The relationship between the soleus H-reflex amplitude and vibratory inhibition in controls and spastic subjects. I. Experimental results

The effect of continuous Achilles tendon vibration on the soleus H-reflex amplitude was quantified over the entire H-reflex recruitment trajectory in 30 controls and 33 patients with spasticity in the lower limbs. The results show that with increasing stimulus intensities, vibratory inhibition of the Hreflex initially increases, then subsequently decreases. This is probably a direct consequence of how the activation thresholds of the motoneurons are distributed over the motoneuron pool. In patients, vibratory inhibition of the H-reflex was less over the entire recruitment trajectory than in controls. The decrease in vibratory inhibition in spasticity is commonly attributed to a decrease in presynaptic inhibition or post-activation depression. However, the average Hreflex threshold was lower in the patients, suggesting a decrease of the motoneuron activation thresholds. A lower reflex threshold in spasticity, therefore, may contribute to the observed reduction of vibratory inhibition.     

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.     

Modulation of spinal inhibitory reflexes depends on the frequency of transcutaneous electrical nerve stimulation in spastic stroke survivors

Neurophysiological studies in healthy subjects suggest that increased spinal inhibitory reflexes from the tibialis anterior (TA) muscle to the soleus (SOL) muscle might contribute to decreased spasticity. While 50?Hz is an effective frequency for transcutaneous electrical nerve stimulation (TENS) in healthy subjects, in stroke survivors, the effects of TENS on spinal reflex circuits and its appropriate frequency are not well known. We examined the effects of different frequencies of TENS on spinal inhibitory reflexes from the TA to SOL muscle in stroke survivors. Twenty chronic stroke survivors with ankle plantar flexor spasticity received 50-, 100-, or 200-Hz TENS over the deep peroneal nerve (DPN) of the affected lower limb for 30?min. Before and immediately after TENS, reciprocal Ia inhibition (RI) and presynaptic inhibition of the SOL alpha motor neuron (D1 inhibition) were assessed by adjusting the unconditioned H-reflex amplitude. Furthermore, during TENS, the time courses of spinal excitability and spinal inhibitory reflexes were assessed via the H-reflex, RI, and D1 inhibition. None of the TENS protocols affected mean RI, whereas D1 inhibition improved significantly following 200-Hz TENS. In a time-series comparison during TENS, repeated stimulation did not produce significant changes in the H-reflex, RI, or D1 inhibition regardless of frequency. These results suggest that the frequency-dependent effect of TENS on spinal reflexes only becomes apparent when RI and D1 inhibition are measured by adjusting the amplitude of the unconditioned H-reflex. However, 200-Hz TENS led to plasticity of synaptic transmission from the antagonist to spastic muscles in stroke survivors.     

Influence of stimulus intensity on the soleus H-reflex amplitude and modulation during locomotion

Diverging results have been reported regarding the modulation and amplitude of the soleus H-reflex measured during human walking and running. A possible explanation to this could be the use of too high stimulus strength in some studies while not in others. During activities like walking and running it is necessary to use a small M-wave to control the effective stimulus strength during all phases of the movement. This implies that the descending part of the H-reflex recruitment curve is being used, which may lead to an unwanted suppression of the H-reflex due to limitations imbedded within the H-reflex methodology itself.Accordingly, the purpose of the present study was to study the effect on the soleus H-reflex during walking and running using stimulus intensities normally considered too high (up to 45% Mmax).Using M-waves of 25–45% Mmax as opposed to 5–25% Mmax showed a significant suppression of the peak H-reflex during the stance phase of walking, while no changes were observed during running. No differences were observed regarding modulation pattern. So a possible use of too high stimulus intensity cannot explain the differences mentioned. The surprising result in running may be explained by the much higher voluntary muscle activity, which implies the existence of a V-wave influencing the H-reflex amplitude in positive direction.     

Time-dependent effects of neuromuscular electrical stimulation on changes in spinal excitability are dependent on stimulation frequency: A preliminary study in healthy adults

Neuromuscular electrical stimulation (NMES) can be used as treatment for spasticity. The present study examined differences in time-dependent effects of NMES depending on stimulation frequency. Forty healthy subjects were separated into four groups (no-stim, NMES of 50, 100, and 200?Hz). The un-conditioned H-reflex amplitude and the H-reflex conditioning-test paradigm were used to measure the effectiveness on monosynaptic Ia excitation of motoneurons in the soleus (SOL) muscle, disynaptic reciprocal Ia inhibition from tibialis anterior (TA) to SOL, and presynaptic inhibition of SOL Ia afferents. Each trial consisted of a 30-min period of NMES applied to the deep peroneal nerve followed by a 30-min period with no stimulation to measure prolonged effects. Measurements were performed periodically. Stimulation applied at all frequencies produced a significant reduction in monosynaptic Ia excitation of motoneurons in the SOL muscle, however, only stimulation with 50?Hz showed prolonged reduction after NMES. NMES frequency did not affect the amount of disynaptic reciprocal Ia inhibition and presynaptic inhibition of Ia afferents. The results show a frequency-dependent effect of NMES on the monosynaptic Ia excitation of motoneurons. This result has implications for selecting the optimal NMES frequency for treatment in patients with spasticity.     

Presynaptic inhibition in humans: a comparison between normal and spastic patients.

During the last 40 years, several studies in man have been devoted to the pathophysiological mechanisms underlying spasticity. Spasticity is characterised by a velocity dependent increase in muscle tone. Many spinal pathways control stretch reflex excitability and a malfunction in any one of them could theoretically produce the exaggeration of the stretch reflex. Delwaide showed that the vibration-induced inhibition of Ia fibres is reduced in spastic patients. However, the relation between a decrease in presynaptic Ia inhibition and the pathophysiology of spasticity has been recently questioned since it was argued that homosynaptic depression (or post-activation depression) also contributes to the vibratory-induced depression of monosynaptic reflexes. This paper is thus devoted to a review of the methods recently developed to study selectively presynaptic Ia inhibition in man and to a reevaluation of the relations between modifications in presynaptic Ia inhibition and spasticity in hemiplegic and spinal spastic patients.     

Inter-individual variation in reciprocal Ia inhibition is dependent on the descending volleys delivered from corticospinal neurons to Ia interneurons

IntroductionWe investigated the extent to which the corticospinal inputs delivered to Ia inhibitory interneurons influence the strength of disynaptic reciprocal Ia inhibition.MethodsSeventeen healthy subjects participated in this study. The degree of reciprocal Ia inhibition was determined via short-latency (condition-test interval: 1–3 ms) suppression of Sol H-reflex by conditioning stimulation of common peroneal nerve. The effect of corticospinal descending inputs on Ia inhibitory interneurons was assessed by evaluating the conditioning effect of transcranial magnetic stimulation (TMS) on the Sol H-reflex. Then, we determined the relationship between the degree of reciprocal Ia inhibition and the conditioning effect of TMS on the Sol H-reflex.ResultWe found that the degree of reciprocal Ia inhibition and the extent of change in the amplitude of the TMS-conditioned H-reflex, which was measured from short latency facilitation to inhibition, displayed a strong correlation (r = 0.76, p < 0.01) in the resting conditions.ConclusionThe extent of reciprocal Ia inhibition is affected by the corticospinal descending inputs delivered to Ia inhibitory interneurons, which might explain the inter-individual variations in reciprocal Ia inhibition.     

Primary afferent depolarization due to selective activation of propriospinal pathways

Depolarization of primary afferent terminals in the lumbosacral portion of the spinal cord evoked by selective activation of propriospinal pathways was investigated in anesthetized cats. The strongest depolarization developed as a result of activation of short (two to five segments) propriospinal pathways in the lateral funiculus; stimulation of the long propriospinal pathways of this funiculus also induced depolarization, but of lower amplitude. Stimulation of propriospinal pathways of the ventral funiculi was ineffective. Significant primary afferent depolarization developed only following the use of a series of stimuli and strong stimulation of the propriospinal pathways. Excitation of these pathways caused depolarization of afferent terminals of both cutaneous and muscular nerves, including muscular sensory fibers of group Ia, although in the latter case its intensity was low. Neuronal mechanisms involved in the generation of this depolarization and its possible functional role are dicussed.     

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).     

Sway-dependent modulation of the triceps surae H-reflex during standing.

Previous research has shown that changes in spinal excitability occur during the postural sway of quiet standing. In the present study, it was of interest to examine the independent effects of sway position and sway direction on the efficacy of the triceps surae Ia pathway, as reflected by the Hoffman (H)-reflex amplitude, during standing. Eighteen participants, tested under two different experimental protocols, stood quietly on a force platform. Percutaneous electrical stimulation was applied to the posterior tibial nerve when the position and direction of anteroposterior (A-P) center of pressure (COP) signal satisfied the criteria for the various experimental conditions. It was found that, regardless of sway position, a larger amplitude of the triceps surae H-reflex (difference of 9-14%; P = 0.005) occurred when subjects were swaying in the forward compared with the backward direction. The effects of sway position, independent of the sway direction, on spinal excitability exhibited a trend (P = 0.075), with an 8.9 +/- 3.7% increase in the H-reflex amplitude occurring when subjects were in a more forward position. The observed changes to the efficacy of the Ia pathway cannot be attributed to changes in stimulus intensity, as indicated by a constant M-wave amplitude, or to the small changes in the level of background electromyographic activity. One explanation for the changes in reflex excitability with respect to the postural sway of standing is that the neural modulation may be related to the small lengthening and shortening contractions occurring in the muscles of the triceps surae.     

Descending modulation of reflex reactions in spinal motoneurons produced by spinal cord injury in man

A study was made of changes in the amplitude of H-reflexes in m. gastrocnemius and the intensity of Ia inhibition in healthy subjects versus patients with midthoracic injury to the spinal cord before, during, and after voluntary tensing of the masticatory, cervical, and finger muscles. Tensing these muscles brought about facilitation of H-reflex and reduced intensity of Ia response in healthy subjects and patients with paraparesis but produced the opposite effect on paraplegics (or had no influence on reactions). This leads to a discussion of the relationship between the changes observed in reflex reactions and posttrauma damage to structure and function of the spinal cord.A. A. Bogomolets Institute, of Physiology, Academy of Sciences of the Ukrainian SSR. Kiev. Translated from Neirofiziologiya, Vol. 20, No. 1, pp. 105–113, January–February, 1988.     

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 acute effect of whole-body vibration on the hoffmann reflex

The extent to which motoneuron pool excitability, as measured by the Hoffmann reflex (H-reflex), is affected by an acute bout of whole-body vibration (WBV) was recorded in 19 college-aged subjects (8 male and 11 female; mean age 19 +/- 1 years) after tibial nerve stimulation. H/M recruitment curves were mapped for the soleus muscle by increasing stimulus intensity in 0.2- to 1.0-volt increments with 10-second rest intervals between stimuli, until the maximal M-wave and H-reflex were obtained. After determination of Hmax and Mmax, the intensity necessary to generate an H-reflex approximately 30% of Mmax (mean 31.5% +/- 4.1%) was determined and used for all subsequent measurements. Fatigue was then induced by 1 minute of WBV at 40 Hz and low amplitude (2-4 mm). Successive measurements of the H-reflex were recorded at the test intensity every 30 seconds for 30 minutes post fatigue. All subjects displayed a significant suppression of the H-reflex during the first minute post-WBV; however, four distinct recovery patterns were observed among the participants (alpha = 0.50). There were no significant differences between genders across time (P = 0.401). The differences observed in this study cannot be explained by level or type training. One plausible interpretation of these data is that the multiple patterns of recovery may display variation of muscle fiber content among subjects. Future investigation should consider factors such as training specificity and muscle fiber type that might contribute to the differing H-reflex response, and the effect of WBV on specific performance measures should be interpreted with the understanding that there may be considerable variability among individuals. Recovery times and sample size should be adjusted accordingly.     

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.     

Noradrenergic modulation of tactile responses in rat cortex. Current source-density and unit analyses

This study describes the noradrenergic modulation of tactile afferent information in the sensorimotor cortex of urethane-anesthetized rats. Synaptic and spike responses to a mechanical stimulation of the hand palm were evaluated by means of current source-density analysis and unit activity recording in all cortical layers. Results showed that activation of the locus coeruleus decreased and shortened afferent synaptic excitation in supragranular, but not in deep layers. On the average, unit responses exhibited facilitated latency, moderately increased amplitude, enhanced postexcitatory inhibition and synchronization of responses across layers. The apparent paradox of this global phasic facilitation correlated with a decrease in input synaptic currents was discussed according to hypotheses which might explain its functional significance.     

Changes in somatosensory evoked potentials in patients with vertebrogenic pain syndromes treated by electroacupuncture

Application of electroacupuncture (EAP) of the segmental points to patients with vertebrogenic algesic syndromes decreased amplitude of N150 and P240 waves recorded from vertex to painful electrocutaneous stimulation in the region innervated by an affected root. As distinct from EAP of segmental point auricular EAP not only decreased the amplitude of late components of evoked potentials (EP), but also increased it, direction of EP changes depending on the character of sensitivity disorders. It is suggested that effect of EAP-evoked EP changes in patients with hypalgesia is determined by two oppositively acting factors: by a decrease of nociceptive afferent impulsation intensity as a result of the antinociceptive system activation and by an increase of the afferent impulsation intensity due to recovery of function of central terminals in primary sensory neurons.     

Presynaptic selection of afferent inflow in the spinal cord.

The synaptic effectiveness of sensory fibers ending in the spinal cord of vertebrates can be centrally controlled by means of specific sets of GABAergic interneurons that make axo-axonic synapses with the terminal arborizations of the afferent fibers. In the steady state, the intracellular concentration of chloride ions in these terminals is higher than that predicted from a passive distribution, because of an active transport mechanism. Following the release of GABA by spinal interneurons and activation of GABA(A) receptors in the afferent terminals, there is an outwardly directed efflux of chloride ions that produces primary afferent depolarization (PAD) and reduces transmitter release (presynaptic inhibition). Studies made by intrafiber recording of PAD, or by measuring changes in the intraspinal threshold of single afferent terminals (which is reduced during PAD), have further indicated that muscle and cutaneous afferents have distinctive, but modifiable PAD patterns in response to segmental and descending stimuli. This has suggested that PAD and presynaptic inhibition in the various types of afferents is mediated by separate sets of last-order GABAergic interneurons. Direct activation, by means of intraspinal microstimulation, of single or small groups of last-order PAD-mediating interneurons shows that the monosynaptic PAD elicited in Ia and Ib afferents can remain confined to some sets of the intraspinal collaterals and not spread to nearby collaterals. The local character of PAD allows cutaneous and descending inputs to selectively inhibit the PAD of segmental and ascending intraspinal collaterals of individual muscle spindle afferents. It thus seems that the intraspinal branches of the sensory fibers are not hard wired routes that diverge excitation to spinal neurons, but are instead dynamic pathways that can be centrally controlled to address information to selected neuronal targets. This feature appears to play an important role in the selection of information flow in muscle spindles that occurs at the onset of voluntary contractions in humans.     

Study of the audiospinal effect on the H-reflex

Studies of the audiospinal effect on the H-reflex demonstrated that in normal test subjects and in patients with injuries to the spinal cord coupled with parapareses and in part of patients with paraplegia of the lower limbs, there was a sound-induced 30-70% increase in the amplitude of the H-reflex. As the interval between the conditioning sound and testing electric stimulations was raised, two maxima of the increment of the H-reflex amplitude within 30-40 ms and 80-100 ms were revealed. The increased H-response within these intervals seems likely to be connected with the conduction of excitation from the brain cortex via the pyramidal tract and the reticulospinal tract. Part of the patients with spinal cord injuries and paraplegia of the lower limbs did not manifest any sound-induced increase in the H-reflex. Apparently, such lack of increase is either a consequence of the functional blockade of the afferent conduction tract or that of their anatomical disturbance. The method of the audiospinal effect on the H-reflexes may be used for diagnostic purposes, namely for the determination of the conduction via the afferent cerebrospinal tract.     

The influence of increased muscle spindle sensitivity on Achilles tendon jerk and H-reflex in relaxed human subjects

Whether the fusimotor system contributes to reflex gain changes during reinforcement maneuvers is re-examined in the light of new data. Recently, from direct recordings of spindle afferent activity originating from ankle flexor muscles, we showed that mental computation increased the muscle spindle mechanical sensitivity in completely relaxed human subjects without concomitant alpha-motoneuron activation, providing evidence for selective fusimotor drive activation. In the present study, the effects of mental computation were investigated on monosynaptic reflexes elicited in non-contracting soleus muscle either by direct nerve stimulation (Hoffmann reflex, H) or by tendon tap (Tendinous reflex, T). The aim was to relate the time course of the changes in reflex size to the increase in spindle sensitivity during mental task in order to explore whether fusimotor activation can influence the size of the monosynaptic reflex. The results show changes in reflex amplitude that parallel the increase in muscle spindle sensitivity. When T-reflex is consistently facilitated during mental effort, the H-reflex is either depressed or facilitated, depending on the subjects. These findings suggest that the increased activity in muscle spindle primary endings may account for mental computation-induced changes in both tendon jerk and H-reflex. The facilitation of T-reflex is attributed to the enhanced spindle mechanical sensitivity and the inhibition of H-reflex is attributed to post-activation depression following the increased Ia ongoing discharge. This study supports the view that the fusimotor sensitization of muscle spindles is responsible for changes in both the mechanically and electrically elicited reflexes. It is concluded that the fusimotor drive contributed to adjustment of the size of tendon jerk and H-reflex during mental effort. The possibility that a mental computation task may also operate by reducing the level of presynaptic inhibition is discussed on the basis of H-reflex facilitation.