Neural mechanisms that contribute to cyclical modulation of the soleus H-reflex in walking in humans

The amplitude of the Hoffmann reflex (H-reflex) of the human soleus muscle is modulated in a cyclical way during walking. This paper addresses two questions associated with the neural mechanisms that might generate this modulation: (1) Does the amplitude of the H-reflex simply rise and fall as a function of the background excitability of the soleus motoneuron pool? (2) Is the modulation of the H-reflex dependent on events associated with activation of the antagonist muscle? The amplitude of the soleus H-reflex was compared under three conditions: natural walking, walking without activating the tibialis anterior muscle, and walking with activation of the soleus muscle in the swing phase. Human subjects were able to perform these three tasks with minimal training. The results indicated that the soleus H-reflex remained very depressed in the swing phase of walking, even when a voluntary contraction of the soleus muscle was superimposed during this time. Moreover, the presence of tibialis anterior activity had a very minor effect on the amplitude of the soleus H-reflex during walking. It is concluded that modulation of the soleus H-reflex is not simply a reflection of the background excitability of the motoneuron pool, and the modulation is not dependent on activation of the antagonist muscle. Other more powerful mechanisms are acting to modulate the reflex, most likely presynaptic inhibition of the primary afferents.     

Modulation of motor unit discharge rate and H-reflex amplitude during submaximal fatigue of the human soleus muscle

Declining motor unit discharge rates and H-reflex amplitude have been observed in separate experiments during fatiguing submaximal contractions in humans. The purpose of this experiment was to investigate motor unit discharge rate, H-reflex amplitude, and twitch contractile properties concurrently during a fatiguing submaximal isometric contraction of the ankle plantarflexors. Eleven healthy subjects performed fatiguing contractions of low force (25% maximal voluntary contraction (MVC)) or high force (42–66% MVC). Hoffmann (H)-reflexes, muscle compound action potentials (M-waves), twitch contractile properties, and motor unit discharges were recorded from the soleus muscle. In the low-force fatigue task, motor unit firing rate increased gradually over time, whereas the resting H-reflex was significantly depressed at 15% of endurance time and remained quasiconstant for the rest of the task. This suggests that the processes mediating the resting H-reflex depression are relatively independent of those modulating the motor unit firing rate during a low-force fatigue task. In the high-force fatigue task, a decline in the average motor unit discharge rate was accompanied by a decrease in the resting H-reflex amplitude and a prolongation of the twitch half-relaxation time (HRT) at the completion of the fatigue task. Overall, motor unit firing rate was modulated in parallel with changes in the twitch HRT, consistent with the muscle wisdom hypothesis.     

Sural nerve facilitation of the soleus muscle H-reflex in high level gymnasts

The effect of a non-nociceptive sural nerve stimulation on the H-reflex was examined in 6 young female gymnasts and 12 control subjects. At the 70–90 ms delays investigated between conditioning and test stimulations, the sural nerve stimulation produced a facilitation that did not differ significantly between the gymnast group (6.15% of the maximal H-reflex size, H_max) and the control group (8.12% H_max). The inter-subject dispersion was significantly larger in the control group (0.30%–21.04% H_max) than in the gymnast group (4.44%–7.70% H_max). It is suggested that this narrow range of sural nerve facilitation may have resulted from the prolonged specific training of these sportswomen. Accepted: 15 March 2000     

Excitability of the soleus H-reflex arc during walking and stepping in man

Summary In eight normal subjects, the excitability of the soleus (Sol) H-reflex was tested in parallel with Sol length changes, EMGs of leg and thigh muscles and ground contact phases, during three different pacing movements: bipedal treadmill walking, single limb treadmill walking, and single-limb stepping on one spot. A computerized procedure was used which compensated for changes in stimulus effectiveness that occurred during free motion. In the three paradigms examined, significant excitability modulations were observed with respect to a control level determined in standing weight-bearing position. During bipedal treadmill walking, excitability was decreased in the early stance, maximally enhanced in the second half of the stance, and again decreased during the end-stance and the whole swing phase, with a minimum value around the toe off period. The main modulation pattern was retained during single-limb treadmill walking. During single-limb stepping on one spot, the stance-phase increase in excitability and the swing phase depression were still present. However, in the second half of the swing phase, reflex responsiveness returned to reference level, which was maintained during the subsequent contact period. Moreover, a decrease in reflex excitability was detected around the mid-stance. The time course of the described modulations was only partly correlated with the EMG and length changes of the Sol muscle. Furthermore, in the three movements tested, during the early stance phase, the excitability of the H-reflex arc did not correspond to the one expected on the basis of the available H-reflex studies performed under static conditions. It is suggested that, at least in certain stride phases (e.g. around the early contact period), an active regulation affects the transmission in the Sol myotatic arc during the pacing movements investigated.     

Enhanced stretch reflex excitability of the soleus muscle in experienced swimmers

The purpose of this study was to investigate effects of long-term participation to swimming on adaptations of spinal reflex excitability. To this end, mechanically induced stretch reflex (SR) and electrically induced Hoffmann (H-) reflex of the soleus muscle were investigated between swimmers with experience of more than 10 years and non-trained individuals while sitting at rest. The amplitude and the gain (stretch velocity vs. amplitude of the reflex response) of the SR were significantly greater in the swimming group than in the non-trained control group. Similarly, the responses of the H-reflex were also significantly greater in the swimming group than in the non-trained control group. Results of this study demonstrated that the spinal reflex excitability in experienced swimmers was far more enhanced than in non-trained individuals.     

The differences in human spinal motoneuron excitability during the foreperiod of a motor task

Summary Changes in excitability of the spinal motoneuron pool during the foreperiod, which was fixed at 0.8 s, in simple and choice reaction time experiments using ankle dorsiflexion and plantar flexion were studied in fourteen healthy normal subjects by combining the visually guided tracking and H-reflex testing methods. Almost all cases showed a significant facilitation in the soleus H-reflex within the time interval between 100 and 300 ms after a warning signal (Phase I), irrespective of movement direction and task modality. The pretibial H-reflex was also facilitated. On the other hand, variable effects were noted in the later half of the foreperiod, particularly within the 200 ms prior to the response signal (Phase II). Using a simple reaction task with dorsiflexion, six cases showed no changes in the soleus H-reflex, while four others showed statistically significant inhibitory changes and the remaining four showed facilitation. The inhibition and facilitation were often accompanied with very weak and unintended EMG activities in the pretibial and Sol muscles respectively. A similar finding was obtained in the simple plantar flexion task and the choice reaction task with dorsiflexion or plantar flexion. We suggest that the facilitation at Phase I represents a perceptual orienting response to a warning signal and the effects seen in Phase II represent the difference in the waiting attitude of each subject anticipating initiation of the coming task, or the preparatory set which primed the spinal motor structure in a biased position.     

Contribution of peripheral afferents to the activation of the soleus muscle during walking in humans

Summary Small, rapid stretches were applied to the soleus muscle during the stance phase of walking by lifting the forefoot with a pneumatic device. Stretch responses were induced in the soleus muscle by the disturbance. The amplitude and time course of the responses from the soleus muscle were a function of both the kinematics of the disturbance and the time in the step cycle when the disturbance was applied. The step cycle was divided into 16 equal time parts, and data obtained within each of these parts were averaged together. The electromyographic (EMG) response of the soleus muscle showed a time course that was similar to the time course of the angular velocity induced by the disturbance at the ankle. Three linear equations were used to predict the EMG response from the soleus muscle as a function of the angular kinematics of the disturbance: 1) velocity, 2) velocity and displacement, 3) velocity, displacement and acceleration. Introduction of a pure delay between the EMG and the kinematics substantially improved the predictions. Most of the variance (70%) in the EMG response could be accounted for by the velocity of the disturbance alone with an optimal delay (average 38 ms). Inclusion of a displacement term significantly increased the variance accounted for (85%), but further addition of an acceleration term did not. Since the velocity of the disturbance accounted for most of the variance, the reflex gain was estimated from the velocity coefficient. This coefficient increased in a ramp-like fashion through the early part of the stance phase, qualitatively similar to the increase in the H-reflex. Based on these identified gains, this reflex pathway was estimated to contribute substantially (30% to 60%) to the activation of the soleus muscle particularly during the early part of the stance phase.     

Changes in presynaptic inhibition of Ia fibres to soleus motoneurones during voluntary dorsiflexion of the foot

Summary Variations of presynaptic inhibition in heteronymous Ia fibres projecting to soleus motoneurones were studied during the first 250 ms of phasic voluntary isometric contractions of the antagonist tibialis anterior muscle in human subjects. During the first 60–80 ms of TA e.m.g activity, presynaptic inhibition was often more marked than at rest, but not in all experimental sessions. After 60–80 ms, presynaptic inhibition was always increased compared to rest and to the onset of TA e.m.g. activity. A rebound in femoral nerve induced Ia facilitation was often observed between 90–150 ms. The early increase in presynaptic inhibition was widespread and non specific since it was observed at the onset of extensor carpi radialis contractions of maximal strength. The rebound in heteronymous Ia facilitation was interpreted as a relative decrease in presynaptic inhibition to which nonspecific suprasegmental and cutaneous effects contributed. The late increase in presynaptic inhibition in Ia fibers to soleus motoneurones was considered as reciprocally inhibiting the Sol H-reflex, thus counteracting the phasic stretch of the antagonist muscle during TA contraction.     

Sustained increase in the excitability of myelinated peripheral axons to depolarizing current is mediated by Nav1.6

Changes in the excitability of peripheral myelinated axons in response to long-lasting subthreshold depolarizing or hyperpolarizing currents (threshold electrotonus) are used as a complementary electrophysiological parameter in the study of peripheral nerve diseases in people. However, the contribution made by various axonal ion channels to specific components of threshold electrotonus remains incompletely understood. In this study, we have recorded threshold electrotonus responses from isolated nerve segments of sural nerve from control and Scn8amed mice, which lack functional Nav1.6 voltage-gated sodium channel. In med mice, the increase in axonal excitability produced by application of subthreshold depolarizing currents for 100-200ms was not sustained. In contrast, there was no difference in threshold electrotonus responses to subthreshold hyperpolarizing current application between Scn8amed and control mice. These data reveal the specific functional role of an identified subtype of voltage-gated sodium channel (Nav1.6) in mediating the depolarizing threshold electrotonus response of peripheral myelinated nerve fibers.     

Contribution of peripheral 5-HT2A or 5-HT3 receptors to Fos expression in the trigeminal spinal nucleus produced by acute injury to the masseter muscle during persistent temporomandibular joint inflammation in rats

We investigated the contribution of peripheral 5-HT2A or 5-HT3 receptors to Fos expression in the trigeminal spinal nucleus (VSP) following acute masseter muscle injury in male rats with or without temporomandibular joint (TMJ) inflammation persisting for 7 days. TMJ inflammation was evoked by an injection of complete Freund’s adjuvant (CFA). Two hours after formalin injection into the masseter muscle produced Fos-like immunoreactivity (Fos-LI) in several regions of the VSP and upper cervical spinal cord (C2), such as ventrolateral (vl) area of the trigeminal subnucleus caudalis (Vc)/subnucleus interpolaris (Vi) transition (vl-Vi/Vc), paratrigeminal nucleus (dPa5), middle portion of the Vc (mid-Vc) and Vc/C2 transition (Vc/C2) regions in both groups. Significant increases in the number of Fos-LI were observed in these areas in CFA group compared with non-CFA group. TMJ inflammation alone did not induce a significant level of Fos-LI in the VSP. In order to assess the effect of antagonizing 5-HT2A or 5-HT3 receptors on formalin-induced Fos-LI, rats were pre-treated with local (masseter muscle) administration of ketanserin or tropisetron (0.01, 0.1 mg/rat) 20 min prior to formalin injection. In CFA group, these antagonists given locally reduced the Fos-LI response in the laminae I–II at the mid-Vc and Vc/C2 regions. These antagonists reduced the Fos-LI response in the dPa5, but not in the vl-Vi/Vc region. The Fos-LI response was not affected by i.v. administration of ketanserin (0.01, 0.1 mg/rat) or tropisetron (0.01 mg/rat). In non-CFA group, these antagonists given locally did not reduce the Fos-LI response. These results suggest that peripheral 5-HT2A and 5-HT3 receptors contribute to nociceptive processing in the masseter muscle in TMJ inflammatory conditions.