Excitability cycle of the Hoffmann reflex of the soleus in a constant pool of motoneurons. Changes in man as a function of age

The study of the recovery cycle of the H reflex of the soleus, in constant pool, was made on 88 normal men of different ages. The recurrent inhibition has been demonstrated in most of the adults and elderly subjects. In young children, there were powerful inhibitory mechanisms, among which the Renshaw inhibition can be isolated.     

Proprioceptive proximo-distal relationships between the quadriceps and soleus muscles in man

Electrical stimulation of femoral nerve modulates voluntary tonic activity o of ipsilateral soleus muscle. Stimulus time-locked inhibitory and facilitatory phases can be distinguished. EMG temporal analysis suggests that early perturbations are correlated with spinal effects of centripetal electrical activity. The inhibitory effects which momentarily abolish voluntary soleus activity are thought to result from quadriceps Ib fibres recruitment. While no heteronymous activity is induced at rest, femoral nerve Ia fibres activation can produce soleus muscle reflex when soleus motor nucleus excitability is increased by voluntary command. Recurrent discharge resulting from soleus reflex response enhances inhibition initially due to quadriceps Ib volley. Secondary effects of isometric quadriceps contraction (and soleus contraction when the femoral stimulus elicits a reflex in this muscle) have their own effects later. These findings suggest that proprioceptive relationships of the two muscular groups are efficient during tonic isometric voluntary command.     

On the methods employed to record and measure the human soleus H-reflex

The aim of this study was to investigate if the magnitude of the soleus H-reflex is different depending on the method employed to measure its size (peak-to-peak amplitude vs. area). In this study, 13 healthy human subjects participated, while the soleus H-reflex was induced via conventional methods. In the first experiment, the soleus H-reflex was recorded via two monopolar electrodes and was evoked at least at eight different stimulation intensities in respect to the recovery curve of the H-reflex and at three different inter-stimulus intervals (ISIs) (8, 5, and 2 s). The ISI refers to the time delay between the single pulses delivered to the posterior tibial nerve within a single trial. In the second experiment, the effects of common peroneal nerve (CPN) stimulation at short (2-4 ms) and at long (60-120 ms) conditioning test (C-T) intervals on the soleus H-reflex elicited every 5 s were established. Control and conditioned reflexes were recorded via a single differential bipolar electrode. In both experiments, H-reflexes were quantified by measuring their size as peak-to-peak amplitude and as area under the full-wave rectified waveform. The reflex responses recorded through two monopolar electrodes across stimulation intensities and ISIs measured as peak-to-peak amplitude had larger values than measured as area. In contrast, the magnitude of the reflexes, conditioned by CPN stimulation at either short or long C-T intervals and recorded via a single differential electrode, were not significantly different when measured as peak-to-peak amplitude or as area. Our findings indicate that monopolar recordings yield different reflex sizes depending on the method employed to measure the reflex size, and that the H-reflex measured as area might detect better the homosynaptic reflex depression. The lack of observing such differences with bipolar recordings might be related to changes of the reflex shape at a given stimulus intensity due to inhibitory inputs. The implications of our findings are discussed in respect to human reflex studies.     

On the methods employed to record and measure the human soleus H-reflex

The aim of this study was to investigate if the magnitude of the soleus H-reflex is different depending on the method employed to measure its size (peak-to-peak amplitude vs. area). In this study, 13 healthy human subjects participated, while the soleus H-reflex was induced via conventional methods. In the first experiment, the soleus H-reflex was recorded via two monopolar electrodes and was evoked at least at eight different stimulation intensities in respect to the recovery curve of the H-reflex and at three different inter-stimulus intervals (ISIs) (8, 5, and 2?s). The ISI refers to the time delay between the single pulses delivered to the posterior tibial nerve within a single trial. In the second experiment, the effects of common peroneal nerve (CPN) stimulation at short (2–4?ms) and at long (60–120?ms) conditioning test (C-T) intervals on the soleus H-reflex elicited every 5?s were established. Control and conditioned reflexes were recorded via a single differential bipolar electrode. In both experiments, H-reflexes were quantified by measuring their size as peak-to-peak amplitude and as area under the full-wave rectified waveform. The reflex responses recorded through two monopolar electrodes across stimulation intensities and ISIs measured as peak-to-peak amplitude had larger values than measured as area. In contrast, the magnitude of the reflexes, conditioned by CPN stimulation at either short or long C-T intervals and recorded via a single differential electrode, were not significantly different when measured as peak-to-peak amplitude or as area. Our findings indicate that monopolar recordings yield different reflex sizes depending on the method employed to measure the reflex size, and that the H-reflex measured as area might detect better the homosynaptic reflex depression. The lack of observing such differences with bipolar recordings might be related to changes of the reflex shape at a given stimulus intensity due to inhibitory inputs. The implications of our findings are discussed in respect to human reflex studies.     

The effects of recurrent inhibition on the cross-correlated firing patterns of motoneurones (and their relation to signal transmission in the spinal cord-muscle channel)

Cross-correlation histograms (CCH) were computed for discharge sequences of pairs of motoneurones which were excited by sinusoidal muscle stretches. These CCH's were compared before and after opening of the recurrent inhibitory loop by Renshaw cell blocking agents. Periodic patterns in the CCH's indicative of specifically timed phase relations between discharges of different motoneurones were enhanced after Renshaw cell blockage. This was confirmed by power spectra computed for the CCH's. They contained power peaks about 50Hz which tended to increase after depression of recurrent inhibition. The correlation was thus due predominantly to line current interference which seemed to act as a common entrainment input at the spinal level. It is concluded that Renshaw cells de-correlate discharge patterns of different motoneurones of the same pool by injecting uncorrelated signals into them. This de-correlation is an important prerequisite for distortion suppression of signal transmission in a multi-channel system, like that of stretch reflex, and for its linearization.     

Modulation of the soleus muscle H reflex caused by ballistic voluntary arm movements in humans

In healthy humans, we studied the influence of conditioning voluntary arm movements on the H reflex induced by transcutaneous stimulation of the tibial nerve and recorded from the soleus muscle. We examined the effects of flexion and extension of the forearm, as well as of finger clenching performed with the maximum rate. Conditioning arm movements were self-induced or realized upon presentation of a visual signal (light flash). We found that the pattern of changes in the H reflex is determined by the position of the subject’s body in the course of tests. The ipsilateral arm flexion in the elbow joint in the standing position resulted in depression of the H reflex lasting about 100 msec from the beginning of the movement, while the effect observed in the lying position (on the couch with the feet hanging free in the air) looked like a facilitation of the reflex lasting about 100 to 200 msec. The direction and dynamics of modifications of the H reflex under conditions of the use of different conditioning movements (forearm flexions/extensions and finger clenching of the ipsilateral arm, as well as contralateral forearm flexions in the elbow joint) were rather similar. We also showed that the observed facilitation of the H reflex began earlier than the voluntary arm movement (40 to 50 msec prior to the beginning). We hypothesize that these conditioning influences result from the action of central motor commands and represent the factor related to anticipatory postural rearrangements. Such rearrangements are directed toward the maintenance of equilibrium of the body in the course of a future movement. These commands depend significantly on the spatial position of the subject’s body. Neirofiziologiya/Neurophysiology, Vol. 40, No. 2, pp. 147–154, March–April, 2008.     

Neurophysiological characteristics of human leg muscle action potentials evoked by transcutaneous magnetic stimulation of the spine

The objectives of this study were to establish the neurophysiological properties of the compound muscle action potentials (CMAPs) evoked by transcutaneous magnetic stimulation of the spine (tsMSS) and the effects of tsMSS on the soleus H‐reflex. In semi‐prone seated subjects with trunk semi‐flexed, the epicenter of a figure‐of‐eight magnetic coil was placed at Thoracic 10 with the handle on the midline of the vertebral column. The magnetic stimulator was triggered by monophasic single pulses of 1 ms, and the intensity ranged from 90% to 100% of the stimulator output across subjects. CMAPs were recorded bilaterally from ankle and knee muscles at the interstimulus intervals of 1, 3, 5, 8, and 10 s. The CMAPs evoked were also conditioned by posterior tibial and common peroneal nerve stimulation at a conditioning‐test (C‐T) interval of 50 ms. The soleus H‐reflex was conditioned by tsMSS at the C‐T intervals of 50, 20, ?20, and ?50 ms. The amplitude of the CMAPs was not decreased when evoked at low stimulation frequencies, excitation of group I afferents from mixed peripheral nerves in the leg affected the CMAPs in a non‐somatotopical neural organization pattern, and tsMSS depressed soleus H‐reflex excitability. These CMAPs are likely due to orthodromic excitation of nerve motor fibers and antidromic depolarization of different types of afferents. The latency of these CMAPs may be utilized to establish the spine‐to‐muscle conduction time in central and peripheral nervous system disorders in humans. tsMSS may constitute a non‐invasive modality to decrease spinal reflex hyperexcitability and treat hypertonia in neurological disorders. Bioelectromagnetics 34:200–210, 2013. © 2012 Wiley Periodicals, Inc.     

Conditioned reflex dopamine release in the nucleus accumbens in rats with disrupted hippocampal formation

Lesion of the hippocampal formation affects in different ways the dopamine release in response to the two phases of emotional conditioning: increases the acquisition and exerts no effect on the expression of the reflex in rats.     

Detection and analysis of recurrent inhibition of firing motoneurons in man

During regular firing of "small" motor units, activated during weak voluntary contraction of the human soleus muscle, thick efferent fibers of n. tibialis were stimulated (a small M response was evoked, in which the small units did not participate). Peristimulus histograms of potentials of single motor units were constructed and the effect of stimulation on interspike interval duration was analyzed. The firing rate of the motor units was 4.5–7.6 spikes/sec. Stimulation of the nerve led to a sharp decrease in probability of their discharge or even complete temporary cessation of firing, i.e., it had a well marked inhibitory effect (lasting 10–20 msec). The latent period of inhibition (35–40 msec) was only a little longer than the latent period of the monosynaptic reflex of the soleus muscle. The effect of an inhibitory volley on duration of the interspike interval of the motor units depended on the time when the volley arrived during the interval. Lengthening of the interval was observed only if the inhibitory volley arrived in the second half or at the end of the interval. It is concluded that inhibition of firing of small motor units is due to Renshaw cells, activated on stimulation of axons of large motoneurons. The efficiency of a short (compared with the duration of the interspike interval) inhibitory volley reaching a motoneuron firing at low frequency characteristic of its adequate activation, is discussed.Institute for Problems of Information Transmission, Academy of Sciences of the USSR, Moscow. Translated from Neirofiziologiya, Vol. 16, No. 1, pp. 88–96, January–February, 1984.     

Changes in the reflex excitability of the soleus spinal center in humans performing various motor tasks

The reflex excitability of the soleus spinal motoneurons was assessed in healthy subjects performing different types of motor tasks: voluntary contraction of the flexor (dorsal flexion) and extensor (plantar flexion) muscles of the foot. The effect of the contraction strength of these muscles was also evaluated. During dorsal flexion of the ipsi-and contralateral feet, changes in the reflex ecitability of the soleus motoneurons were unidirectional: the excitability decreased. The decrease in the reflex excitability was more profound during dorsal flexion with the maximum strength than with the half-maximum strength. During the plantar flexion of the ipsi-and contralateral feet, the excitability of the soleus motoneurons changed in opposite directions: in some subjects it increased, while in the others it decreased. The reflex excitability of the soleus motoneurons changed to a greater extent during dorsal or plantar flexion of the ipsilateral foot. In the case of plantar flexion, the soleus motor center is possibly affected by a broader spectrum of influences than in the case of dorsal flexion, which can explain the variations in the reflex excitability changes during plantar flexion.     

Stretch reflex inhibition using electrical stimulation in normal subjects and subjects with spasticity

The effect of electricallys timulating the tibialis anterior muscle on the stretch reflex of the soleus muscle in normal subjects and subjects with spasticity is investigated. Stimulation of the tibialis anterior just prior to the onset of a mechanical disturbance, which causes a stretch in the soleus, inhibits the stretch reflex of the soleus in normal subjects and may inhibit clonus in subjects with spasticity.     

Down training of the elderly soleus H reflex with the use of a spinally induced balance perturbation.

The purpose of this study was to determine the ability of the elderly central nervous system to modulate spinal reflex output to functionally decrease a spinally induced balance perturbation. In this case, the soleus H reflex was used as the source of perturbation. Therefore, decreasing (down training) of the soleus H reflex was necessary to counteract this perturbation and to better maintain postural control. In addition to assessing the effect of this perturbation on the H reflex, static postural stability was measured to evaluate possible functional effects. Ten healthy young subjects (age: 27.0 +/- 4.6 yr) and 10 healthy elderly subjects (age: 71.4 +/- 5.1 yr) participated in this study. Subjects underwent balance perturbation on 2 consecutive days. On day 1 of perturbation, significant down training of the soleus H reflex was demonstrated in both young (-20.4%) and elderly (-18.7%) subjects. On day 2 of perturbation, significant down training of the soleus H reflex was again demonstrated in both young (-24.6%) and elderly (-21.0%) subjects. Analysis of static stability after the 2 days of balance perturbation revealed a significant 10.1% decrease in the area of sway in elderly subjects. In conclusion, this study demonstrated that healthy, elderly subjects compared with young subjects were equally capable of down training the soleus H reflex in response to a balance perturbation. Furthermore, the improvement in static stability through balance training may provide further evidence that balance can be retrained and rehabilitated in subjects with decreased reflex function.     

Response of Renshaw cells to sinusoidal stretch of hindlimb extensor muscles.

1. Renshaw cells responding disynaptically to electrically induced group I volleys in the intact gastrocnemius-soleus (GS) nerve, were submitted to small-amplitude, high-frequency vibration applied longitudinally to the deefferented GS muscle in precollicular decerebrate cats. 2. Vibration of the GS muscle at 200/sec, 180 mu peak-to-peak amplitude for 80-100 msec produced a sudden increase in the discharge rate of Renshaw cells, which gradually decreased within 25-50 msec to reach a steady level higher than that recorded in the absence of vibration. 3. Excitation of Renshaw cells appeared at a threshold amplitude of vibration (at 200-250/sec) of 5-20 mu and increased to a maximum value for amplitudes of about 70-80 mu, i.e., when all the primary endings of the spindles from the GS muscle had been driven by the stimulus. Recruitment of the secondary endings of the muscle spindles, due to large amplitude muscle vibration, did not modify the response of the Renshaw cells to the mechanically induced group Ia volleys. 4. These findings were obtained with the GS muscle pulled at 8 mm of initial extension. A threshold response of Renshaw cells to vibration appeared at 4 mm of static stretch, while maximal responses occurred at 8 mm. No further increase and actually a slight decrease in the response appeared for initial extensions of the muscle of 10-12 mm. 5. For a given vibration amplitude, the response of the Renshaw cells increased with increasing frequencies of vibration to reach the maximum at frequencies of 150-250/sec. Bursts of Renshaw cell discharges synchronous to each stroke of vibrator occurred only for low frequencies of stimulation (less than 25/sec). 6. It is concluded that vibration of the GS muscle represents a very effective method in exciting the Renshaw cells and that this response depends upon selective stimulation of homonymous motoneurons monosynaptically excited by the orthodromic volleys originating from the primary endings of the corresponding muscle spindles.     

The sensitivity of Renshaw cells to velocity of sinusoidal stretches of the triceps surae muscle.

1. The electrical activity of Renshaw cells monosynaptically excited by ventral root stimulation and disynaptically excited by electric stimulation of the group I afferents in the GS nerve has been recorded and their response to individual sinusoidal stretches of the deefferented GS muscle tested for different amplitudes and durations of the stimulus. 2. The experimental data indicate that the Rensahw cell responses are not only length dependent but also rate dependent. This finding indicates that the same Renshaw cells receive recurrent collaterals of both tonic and phasic motoneurons. 3. The observation that the discharge of Renshaw cells is particularly sensitive to the velocity of stretch suggests that the recurrent collaterals of large phasic motoneurons, which are recruited during high velocity stretches, exert a stronger excitatory action on Renshaw cells than do axon collaterals of the smaller tonic motoneurons, which are selectively stimulated during low velocity stretches.     

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.     

The relative sensitivity of Renshaw cells to orthodromic group Ia volleys caused by static stretch and vibrations of extensor muscles.

1. Activity of Renshaw cells monosynaptically excited by ventral root stimulation and disynaptically excited by electric stimulation of the group Ia afferents in the gastrocnemius-soleus (GS) nerve, was recorded in precollicular decerebrate cats. The response of these units to prolonged vibration applied longitudinally to the deefferented GS muscle was then compared with that elicited by static stretch of the homonymous muscle, for comparable frequencies of discharge of the group Ia afferents. 2. Small-amplitude vibration of the GS muscle at 200/sec for one second produced a sudden increase in the discharge rate of Renshaw cells, which gradually decreased within the first 100 msec of vibration to reach steady albeit lower level than that obtained during the first part of vibration. The response of the Renshaw cells during the first 100 msec of vibration (phasic response) and that elicited during the last 500 msec of vibration (tonic response) were evaluated for different frequencies of sinusoidal stretch. The mean increase in the firing frequency per imp./sec in the Ia afferents was also calculated using the total one-second period. 3. The response of Renshaw cells to muscle vibration increased with the frequency of vibration and, over the value of 10/sec, appeared to be linearly related to the frequency of the input, at least up to the frequency of 150/sec. Since vibration was of sufficient amplitude to produce driving of all the primary endings of muscle spindles, the responses were expressed as mean increases in the discharge rate of Renshaw cells per average impulse/sec in the Ia afferents. The discharge of the Renshaw cell increased on the average by 2.90 and 1.08 imp./sec per each imp./sec in the Ia afferents during the phasic and the tonic component of the response respectively, while the response calculated during the whole period of vibration corresponded on the average to 1.45 imp./sec per each imp./sec in the Ia afferents. 4. The Renshaw cells tested above responded also with increasing frequencies of discharge to increasing levels of static extension of the GS muscle. In particular the discharge frequency of Renshaw cells was on the average linearly related to muscle extension, at least for values ranging from 0 to 8 mm. The mean increase in discharge rate as a function of the static extension corresponded on the average to 0.89 imp./sec/mm. Since the discharge rate of the primary endings of muscle spindles recorded from the deefferented GS muscle increased by 2.62 imp./sec/mm, it appears that the mean increase in the discharge rate of Renshaw cells as a function of static extension corresponded to 0.34 imp./sec per each imp./sec in the Ia afferents.     

Assessment of soleus motoneuronal excitability using the joint angle dependent H reflex in humans.

As variations in the amplitude of H reflex potentials can be influenced by changes in muscle length, motoneuronal excitability in terms of H reflex during free movement has long been argued. With the maximal M response controlled, the present study compared several H reflex parameters in order to assess motoneuronal excitability of the resting soleus for different ankle angles (plantarflexion 20 degrees, neutral, and dorsiflexion 20 degrees ). All H-related parameters were dependent on joint angle, suggesting that soleus motoneuronal excitability in the dorsiflexed position was significantly suppressed. By contrast, soleus motoneuronal excitability in the plantarflexed position was not effectively modulated since H-related parameters did not differ from their neutral-position analogs. Methodologically, assessment of joint angle-dependent modulation of motoneuronal excitability requires meticulous control of M responses and selection of appropriate parameters that are insensitive to possible physical modulation and spatial shift of the M recruitment curve confounded by geometrical factors.     

Long-lasting inhibition of the soleus muscle H reflex related to realization of voluntary arm movements in humans

In healthy humans, we recorded the H reflex induced by transcutaneous stimulation of the tibial nerve (recording from the soleus muscle). In subjects in the lying position, we studied changes in the H reflex values after preceding voluntary arm movements realized with a maximum velocity after presentation of an acoustic signal. On the 200th to 300th msec after forearm flexion, long-lasting inhibition of the H reflex developed following a period of initial facilitation and reached the maximum, on average, 700 msec from the moment of the movement. Flexion of the contralateral upper limb in the elbow joint induced deeper inhibition than analogous movement of the ipsilateral arm. Long-lasting clear inhibition of the H reflex developed after arm flexion in the elbow joint but was slightly expressed after finger clenching. After inhibition reached the maximum, its time course was satisfactorily approximated by a logarithmic function of the time interval between the beginning of the conditioning voluntary movement and presentation of the test stimulus. Durations of inhibition calculated using a regression equation were equal to 6.6 sec and 8.5 sec after ipsilateral and contralateral elbow-joint flexions, respectively. Inhibition was not eliminated under conditions of tonic excitation of motoneurons of the tested muscle upon voluntary foot flexion. Long-lasting inhibition of the H reflex was also observed after electrical stimulation-induced flexions of the upper limb. The obtained data indicate that movements of the upper limb cause reflex long-lasting presynaptic inhibition of the soleus-muscle H reflex that can play a noticeable role in redistribution of the muscle tone during motor activity. Neirofiziologiya/Neurophysiology, Vol. 40, No. 3, pp. 221–227, May–June, 2008.     

Effects of membrane potential on just detectable movement in rat skeletal muscle: Effects of denervation

The potential, Vt, at which a brief test depolarization first elicited movement was determined using two-microelectrode point voltage clamp. We expected that inactivation of excitation-contraction coupling at conditioning potentials between ?60 and 0 mV would shift Vt to more positive potentials, and that fibers would become inactivatable with less conditioning depolarization in EDL than soleus. The curve relating Vt to conditioning potential had a negative slope (which was insensitive to addition of 1 mm cobalt or replacement of calcium with 20 mm CaEGTA) between ?60 and ?35 mV and a steep positive slope with further depolarization. Unexpectedly, fibers became inactivatable with less conditioning depolarization in soleus than in EDL when Vt was measured with 50 msec test pulses. However, the positive shift in Vt became less steep as test pulse duration lengthened in soleus fibers. When Vt obtained with test pulses approaching rheobase (10 msec in EDL and 500 msec in soleus) was compared, EDL fibers became inactive with less conditioning depolarization than soleus fibers. The increase in Vt became steeper with 1 mm cobalt or 20 mm CaEGTA and was shifted to more positive potentials by denervation in soleus fibers. We conclude that inactivation (i) does not strongly influence threshold contractions at conditioning potentials between ?60 and ?40 mV and (ii) influences Vt between ?40 and 0 mV in a manner that depends on test pulse duration.     

Direct corticospinal pathways contribute to neuromuscular control of perturbed stance.

The antigravity soleus muscle (Sol) is crucial for compensation of stance perturbation. A corticospinal contribution to the compensatory response of the Sol is under debate. The present study assessed spinal, corticospinal, and cortical excitability at the peaks of short- (SLR), medium- (MLR), and long-latency responses (LLR) after posterior translation of the feet. Transcranial magnetic stimulation (TMS) and peripheral nerve stimulation were individually adjusted so that the peaks of either motor evoked potential (MEP) or H reflex coincided with peaks of SLR, MLR, and LLR, respectively. The influence of specific, presumably direct, corticospinal pathways was investigated by H-reflex conditioning. When TMS was triggered so that the MEP arrived in the Sol at the same time as the peaks of SLR and MLR, EMG remained unaffected. Enhanced EMG was observed when the MEP coincided with the LLR peak (P < 0.001). Similarly, conditioning of the H reflex by subthreshold TMS facilitated H reflexes only at LLR (P < 0.001). The earliest facilitation after perturbation occurred after 86 ms. The TMS-induced H-reflex facilitation at LLR suggests that increased cortical excitability contributes to the augmentation of the LLR peaks. This provides evidence that the LLR in the Sol muscle is at least partly transcortical, involving direct corticospinal pathways. Additionally, these results demonstrate that approximately 86 ms after perturbation, postural compensatory responses are cortically mediated.