J. E. Misiaszek

The relationship between the kinematics of passive movement, the stretch of extensor muscles of the leg and the change induced in the gain of the soleus H reflex in humans

The gain of the H reflex attenuates during passive stepping and pedalling movements of the leg. We hypothesized that the kinematics of the movement indirectly reflect the receptor origin of this attenuation. In the first experiment, H reflexes were evoked in soleus at 26 points in the cycle of slow, passive pedalling movement of the leg and at 13 points with the leg static (the ankle was always immobilized). Maximum inhibition occurred as the leg moved through its most flexed position (P < 0.05). Inhibition observed in the static leg was also strongest at this position (P < 0.05). The increase in inhibition was gradual during flexion movement, with rapid reversal of this increase during extension. In the second experiment, the length of stretch of the vasti muscles was modelled. Variable pedal crank lengths and revolutions per minute (rpm) altered leg joint displacements and angular velocities. Equivalent rates of stretch of the vasti, achieved through different combinations of joint displacements and velocities, elicited equivalent attenuations of mean reflex magnitudes in the flexed leg. Reflex gain exponentially related to rate of stretch (R2 = 0.98 P < 0.01). The results imply that gain attenuation of this spinal sensorimotor path arises from spindle discharge in heteronymous extensor muscles of knee and/or hip, concomitant with movement.

Crossed inhibition of the soleus H reflex during passive pedalling movement

We hypothesized that sensory input from the moving leg induces presynaptic inhibition of the soleus H reflex pathway in the contralateral stationary leg. The results showed a crossed inhibition during passive pedalling movement of the leg, which was not removed by low levels of tonic contraction of soleus in the stationary leg. The inhibition was correlated exponentially to the rate of the movement (R2 = 0.934, P < 0.05) and was not dependent on the quadrants through which the moving leg was passing. Static flexion of the stationary leg caused ipsilateral inhibition of the reflexes (t = 5.590, P < 0.05), independent of the orientations of the other leg. We concluded that sensory inflow from the moving leg induces presynaptic inhibition in the stationary leg, that a complex transformation of the sensory input in the spinal cord or brain underlies the tonic crossed inhibition and phasic ipsilateral inhibition, and that descending motor commands exert a powerful control over these sensorimotor modulatory mechanisms.

Movement-induced gain modulation of somatosensory potentials and soleus H-reflexes evoked from the leg. I. Kinaesthetic task demands

Abstract Movement-related gating of cerebral somatosensory evoked potentials (SEPs) occurs during active and passive movements of both the upper and the lower limbs. The general hypothesis was tested that the brain participates in setting the gain of the ascending path from somatosensory receptors of the human leg to the somatosensory cortex. In experiment 1, SEPs from Cz’ and soleus H-reflexes were evoked by electrical stimulation of the tibial nerve in the popliteal fossa during passive movement about the right ankle. Early SEPs and H-reflexes sampled during simple passive movement were significantly attenuated when compared with stationary controls (P<0.05). The additional requirement of tracking the passive ankle movement with the other foot led to a significant relative facilitation of mean SEP, but not H-reflex amplitude, compared with means from passive movement alone (P<0.05). In experiment 2, SEPs were evoked in the active (tracking) leg during a forewarned reaction-time task. Subjects were required to move in a preferred direction or to track the passive movement of their right foot with their left. Significant attenuation of early SEP components occurred 100 ms prior to EMG onset (P<0.05), with no apparent effect due to tracking. In the 3rd experiment, SEPs and H-reflexes were evoked in the passively moved leg (the target for active movement of the left leg) during the same forewarned reaction-time task. During the warning period, SEPs were significantly attenuated compared with stationary controls for non-tracking movements, but not for movements involving tracking (P<0.05). It is concluded that centrifugal factors are important in modulating SEP gain required by the kinaesthetic demands of the task.

Long-lasting inhibition of the human soleus H reflex pathway after passive movement.

Human soleus H reflexes are attenuated during passive pedalling movements. This depression occurs within 70 ms of movement onset. We hypothesized that the reflex gain would return to control values with a similar brevity following movement. However, H reflexes sampled following a slow (10 rpm) passive pedalling movement of a single leg remained below control values for the duration of a 200 ms collection period, for all four pedal positions tested. The extent of the attenuation after movement was position dependent in a manner similar to that observed during movement. This position effect was more precisely defined by sampling reflexes 200 ms post-movement at 10 pedal crank positions. Also, the full course of reflex recovery was investigated by sampling up to 8 s post-movement at four pedal positions. Reflex gain remained reduced 1-4 s post-movement, in a position dependent manner. There was a subsequent facilitation of the reflex. Thus, following a locomotor-like movement there is sustained attenuation of the soleus H reflex. The early post-movement period is likely the continued expression of movement-induced reflex inhibition while the later period may arise from descending influences consequent to the termination of movement. Presynaptic inhibition is implicated, as reflexes still showed the gain modulation when sampled while soleus was tonically contracted, both following and during the passive movement.

Locomotor-Like Rotation of Either Hip or Knee Inhibits Soleus H Reflexes in Humans

Human soleus H reflexes are depressed with passive movement of the leg. We investigated the limb segment origin of this inhibition. In the first experiment, H reflexes were evoked in four subjects during (1) passive pedaling movement of the test leg at 60 rpm; (2 and 3) pedaling-like flexion and extension of the hip and the knee of the test leg separately; and (4) stationary controls. In the second experiment, with the test leg stationary, the same series of movements occurred in the opposite leg. Rotation of the hip or the knee of the test leg significantly reduced mean reflex amplitudes (p < 0.01) to levels similar to those for whole-leg movement (mean H reflexes: stationary, 71%; test leg pedaling movement, 10%; knee rotation, 15%; hip rotation, 13% [all data are given as percentages of Mmax]). The angle of the stationary joint did not significantly affect the results. Rotation of the contralateral hip significantly reduced mean reflex magnitudes. Rotation of the contralateral knee had a similar effect in three of the four subjects. We infer that a delimited field of receptors induces the movement conditioning of both the ipsilateral and contralateral spinal paths. It appears that somatosensory receptor discharge from movement of the hip or knee of either leg induces inhibition as the foundation for the modulation of H reflexes observed during human movement.

Long-lasting conditioning of the human soleus H reflex following quadriceps tendon tap.

Percussion of the quadriceps tendon was used to test the hypothesis that knee extensor muscle spindle discharge initiates down-regulation of the gain of the soleus H reflex. Seven subjects participated. Soleus H reflex magnitude was observed for up to 15 s, following conditioning tendon taps of 60 N or 80 N force and 10 ms duration, with the knee at 60 degrees or 90 degrees of flexion. The tap elicited quadriceps stretch reflexes in four subjects, with a mean latency of 42 ms. The major component of the conditioning of the soleus H reflex was significant attenuation of magnitude by 30-90% of controls, starting as early as 36 ms post-percussion and lasting as long as 3-8 s. The attenuation of reflex magnitude was evident, whichever combination of duration and force of tap was used. Preceding and/or following this inhibition, there was mild facilitation. Static stretch of quadriceps also significantly reduced soleus H reflex magnitude. These results support the spindle receptor origin for the gain attenuation seen during movement. The time course of the gain attenuation suggests a spinal route, by which the spindle discharge of the heteronymous extensor muscles initiates presynaptic inhibition of transmission through the reflex pathway.

Mechanisms within the human spinal cord suppress fast reflexes to control the movement of the legs

Passive locomotor-like movement induces depression of the gain of a fast conducting spinal sensorimotor path in humans. It was hypothesized that this gain control is mediated through a spinal circuit. In the first experiment, passive pedalling motion was rapidly initiated in eight able bodied subjects. Soleus H-reflexes (used to reveal the gain of the short latency stretch reflex) were recorded over the first 250 ms after the movement started. Significant depression in H-reflex magnitude was observed by 50 ms after the onset of movement. On the basis of the timing, this gain attenuation was likely mediated through a spinal circuit. In a second experiment we tested chronic quadriplegics with clinically complete lesions of the spinal cord. Of five subjects tested, three expressed the reflex and all three showed significant inhibition with passive pedalling movement (mean depression was to 39% of controls). Both the rapid onset of the gain change (Expt. 1) and the presence of movement-induced inhibition in individuals with spinal lesions (Expt. 2) provide evidence that this component of human locomotor control is located in the spinal cord. The initiating source is probably somatosensory receptor discharge due to the movement.

Movement-induced modulation of soleus H reflexes with altered length of biarticular muscles

Passive pedaling movements of the leg results in the phasic modulation of the soleus H reflex of that leg. In contrast, the H reflex of the contralateral leg is attenuated tonically. The phasic modulation of the reflex ipsilaterally can be attributed to the afferent discharge associated with the cyclic lengthening of the extensor muscles. We hypothesized that the tonic attenuation of the contralateral reflex could be explained if the afferent feedback arising from the lengthening of the biarticular muscles had an increased importance in regulating the amplitude of the contralateral reflex. To test this, the passive pedaling movements were reduced to those about either the knee or hip alone. Despite the alteration in the pattern of stretching of the biarticular muscles, the contralateral soleus H reflex was tonically attenuated during both forms of single joint movements. We suggest that the same phasic afferent discharge responsible for the modulation of the ipsilateral soleus H reflex initiates the tonic attenuation contralaterally, but that the signal undergoes a complex transformation in crossing the cord. These results do not rule out the possibility that the stretching of the biarticular muscles contributes to the attenuation of the ipsilateral soleus H reflex, which is subsequently masked by a powerful influence from the stretching of the uniarticular extensor muscles. To test this possibility, a second experiment manipulated the lengths of the muscles of the leg by altering the positions of the static joints during isolated rotation of either the knee or hip and measuring the amplitude of the ipsilateral soleus H reflex. From the results, it was clear that stretching the uniarticular extensor muscles produced the most dramatic effects. However, the stretch of the biarticular muscles yielded mild inhibitory influences if these muscles were near their maximal lengths.

Movement-induced gain modulation of somatosensory potentials and soleus H-reflexes evoked from the leg II. Correlation with rate of stretch of extensor muscles of the leg

Abstract Attenuation of initial somatosensory evoked potential (SEP) gain becomes more pronounced with increased rates of movement. Manipulation of the range of movement also might alter the SEP gain. It could alter joint receptor discharge; it should alter the discharge of muscle stretch receptors. We hypothesized that: (1) SEP gain reduction correlates with both the range and the rate of movement, and (2) manipulation of range and rate of movement to achieve similar estimated rates of stretch of a leg extensor muscle group (the vasti) results in similar decreases in SEP gain. SEPs from Cz’, referenced to Fpz’ (2 cm caudal to Cz and Fpz, respectively, according to the International 10–20 System), along with soleus H-reflexes were elicited by electrical stimulation of the tibial nerve at the popliteal fossa. Stable magnitudes of small M-waves indicated stability of stimulation. A modified cycle ergometer with an adjustable pedal crank and electric motor was used to passively rotate the right leg over three ranges (producing estimated vasti stretch of 12, 24 and 48 mm) and four rates (0, 20, 40 and 80 rpm) of movement. Two experiments were conducted. Ranges and rates of pedalling movement were combined to produce two or three equivalent estimated rates of tissue stretch of the vasti muscles at each of 4, 16, 32 and 64 mm/s. Tibial nerve stimuli were delivered when the knee was moved through its most flexed position and the hip was nearing its most flexed position. Means of SEP, H-reflex and M-wave magnitudes were tested for rate and range effects (ANOVA). A priori contrasts compared means produced by equivalent estimated rates of vasti stretch. Increasing the rate of movement significantly increased the attenuation of SEP and H-reflex gain (P<0.05). Increasing the range of movement also significantly increased these gain attenuations (P<0.05). Combining these to achieve equivalent rates of stretch, through different combinations of rate and range, resulted in equivalent depressions of SEP gain. H-reflex gains were similarly conditioned. These results suggest that muscle stretch receptors play a more important role than joint or cutaneous receptors in regulating SEP gain consequent to movement. We note that the present calculation only considers the knee extensors; however, the biomechanical model of stretch applies also to receptors in the hip extensors. This paper and the companion one show that primary factors in the kinaesthetic components of the movement regulate activity-induced gain attenuation of SEPs.

Movement-induced depression of soleus H reflexes is consistent in humans over the range of excitatory afferents involved

The presumption that the H reflex arises exclusively from Ia afferent discharge has been challenged. If the reflex is comprised of many afferent responses, then movement-induced H reflex inhibition witnessed at one point in the recruitment curve may be quite different from the inhibition at another point in the curve. H reflex recruitment curves were constructed for three subjects during passive pedalling, isolated knee rotation and isolated hip rotation. Compared to control recruitment curves, these curves were reduced across the full spectrum of stimulus intensities. This suggests one of two possibilities: (1) all afferents contributing to the H reflex are subject to the same source and modality of inhibition; or (2) there is only one afferent type contributing to the reflex.