’s ability to dynamically balance while in an unstable posture. This study examined the relationship between dynamic balancing ability and soleus H-reflex posture-related modulation. Thirty healthy adults participated. The soleus maximal H-reflex (Hmax), motor response (Mmax), and background EMG activity (bEMG) were obtained during three postural conditions: prone, open-legged standing, and closed-legged standing. Hmax/Mmax ratios were normalized via the corresponding bEMG in order to remove the effects of background muscle activity from the obtained H-reflex. Reflex modulation was calculated as the ratio of the normalized Hmax/Mmax ratios in one postural condition to another posture in a more difficult condition. Dynamic balancing ability was assessed by testing stability while standing on a wobble board. A significant negative correlation was observed between balancing scores and reflex modulation from open-legged standing to closed-legged standing. This suggests that the ability to modulate monosynaptic stretch reflex excitability in response to a changing posture is a significant factor for dynamic balancing.     

Effects of exercise training on alpha-motoneurons.

Evidence is presented that one locus of adaptation in the "neural adaptations to training" is at the level of the alpha-motoneurons. With increased voluntary activity, these neurons show evidence of dendrite restructuring, increased protein synthesis, increased axon transport of proteins, enhanced neuromuscular transmission dynamics, and changes in electrophysiological properties. The latter include hyperpolarization of the resting membrane potential and voltage threshold, increased rate of action potential development, and increased amplitude of the afterhyperpolarization following the action potential. Many of these changes demonstrate intensity-related adaptations and are in the opposite direction under conditions in which chronic activity is reduced. A five-compartment model of rat motoneurons that innervate fast and slow muscle fibers (termed "fast" and "slow" motoneurons in this paper), including 10 active ion conductances, was used to attempt to reproduce exercise training-induced adaptations in electrophysiological properties. The results suggest that adaptations in alpha-motoneurons with exercise training may involve alterations in ion conductances, which may, in turn, include changes in the gene expression of the ion channel subunits, which underlie these conductances. Interestingly, the acute neuromodulatory effects of monoamines on motoneuron properties, which would be a factor during acute exercise as these monoaminergic systems are activated, appear to be in the opposite direction to changes measured in endurance-trained motoneurons that are at rest. It may be that regular increases in motoneuronal excitability during exercise via these monoaminergic systems in fact render the motoneurons less excitable when at rest. More research is required to establish the relationships between exercise training, resting and exercise motoneuron excitability, ion channel modulation, and the effects of neuromodulators.     

Discharge frequency and excitability of human firing motoneurone

The excitability of firing motoneurones activated by voluntary contraction of the flexor carpi ulnaris or tibialis anterior was tested by single excitatory Ia afferent volleys. In order to estimate the stimulation effects, the peri-stimulus time histograms of single motoneurones were plotted, and the firing indices were calculated. It was shown that the firing-frequency effect was absent within the range of 4-14 imp/s during testing by low-intensity excitatory volley. At higher intensity of afferent volley, the excitability increased at a low firing rate. It is suggested that the characteristics of the interspike-interval excitability trajectories underlie these relations. These findings made it possible to explicate some conflicting literature data which were usually reported without taking the afferent volley intensity effect into account. The mechanisms controlling the firing motoneurone excitability and possible trajectories of interspike-interval membrane potential in human motoneurones are discussed.